Research-Relevant Conditions and Pathology of Laboratory Mice, Rats, Gerbils, Guinea Pigs, Hamsters, Naked Mole Rats, and Rabbits

Timothy K Cooper; David K Meyerholz; Amanda P Beck; Martha A Delaney; Alessandra Piersigilli; Teresa L Southard; Cory F Brayton

doi:10.1093/ilar/ilab022

. 2022 Jan 4;62(1-2):77–132. doi: 10.1093/ilar/ilab022

Research-Relevant Conditions and Pathology of Laboratory Mice, Rats, Gerbils, Guinea Pigs, Hamsters, Naked Mole Rats, and Rabbits

Timothy K Cooper ¹, David K Meyerholz ², Amanda P Beck ³, Martha A Delaney ⁴, Alessandra Piersigilli ⁵, Teresa L Southard ⁶, Cory F Brayton ^7,^✉

PMCID: PMC9291387 PMID: 34979559

Abstract

Animals are valuable resources in biomedical research in investigations of biological processes, disease pathogenesis, therapeutic interventions, safety, toxicity, and carcinogenicity. Interpretation of data from animals requires knowledge not only of the processes or diseases (pathophysiology) under study but also recognition of spontaneous conditions and background lesions (pathology) that can influence or confound the study results. Species, strain/stock, sex, age, anatomy, physiology, spontaneous diseases (noninfectious and infectious), and neoplasia impact experimental results and interpretation as well as animal welfare. This review and the references selected aim to provide a pathology resource for researchers, pathologists, and veterinary personnel who strive to achieve research rigor and validity and must understand the spectrum of “normal” and expected conditions to accurately identify research-relevant experimental phenotypes as well as unusual illness, pathology, or other conditions that can compromise studies involving laboratory mice, rats, gerbils, guinea pigs, hamsters, naked mole rats, and rabbits.

Keywords: Cricetinae, Gerbillinae, guinea pigs, mice, mole rats, rabbits, rats

INTRODUCTION

Animals have been used in biomedical research in increasing numbers since the 19th century.^1–5 Rodent models have provided a useful foundation for many studies, and technological advances such as somatic cell nuclear transfer and, more recently, improved genome editing (eg, CRISPR/Cas9)^6–10 offer enhanced and faster genetic manipulations in rodents and other species.

In traditional experimental settings, animals are studied in treatment groups and evaluated for group-specific treatment-related phenotypes.¹¹^,¹² A phenotype can be defined as any morphologic, physiologic, or other quantifiable trait of a cell or organism. Phenotypes result from and are influenced by interactions between genetic and environmental influences, as discussed by Darwin, Lamarck, and others, finally referred to as “phenotypes” by Johannsen in 1909.¹³^,¹⁴

Genetic (intrinsic) factors are conferred by species, family, stock, or strain genetics, and sex, and can be modified by intended manipulations (irradiation, genotoxins, gene editing).

Experimental genetic manipulations can further introduce off-target genetic effects related to copy number, insertion sites, and perhaps more commonly from flanking or additional background genetic contributions from the multiple strains contributing to many genetically modified (GM) mice.¹⁵ Spontaneous conditions, including neoplasia or degenerative lesions, related to genetic backgrounds can be misinterpreted as research-relevant effects of intended experimental interventions. Thus, it is important to be aware of genetic backgrounds and their implications. Environmental (extrinsic) factors that influence phenotype are increasingly recognized. Examples include diet, housing and social conditions, conspecific aggression, lighting, noise, bedding, temperature, handlers, and any clinical and experimental interventions.^16–19 Microbial status and the microbiome may be considered with extrinsic influences (as allochthonous agents) or intrinsic influences (as autochthonous agents), or somewhere in between. Increasingly, microbial status and the microbiome are recognized to influence phenotypes and research. Although serious attrition related to common agents is not expected in today’s research programs, immune modulation by microflora is expected, and intestinal microbiome has proven to be a “fingerprint” for different rodent vendors and facilities. Mice of similar age, sex, and strain obtained from different sources may have quite different research-relevant phenotypes, which may be construed as research problems or may lead to useful insights.^20–22^,²³

Adventitious infectious diseases have been a major cause of loss of experimental animals. Overt disease and death from infections are far less likely today, with previously common pathogens now excluded from many research programs. Animals are expected to be immunologically naïve when they are maintained in strict barriers such as reputable vendor colonies with rigorous exclusion practices. Animals are less immunologically naïve in more conventional conditions that are less microbially restricted, with more liberal access to personnel and animals and exclusion of fewer agents.²⁴^,²⁵^,²⁶

Immune-deficient animals maintained near or with immune-sufficient animals, with handlers and equipment in common, are at risk of disease from exposures to common opportunists as well as from agents administered unintentionally in biologics, such as serum, cell cultures, and patient-derived tissues. Animals receiving human-derived biologics are at further risk of research-limiting complications from human agents such as Epstein Barr virus (EBV).²⁷ Contemporary interest in pet store or wild flora poses potential risks to animals and personnel.²⁸^,²⁹ Thus, infectious conditions in the summary tables below may still occur, and their impacts on research reproducibility and validity as well as on morbidity and mortality should be considered. Further, biosecurity is essential to personnel safety as well as animal health. Surveillance recommendations for adventitious infections and reviews of relevant zoonoses of laboratory animals are published elsewhere.⁴^,³⁰^,³¹^,²³^,³²^,³³

In recent years, concerns for research rigor and reproducibility have attracted much attention.⁴^,¹⁸^,³⁴ Recognition of error and a “full appreciation of possible sources of error” is recognized as critical to rigorous science.³⁴ The validity and utility of animal model data have been questioned, in part, because of flawed interpretations attributable to insufficient consideration of other influencing factors.^35–38 Thus, recognition and understanding of potential factors that affect phenotypes and study data are essential.⁴^,³⁹^,⁴⁰ Herein are reviewed expected conditions and pathology, “background,” findings and influencing factors in several common and emerging animal models, including laboratory mice, rats, gerbils, guinea pigs, hamsters, naked mole rats, and rabbits. Although the similarities between these animals and humans have led to important biomedical discoveries and various biological and disease features are shared among these animals (eg, malocclusion in elodontic teeth or Tyzzer’s disease due to Clostridium piliforme infection), differences in their anatomy, physiology, and disease susceptibilities are important to their care, welfare, pathology, and research interpretation. This review and its references are intended to be a resource for researchers, veterinarians, and pathologists who work with these animals.

MICE

Laboratory Mice: Order Rodentia, Suborder Myomorpha; Mus musculus ssp.

The laboratory mouse is the most commonly studied mammal in human disease and basic biology research.⁴¹ The similarities with human genetics, physiology, and anatomy, combined with logistic advantages such as a short lifespan and gestation, high fertility, and available technologies and resources, are favorable for many types of studies.²⁶^,⁴² The laboratory mouse originates from interbreeding of several Mus musculus subspecies. Hundreds of inbred strains represent 7 clades or major branches of their family tree that have distinct traits (ie, phenotypes).⁴³^,⁴⁴

Individuals of an inbred strain should be genetically identical (isogenic) and homozygous at every locus. More than 99.9% homozygosity is predicted (mathematically) after 40 brother-sister matings. Since approximately 1909, laboratory mice were selected and inbred for traits of research interest. Substrains of an inbred strain are suspected or known to be genetically different. Substrains are expected to arise when branches of a strain are separated after 20 but before 40 generations of inbreeding due to residual heterozygosity, and genetic drift is expected when branches are separated.⁴⁵^,⁴⁶ The various C57BL/6N and C57BL/6J substrains offer important examples of substrain variations relevant to metabolic, immune, and other studies, relevant to expected consequences of establishing new colonies from a parent strain, and relevant to the importance of complete nomenclature in reporting research.^47–51

Outbred mice should be more heterogeneous and harbor more heterozygosity. However, a majority of the widely used “outbred” stocks originate from a single (Swiss) branch of the mouse family tree and do not represent the spectrum of heterogeneity of laboratory mice. Further, stocks (of the same name) maintained in closed colonies can be expected to accumulate differences over years, and heterozygosity in some stocks and colonies is quite limited.⁵² In contrast, the Diversity Outbred (DO) stock was developed by crossing Collaborative Cross recombinant inbred lines, which derive from 8 strains selected to represent mouse genetic diversity. The Diversity Outbred breeding strategy and ongoing genetic testing are key to maintaining their heterogeneity and heterozygosity.⁵³

In recent decades, surveillance and exclusion of previously common agents have reduced overt disease and animal loss; however, numerous viruses, bacteria, and parasites are still sporadically or regularly detected.²⁶ Additionally, as formerly common agents such as mouse hepatitis virus are increasingly excluded, “new” agents such as mouse kidney parvovirus are “discovered.”⁵⁴^,⁵⁵^,⁵⁶ Research colony microbial status and significance of the agents present should be considered in study design and interpretation. The current interest in pet store and wild rodents to “normalize” flora and immune responses and better represent human conditions may provide great entertainment for pathologists and a resurgence of disease conditions that were excluded from reputable vendor rodent colonies because of adverse effects on research. Vendor-sourced animals, as used in highly cited studies regarding the merits of “normalizing” flora, should be more microbially and immunologically naive than those bred and used in research facilities with less stringent barrier conditions.²⁴^,²⁵ Research-relevant features and non-infectious conditions of laboratory mice are summarized in Tables 1–4. Infectious agents that may be identified or may cause disease in mice are summarized in Tables 5–7. Although many of the agents are not expected in contemporary research colonies, they remain relevant given the risks posed by biological contaminants, immune-deficient animals, and feral or pet rodents.

Table 1.

Laboratory Mice: Taxonomy, Genetics, Nomenclature, and Common Strains/Stocks of Laboratory Mice²⁶^,^138–148^,¹⁴⁹

Strain or Stock (Abbreviation)	Expected Phenotypes
129/ ^a	Acallosity-hypocallosity; acidophilic macrophage pneumonia; hyalinosis; portosystemic shunts;¹⁵⁰ megaesophagus; ulcerative blepharitis; cataracts; lung tumors; teratomas (Dnd1^Ter); Harderian gland tumors.^151–153
A/	Amyloidosis; muscular dystrophy (Dysf^prmd); T_H2 immune bias; liver tumors, lung tumors (Pas1^A/J); rhabdomyosarcoma.¹⁵⁴^,¹⁵⁵
AKR/ (AK)	Thymic lymphoma due to ecotropic retroviruses (Emv11, Emv12), most die by 1 y; mouse urologic syndrome; hair interior defect (Soat1^ald).¹⁵⁶
B6C3F1	First filial generation hybrid of C57BL/6 females and C3H/He males. Hyaline glomerulopathy; fibro-osseous lesions; lymphoma; lung and liver tumors.^157–166
Bagg albino BALB/c (C) BALB/cBy (CBy)	Acallosity-hypocallosity; conspecific (male) aggression; cardiac calcinosis; atrial thrombi; vaginal septa; T_H2 immune bias; Reye’s-like syndrome, lung tumors; Harderian gland tumors; myoepithelioma; rhabdomyosarcoma; induced plasmacytoma; ^167–170 Prkdc^dxnph mutation.¹⁷¹
C3H/ (C3)	Blind (Pde6b^rd1); cardiac calcinosis, soft tissue mineralization; alopecia areata; mammary tumors in females; liver tumors in males; adrenal cortical adenomas. Endotoxin resistance in C3H/HeJ due to Tlr4^LPS-d mutation.¹⁷²^,¹⁷³
C57BL/6 (B6)	Hydrocephalus; microphthalmia (also B10); ulcerative dermatitis; amyloidosis; T_H1 immune bias; acidophilic macrophage pneumonia; hyalinosis; retinal dysplasia in B6N (Crb1^rd8); portosystemic shunts in some B6J;¹⁷⁴ polyarteritis; lymphoma; histiocytic sarcoma; genetic variations between N and J substrains (eg, Aanat, Crb1, Dock2, Nlrp12, Nnt, Snca).⁴⁸^,⁵⁰^,¹⁵¹^,¹⁶⁹^,^175–179
Dilute brown non-agouti DBA/1 (D1) DBA/2 (D2)	Myo5a^d/d; Tyrp1^b/b; a/a. Cardiac calcinosis, soft tissue mineralization (male>female); seizures; NK cell dysfunction (Klrd1^DBA/2J deletion) and T_H2 immune bias in DBA/2; glaucoma (Gpnmb^R150X, Tyrp^isa); intestinal adenoma; leiomyomas.¹⁸⁰^,¹⁸¹
Friend virus B FVB/N	Blind (Pde6b^rd1); seizures (Sicd1^FVB/NJ); mammary hyperplasia/neoplasia; prolactin-secreting pituitary tumors; eartag-associated tumors; lung tumors.^182–184
KK/	Polygenic diabetes; hyperglycemia, hyperinsulinemia, glucose intolerant, insulin resistant, obese, large pancreatic islets degranulated β-cells; Soft tissue mineralization; yellow coat color.¹⁸⁵
Non-obese diabetic NOD/	Type I diabetes mellitus (T1DM); immune defects; osteosarcomas; mammary tumors; lymphoma/leukemia.¹⁸⁶
Swiss Jim Lambert SJL/J	Blindness (Pde6b^rd1); senile amyloid (Apoa2^c); conspecific (male) aggression; muscular dystrophy (Dysf^im); B cell lymphoma (Mtv29), radioresistant. ¹⁵⁵^,¹⁸⁷^,¹⁸⁸
Swiss (‘outbred’)	Includes :CD-1, :ICR, :NMRI, :ND4, :SW ^b etc stocks; variations in: blindness (Pde6b^rd1); acidophilic macrophage pneumonia; amyloidosis; brainstem infarcts; nephropathy; mouse urologic syndrome; lymphomas; lung tumors; liver tumors; skin tumors.¹⁹^,¹⁶⁵^,¹⁶⁶^,^189–197
Nude nu/nu	Inbred or outbred; Foxn1^nu/nu; T cell deficient (leaky); hair follicle dysplasia; thymic remnant not populated (athymic/hypothymic). Eye lesions with some caging systems.¹⁹⁸^,¹⁹⁹
Severe combined immune deficiency scid	Inbred or outbred; Prkdc^scid; B and T cell deficient (leaky); lymphoid hypoplasia (not depletion); small thymus, spleen and lymphoid tissues; thymic lymphomas.²⁰⁰^,²⁰¹
NOD scid	scid congenic to NOD; (B and T cell deficient (less leaky); low natural killer (NK) cell activity); lymphoid hypoplasia; small thymus, spleen and lymphoid tissue; expect thymic lymphomas starting approximately 6 mo, and early death.
NOD scid gamma NOG, NSG, NCG	NOD scid with Il2rg mutation: lack NK cells, no leakiness, fewer lymphomas, and longer life span (in barrier conditions) than NODscid.^202–204 NOG, NSG, NCG are on similar backgrounds, carry similar mutations, are not identical.

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^a‘/’ After strain/root abbreviation indicates inbred and is followed by the source laboratory code.

^b‘:’ Before stock abbreviation indicates outbred and is preceded by the source laboratory code.

Table 4.

Laboratory Mice: Neoplastic Conditions¹⁴⁶^,²⁵⁶^,³⁷⁷

System Organ/Tissue	Neoplastic Condition
Alimentary	²¹⁴ ^, ²⁸²
Intestine	Adenomas in DBA/2; otherwise uncommon unless induced or in mutants (eg, Apc^Min).¹⁸⁰
Liver	Adenoma, carcinoma, hepatoblastoma. Expected in male C3H and CBA; less common in females or other strains.
Pancreas	Uncommon except in GEMs.³⁷⁸
Salivary glands	Adenoma/adenocarcinoma: sporadic. Myoepithelioma in female BALB/c; can also be of mammary origin.²⁶^,³⁷⁹^,³⁸⁰
Cardiovascular	²⁹⁷
Heart, vessels	Hemangiosarcoma: liver, spleen, other sites²⁹⁷^,³⁸¹
Endocrine	³⁰⁶
Adrenal	Cortical adenoma and adenocarcinoma are rare.
	Medullary tumors (benign and malignant pheochromocytoma, ganglioneuroma) are uncommon except in some mutants.
Pituitary	Adenoma of pars distalis most common, especially in FVB/N.¹⁸³^,³⁸²^,³⁸³
Thyroid	Follicular and C-cell tumors are rare. Follicular tumors common in some GEMs.³⁸⁴
Hematolymphoid	¹⁹⁴ ^, ³¹² ^, ³⁸⁵ ^, ³⁸⁶
	Lymphoma is the most common tumor in mice.
	Histiocytic sarcoma: common in old mice (>1 year); females; usually involves liver, uterus, and/or spleen; marrow involvement in advanced disease. Possible hyaline droplets in renal tubules.
	Leukemias infrequent unless induced.
	Lymphoproliferative conditions. SJL/J, lupus models (eg, Fas^lpr, Fas^gld).
Thymus	T lymphoblastic lymphoma in AKR, C58, NOD scid mice; early onset beginning approximately 6 mo with high mortality by 1 y of age; massive thymomegaly with leukemia in advanced disease. B cell neoplasms may occur in thymus, usually in older mice.
	Thymoma.³⁸⁷
	Mast cell neoplasia uncommon, may be systemic.³⁸⁸ Prominent mast cells noted in NSG-SGM3 pancreas.
Integument	³¹⁷ ^, ³¹⁸
Mammary gland	Adenomas, adenocarcinomas. C3H females; also A, BALB/c, DBA. Association with pituitary adenomas in FVB/N.¹⁸³^,³⁸²
Preputial/clitoral gland	Uncommon, must be differentiated from inflammatory and cystic degeneration in aging mice.³⁸⁹
Skin	Squamous cell papilloma common in aged mice. Squamous cell carcinoma unusual unless induced; associated with ear tags in FVB/N.³⁹⁰
	Sarcomas arising from soft tissues of subcutis are sporadic, some associated with ear tag or other trauma.
Harderian gland	Adenomas more common than adenocarcinomas. 129 and C3H ³⁹¹
Musculoskeletal	³³² ^, ³⁹²
Bone	Chondromas are very rare.
	Osteoma in CF-1; Osteosarcoma common in some strains (NMRI, NOD scid, NOD).³⁹³
Skeletal muscle	Rhabdomyosarcoma. Age related in A/J; sporadic in BALB/c.¹⁵⁴
Nervous	²⁴⁴ ^, ³³⁸
Brain	Glioma, oligodendroglioma, glioblastoma, and astrocytoma uncommon. Spontaneous oligodendroglioma in BALB/c.
Respiratory	³⁴⁴
Lung	Adenomas more common than adenocarcinomas; multiple tumors in A strain by 1 y; fairly common in 129, BALB/c, FVB/N, and Swiss; less common in C57BL. ³⁹⁴
Urogenital	³⁶³
Kidney/urinary bladder	Rare, except in some GEM; kidney tumors induced by streptozotocin.³⁹⁵
Female reproductive	Unusual in most strains.³⁶¹ FVB/N may have more ovarian tumors including teratoma; ovarian granulosa cell tumors and endometrial yolk sac carcinomas reported in retired NSG breeders, may be influenced by parity.
Male reproductive	Unusual in most strains. Males of certain 129 strains may have testicular teratomas, detected in young animals, and prenatally.³⁶²^,³⁹⁶
Extragonadal	Teratomas (teratocarcinomas) reported in B6,129 embryonic stem cell chimeras, usually on midline, including tail.³⁹⁷^,³⁹⁸

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Table 5.

Laboratory Mice: Viruses²⁶^,¹⁴⁶^,^399–401

Family, Genus	Agent	Comments
Adenoviridae, Mastadenovirus	Mouse adenovirus 1 and 2 (MAdV-1 and -2)	Common in wild mice. MAdV-1: adults- subclinical infection; experimental lethal infections in susceptible strains (B6, SJL/J) or immune deficient may have necrosis inflammation intranuclear inclusions in CNS spleen, liver, kidney, etc. MAdV-2: subclinical infections; intranuclear inclusions in enterocytes.⁴⁰²
Arenaviridae, Mammarenavirus	Lymphocytic choriomeningitis virus (LCMV)	Zoonotic; contaminant of cell and tumor lines; usually subclinical in immune sufficient; susceptible strains may have growth retardation, immune complex glomerulonephritis, vasculitis, perivascular lymphoid aggregates in CNS.
Arteriviridae, Gammaarterivirus	Lactate dehydrogenase-elevating virus (LDV)	Common in wild mice; contaminant of cell lines and biologicals; subclinical elevation of multiple serum enzymes, particularly LDH, related to macrophage tropism; some immune deficient strains may develop CNS lesions.
Astroviridae, Mammastrovirus	Murine astrovirus	Common detection, subclinical infection, found in liver, intestine and other organs. Infected intestines have increased permeability.⁴⁰³^,⁴⁰⁴
Caliciviridae, Norovirus	Mouse norovirus (MNV)	Common; subclinical in immune sufficient and many immune deficient mice; identified in subclinical inflammatory foci in mouse livers; morbidity and mortality in some strains with defective innate immunity (eg, Stat1, Ifngr1) resulting in necrosis/ inflammation in liver, gastrointestinal, spleen, brain, lymph nodes.⁴⁰⁵^,⁴⁰⁶
Coronaviridae, Betacoronavirus	Mouse hepatitis virus (MHV)	Formerly common with epizootic infections and mortality; contemporary infections are usually subclinical; 2 tropisms: 1) Respiratory type → systemic dissemination → classic necrotic foci with syncytia in liver, young mice lacking protective Ab are susceptible; 2) Enterotropic is most common, infection in intestine with minimal lesions and syncytia. Immune deficient mice are susceptible to both types.
Hantaviridae	Multiple	Zoonotic; may be a contaminant in mice, cells, biologicals. Laboratory mice are not expected to be susceptible to Hantavirus infection.
Herpesviridae, muromegalovirus	Mouse cytomegalovirus (CMV)	Common in wild mice; characteristic karyocytomegaly and intranuclear inclusions. Subclinical infection of salivary gland ductal epithelium in immune sufficient; in immune deficient mice, mortality with systemic infection and necrosis in multiple tissues. Klra8 alleles affect susceptibility.
Herpesviridae, unassigned	Mouse thymic virus	Common in wild mice; biological contaminant; Subclinical infection in adults, pups may have inclusions and necrosis in lymphoid organs (thymus), may cause protracted immune suppression.
Herpesviridae, Lymphocryptovirus	Epstein-Barr virus	Post-transplant lymphoproliferative disease (human B cells) in humanized and patient-derived xenograft (PDX) bearing mice.²⁷
Pneumoviridae, Orthopneumovirus	Pneumonia virus of mice (PVM)	Subclinical infection of respiratory tract; immune deficient mice may have persistent lung infection and potential death.
Paramyxoviridae, Respirovirus	Sendai virus	Respiratory infection, very contagious via aerosols; subclinical in immune sufficient adults; dyspnea, poor growth, and death in young animals and immune deficient.
Parvoviridae, Protoparvovirus	Mouse minute virus (MMV), mouse parvovirus (MPV)	Usually subclinical; replicate in dividing cells (S phase) with effects on developing tissues, immune cells, tumors; contaminant of cell lines.
Parvoviridae, unclassified	Murine chapparvovirus, (mouse kidney parvovirus)	Common; subclinical in immune sufficient; intranuclear inclusions in renal tubule epithelium, usually in older animals. Clinical disease in older immune deficient mice with severe chronic renal disease and tubule degeneration.²⁹^,⁵⁴^,⁴⁰⁷
Picornaviridae, Cardiovirus	Theiler's Murine Encephalomyelitis Virus (TMEV, GDVII)	Usually subclinical infection; CNS disease in spontaneously infected susceptible mice is uncommon. Haplotype at the MHCII H2 locus determines susceptibility.
Polyomaviridae, Alphapolyomavirus	Mouse polyomavirus (MPyV-1)	Lesions in immune deficient mice; polytropic virus infects multiple tissues with cytopathic and proliferative lesions (eg, airway, renal pelvis and ureteral epithelium); nude mice especially prone to wasting, paralysis, tumors; oncogenic strains can cause tumors of salivary glands (myoepitheliomas with inflammation), hair follicles, mesenchymal cells, mammary glands, etc. in susceptible strains; persistent infection in lung, kidney; biological contaminant.
Polyomaviridae, Betapolyomavirus	Mus musculus polyomavirus-2, (MPyV-2, K virus, mouse pneumotropic virus)	Subclinical infections; young immune deficient/ suppressed can have interstitial pneumonia; persistent infections, biological contaminant.
Poxviridae, Orthopoxvirus	Ectromelia virus (mousepox virus)	Unsurprising in wild mice, pet mice; not expected in contemporary research colonies; contaminated biologicals implicated; subclinical to high mortality, necrotic, skin lesions, conjunctivitis; ectromelia (loss of digits, extremities); spleen and liver necrosis; intracytoplasmic inclusions. Nude mice particularly susceptible.
Reoviridae, Orthoreovirus	Reovirus 3	Infant mice from naïve colonies may be susceptible; runting, jaundice, steatorrhea, cytolytic changes in tissues; can be a biological contaminant.
Reoviridae, Rotavirus	Epizootic diarrhea of infant mice virus (EDIM)	Several strains; all ages susceptible to subclinical infection; clinical infection restricted to <2-wk-old pups; runting, steatorrhea, dilated intestines, hydropic degeneration of villus tips, with similar disease course in immune sufficient and immune deficient mice.
Papillomaviridae, Pipapapillomavirus	Mus musculus papillomavirus-1 (MmuPV-1)	Discovered as a spontaneous infection in nude mice; important experimental model system.⁴⁰⁸
Retroviridae		Exogenous retroviruses include MMTV (Bittner agent); MuLV; Moloney and Harvey murine sarcoma viruses; and Friend and Abelson murine leukemia viruses. There are also endogenous (retro-elements) in genome; can cause insertional mutagenesis; influence immunity or oncogenesis.

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Table 7.

Laboratory Mice: Eukaryotes: Fungi, Protists, Metazoan Parasites²⁶^,¹⁴⁶^,³⁹⁹^,⁴⁰¹^,⁴⁴²

Class Agent	Comments
Fungi
Candida spp.	C pintolopesii: yeasts can colonize glandular stomach, without invasion or formation of filaments; C albicans: clinical disease associated with superficial yeasts and pseudohyphae, and invasive hyphae in cornified layers and deeper tissues of squamous mucosae (eg, stomach, vagina, oral cavity) and skin; clinical disease and lesions usually associated with immune dysfunction and dysbiosis.
Encephalitozoon cuniculi	Uncommon, usually subclinical disease and granulomatous inflammation (kidney, brain, liver).
Pneumocystis murina	Host-specific organisms; mice susceptible to typical Pneumocystis pneumonia (PCP)
Trichophyton spp.	Uncommon, subclinical colonization of the skin, rare clinical dermatitis.
Protists
Cryptosporidium muris, C parvum	Unsurprising in wild mice; not expected in contemporary research colonies; subclinical infection of gastric glands (C muris), or distal small intestine (C parvum); developing stages are small intracellular/extracytoplasmic < 6 μm in/on cell surface; small oocysts <8 μm refractile, acid-fast, in feces. Immune deficient mice may have enteritis and hepatobiliary involvement with C parvum⁴⁴³^,⁴⁴⁴
Eimeria spp.	Unsurprising in wild mice; not expected in contemporary research colonies; usually subclinical, or typhlocolitis; intraepithelial developmental stages; oocysts in feces.
Klossiella muris	Unsurprising in wild mice; not expected in contemporary research colonies; subclinical; developmental stages in renal tubules with minimal inflammation; oocysts in urine.
Sarcocystis muris	Unsurprising in wild mice; not expected in contemporary research colonies; subclinical; cysts in skeletal/cardiac muscles; requires cat intermediate host or propagation through cannibalism.
Giardia muris	Unsurprising in wild mice; not expected in contemporary research colonies; usually subclinical; mice are natural host of G muris; binucleate pyriform flagellate (diplomonad) trophozoites adhere to mucosa of duodenal villi; heavy infestations may cause enteritis, ruffled hair coat, distended abdomen; expect immunomodulation.⁴⁴⁵
Spironucleus muris	Unsurprising in wild mice; not expected in contemporary research colonies; usually subclinical; binucleate pyriform flagellate (diplomonad) trophozoites in duodenal crypts; young and immune deficient/suppressed mice may develop clinical disease (diarrhea, enteritis, weight loss, mortality); expect immunomodulation.⁴⁴⁵
Others (eg, Chilomastix spp; Hexamastix spp.; Trichomonas spp. Tritrichomomas muris; Entamoeba muris)	Common, subclinical in cecum and colon of laboratory mice, expect immunomodulation.⁴⁴⁶^,⁴⁴⁷
Nematodes
Aspiculuris tetraptera, Syphacia obvelata	Pinworms. Common, subclinical infection with immunomodulation; heavy burden can cause rectal prolapse, intussusception, fecal impaction, diarrhea; mice are also susceptible to infection by rat pinworm (S muris).
Calodium hepaticus (Capillaria hepatica)	Unsurprising in wild mice; not expected in contemporary research colonies; adult nematodes and capillarid eggs in liver. ⁴⁴⁸
Cestodes
Rodentolepis nana (dwarf tapeworm), R microstoma (bile duct tapeworm), and Hymenolepis diminuta (rat tapeworm)	Unsurprising in wild mice; not expected in contemporary research colonies; usually subclinical, produce adult tapeworms in intestinal/biliary lumen; lesions can include cysticerci in lamina propria; R microstoma adults can reside in pancreatic and bile ducts inciting local inflammation; zoonotic (H diminuta and R nana).
Arthropods
Polyplax serrata, P spinulosa	Pediculosis. Rare in laboratory unless exposure to wild mice; subclinical to pruritus/dermatitis.⁴⁴⁹
Myobia musculi, Radfordia affinis, Myocoptes musculinus	Fur mites. Uncommon; skin lesions often associated with scratching leading to excoriations, ulcerations and secondary bacterial infections; M musculi infestation (most common) associated with significant hypersensitivity reaction.
Demodex musculi	Subclinical infection more frequently detected by PCR; immune deficient/suppressed animals (notably those lacking T or NK cells) are more prone to clinical disease.⁴⁵⁰
Psorergates simplex	Rare in laboratory mice but common in wild rodents; causes follicular comedones (white nodules) on skin.

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Table 2.

Laboratory Mice: Anatomic and Physiologic Features¹⁴⁶^,¹⁶²^,^205–211

System Organ/Tissue	Phenotypes/Conditions; Comments
Alimentary
Teeth	Elodont (continuously erupting) incisors; anelodont molars
Salivary glands	Sexual dimorphism, particularly submandibular gland, larger with more acidophilic ductules in male; variations with androgen influences and pregnancy.²¹²
Stomach	Forestomach with stratified squamous epithelium.
Intestine	Paneth cells prominent in small intestine. Intestinal mast cells, globule leukocytes.²¹³
Liver	Variable lobation among strains.²⁰⁵^,²¹⁴
	Hepatocyte size variability (anisocytosis), bi- or multinucleation (polykarya /polyploidy) can be prominent, increases with age.²¹⁵
	Extramedullary hematopoiesis common.²¹⁴
Cardiovascular	²¹⁶
Endocrine
Adrenal	Zona reticularis inconspicuous in laboratory mice vs wild mice. Sexual dimorphism: X zone undergoes vacuolar degeneration in females. Subcapsular cell hyperplasia, more common in females than in males in some strains and stocks (eg, CD-1).
Pancreas	Different density and distribution of islets across the organ and between conspecifics. Larger islets in obese animals and in some diabetic models.
Hematolymphoid	^217–219 ^, ²²⁰
	Extramedullary hematopoiesis is expected in spleen and common in liver. Hematopoiesis in bone marrow occurs throughout life.²²¹
	Mast cells common in many tissues.²¹³^,²²²^,²²³
	MHC haplotype diversity among strains.⁴³
Blood, hemogram	Hematocrit typically ranges from 35% to 52%. Low numbers of nucleated red blood cells (<5%) in health. Lymphocytes are 70% to 80% of white blood cells in immune sufficient strains.^224–226
Lymph nodes	²¹⁷ ^, ^227–229
Spleen	Intra-histiocytic hemosiderin tends to increase with age. Melanin in pigmented strains.²¹⁷^,²³⁰^,²³¹
Thymus	Involutes with age but frequently persists beyond 1 y.
Tonsils	Absent
Integument
Haired skin	Melanin (when present) limited to hairshafts/follicles.²³² Location of follicular bulb/dermal papilla varies with stage of hair growth.²³³
Sebaceous glands	Zymbal's and preputial/clitoral glands
Lacrimal glands	Exorbital (extraorbital) and infraorbital. Exorbital gland can have striking karyomegaly, anisocytosis, and pseudoinclusions.
Harderian glands	Retroorbital
Mammary glands	Alveolar components form only during pregnancy/lactation, and regress afterwards. [vs humans, in which puberty marks a full anatomic development of lobular units that persist throughout life; prominent fibrous stroma in human breasts vs scant in mice mammary tissue].
Musculoskeletal	²³⁴ ^, ²³⁵
Bone	No Haversian system. Epiphyseal closure occurs late.
	Bone density and quality influenced by strain/substrain. C3H/HeJ and C57BL/6J mice have the highest and the lowest bone density, respectively. A/J bone is relatively brittle; B6 substrain differences in bone density.^236–238
Nervous	¹⁷⁶ ^, ^239–245
Brain	Lissencephalic. Strain and sex variations in brain/ventricle size,¹⁷⁶^,²⁴⁶^,²⁴⁷ and corpus callosum and cerebellum morphology.
Respiratory	¹⁴⁰ ^, ²⁴⁸ ^, ²⁴⁹
Nose/head	Obligate nose breather. Prominent vomeronasal organs with incisive fissures (nasopalatine ducts) connecting oral and nasal cavities (not cleft palate).
Lungs	1 left + 4 right lobes. Intrapulmonary airways are bronchioles and not bronchi (lack cartilage and submucosal glands). Cardiac (striated) muscle in the tunica media of pulmonary veins.
Urogenital	²⁵⁰
	Unipapillate kidneys. Parietal Bowman’s epithelium may be sexually dimorphic (more cuboidal in males). Urethral meatus opens outside of vagina.
	Bicornuate uterus. Cyclic changes to vaginal mucosa.²⁵¹
Miscellaneous
Pineal gland	Comparatively small in laboratory mice.
Adipose, brown	Interscapular, adjacent large vessels and near/within some viscera; admixed with white adipose tissue within the inguinal fat pads.²⁵²
Adipose, white	Primarily in the subcutis and fat pads. Trans differentiation between different fat types can occur.²⁵³
Retroorbital sinus	Vascular sinus in mice used for injections or blood collection.²⁵⁴

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Table 3.

Laboratory Mice: Non-Infectious Non-Neoplastic Conditions²⁶^,¹⁴⁶^,¹⁶²^,¹⁷⁸^,^205–208^,^255–258

System Organ/Tissue	Conditions; Comments
Multisystemic	Amyloidosis: extracellular accumulation of misfolded, non-degradable fibrillary material causing compression and loss of function of the affected tissue.¹⁴⁴^,^259–262
	Amyloidosis, reactive from serum amyloid A (SAA) protein: secondary to chronic immune stimulation; deposition in intestine, liver, spleen, lung, kidney.^263–268
	Amyloidosis, senile from apolipoprotein A-II (AAPOAII): Lung, ileum, heart are predilection sites. Variation in Apoa2 alleles: A/J, SJL/J, and SAMP are highly susceptible (Apoa2^c); B6 less susceptible (Apoa2^a); C3H and BALB/c (Apoa2^b) resistant.^269–276
	Mineralization of soft tissue (A/, BALB/c, C3H/, DBA/, KK/).^277–281
Alimentary	²⁸²
Teeth ²³⁴	Incisor dysplasia. Often incidental and bilateral in older mice; consider previous damage to odontoblasts and ameloblasts; well differentiated denticles or disorganized tooth structures; may enlarge to interfere with eating.¹⁸⁰^,²⁸³^,²⁸⁴
	Incisor fragility. Consider irradiation or toxic damage to odontoblasts and ameloblasts.^285–287
	Incisor malocclusion and overgrowth. Elodont incisors grow continually; abnormal wear leads to malocclusion and overgrowth; mandibular incisors typically extend in front of the maxillary incisors that curve back and up toward the maxilla; clinically presents as weight loss; genetic factors, physical trauma, damage to odontoblasts and ameloblasts, soft diet may contribute.²⁸³^,²⁸⁸
	Periodontal disease. Soft tissue inflammation with foreign material (food or hairs) in gingival pocket, usually involving molars; can progress to bone remodeling (and loss) and hypercementosis. Long term use of acidified water implicated.¹⁴⁴^,²⁸⁹
Stomach	Gastric ulcers (non-glandular and/or glandular) due to stress.
	Hyalinosis. Ym1 (Chitinase-like protein 3) crystals in glandular epithelial cells.²⁹⁰
Intestine	Ileus. Impaired motility (atony) and dilation of intestines. Associated with lactation and certain drugs (chloral hydrate, tribromoethanol).²⁹¹^,²⁹²
	Megacecum. Germfree mice or treated with antibiotics.²⁹³
	Abnormal development of gut-associated lymphoid tissue (GALT), eg, in immune deficient and germ-free mice.²⁹⁴
Liver	²¹⁴
	Foci of hepatocellular alteration; often induced (drugs/interventions); metabolically (enzymatically) and histologically/tinctorially distinct with a presumed pre-neoplastic significance; no correlate in human pathology. ²⁹⁵
	Portosystemic (portocaval) vascular shunts reported in B6 and 129 mice.¹⁷⁴^,²⁹⁶
	Angiectasis (peliosis hepatis, telangiectasia). Single or multiple foci of distended sinusoids; distinguish from hemangiosarcoma.
Gallbladder	Mucosal hyperplasia; hyalinosis (YM1 crystals) in epithelium; older mice.²¹⁴
Pancreas, exocrine	Zymogen depletion: reduced zymogen granules with reduced acinar size; expected with inanition of any cause.
	Acinar atrophy: reduced size and number associated with age, inflammation or experimental conditions; frequent infiltration or replacement by adipose tissue.
Cardiovascular	²⁹⁷
	Myocardial lesions (degeneration, necrosis, inflammation, or fibrosis) are usually modest in even in older mice.²⁹⁸ Cardiac calcinosis or mineralization, and/or fibrosis expected in BALB/c, C3H, DBA, KK, A, C57BL/10.²⁷⁸^,²⁹⁹^,³⁰⁰
	Atrial or auricular thrombi (usualy left), reported most frequently in Swiss or BALB/c.²⁷⁸^,³⁰¹^,³⁰²
	Myxomatous degeneration of cardiac valves (endocardiosis).³⁰³
	Polyarteritis. Inflammatory and necrotizing lesions in small to medium systemic arteries in multiple tissues, particularly musculoskeletal and visceral; spares lungs. Expected in some ‘autoimmune’ models such as Murphy Roths Large (MRL); ³⁰⁴^,³⁰⁵ association with hypertension.³⁰⁴
Endocrine	³⁰⁶
Adrenal	Accessory adrenal cortical nodules: may be more common females than in males; differentiate from neoplasia. Ceroid laden macrophages may accumulate in cortex with age.¹⁹⁵
Pituitary	Cystic remnants of Rathke’s pouch.
Thyroid	Ectopic follicles can be found in neck, mediastinum, thymus.
	Hyperplasia and hypothyroidism can be induced by irradiation and toxic damage, including trimethoprim-sulfamethoxazole.³⁰⁷^,³⁰⁸
Parathyroid	Ectopic tissue can be found in neck, mediastinum, thymus.
Hematolymphoid	¹⁹² ^, ²¹⁸ ^, ^309–312
C5 deficiency	Abnormal complement function (Hc⁰ nonsense mutation) in A/HeJ, AKR/J, DBA/2J, FVB/N, NZB/B1NJ, SWR/J
Bone marrow	Endosteal bone proliferation with replacement/loss of hematopoietic marrow induced by exogenous estrogens.¹⁹⁴^,³¹³^,³¹⁴ Fibro-osseous change (fibro-osseous lesion). More likely in aging females of certain strains (B6C3F1, 129, KK), influenced by exogenous estrogens.¹⁹⁴^,³¹³^,³¹⁴
Lymph node	²¹⁷
Spleen	Osseous metaplasia, incidental.³¹²
Thymus	Lymphocyte apoptosis common in stressed animals.
	Cysts (ultimobranchial remnants) are common. Ectopic thymus anywhere on neck is not unusual. Ectopic thyroid or parathyroid in the thymus is not unusual.²¹⁷^,³¹⁵^,³¹⁶
Integument	¹⁴¹ ^, ³¹⁷ ^, ³¹⁸
Skin	Alopecia. Striking hair loss patterns with conspecific grooming (barbering). Several strains have alopecia related to follicular dysplasia eg, nude (Foxn1^nu/nu) or hairless (Hr^hr ).^319–322
	Alopecia areata. Polygenic immune-mediated disease in C3H/HeJ, A/J, SJL/J.³²³^,³²⁴
	Mineralization ectopic; vibrissae, muzzle 129S1, C3H/HeJ, DBA/2J, KK/1J²⁹⁹
	Graying of hairs from aging, irradiation.^325–327
	Ringtail. Annular constrictions on tail with possible distal necrosis/dry gangrene/amputation. Extremities (digits) may also be affected. Low humidity, cotton string from nesting material, or hypothermia (eg, cage flooding).³²⁸
	Bite wounds. Conspecific aggression (usually males, especially SJL/J and BALB/c). Crescentic skin lacerations, particularly around perineum/tail.³²⁹
	Ulcerative dermatitis is particularly common in B6 and Swiss backgrounds.³³⁰^,³³¹
Musculoskeletal	²³⁴ ^, ²³⁵ ^, ³³²
	Osteoporosis, aging.²³⁵^,³³³
Joints	Degenerative joint disease, aka osteoarthritis. Onset and incidence influenced by genetic background and immune mediated mechanisms. May involve temporomandibular joints¹⁸⁰^,³¹³^,^333–337
Nervous	¹⁷⁶ ^, ^239–244 ^, ³³⁸
Brain	Hydrocephalus. Congenital; frequent in C57BL strains; domed head and variable failure to thrive before weaning; later onset in MRL/MpJ not associated with domed head.³³⁹^,³⁴⁰
	Seizures. FVB/N; audiogenic in DBA/2; may be associated with neuronal necrosis, especially in hippocampus.³⁴¹
	Vacuolation is a common artifact of histologic processing, especially in white matter. Dark neuron artifact with handling of unfixed brains.³⁴²
	PAS+ granular inclusions, particularly in hippocampus and cerebellum in older mice, identified as ‘degenerative structures’ (has been reported as amyloid and tau like);³⁴³ Lipofuscin/ceroid in neurons in older animals also is PAS positive.
Respiratory	¹⁴⁰ ^, ²⁴⁸ ^, ³⁴⁴
Nasal cavity	Nasal septum submucosal eosinophilic substance; accumulates with age; not amyloid.³⁴⁵
Lungs	Acidophilic macrophage pneumonia (eosinophilic crystalline pneumonia); accumulation of YM1 crystals in macrophages, free in airspaces, particularly B6, 129, Swiss strains particularly; frequent giant cells; Hyalinosis refers to hyaline eosinophilic accumulations of these proteins in airway epithelial cytoplasm; upregulation of these proteins, associated with immune stimulation (allergen, infection, etc).³⁴⁶^,³⁴⁷
	Aspiration pneumonia. Anesthesia or gavage accidents. Typical findings include skin squames, bedding, or food material (eg, birefringent plant matter) in airways.
Special senses	¹⁹³ ^, ³⁴⁸
Eye	Cataracts (lens opacities): genetic (eg, Bfsp2^Dundee); light-induced; can be associated with cold, anesthesia, or other chemicals (MNU/ENU); can resemble corneal opacities.^349–354
	Microphthalmia, congenital; common in some C57BL; particularly in female, right eye.³⁵⁵^,³⁵⁶
	Blindness due to retinal degeneration. Genetic in strains homozygous for Pde6b^rd1 allele (eg, CBA/J, FVB/N, C3H/) resulting in blindness at weaning. Husbandry-related phototoxicity in albino strains.^357–359
Ear	Progressive deafness due to degeneration of the organ of Corti (Cdh23^ahl). Common in many strains including B6, 129, FVB/N.³⁶⁰
Urogenital	Female³⁶¹; Male³⁶²; and Urinary³⁶³
Kidney	Renal amyloidosis. Deposition of amorphous congophilic material in glomeruli and interstitium; in A/J may present as deposition in and necrosis of papilla, with cortex atrophy, loss. Periodic acid-Schiff (PAS) negative. ²⁶³
	Glomerulonephritis. Immune mediated in susceptible strains and in models of autoimmune diseases.
	Chronic progressive nephropathy. Less common than in rats.
	Hyaline glomerulopathy. Abundant PAS+ material in glomeruli; Congo red negative.²⁶³
	Hydronephrosis. Distention of the pelvis; progresses to cortical atrophy; possible outflow obstruction; unilateral or bilateral; differentiate from polycystic kidneys.³⁶⁴^,³⁶⁵
	Urolithiasis. Struvite urolithiasis with urinary tract obstruction or infection in estrogenized mice. Cystine urolithiasis in 129S2/SvPasCrl due to Slc3a1 mutation. Also diet or xenobiotics.³⁶⁶^,³⁶⁷
	Mineralization. Usually in medullary tubules, collecting ducts; 129S1, C3H/HeJ, DBA/2J, KK/1J carry an Abcc6 mutation associated with ectopic mineralization and renal tubule mineralization that can be severe.²⁹⁹
	Obstructive uropathy (mouse urologic syndrome); may lead to hydronephrosis; can be a common cause of mortality among co-housed males; associated with estrogen implants (estrogenized females).³⁶⁸
Female reproductive	Ovaries: atrophy, cysts, ceroid lipofuscin increase with age. Uterus: endometrial atrophy, increases with age; myometrial hemosiderin and mineralization (embryo implantation sites); enlarged uterus with endometrial hyperplasia, cystic – consider estrogenic compounds in diet or environment; Mucometra/hydrometra due to ‘imperforate vagina’ (including Lhfp12^vgim mutants), vaginal septa.³⁶⁹^,³⁷⁰
Male reproductive³⁷¹	Testis: degenerative changes and multinucleate giant cells increase with age; seminal vesicles can become large or discolored in older mice; cystic bulbourethral glands can present as bilateral perineal masses;³⁷² scrotal hernias can present as perianal masses and include seminal vesicle, cecum or other tissues;³⁷³ lateral femoral hernias present as flank masses.³⁷⁴
Intersex, hermaphrodite	Ovotestes and ambiguous genitalia in B6,129 embryonic stem cell chimeras ³⁷⁵
Gestation etc	18.5–21d; Litter size 2–12+ pups; weaning age 16–28 d; sexual maturity 5–8 wk. Strain variations.³⁷⁶
Pup features	Milk in stomach ‘milk spot’ should be evident by approximately 6 h; hair begins to appear at 2–4 d, ears open at 3–5 d, eyes open at about 14 d; vagina opens at 24–28 d of age.³⁷⁶

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Table 6.

Laboratory Mice: Bacteria²⁶^,¹⁴⁶^,³⁹⁹^,⁴⁰¹^,⁴⁰⁹^,⁴¹⁰

Genus and Species	Comments
Bordetella bronchiseptica	Respiratory tract; subclinical colonization; clinical infection rare.⁴¹¹
Bordetella hinzii	Subclinical to mild rhinitis/bronchiolitis.⁴¹²
Bordetella pseudohinzii	Subclinical infection; impairs cilia and increases inflammation in respiratory tract.⁴¹³^,⁴¹⁴
Citrobacter rodentium	Transmissible colonic hyperplasia, attaching and effacing lesions. More severe in Swiss, AKR, FVB/N, and C3H.⁴¹⁵
Clostridium piliforme	Tyzzer’s disease. Often subclinical; immune deficient etc. susceptible mice have intracellular bacilli and necrosis in liver, cecum, and heart.⁴⁰⁹^,⁴¹⁶
Corynebacterium bovis	Gross hyperkeratosis in nude mice and some skin mutants (eg, SKH1-Hr^hr, Zdhhc21^dep); poor breeding survival and less obvious skin changes in haired immune deficient (scid, NSG etc): hyperkeratosis, acanthosis, intracorneal Gram-positive bacteria.⁴¹⁴^,⁴¹⁷
Corynebacterium kutscheri	Subclinical infection common; abscesses “pseudotuberculosis” in immune deficient.⁴¹⁸
Filobacterium rodentium (formerly cilia associated respiratory bacillus (CARbacillus))	Subclinical infection; historic co-infection with M pulmonis; clinical disease can include chronic bronchioltis/bronchopneumonia, lymphocyte proliferation.⁴¹⁹
Helicobacter spp.	Subclinical infection; H bilis and H hepaticus are often associated with clinical disease in immune sufficient (incl. A and C3H); chronic inflammation and neoplasia in colon and liver; immune deficient mice are susceptible to broader range of species; H bilis and H pullorum (among others) are zoonotic; H muridarum associated with enteritis in SCID mice. Immune recomposition can lead to severe disease^420–424
Klebsiella spp.	Opportunist; may be part of murine flora, possibly from humans; can cause urinary tract infection, otitis, pneumonia, etc.^425–427
Mycoplasma pulmonis	Murine respiratory mycoplasmosis; clinical disease can include otitis, rhinitis, bronchiolitis, arthritis, metritis, etc.; suppurative inflammation in earlier disease, bronchiolectasis and peribronchiolar and perivascular lymphocytic cuffing.
Pseudomonas aeruginosa	Opportunist in mice with dysfunctional neutrophils (eg, Myd88^tm1.1Defr) or neutropenia (irradiation); conjunctivitis/otitis to bacteremia /sepsis/death; forms biofilms in watering systems, chlorhexidine solutions. Other saprophytes (Stenotrophomonas maltophilia, Burkholderia cepacia complex) may cause similar disease.^428–430
Rodentibacter pneumotropicus, R heylii (formerly Pasteurella pneumotropica)	Common; opportunist; subclinical, or periorbital abscesses, bronchopneumonia, conjunctivitis, rhinitis, lymphadenitis, reproductive tract infections.^431–433^,⁴³⁴
Salmonella enterica (formerly S typhimurium)	Subclinical; clinical disease with inflammation/necrosis in liver, cecum, spleen, and lymphoid tissues; zoonotic.⁴³⁵
Segmented filamentous bacteria (SFB, genus candidatus Savagella, or Arthromitus)	Common; commensal/symbiont gram positive filamentous spore forming bacteria adhered to villi of distal small intestine; important in development of Th17 responses; usually inconspicuous in immune sufficient adults producing IgA.²²^,⁴³⁶
Staphylococcus aureus	Commensal/opportunist organism, often not a detriment to research, but clinical diseases (abscesses, botryomycosis, dermatitis) can exclude animals from studies.⁴³⁷^,⁴³⁸
Staphylococcus xylosus	Coagulase negative Staphylococcus, commensal organism that can cause disease (clinical spectrum similar to S aureus) in immune deficient mice, especially those with defective NADPH oxidase (eg, Cybb^tm1Din).^439–441
Streptobacillus moniliformis	Infected mice often have clinical disease with systemic symptoms (septicemia, polyarthritis, lymphadenitis, wasting, etc.); acquired from carrier rats; zoonotic.
Streptococcus pneumoniae	Mice can be carriers without significant impacts to research, in young or immune deficient/suppressed animals can be a secondary pathogen; zoonotic.⁴²⁶
Streptococcus spp. – β-hemolytic, Group B	Human carriers; occasional isolates from abscesses.
Streptococcus spp. – β-hemolytic, Group G	Pathogenic Enterococci – rare disease in neonate.

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RATS

Laboratory Rats: Order Rodentia, Suborder Myomorpha; Rattus norvegicus

Rats have been part of the historical record for centuries, and have been at times associated with human disease.⁵⁷ The emergence of rats as research subjects began in the 19th century.⁵⁸^,⁵⁹ Brown (Norway) rats (Rattus norvegicus [Berkenhout, 1769]) were among the first animals to be raised primarily for research.⁶⁰ Most contemporary research strains and stocks originate from the Wistar Institute, Philadelphia, PA, and Henry Herbert Donaldson’s efforts to standardize albino rats and husbandry conditions for research, beginning around 1906. These Wistar rats were “random bred” and widely distributed, with various crosses resulting in most of the contemporary strains and stocks. The Brown Norway strain also originated at Wistar but from local wild rats inbred by Helen King, and these do not cluster genetically with most strains. Long and Evans’ (Long Evans) hooded rats are reported to derive from Wistar white rat crossed with a wild gray rat on the University of California, Berkeley campus circa 1915. Scientific investigations into behavior, nutrition, endocrinology, physiology, and cancer research increasingly embraced the rat model. From these early studies, scientists identified differences in longevity and susceptibility to cancer between stocks or strains of rats, fueling interests into the influence of genetics. Gene editing in rats is increasingly accessible.^61–63 Research-relevant features and non-infectious conditions of laboratory rats are summarized in Tables 8–10. Infectious agents that may be identified or may cause disease in rats are summarized in Tables 11–14. Again, although many of the agents are not expected in contemporary research colonies, they remain relevant given the risks posed by biological contaminants and feral or pet rodents.

Table 8.

Laboratory Rats: Taxonomy, Genetics, Nomenclature, and Common Strains/Stocks^451–455.

Strain or Stock	Comments = Inbred
ACI/ ^a	Frequent tumors; congenital genitourinary anomalies, prostate tumors.⁴⁵⁶^,⁴⁵⁷
BB/	T1DM in outbred Wistars at Biobreeding Labs; lymphocytic insulitis and thyroiditis. Lymphopenia and NK cell deficiency.⁴⁵⁸
Belgrade (BG/)	Slc11a2^mk missense mutant with iron deficiency anemia.⁴⁵⁹
Brown-Norway (BN/)	“Allergy” phenotype with polarized T_H2 responses; eosinophilic granulomatous pneumonia; myeloid leukemia; autosomal polygenic hydronephrosis; arterial elastic lamina fragility.^460–462
Buffalo (BUF/)	Endocrine tumors: pituitary, adrenal cortex, thyroid (medullary); thymoma; autoimmune thyroiditis.
Brattleboro	Autosomal recessive (Avp-/-) diabetes insipidus⁴⁶³
Copenhagen (COP/)	Brown hood; resist induced mammary tumors; source of Dunning R3327 rat prostate tumor cell lines (G, AT-1, AT-2, AT-3, MAT-LyLu, MAT-Lu)⁴⁶⁴
Dahl Salt sensitive	3 strains (DSS/1-3); Hypertension, “cardiomyopathy” on high-salt diet; also obese, hyperlipidemic, hyperinsulinemic DSS/N-cp.
Eker	Tsc2^Eker (retrotransposon insertion) mutation arising in LE. Homozygous lethal; dominantly inherited renal carcinoma and uterine leiomyoma; splenic hemangiomas.⁴⁶⁵^,⁴⁶⁶
Fischer 344 (F344/)	Formerly most common in toxicology and cancer studies; fairly small size; high incidence of testicular interstitial cell tumors and mononuclear cell (LGL) leukemia, mesothelioma.¹⁶⁰^,¹⁶⁶^,^467–471
Gunn	Icterus, hyperbilirubinemic model of Ugt1a1^j mutation; (dominant mutation for hydronephrosis in some stocks).
Hairless	Prss8^hr from a Crl:CD(SD) in 1980s (Crl:CD-Prss8^hr ).
Lewis (LEW/)	Developed by Lewis from Wistar stock, used for immunology. Frequent neoplasia including hematopoietic, endocrine, mammary, and endometrial carcinoma.⁴⁷²
Long-Evans (:LE)^b	Black hooded; known for resistance to infectious disease with fewer mammary tumors.
Long-Evans cinnamon (LEC/)	Icteric hyperbilirubinemic model of Wilson’s disease with mutation in Atb7b^hts, mortality due to hepatitis at about 4 mo or later; hepatic cancer; cinnamon-like coat color.⁴⁷³
Osborne-Mendel (OM/)	Model of diet-induced obesity (DIO). Endocrine neoplasia; age-related retinal degeneration.⁴⁷⁴
PCK/	Pkhd1^pck polycystic kidney disease, identified in CD colony, inbred model of ARPKD
RNU	Foxn1^rnu “athymic” nude, T deficient. Identified in 8-way cross at National Institutes of Health: Crl:NIH-Foxn1^rnu , Tac:NIH-Whn. Also from Rowett Institute (Rh) Scotland: HSD:RH- Foxn1^rnu
SHHF/	Spontaneously hypertensive heart failure rat: SHROB backcrossed to SHR/N developed heart failure (McCune) + hypertension, nephropathy, insulin resistance – carries Lepr^cp
SHR/	Spontaneous hypertensive rat - derived from WKY – several related strains.⁴⁷⁵
SHROB/	SHR Obese: Lepr^cp corpulent mutation identified in SHR female x SD male (Koletsky @ CWRU); hypertension, hyperlipidemia, hyperinsulinemia, and nephropathy.
SHRSP/	SHR stroke-prone: cerebral hemorrhage
Sprague Dawley	Most common in literature and in toxicology and carcinogenicity studies. Origin c1925 Dawley bred Wistar female x hooded male. SD = Envigo (Harlan); CD = Charles River Laboratories. Polyarteritis, chronic progressive nephropathy, myocardial degeneration, mammary fibroadenoma. ¹⁶⁶^,⁴⁷⁰^,^476–483
Wistar (:WI)	First lab rat, circa 1906 @ Wistar Institute. Thymomas.^483–485
Wistar-Furth (WF/)	Furth c1945 developed high leukemia strain from Wistar stock – poor survival
Wistar-Kyoto (WKY/)	“Control” strain for SHR but different haplotype – inbred from Wistar stock @ Kyoto to NIH 1971. Resistant to induced mammary tumors.⁴⁸⁶
Zucker Fatty (ZUC)	Lepr^fa fatty allele in Lepr; Inbred or outbred, DIO. Also T2DM (ZDF)

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^a‘/’ After strain/root abbreviation indicates inbred and is followed by the source laboratory code.

^b‘:’ Before stock abbreviation indicates outbred and is preceded by the source laboratory code.

Table 10.

Laboratory Rats: Non-infectious Non-neoplastic Conditions²⁶^,²⁰⁵^,⁴⁵⁴^,⁴⁸⁷^,⁵⁰³^,⁵⁰⁴

System Organ/Tissue	Condition; Comments
Multisystem	Mineralization of soft tissue; in arteries, lungs, kidney, heart, gastric mucosa; usually renal secondary hyperparathyroidism.
Alimentary	²⁸² ^, ⁵⁰⁵
Teeth	Incisor (dental) dysplasia; as in mice, associated with damage, soft or powdered diet.²⁸³^,^285–287^,⁵⁰⁶^,²⁸²^,^284–286^,⁵⁰⁵
	Incisor fragility; as in mice, consider irradiation or toxic damage to odontoblasts and ameloblasts.⁵⁰⁶^,⁵⁰⁷
	Incisor malocclusion and overgrowth. As in mice, elodont incisors grow continually; abnormal wear leads to malocclusion and overgrowth; can interfere with eating; genetic factors, physical trauma, damage to odontoblasts and ameloblasts, soft diet may contribute.⁵⁰⁸
Intestine	Ileus. Chloral hydrate (intraperitoneal).⁵⁰⁹ Indomethacin produces mesenteric infarcts in the intestine that may cause ileus.⁵¹⁰
Liver	²¹⁴ ^, ²⁹⁵
	Peliosis hepatis (telangiectasia), aging rats.
	Hemochromatosis in Hsd:HHCL (Wistar) rats with Tfr2 mutation.⁵¹¹
	Hepatodiaphragmatic nodules (small diaphragmatic hernias), F344 > SD.
	Foci of hepatocellular alteration.⁵¹²
Pancreas, exocrine	⁵¹³
	Drug metabolizing enzyme induction.⁵¹⁴
Cardiovascular	²⁹⁷
Heart	Cardiomyopathy. Common, esp. in male SD >1 y old; myocardial degeneration, inflammation, and fibrosis.⁴⁸¹
	Valvular endocardiosis.³⁰³
	Congenital defects. Ventricular septal defect most common.⁵¹⁵ Patent ductus arteriosus in BN.
Vasculature	Polyarteritis (polyarteritis nodosa PAN). Arterial tortuosity, aneurysm, inflammation and fibrinoid change; mesenteric, pancreatic and testicular arteries; arterial rupture associated with hemoabdomen; aged SD rats; hypertensive rats SHR, etc strains; histologic similarities to hypertensive lesions.^516–518
	Internal elastic lamina (IEL) rupture. Fragmentation of IEL, medial lamina, occasionally progressing to aneurysm/dissection. Polygenic elastin deficiency in BN.
Endocrine	³⁰⁶ ^, ^519–521
	Lymphocytic thyroiditis. BUF and BB/W.
	Larger pancreatic islets not surprising in obese or diabetic models
Integument	³¹⁷
Skin	Ringtail. Similar to mice.
	Pododermatitis. Ulcerative skin lesions over the plantar metacarpals and metatarsals. Obese rats on wire bottom cages are prone.⁵²²
Musculoskeletal	²³⁴ ^, ³³²
Joints	Degenerative osteoarthritis.⁵²³
Nervous	²⁴⁴ ^, ³³⁸
	Hydrocephalus. Sporadic; genetic and acquired causes; often due to obstruction of aqueduct.
	Radiculoneuropathy. Posterior paresis and demyelination of cauda equina of aging rats (SD >2 y).
	Spongiform change. Vacuoles in neurons of aging rats; rule out processing artifact (white matter vacuolation).
	Bilateral symmetrical idiopathic necrotizing encephalopathy; necrosis, loss of neuropil; aging SD.⁵²⁴
Respiratory	³⁸ ^, ²⁴⁸ ^, ³⁴⁴ ^, ⁵²⁵
Lung	Alveolar histiocytosis. Aggregates of foamy macrophages in alveoli and terminal airways.
	Eosinophilic granulomatous pneumonia. Eosinophils, macrophages and multinucleate giant cells. ‘Allergic’ phenotype in young (3–4 mo). BN have airway hyperresponsiveness, polarized T_H2 responses, and increased IgE production.
	Inhalation pneumonia. Gavage accidents, micro-aspiration.
Special senses	³⁴⁸ ^, ⁴⁷⁹
Eye	Retinal degeneration. Light-induced (phototoxicity) in albinos; genetic (RCS and Campbell). Toxic (ENU/MNU, also cataracts).⁵²⁶
Urogenital	Female,³⁶¹ male,³⁶²^,⁵²⁷ and urinary³⁶³^,⁵²⁸
Kidney	Chronic progressive nephropathy (CPN). Glomerulosclerosis, tubule degeneration/regeneration, interstitial fibrosis +/− inflammation, +/− arteriolosclerosis, +/− nephrocalcinosis, +/− hyaline droplet change. Major life-limiting disease, especially SD and males. Can progress to hyperparathyroidism with soft tissue mineralization. Increased/accelerated by ad libitum feeding in chronic studies.⁵²⁹^,⁵³⁰
	α_2u-globulin nephropathy. Male rats.⁵³¹
	Nephrocalcinosis. May be “crunchy” with macroscopic mineral at corticomedullary junction, and soft tissue mineralization at other sites. Consider chronic renal disease and secondary hyperparathyroidism; possibly dietary Ca:P imbalance.
	Hydronephrosis. More common in right kidney, rule out obstruction. High estrogen may accelerate (esp. in Gunn and BN).⁵³²
	Tubule mineralization. Mineralization in tubules and collecting ducts, more common in females.
Kidney, lower urinary tract	Urolithiasis. Mixed mineral calculi often in urinary bladder; associations with cystitis or Trichosomoides crassicauda.
Ovaries/uterus	Cysts, ovarian, parovarian, ‘polycystic ovary syndrome’ Cystic ovaries, cystic endometrial hyperplasia, uterine hypertrophy; associated with estrogenic influences or prolonged photoperiod.⁵³³^,⁵³⁴
Vagina	Transverse vaginal septum. Congenital/developmental in WI and SD.⁵³⁵
Male repro	Testicular and seminal vesicle atrophy; associated with aging, estrogens.
Miscellaneous	Auricular chondritis. Bilateral nodular inflammatory/proliferative lesions of cartilage in ear pinnae. Especially in SD, WI, and Fawn Hooded.⁵³⁶^,⁵³⁷
	Chromodacryorrhea. Autofluorescent porphyrin from Harderian glands around eyes and on face/paws. Dehydration and stress may predispose.
	Hyperthermia. May see ptyalism, dehydration, or chromodacryorrhea.

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Table 11.

Laboratory Rats: Neoplastic Conditions⁴⁵⁴^,⁴⁷⁰^,⁴⁸⁷

System Organ/Tissue	Condition; Comments
Alimentary	²⁸²
Liver	Adenoma, carcinoma, hepatoblastoma; unusual unless induced.²¹⁴
Cardiovascular	²⁹⁷ ^, ⁵³⁸
	Hemangiosarcoma, sporadic.
	Endocardial schwannoma, sporadic.⁵³⁹
Endocrine	³⁰⁶ ^, ⁵²¹
Pituitary	Pars distalis adenoma most common; prolactin is a common secretory product, and associated with galactorrhea; SD, WI, etc.³⁸³^,⁴⁸²^,⁵⁴⁰
Adrenal gland	Pheochromocytoma. F344 and M520.⁵⁴¹
Thyroid	Thyroid medullary (C cell) tumors. Aging studies (SD, BUF).³⁸⁴
Hematolymphoid	³¹²
	Mononuclear cell leukemia, aka large granular lymphocyte (LGL) leukemia; splenomegaly and leukocytosis. Azurophilic granules demonstrated by Wright-Giemsa stains. Common in F344.⁵⁴²
	Lymphoid or myeloid leukemia. Can present as paraplegia/ paraparesis due to extradural compression from bone marrow expansion.
	Lymphoma.
	Histiocytic sarcoma; anywhere, particularly skin (WI and SD), subcutis, peritoneum, common lung metastases.
	Thymoma.⁵⁴²
Integument	³¹⁷ ^, ³¹⁸
Mammary	Fibroadenoma most common spontaneous mammary tumor; benign, abundant collagen with sparse ducts/lobules; locally invasive and difficult to fully resect.⁴⁸² Adenomas/adenocarcinomas uncommon, can be induced with MNU/ENU/DMBA⁵⁴³
Skin	Fibroma; benign tumor with abundant collagen; common in rats; malignant fibrosarcoma is less common.
	Spindle cell sarcomas, peripheral nerve sheath tumors reported.⁵⁴⁴
	Keratoacanthoma, crateriform nodule with central keratin core.⁵⁴⁵
	Amelanotic melanoma; often on pinna or eyelid, seen more in F344.⁵⁴⁶
	Zymbal’s gland tumors; neck/ear base mass with adenosebaceous squamous differentiation; may progress to squamous cell carcinoma.
	Preputial/clitoral gland tumors; ventral inguinal mass with adenosebaceous differentiation.⁵⁴⁷
Musculoskeletal	²³⁴ ^, ³³²
	Rhabdomyosarcoma⁵⁴⁸
	Chordoma; paravertebral (often tail), vacuolated physaliferous cells, notochord derived.⁵⁴⁹
	Chondrosarcoma, rare.⁵⁵⁰
	Osteosarcoma, rare.
Nervous	²⁴⁴ ^, ³³⁸ ^, ⁵⁵¹ ^, ⁵⁵²
Brain	Glioma, glioblastoma, astrocytoma, oligodendroglioma; glioblastoma multiforme can cross midline⁵⁵³
Meninges	Meningioma or granular cell tumor; discrete circumscribed tumor in cortex/meninges; usually benign; Granular cell tumors contain PAS positive granules (lysosomes)
Respiratory	³⁴⁴
	Primary lung tumors uncommon, rule out metastases.
Urogenital	Female,³⁶¹^,⁵⁴⁰ male,³⁶² urinary³⁶³
Testes	Leydig (interstitial) cell tumors; usually benign; most male F344 > 1 y of age.
Prostate	Adenocarcinoma; aged Lobund-Wistar⁵⁵⁴
Ovary	Sporadic.⁵⁵⁵^,⁵⁵⁶
Uterus	Endometrial carcinoma; LEW.⁴⁷²
	Uterine stromal tumors; sporadic, polypoid mass of stroma and capillaries with invasion.
	Leiomyoma; Eker rats.⁵⁵⁷
	Deciduoma; virgin females.
Uterine cervix	Granular cell tumors; eosinophilic cytoplasmic granules (PAS positive)⁵⁵⁸
Kidney	Amphophilic-vacuolar renal tubular adenoma/carcinoma. Spontaneous in young female SD.⁵⁵⁹
	Nephroblastoma; sporadic, developmental/early onset, but not usually evident until adult,⁵⁶⁰ considered malignant⁵⁶¹
	Renal mesenchymal tumor (RMT); primitive mesenchyme with entrapped tubules (non-blastemal), frequent invasion of pelvis, differentiate from nephroblastoma.⁵⁶¹
	Renal tubular adenoma/carcinoma; hereditary in Eker rats,⁵⁶² seen in Nihon rats; litter effect in F344.⁵⁶³ May be induced by streptozotocin.⁵⁶⁴
	Oncocytoma; originates from the collecting duct; sporadic and usually benign.⁵⁶⁵
Urinary bladder	Urothelial (transitional cell) hyperplasia/neoplasia; often associated with calculi or Trichosomoides crassicauda infection.
Miscellaneous	Mesothelioma arising from testicular tunica vaginalis, F344.³³²
	Hibernomas; brown adipose neoplasm, usually benign.⁵⁶⁶
Pineal glad	Pineal tumors in WI⁵⁶⁷

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Table 14.

Laboratory Rats: Eukaryotes: Fungi, Protists, Metazoan Parasites²⁶^,⁴⁴²^,⁴⁵⁴^,⁴⁸⁷

Agent	Comments
Fungi
Trichophyton mentagrophytes	Ringworm/dermatophytosis; arthrospores in keratin of follicles; zoonotic.
Pneumocystis carinii (formerly rat respiratory virus)	Host-species specific. Interstitial pneumonia; resolves in immune sufficient rats.⁵⁷⁶ May cause typical PCP in immune deficient rats.⁵⁷⁷
Aspergillus spp.	Rhinitis and sinusitis.⁵⁷⁸
Protists	⁵⁷⁹
Cryptosporidium parvum	Diarrhea to proliferative enteritis, infant pups are prone; Opportunist that can cause runting to high mortality.
Eimeria spp.	Intestinal coccidiosis. Proliferative and necrotizing enteritis (E nieschlzi) to typhlocolitis (E separata); common in wild rats.
Giardia muris, G duodenalis	Opportunist, subclinical to clinical enteritis.
Spironucleus muris	Opportunist, subclinical to clinical enteritis.
Large intestine flagellates	Chilomastix, trichomonads; considered commensal.
Entamoeba spp.	Considered commensal.
Trypanosoma lewisi	Subclinical, transmitted to rat by fleas; zoonotic.⁵⁸⁰
Nematodes	⁵⁷⁹
Aspiculuris tetraptera	Mouse pinworm. Adults in colon, eggs in feces, usually asymptomatic.
Syphacia muris	Rat pinworm. Adults in cecum primarily and (flattened) eggs on perineum; usually asymptomatic.⁵⁸¹
Calodium hepaticum (formerly Capillaria hepatica)	Pyogranulomatous hepatitis; common in wild rats.⁵⁸²
Strongyloides ratti	Threadworm. Larvae enter thru skin, migrate to lungs; adults found in proximal intestine.⁵⁸³
Trichosomoides crassicauda	Bladder threadworm. Ingested larvae migrate from stomach to lungs and then to urinary tract; females found in bladder to renal pelvis epithelium; smaller males live in lumen or inside female uterus; nidus for urinary calculi; wild rats prone.
Cestodes	⁵⁷⁹
Cysticercus fasciolaris (Taenia taeniaeformis)	Cysts (strobilocerci) in liver; ingestion of feces from definitive host (cat); infection common in wild rats.⁵⁸⁴
Hymenolepis diminuta	Rat tapeworm. Enteritis.
Rodentolepis nana	Dwarf tapeworm. Larvae with armed rostellum in lamina propria; direct and indirect life cycles are possible; humans are definitive host; subclinical to poor weight gain and catarrhal enterititis.
Arthropods	⁵⁷⁹
Demodex ratti, D nanus	Nonpathogenic, incidental finding.
Laelaps echidnina	Spiny rat mite. Bites, sucks and leaves; transmits Hepatozoon spp.
Notoedres muris	Ear mange mite. Proliferative dermatitis on pinnae, mites in cornified epithelium.
Ornithonyssus bacoti	Tropical rat mite. Bites, sucks and leaves, rash may develop on handlers.
Radfordia ensifera	Rat fur mite. Subclinical to pruritus/dermatitis.
Polyplax spinulosa	Spined rat louse. Subclinical to pruritus/dermatitis⁴⁴⁹
Hoplopleura pacifica	Tropical rat louse. Subclinical to pruritis/dermatitis.

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Table 9.

Laboratory Rats: Anatomical and Physiological Features¹⁴⁹^,⁴⁵⁴^,⁴⁸⁷^,⁴⁵,⁴

System Organ/Tissue	Phenotypes/Comments
Alimentary
Teeth	Elodont incisors and anelodont molars.
Salivary glands	Sexual dimorphism. Mature male submandibular salivary glands have prominent convoluted (granular) ducts with more eosinophilic secretory granules than females; androgen sensitive/dependent.
Stomach	Squamous non-glandular stomach with limiting ridge.
Liver²⁰⁵^,²¹⁴	4 lobes with consistent lobation (unlike mouse): median, right lateral, left and caudate; polykarya (polyloidy).
Gallbladder	Absent
Hematolymphoid	⁴⁸⁸
Tonsils	Absent
Thymus	Involutes; cysts (ultimobranchial remnants) are not unusual.
Spleen	Accessory spleens may be present.
	Hemosiderin, females > males, increase with age.
Hematopoiesis	Extramedullary hematopoiesis common in liver and spleen (less than mice).
	Hematopoiesis remains active in long bones.
Hematology	WBC up to 80% lymphocytes.²²⁴^,⁴⁸⁹
Mast cells	Common in many tissues.
Integument	Yellow with age from oxidation of sebum.
Musculoskeletal	No Haversian bone.
	Epiphyses close, some remain open beyond 1 y
Nervous	^490–493
Brain	Lissencephalic
Respiratory	²⁴⁸ ^, ²⁴⁹ ^, ⁴⁹⁴
Nose	Obligate nose breathers.
	Prominent vomeronasal organs.
	Incisive fissures (nasopalatine ducts) connect oral and nasal cavities, not cleft palate.
	Maxillary recess (not sinus) lateral to nasal cavity, common site of mild neutrophilic inflammation.
Lungs	1 left + 4 right lobes
	Intrapulmonary airways are bronchioles and not bronchi, lack cartilage and submucosal glands.
	Serous cells in respiratory epithelium (unique to rat).
	Cardiac muscle extends around large pulmonary veins.
	Eosinophilic crystals, hemoglobin derived⁴⁹⁵^,⁴⁹⁶
Urogenital	Female,⁴⁹⁷^,⁴⁹⁸ male,³⁶² and urinary³⁶³
Kidney	Hyaline (eosinophilic) droplets in cytoplasm of tubule epithelium, male > female. α_2u-Globulin.⁴⁹⁹
Urine	Proteinuria higher in males. Urine albumin should be measured specifically if research relevant.
Uterus	Bicornuate. Cyclic granulocyte infiltration of endometrium.
Vagina	Characteristic vaginal cytology and histology changes during estrus cycle.²⁵¹^,⁵⁰⁰
Gestation	21–23 d
Pups	N = 6–12/L, 5–6 g/pup; eyes open approximately 14–17 d; wean approximately 21 d.⁵⁰¹
Miscellaneous
Lacrimal glands	Exorbital (extraorbital) gland can have striking karyomegaly, anisocytosis, and pseudoinclusions; infraorbital gland.
Harderian gland	Retrobulbar gland secretes porphyrin-rich material that lubricates eyes and lids; chromodacryorrhea refers to periocular and nasal red (autofluorescent) porphyrin secretions in ill and dehydrated rats.
Pineal gland	Prominent compared with mice.
Retroorbital plexus	Most reports call this a plexus not a sinus, used for blood collection.⁵⁰²

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Table 12.

Laboratory Rats: Viruses²⁶^,⁴⁰⁰^,⁴⁵⁴^,⁴⁸⁷

Family, Genus	Agent	Comments
Adenoviridae, Unclassified	Rat adenovirus	Intranuclear inclusions in enterocytes of the small intestine (especially young).
Coronaviridae, Betacoronavirus	Sialodacryoadenitis virus (SDAV)	Sialoadenitis, dacryoadenitis, necrotizing rhinitis, tracheitis, bronchitis, interstitial pneumonia; may be more severe in Lewis (ophthalmic sequelae) and SHR.⁵⁶⁸
Hantaviridae, Orthohantavirus	Seoul virus	Asymptomatic reservoirs with zoonotic potential
Herpesviridae, Muromegalovirus	Rat CMV	Karyomegaly and intranuclear inclusions in salivary and lacrimal epithelium, especially submandibular gland; common in wild rats.
Paramyxoviridae, Respirovirus	Sendai virus	Mild necrotizing to proliferative lesions with syncytia, inclusions, and squamous metaplasia; RNU may have infant mortality or wasting; otherwise subclinical with similar lesions to resistant mouse strains.
Pneumoviridae (Paramyxoviridae), Orthopneumovirus	PVM	Perivascular and interstitial lymphocytic infiltrates in seropositive (recovered) rats; usually subclinical.
Parvoviridae, Protoparvovirus	Rat virus (RV), Toolan H-1 virus (H1), Rat parvovirus (RPV, Kilham rat virus)	RV: Fetal resorption, neonatal cerebellar hypoplasia, hepatitis, jaundice, and steatorrhea; adult necrosis/hemorrhage in CNS & testis. H1: transient biliary hyperplasia, subclinical.⁵⁶⁹^,⁵⁷⁰
Picornaviridae, Cardiovirus	Rat Theilovirus	Subclinical, cross reacts with TMEV.
Polyomaviridae, Betapolyomavirus	Rattus norvegicus polyomavirus 2	Wasting in RNU and scid rats; sialoadenitis with intranuclear inclusions parotid gland.⁵⁷¹
Poxviridae, Orthopoxvirus	Cowpox virus	Necrotizing rhinitis; experimental skin lesions; seen in pet rats (Europe); zoonotic.⁵⁷²
Reoviridae, Orthoreovirus	Reovirus 1, 2, 3	None
Reoviridae, Rotavirus	Infectious diarrhea of infant rats (IDIR) virus	Suckling (<2 wk old) can have diarrhea, villus blunting and fusion with inclusions and pathognomonic syncytia, especially distal small intestine.
Retroviridae	Rat leukemia virus	Endogenous proviruses, experimental murine sarcoma agents.

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Table 13.

Laboratory Rats: Bacteria²⁶^,⁴⁵⁴^,⁴⁸⁷

Genus and Species	Comments
Bordetella bronchiseptica	Opportunist or co-pathogen; rhinitis, otitis, and pneumonia.
Campylobacter jejuni	Subclinical; reservoir host, zoonotic.
Clostridium piliforme (Tyzzer’s disease, fat rat syndrome)	Necrotizing lesions in heart, liver, cecum, ileitis to colitis with flaccid dilatation of intestine (megaloileitis). Intracellular bacilli.
Corynebacterium kutscheri (pseudotuberculosis)	Cervical lymphadenomegaly to bacteremia with embolic caseating abscesses in lungs etc tissues.
Enterococcus faecium durans-2, E. hirae	Enterococcal enteropathy of infant rats. Uncommon. Runting, diarrhea, and high mortality in suckling rats; abdominal distention.
Filobacterium rodentium (CAR-Bacillus)	Subclinical bronchitis with lymphoid cuffing; often co-infection with M pulmonis.⁴⁹⁵
Helicobacter bilis, H hepaticus, and H trogontum	Proliferative and ulcerative typhlitis to proctitis in RNU with H bilis; possible roles in other enterohepatic phenotypes; additional species identified by PCR.
Hemophilus spp.	Mild pneumonitis.
Klebsiella pneumoniae	Rare; mild rhinitis to abscesses.
Lawsonia intracellularis	None; possible reservoir.
Leptospira interrogans ser. icterohemorrhagiae or ballum	Asymptomatic and shed in urine; common in wild rats; zoonotic.
Mycoplasma pulmonis	Sneezing, snorting, chattering, suppurative-chronic rhinitis/otitis /pneumonia with bronchiolectasis and prominent lymphoid cuffing. Latter can be misinterpreted as lymphoma. ⁴⁹⁵^,⁵⁷³
Mycoplasma haemomuris (formerly Hemobartonella muris)	Usually subclinical anemia; bacteria on RBC membrane after splenectomy; Polyplax spinulosa and Hoplopleura pacifica are vectors.
Rodentibacter pneumotropicus, R heylli (formerly Pasteurella pneumotropica)	Pneumonia, otitis, conjunctivitis, metritis; opportunist, co-pathogen with Sendai virus or Mycoplasma spp.
Pseudomonas aeruginosa	Bacteremia/sepsis/death in immune deficient; common in water and environment.
Salmonella enterica	Usually subclinical with shedding; rare clinical ulcerative typhlitis
Spirillum minus	Subclinical; zoonotic (Asian rat bite fever in humans)
Staphylococcus spp.	Opportunist; mastitis, dermatitis.
Streptobacillus moniliformis	Generally asymptomatic; rare opportunistic respiratory disease; zoonotic (rat bite fever or Haverhill fever in humans).⁵⁷⁴
Streptobacillus notomytis	Otitis media/interna⁵⁷⁵
Streptococcus agalactiae	Pup mortality, bacteremia, and abscesses.
Streptococcus pneumoniae	Fibrinosuppurative pneumonia, rhinitis, otitis, and serositis; high mortality in suckling rats; many subclinical carriers (as in humans).
Streptococcus spp. (Enterocccus)	Uncommon, runting, diarrhea, abdominal distension, mild inflammation, high mortality in suckling rats.

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GERBILS

Mongolian Gerbils: Order Rodentia, Suborder Myomorpha; Meriones unguiculatus

Gerbils are also known as jirds, desert rats, sand rats, and Mongolian desert mice. They are murid rodents of the sub-family Gerbillinae, which includes approximately 110 species native to Africa and Asia.²⁶^,⁶⁴^,⁶⁵ Although several species have been used as experimental models, the Mongolian gerbil (Meriones unguiculatus [Milne-Edwards, 1867]), is most common and emphasized here. Gerbils are adapted for survival in arid and semi-arid areas of Africa and Asia. They do best in relatively dry environments (below 50% humidity), and, in the wild, build extensive burrows to maintain relatively constant temperatures during day and night. Gerbils alternate active and sleep periods during the day and night and do not hibernate.⁶⁶ They can cool themselves by spreading saliva over their fur for evaporative cooling or by exchanging heat via the ventral gland by pressing it against a cooler substrate. Sand-bathing is beneficial for gerbils to prevent their coats from becoming oily and soiled.²⁶^,⁶⁴^,⁶⁵^,⁶⁷^,⁶⁸

The gerbil lifespan is approximately 3 years but occasionally up to 4 years.⁶⁶^,⁶⁹^,⁷⁰ Expected adult weights are 50–100 g, with males slightly larger, with a body length of 11–15 cm and tail length of 10–19 cm.^64–66^,⁶⁹ Their diet in the wild consists of green vegetation, roots, bulb seeds, cereals, fruits, and insects. In research settings, they are usually maintained on a commercial gerbil, hamster, or rodent diet containing 18% to 20% protein. Gerbils (and other thrifty rodents originating from austere conditions in the wild), especially males, develop high blood cholesterol and lipemia on diets containing >4% fat.⁶⁴^,⁶⁵^,⁶⁸

Gerbils are known for a mild temperament and are generally easy to handle. They tend to be curious, often stand on their hindlimbs, and readily investigate novel stimuli.⁶⁵^,⁶⁶^,⁶⁹ Gerbils mark their territory with secretions from their ventral glands or Harderian glands.⁶⁶^,⁷¹^,⁷² They are social and generally do best when housed with other gerbils, though both male and female gerbils can be very aggressive towards intruders. Gerbils tend to form lifelong monogamous pairs, beginning to breed at about 2–3 months of age and usually continuing until the female is 17–18 months old. The average gestation period is 24–26 days and average litter size is 3–7 pups.⁶⁵^,⁶⁸

Gerbils have been used in biomedical research since the 1960s. Gerbils were introduced into the United States in 1954 when 11 pairs from a Japanese colony were sent to Tumblebrook Farm in New York. These 11 pairs originated from a group of 20 wild pairs originally collected in Mongolia in 1935 and subsequently bred in Japan. Nine descendants of these 11 pairs (5 females, 4 males) provided the foundation of all gerbils in the United States, creating a strong genetic founder effect with low genetic variability compared with other laboratory species. Although most commercially available gerbils are “outbred,” inbred strains do exist.²⁶^,⁶⁴^,²⁶^,⁶⁵^,⁷³

Research-relevant features and non-infectious conditions in gerbils are summarized in Tables 15–16. Neoplasia can be an important cause of morbidity and mortality in toxicity assays in gerbils over 2 years of age. Compared with other laboratory rodents, hematopoietic neoplasms are unusual, and ovarian, adrenocortical, and cutaneous tumors can be fairly common (Table 17).²⁶^,⁶⁴^,⁶⁵^,⁶⁸^,⁷⁰^,^73–75 Infectious agents that may be identified or may cause disease in gerbils are summarized in Tables 18 and 19. Interestingly, naturally occurring viral infections of gerbils are not reported, and reports of fungal or protist infections in laboratory gerbils are rare.²⁶^,⁶⁴^,⁶⁵^,⁶⁸

Table 15.

Mongolian Gerbils: Anatomic and Physiologic Features²⁶^,^64–66^,⁵⁸⁵

System Organ/Tissue	Expected Phenotypes/Conditions
Alimentary	Serum cholesterol response to dietary cholesterol and fat intake, primary bile acids, and enzymes involved in hepatic cholesterol metabolism and cholesterol ester storage all similar to humans. Can develop hepatic lipidosis and cholesterol gall stones with high cholesterol diets.^586–588
Dentition	Elodont incisors, Dental formula: I1/1, C0/0, P0/0, M3/3 = 16
Endocrine	Large adrenal glands; adrenal to body weight ratio is among the highest of any species. Cortisol is primary secretion, similar to humans and unlike other laboratory rodents.
Hematolymphoid	Erythrocyte lifespan is only 10 d. Polychromasia, basophilic stippling, and reticulocytosis are common.
	Large thymus compared with other rodents of similar size; persists in adult animals.
Integument	Ventral gland; specialized sebaceous gland in ventral abdominal midline skin; used in marking territory and establishing dominance; present in both sexes but larger in adult male.
Nervous	Variably incomplete circle of Willis; useful in models of cerebral ischemia via carotid artery ligation; anatomic variations in different populations. ⁵⁸⁹^,⁵⁹⁰
Epilepsy	Common, usually beginning around 2 months of age; induced by various stressors; vary from mild hypnotic episodes to severe myoclonic convulsions; selective breeding can lead to “seizure-prone” and “seizure-resistant” lines or inbred strains.⁶⁶^,⁵⁹¹
Special senses	Prominent ears and keen hearing; sensitive hearing in low frequency range (unlike mice and rats), attributed to large auditory bullae and adaptations of the middle ear and basilar membrane (expect deafness with aging and aural cholesteatomas).
	Well-developed visual systems, including optic tectum and visual cortex; better at discriminating visual cliff than rats, and distinguishes finer spatial frequency grating than hamsters.
Urogenital	Nephrons are highly efficient with very long loops of Henle; can effectively concentrate urine, and survive on very little water (approximately 4–7 mL/100 g BW/d).
Male reproductive	Histologic, histochemical, and ultrastructural features of the adult prostate are comparable with those of the human.⁶⁷
	No preputial glands.
Miscellaneous	Retroorbital sinus for blood collection⁵⁰¹

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Table 16.

Mongolian Gerbils: Non-infectious Non-neoplastic Conditions²⁶^,⁶⁴^,⁶⁵^,⁶⁹^,⁷¹^,⁵⁸⁵^,⁵⁹²^,⁵⁹³

System Organ/Tissue	Condition; Comments
Multisystemic	Metabolic disease. On standard rodent diets, approximately 10% become obese, and some have decreased glucose tolerance, increased serum insulin, with diabetic changes in the pancreas and other tissues.
Alimentary	Malocclusion and overgrowth of elodont incisors; clinical signs can include weight loss, depression, emaciation.
	Periodontal disease after about 6 mo on standard laboratory rodent diets. Also prone to dental caries.
Cardiovascular	Arterial plaques with mineralization degenerative changes in aorta, mesenteric, renal, and peripheral arteries; particularly aged breeder females,⁵⁹⁴ and associated with hyperadrenocorticism, increased serum triglycerides, hepatic lipidosis.
Endocrine	Hyperadrenocorticism. May be more in breeder females. May see arterial plaques, increased serum triglycerides, enlarged pancreatic islets, hepatic lipidosis and/or adrenal lipid depletion and hemorrhage.
	Type 2 diabetes mellitus (T2DM). The Mongolian gerbil exhibits spontaneous obesity and hyperglycemia, increased immunoreactive insulin, glucosuria, and islet hyperplasia with age.
Integument	Tail slip (degloving injury) if picked up by the middle or distal tail; exposed tissue eventually becomes necrotic and will shed, with sloughing of the caudal vertebrae.
	Barbering. Common with overcrowding, usually tail base.
	Greasy haircoat when humidity is greater than 50%, most often in animals kept in solid-topped microisolator cages. Harderian gland secretions increase and haircoat appear greasy, wet, or matted from excess grooming.
	Sore nose/bald nose/facial eczema/nasal dermatitis. Common, multifactorial, especially in weanlings. Stressors (eg, humidity >50%, overcrowding, trauma or weaning) cause increased porphyrin-containing secretion from Harderian gland; secretions around nares and eyes, may contribute to irritation, self-trauma, secondary bacterial infections (Staphylococcus aureus and S xylosus); may extend over head, forelimbs, ventrum, and/or maxillary sinuses. Lesions initially erythematous but progress to alopecia, then moist dermatitis with scabbing and ulceration. Accumulated porphyrins fluoresce under UV light. Sandbaths to treat or prevent.
Nervous	Aminoglycoside toxicity. Very low margin of safety. Causes a direct neuromuscular blocking effect by inhibition of acetylcholine release; acute ascending paralysis with up to 100% mortality.
	Spongiform lesions in brainstem, most prominent in cochlear nucleus, are reported in older gerbils.⁵⁹⁵
Special senses	Aural cholesteatoma. Approximately 50% in >2 y old. Growth in the ear canal, compresses and can displace the tympanic membrane. May have secondary infections, leading to damage in inner ear and bone necrosis. Clinical signs include head tilt, scratching, and circling.
Urogenital	Infertility due to ovarian cysts, advanced age, toxin exposure, nutritional deficiencies, concurrent disease, overcrowding, environmental disturbances, and low temperature.
	Ovarian cysts. >1 y old; 1–50 mm in diameter; unilateral or bilateral. May be subclinical or associated with abdominal swelling, symmetrical alopecia, lethargy, anorexia, infertility and small litter sizes.
	Chronic interstitial glomerulonephritis/glomerulonephropathy. Common in aged, especially males >2 years. Clinical signs include polyuria and polydipsia, anorexia, weight loss and decreased muscle mass. Grossly, kidneys are shrunken and pitted. ⁶⁶

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Table 17.

Mongolian Gerbils: Neoplastic Conditions²⁶^,^73–75^,⁵⁹²^,⁵⁹³^,⁵⁹⁶

System Organ/Tissue	Condition; Comments
Endocrine	Adrenal cortical adenoma/carcinoma
Integument	Squamous cell carcinoma of the ventral marking gland
	Melanoma
	Sebaceous adenoma/adenocarcinoma
Urogenital	Ovarian granulosa cell tumor

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Table 18.

Mongolian Gerbils: Bacteria²⁶^,⁶⁴^,⁶⁵^,⁵⁸⁵

Genus and Species	Comments
Clostridioides difficile	Antibiotic-associated enterocolitis/enterotoxemia. Dysbiosis due to disruption of intestinal microflora. Associated with amoxicillin and metronidazole in diet to treat Helicobacter infections. High environmental contamination with spores also associated with outbreaks. Sudden death and acute liquid diarrhea. Necrosis, edema and hemorrhage of the cecum and colon with acute inflammation.⁵⁹⁷
Clostridium piliforme	Tyzzer’s disease. Sporadic outbreaks with high morbidity and mortality, especially in young animals and pregnant females, although all ages can be affected. Fecal-oral. Depression, unthrifty appearance, varying degrees of watery diarrhea or acute death. Lesions in liver (multifocal hepatic necrosis) or intestine (enteritis, serosal edema), with possible brain and cardiac involvement. Because of high susceptibility, they have been used as sentinels to detect latent infectious in other rodent species.^598–600
Helicobacter spp.	Natural infections by H hepaticus, H rodentium, and H bilis. Uncommon in lab colonies, usually subclinical. Fecal-oral. Experimental H pylori infection is an established model for human disease.⁶⁰¹^,⁶⁰²
Salmonella spp.	Uncommon. Fecal-oral. Rough hair coat, weight loss, dehydration, depression; occasional diarrhea or acute death. Congested liver with inflammation and/or necrosis, gastrointestinal distension, and fibrinosuppurative peritonitis. Zoonotic.⁶⁰³

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Table 19.

Mongolian Gerbils: Metazoan Parasites²⁶^,⁶⁴^,⁶⁵^,⁴⁴²^,⁵⁸⁵

Agent	Comments
Nematodes
Syphacia obvelata, S muris, Dentostomella translucida	Pinworms usually are subclinical. D translucida are found in upper small intestine.⁶⁰⁴^,⁶⁰⁵ Gerbils are susceptible to Syphacia spp. pinworms of other rodent species. Syphacia spp. are found in lower bowel.
Cestodes
Hymenolepis diminuta, Rodentolepis nana	Found in distal small intestine. Clinical disease with heavy infestation (catarrhal enteritis, diarrhea, emaciation and chronic weight loss). Rare in research colonies. R nana is zoonotic.⁵⁹²^,⁶⁰⁶
Arthropods
Demodex criceti, D aurati	Uncommon in research colonies, usually subclinical. If present, lesions generally occur over dorsum, rump and include rough hair coat, alopecia or scaly dermatitis. D. aurati is considered more pathogenic than D. criceti.⁶⁰⁷

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GUINEA PIGS

Guinea Pig: Order Rodentia, Suborder Hystricomorpha; Cavia porcellus

Domesticated guinea pigs (Cavia porcellus [Linnaeus, 1758]) are rodents in the suborder Hystricomorpha, which also includes porcupines, degus, pacas, agoutis, capybaras, nutrias, and spiny rats. Hystricomorphs are distinguished from other rodents by the morphology of the jaw muscles and their attachments, including an expanded medial masseter or zygo-mandibularis muscle that runs through a large infraorbital foramen. This configuration favors grinding with the molars over gnawing with the incisors and is suited to a diet consisting mostly of grasses.^76–79

Evidence of guinea pig domestication dates back at least to 500 BC, possibly millennia BC in South America, where they were primarily a food source and seem to have been kept as pets and used in religious or healing ceremonies. All contemporary domesticated guinea pigs (for pets, meat, or research) derive from C porcellus domesticated in Peru. They arrived in Europe in the 16th century and in North America in the 19th century.⁸⁰ Guinea pigs were used in the laboratory as early as in the 18th century, including by Lavoisier, who used them to measure body heat production circa 1780. Guinea pigs played major roles in research that led to at least 3 Nobel prizes: Robert Koch identified the causative agent of tuberculosis (Mycobacterium tuberculosis) using guinea pigs in 1882,⁸¹ Pierre Roux and Alexandre Yersin injected guinea pigs with medium from the growth of Corynebacterium diphtheriae to produce clinical signs of diphtheria in 1888,³ and scurvy was first induced in guinea pigs by Norwegian physicians Axel Holst and Theodor Frolich in 1907.⁸² Further, in 1942, Karl Landsteiner and Merrill Chase discovered cell-mediated immunity in studies on guinea pigs.⁸³ The term guinea pig as a synonym for research subject was first used by George Bernard Shaw in his 1891 essay on Ibsenism.⁸⁴

The Hartley (also called English or Dunkin Hartley) shorthair albino guinea pig is primarily used in contemporary biomedical research. Commercially available Hartley guinea pigs are termed outbred but have been breeding in relatively closed colonies for many generations. Of 23 inbred lines developed around 1906 at the USDA Bureau of Animal Industry in Beltsville, MD, inbred strains 2 and 13 were maintained and distributed from BAI, USDA, then from NCI, NIH, with Heston. These are the most evident inbred strains in research literature. Strain 13/N is a tricolored strain, still used to model infections with highly pathogenic viruses.⁴⁵^,⁷⁷^,^85–88 Hairless euthymic guinea pigs have been used in research and have a following in the pet trade. A hairless immunodeficient guinea pig mutant was reported in 1979 but seems not to have been used widely in research.⁸⁹ In the 1980s, guinea pigs were used primarily in safety testing and toxicology but have been largely replaced by mice and rats in those studies. Guinea pig ear anatomy, hearing, cholesterol metabolism, hormonal physiology, susceptibility and immune responses to infectious diseases, and sensitivity to respiratory allergens are relevant to human conditions, and continue to be studied. Their size and docility favors their use in studies of Risk Group 3 and 4 infectious agents. Because of their long gestation period and precocious offspring, guinea pigs are also important models for testing teratogenic effects of pharmaceuticals and other chemicals.⁷⁷^,⁹⁰

Tables 20–23 summarize research-relevant features and conditions in this important species. Tables 24–26 summarize infectious agents that may be identified or may cause disease in guinea pigs.

Table 20.

Guinea Pig: Taxonomy, Genetics, Nomenclature, and Common Strains/Stocks ⁷⁷^,⁷⁸^,⁷⁹^,⁶⁰⁸^,⁶⁰⁹^,⁶¹⁰

Strain or Stock	Expected Phenotypes/Conditions
Dunkin-Hartley (:HA)^*	Most common in research. Acromelanic (genotype eec^ac^a) with black pigment distally (nose, ears, feet); pink eyes with poorly pigmented uveal melanocytes.
Strain 13 (13/N)	Most available of 23 inbred strains developed at BAI/USDA in early 1900’s;⁶¹¹ tricolor, earlier onset and rapid progression of nephrosclerosis; hereditary cataract; infectious disease research. Other strains (2/N, JY-1 to -10, JY-G, Weiser-Maples) uncommon and difficult to obtain,
Hairless	:HA-Hr^hr. Euthymic, derived from Dunkin-Hartley
Pigmented non inbred	Abyssinian, American

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^# ‘/’ After strain/root abbreviation indicates inbred and is followed by the source laboratory code.

^*‘:’ Before stock abbreviation indicates outbred and is preceded by the source laboratory code.

Table 23.

Guinea Pigs: Neoplastic Conditions²⁶^,⁷⁷^,⁷⁸^,²⁶^,⁶³⁸^,⁶⁶⁶^,⁶⁶⁷

System Organ/Tissue	Condition; Comments
Endocrine
Adrenal	Cortical adenomas/carcinomas, with Cushing syndrome
Pancreas	Insulinoma⁶⁶⁸
Thyroid	Uncommon⁶⁶⁹
Hematolymphoid	Lymphoma. Most common spontaneous neoplasm in guinea pigs, viral etiology hypothesized. Often progress to lymphoblastic leukemia.⁶⁷⁰^,⁶⁷¹
Integument
Mammary gland	Often malignant, both sexes, age-related.⁶⁷² Adenomas, adenocarcinomas, and mixed malignant tumors reported.⁶⁷³
Skin	Trichofolliculomas most common⁶⁷⁴
Respiratory
Lung	Bronchogenic papillary adenoma⁶⁷⁵
Urogenital
Kidney/urinary bladder	Urothelial carcinoma; hemangiopericytoma⁶⁷⁶^,⁶⁷⁷
Female reproductive	⁶⁶² ^, ⁶⁶³ ^, ⁶⁷⁸
Ovary	Teratoma common.⁶⁷⁹
Uterus	Polyp; endometrial adenoma/adenocarcinoma; deciduoma; malignant mixed Müllerian tumor; leiomyosarcoma; leiomyoma (may be pedunculated)⁶⁸⁰

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Table 24.

Guinea Pigs: Viruses²⁶^,⁶⁸¹

Family, Genus	Agent	Comments
Adenoviridae, Mastadenovirus	Guinea pig adenovirus	Opportunistic respiratory pathogen. Low morbidity, high mortality; bacterial superinfections common; necrosis of airway epithelium with large intranuclear inclusion bodies (INIB).
Herpesviridae, unassigned	Guinea pig CMV	Latent infection with INIB in salivary gland duct epithelium; INIB also in renal tubule epithelium; rare disseminated disease including pneumonitis with immune suppression.
Arenaviridae, Mammarenavirus	LCMV	Rare spontaneous infection. Mouse is reservoir. Zoonotic.
Paramyxoviridae, Respirovirus	Parainfluenza virus 3	Subclinical respiratory infection
	Other	Can be experimentally infected by many pathogenic viruses of humans, including Ebola, Marburg, Lassa, influenza V, and Nipah viruses.

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Table 26.

Guinea Pigs: Eukaryotes: Fungi, Protists, Metazoan Parasites²⁶^,⁴⁴²^,⁶⁸¹^,^688–691

Class Agents	Comments
Fungi
Encephalitozoon cuniculi	Uncommon, usually subclinical, granulomatous inflammation (kidney, brain)⁶⁹²
Unclassified Pneumocystis	Host-specific, typical PCP lesions in immune deficient
Trichophyton mentagrophytes, Microsporum canis	Uncommon, subclinical colonization of the skin, rare clinical dermatitis. Zoonotic
Protists
Cryptosporidium wrairi	May cause diarrhea in young
Eimeria caviae	Intestinal coccidiosis
Klossiella cobayae	Renal coccidiosis, usually subclinical
Helminths
Paraspidodera uncinata	Cecal worm
Arthropods
Gyropus ovalis	Oval guinea pig louse
Gliricola porcelli	Slender guinea pig louse
Chirodiscoides caviae	Fur mite
Trixacarus caviae	Sarcoptic mange mite
Demodex caviae	Demodectic mange mite

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Table 21.

Guinea Pigs: Anatomic and Physiologic Features²⁶^,⁷⁷^,⁷⁸^,⁶⁰⁹^,⁶¹²^,⁶¹³^,⁶¹⁴

System Organ/Tissue	Conditions; Comments
Alimentary
Dentition	Monophyodont (no deciduous teeth); all teeth are elodont. Dental formula: I1/1, C0/0, P1/1, M3/3.
	Three distinct types of cementum (cellular, acellular, and 1 histologically similar to cartilage).⁶¹⁵
Stomach	No non-glandular forestomach.
Intestine	Calcium absorption proportional to diet (not regulated by vitamin D)
	Hindgut fermenters with a large cecum (40% to 60% of ingesta) located on left side.
Liver	Lipid accumulation common, develops rapidly with anorexia⁶¹⁶
Pancreas, exocrine	High basal serum amylase activity.
	Fatty infiltration and replacement of the exocrine pancreas (and salivary glands) common and age-related; no reported functional consequences
Cardiovascular	^617–619
Vascular	Pulmonary arteries can have prominent segmental smooth muscle in media (beads on a string), not pulmonary hypertension. No cardiomyocytes in media of pulmonary veins.
Heart	Coronary arteries have extensive collateral branching; poor models for myocardial infarction.
	Cardiac electrophysiology is highly similar to humans, often used in Langendorff systems.
Lipoprotein metabolism	Like humans, and unlike rats and mice, Guinea pig plasma cholesterol is primarily in the LDL fraction; their HDL:LDL ratios are more similar to human than are mice, rat, hamster, rabbit ratios.⁶²⁰^,⁶²¹
Endocrine
Adrenal	Normal cortex:medulla ratio is 1:1. Cortex arranged in 4 layers: zona glomerulosa, intermediate zone (small cells with irregular hyperchromatic nuclei), zona fasciculata, zona reticularis (also called X-zone in rodents because studies suggest that cells do not secrete androgens).⁶²² Cells in zona reticularis/X-zone may accumulate lipofuscin.
Hematolymphoid	⁸⁷ ^, ⁶²³ ^, ⁸⁷ ^, ^624–626 ^, ⁶²⁷
Blood	Lymphocyte is predominant circulating leukocyte; neutrophils have been called heterophils.²²⁴
	Foa-Kurloff (Kurloff) cells are a unique circulating leukocyte with NK cell-like activity. Large cytoplasmic inclusions are PAS positive and magenta by Wright-Giemsa, displace nucleus.⁶²⁸ Higher numbers during pregnancy, estrogen treatment.
Lymph nodes	⁶²⁹
Thymus	Cervical/intermandibular (not mediastinal) location.⁶³⁰ Epithelial cell degeneration and heterophil infiltration within Hassall’s corpuscles resembles pustules.
Integument
Skin	Single pair inguinal mammary glands/nipples; supernumerary nipples can occur.
Nervous	Lissencephalic⁶³¹^,⁶³²
Respiratory	⁶³³ ^, ⁶³⁴
Nose/head	Obligate nose breathers. Small palatal ostium makes intubation difficult.
Lungs	Left lung divided into 3 lobes, right lung into four; respiratory bronchioles present.
Special senses
Ear	Size, morphology, physiology, accessibility of middle and inner ear advantageous for research⁶³⁵^,⁶³⁶
Urogenital
Kidney	Main route of calcium excretion
	Urethral meatus outside of vagina
Female reproductive	Sows have a vaginal closure membrane during pregnancy and anestrus; membrane ruptures due to vulvar swelling during estrus or prior to parturition.
	Estrus cycle: 16–17 d. Onset of puberty: 3–4 mo. Vaginal mucosa similar to mouse and rat, including cyclic changes.⁶³⁷ Short uterine body
	Gestation length: 59–73 d; sows can more than double their weight during pregnancy; pups are large and precocious (fully haired with early solid food intake). Discoid hemochorial placentation.
Pregnancy toxemia Eclampsia/ preeclampsia	Eclampsia/preeclampsia like complications of late pregnancy (large uterus) and early lactation; ‘circulatory form’ attributed to vascular changes leading to ischemia of uteroplacental unit; fasting ketosis or metabolic–nutritional form is associated hypoglycemia and hyperlipidemia.
Male reproductive	Penis includes 2 cranial terminal styles (horns), numerous cornified spurs, and an os penis. Seminal vesicles are large, tubular and clear.
	Inguinal canals open.

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Table 22.

Guinea Pigs: Non-infectious Non-neoplastic Conditions²⁶^,⁷⁷^,⁷⁸^,²⁶^,⁶¹⁰^,⁶¹²^,⁶¹⁴^,⁶³,⁸

System Organ/Tissue	Conditions/Phenotypes
Multisystemic	‘Scurvy’ Hypovitaminosis C; GP lack l-gulonolactone oxidase (GULO) enzyme needed to synthesize ascorbic acid; require adequate dietary ascorbate; failed cross-linking of fibrillar collagens and elastin results in connective tissue weakness, spontaneous hemorrhage, and bone defects.⁶³⁹
	Metastatic mineralization. Heart, GI, kidneys. Most common in older boars. Mineral imbalances (Ca, Mg, P; not Se or vitamin E) in diet. Vitamin D toxicity should be considered.⁶⁴⁰
	Amyloidosis. Associated with pododermatitis.⁶⁴¹ Kidneys, liver, spleen, and adrenal glands.
	Pregnancy toxemia (“eclampsia”/pre eclampsia, see liver)
Alimentary
Teeth	Malocclusion; involves incisors and molars; misalignment of maxillary and mandibular arcades results in uneven wear of any teeth; tongue can become entrapped by cheek teeth, with lingual spurs penetrating tongue from the mandible, and buccal spurs penetrating cheek from the maxilla. Overgrowth of reserve (subgingival) crown can penetrate the mandible/ maxilla.
Stomach	Gastric ulcers. Stress.
	Gastric dilatation and volvulus, due to a relatively long mesenteric ligament; frequently fatal.⁶⁴²
Intestine	Rectal prolapse common.
Liver	Focal hepatic necrosis; subcapsular submassive infarcts of undetermined etiology.⁶⁴³^,⁶⁴⁴ Biliary hyperplasia in healing phase.
	Pregnancy toxemia related hepatic lipidosis, associations with ketosis, negative energy balance, large gravid uterus.
Cardiovascular
Heart	Rhadomyomatosis/glycogenosis. Proliferation of subendocardial vacuolated Purkinje cells.⁶⁴⁵^,⁶⁴⁶
Endocrine
Pancreas, endocrine	Type 1 Diabetes Mellitus (T1DM)⁶⁴⁷
Thyroid	Hyperthyroidism⁶⁴⁸
Integument
Skin	Accumulation of sebaceous material in the perianal region of older boars. ⁶⁴⁹
	Pododermatitis (bumblefoot). Wire-bottom or dirty caging, obesity. Opportunistic Staph. aureus infection.
Musculoskeletal
Joints	Spontaneous (and induced) osteoarthritis, particularly stifle (knee)⁶⁵⁰^,⁶⁵¹
Nervous	Peri-ventricular ependymal rosettes⁶⁵²
Respiratory
Lungs	Feed aspiration with foreign body type granulomatous inflammation; association with anesthesia.
	Osseous metaplasia/heterotopic bone
Special senses
Eye	Autosomal dominant congenital cataracts in 13/N.⁶⁵³^,⁶⁵⁴ Spontaneous age-related in others
	Osseous metaplasia/heterotopic bone in the ciliary body⁶⁵⁵
Ear	Bacterial otitis media/interna.⁶⁵⁶^,⁶⁵⁷
Urogenital
Kidney	Nephrosclerosis/chronic progressive renal disease, resembles CPN of rats. Pathogenesis not established. Microscopic changes detected as early as 5 mo, gross changes as early as 8 mo. Histologic changes correlated with age-associated increase in blood pressure.⁶⁵⁸ More severe in 13/N.
	Urinary calculi.⁶⁵⁹^,⁶⁶⁰ Calcium carbonate most common; older sows overrepresented
	Bacterial cystitis, more common in older sows; usually ascending infection with fecal bacteria such as E. coli.⁶⁶¹
Female reproductive	⁶⁶² ^, ⁶⁶³
	Polycystic ovaries due to cystic rete ovarii. Usually bilateral, lined by ciliated epithelium. 63.5% to 90% of middle aged to older sows. Associated with decreased reproductive performance; may cause abdominal distension, mucometra/hydrometra, and bilaterally symmetric alopecia.⁶⁶⁴ Can induce with estrogen.⁶⁶⁵
	Dystocia. Common due to the large size of the feti and failure of the iliosacral ligaments to relax. Fusion of the pelvic symphysis may occur if not bred before 7 mo.

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Table 25.

Guinea Pigs: Bacteria²⁶^,⁶⁸¹^,⁶⁸²

Genus and Species	Comments
Bordetella bronchiseptica	Commensal in the upper respiratory tract, opportunistic pathogen. Often follows adenovirus infection.⁶⁸³ Pneumonia, pleuritis, or otitis media/interna.
Streptococcus equi subsp. zooepidemicus	Suppurative cervical lymphadenitis with swelling of the neck and abscessation.⁶⁸⁴ Septicemia can occur. Zoonotic.
Streptococcus pneumoniae	Suppurative or fibrinous pneumonia/pleuritis/pericarditis, meningitis, or arthritis. Zoonotic.⁶⁷⁵^,⁶⁸⁵
Clostridium piliforme	Tyzzer’s disease. Intracellular bacilli and necrosis in liver, cecum, and heart.
Clostridioides difficile	Dysbiosis due to antibiotics that have enterohepatic circulation and a gram positive spectrum (beta-lactams, macrolides, lincosamides).
Chlamydophila caviae	guinea pig inclusion conjunctivitis. May be subclinical/asymptomatic; clinical infections in young pigs, usually self-limiting.⁶⁸⁶
Salmonella spp.	Rare in laboratory; more common in pet trade. Zoonotic.⁶⁸⁷
Other	guinea pigs can be experimentally infected with a number of bacteria pathogenic to humans including Mycobacterium tuberculosis, Coxiella burnetti, and Bacillus anthracis

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HAMSTERS

Hamsters: Order Rodentia, Suborder Myomorpha

Hamsters are rodents (order Rodentia) in the subfamily Cricetinae. Eighteen hamster species are distributed in the wild across North Africa, parts of Europe, and Asia.²⁶^,^91–94 Five species of hamsters in 4 different genera are used in research (Table 27), with golden (Syrian) hamsters (Mesocricetus auratus Waterhouse, 1839) represented most commonly and emphasized here. Although commercially available as “outbred” stock, all domesticated Syrian hamsters are thought to have descended from a single sibling pair captured in Syria in 1930.²⁶ Because of this evolutionary bottleneck, Syrian hamsters are expected to have limited genetic variability, although they exhibit some diversity in their major histocompatibility complex (MHC) repertoires.⁹⁵

Table 27.

Hamsters: Taxonomy, Genetics, Nomenclature, and Common Species²⁶^,⁹³^,⁹⁴^,^693–696

Genus and Species	Common Name(s)	Comments/Common Research Areas
Mesocricetus auratus (Waterhouse, 1839)	Golden (Syrian or teddy bear) hamster	Most common in research. Domesticated in 1930s with significant founder effect. Average lifespan 2–3 y. Carcinogenesis, cardiomyopathy, infectious disease, metabolic disease (T2DM, gallstone induction, atherosclerosis), and non-neoplastic respiratory disease (COPD, emphysema, pulmonary fibrosis).^94–96^,⁶⁹⁷
Phodopus sungorus (Pallas, 1773)	Striped desert (Siberian, Djungarian, winter white dwarf, or Russian dwarf) hamster	Research use beginning in 1960s. Average lifespan 1–2 y. Smaller than M auratus. Carcinogenesis, cytogenetics, diabetes mellitus, fat metabolism, circadian rhythm, photoperiodism, thermoregulation, reproduction and teratology (shortest reproductive cycle of any eutherian mammal).⁹²^,⁹³^,¹⁰⁴
Cricetulus griseus (Pallas, 1773)	Striped dwarf (Chinese) hamster	First domesticated in 1920s. Average lifespan 2.5–3 y. Cytogenetics, radiation effects, diabetes mellitus (type 1, insulin dependent, hereditary) and toxicology studies. Source of CHO cells.⁶⁹⁸
Cricetulus migratorius (Pallas, 1773)	Gray dwarf (Armenian, migratory grey, grey, or migratory) hamster	Average lifespan 1–3 y. Carcinogenesis, cytogenetics, and infectious disease.⁶⁹⁹
Cricetus cricetus (Linnaeus, 1758)	Common (black-bellied, European, or striped) hamster	Average lifespan 5 y; up to 8 y in wild. Carcinogenesis and chronobiology (hibernation, circadian rhythm, and circannual cycles).^700–702

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Syrian hamsters are larger than gerbils, stocky, with abundant loose skin. In contrast to gerbils, they have a very short tail, and the females are usually larger, stronger, and more aggressive than the males. Their cheek pouches are evaginations of oral mucosa that extend as far back as the scapula and are used to transport food, bedding material, and occasionally young. Hamsters have sebaceous scent glands, particularly well-developed in males, that play a role in territorial marking and mating. These are located on the flank in Syrian hamsters and on the ventral midline in other hamster species (also gerbils). Additional anatomic features of hamsters include large adrenal glands (especially in males) due to their prominent zona reticularis, 7 pairs of mammary glands, and water-conserving kidneys with an elongated single papilla. Hamsters tend to be crepuscular in the wild and nocturnal in the laboratory setting.⁹⁶ After weaning, hamsters prefer a solitary lifestyle, with females tolerating males only during estrus. They live individually in burrow systems that provide protection from predators and extreme climate conditions as well as sites for storing hoarded food. They are permissive hibernators that can enter short periods of hibernation in response to adverse environmental conditions, such as low temperature or decreased food availability.⁹⁷

Tables 28 and 29 summarize research-relevant features and non-neoplastic conditions (emphasis M auratus).²⁶^,⁹³ The cheek pouch is an immunologically privileged site where xenograft tumor transplants can survive. The hamster hepatobiliary and pancreatic duct system, as well as features of their induced tumors, are considered particularly relevant to humans.⁹⁴

Table 28.

Hamsters (M auratus): Anatomic and Physiologic Features²⁶^,⁷⁰³

System Organ/Tissue	Conditions/Phenotypes
Alimentary
Dentition	Elodont incisors, anelodont molars; dental formula: I1/1, C0/0, P0/0, M3/3 = 16
Cheek pouches	Highly distensible, immune privileged site; stratified squamous mucosa, devoid of glands.
Stomach	Glandular and non-glandular stomach; esophagus enters at junction
Antimicrobial sensitivity/ toxicity	Antimicrobial associated dysbiosis, diarrhea; particularly antibiotics active against gram positive flora; beta-lactams, lincosamides, aminoglycosides, and bacitracin are contraindicated.⁷⁰⁴
Cardiovascular	Heart: anomalous coronary arteries⁷⁰⁵ Heart: bicuspid semilunar valves; congenital, high incidence.⁷⁰²
ACE2	High level of sequence homology with human ACE2 relevant to SARS CoV2 susceptibility.⁷⁰⁶^,⁷⁰⁷ [P sungorus, C griseus ACE2 also have relevant sequence homology⁷⁰⁶]
Atherosclerosis	In susceptible lines eg, Bio F₁B⁶²¹
“Cardiomyopathy”	Cardiomyopathy, dilated (and hypertrophic) associated with delta-sarcoglycan-deficient muscular dystrophy due to autosomal recessive Sgcd mutation in Bio14.6 and derived lines (UMX7.1, TO-2, J2N-k etc).^708–712
Lipoprotein metabolism	Plasma/serum cholesterol is primarily in non HDL lipoproteins.⁶²¹
Integument	Flank glands. Modified pigmented sebaceous glands used for scent marking; more prominent in males, involved in conversion of testosterone to dihydrotestosterone. (In non-Syrian hamsters [eg, Djungarian] these are single and located on the ventral midline).
Nervous	Lissencephalic
Respiratory	4 right lung lobes + 1 left lung lobe⁷¹³
Urogenital/reproduction	⁷¹⁴ Gestation 15–18 d; litter size 4–12 pups; birth weight 2–3 g; eyes open 15 d; weaning 21 d.

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Table 29.

Hamsters (M auratus): Non-infectious Non-neoplastic Conditions²⁶^,⁹¹^,¹⁰⁰^,⁶⁹³^,⁶⁹⁸^,⁷⁰¹^,^715–718

System Organ/Tissue	Conditions
Multisystem	Amyloidosis. Common life-limiting disease; secondary (SAA), possibly non AA amyloid as well; kidney deposition can be extensive, and concurrent with chronic glomerulonephropathy (below) leading to enlarged or small pale kidneys with, renal failure, ascites; amyloid deposition occurs also in liver, spleen, adrenal, gut etc; earlier onset and higher frequency in females possibly due to higher serum amyloid P (SAP, also called female protein) in females; SAP is a component of all extracellular amyloid deposits.⁷¹⁹ Secondary atrial thrombi attributed to loss of antithrombin III through glomeruli.
	Polycystic disease. Limited reports of cysts in liver, epididymis, seminal vesicles, pancreas, endometrium; usually incidental (non-clinical); age-associated, and/or possibly congenital.⁷²⁰
Alimentary	Malocclusion and overgrowth of elodont incisors. Predisposes to cheek pouch impaction.⁷²¹
	Periodontal disease and dental caries. May progress to tooth root abscesses that emerge ventral or rostral to the eyes.⁷²²
	Bile duct hyperplasia in aged Chinese and Syrian hamsters, especially females. Sporadic, but prevalence up to 20% in some colonies. Periportal fibrosis and bile duct proliferation.⁶⁹⁸^,⁷²³
Cardiovascular Heart	Atrial thrombi in aged Syrian hamsters, earlier onset in females; left atrium most commonly involved; may cause left sided (dyspnea, hyperpnea, cyanosis) or right sided (subcutaneous edema) heart failure; associated with amyloidosis.^724–726
	Cardiomyopathy, dilated (and hypertrophic) associated with delta-sarcoglycan-deficient muscular dystrophy due to autosomal recessive Sgcd mutation; Bio14.6 and derived lines UMX7.1, TO-2, J2N-k etc; widespread cardiomyocyte necrosis with subsequent cardiomyocyte hypertrophy, cardiac failure and early death; skeletal muscle changes see muscular dystrophy below.⁷¹⁰^,⁷¹¹^,⁷¹²
Endocrine	Chinese hamsters: Diabetes mellitus, Type 1, insulin dependent; recessive inheritance; reduced pancreatic islet numbers; beta cell degeneration.⁶⁹⁸^,⁷²⁷^,⁷²⁸
	Cushing-like syndrome in aged Syrian hamsters. Alopecia, skin hyperpigmentation, polyuria, polydipsia, polyphagia, and elevated levels of serum cortisol and alkaline phosphatase (ALP); may be associated with adrenal cortical tumors, pituitary tumor.⁷²⁹
Musculoskeletal	Muscular dystrophy due to delta-sarcoglycan-deficiency in lines bearing Sgcd mutation; necrosis, mineralization, regeneration, fibrosis, fatty infiltration in skeletal muscles; early death attributed to cardiomyopathy (see above).^710–712
Nervous	Congenital/hereditary hydrocephalus. Clinically evident macrocephalic hydrocephalus is usually lethal before breeding age. Severe hydrocephalus can be found in clinically unremarkable animals.⁷³⁰
	Spontaneous hemorrhagic necrosis of CNS. Fatal disease in last trimester; stillborn or weak pups that are frequently cannibalized. Historical? May be induced with a vitamin E-deficient diet.⁷³¹^,⁷³²
Urogenital	Glomerulonephropathy (nephrosclerosis). Significant morbidity and mortality in aged Syrian, Siberian, and Chinese hamsters, especially females. Resembles arteriolar nephrosclerosis in humans.⁹³^,¹⁰⁵^,⁶⁹⁸^,⁷²⁶ Renal amyloidosis can be concurrent, and is an important differential diagnosis for chronic renal disease in hamsters.
	Ovarian cysts. Age-associated; often incidental, even when large. Genetic predisposition likely.⁹³^,⁷³³
	Cannibalism. Primary cause of preweaning mortality. Contributing factors include group housing females, first litter, environmental noise/disturbances, inadequate nesting material, and lack of food or water.⁷³⁴

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Table 30 summarizes the more commonly reported neoplastic conditions (emphasis M auratus). The frequency of spontaneous tumors in hamsters is relatively high in certain species or stocks, particularly in animals over 2 years of age.^26,^98–101 In Syrian hamsters, the more common tumors include adrenocortical adenoma, hematopoietic tumors (lymphoma), and tumors of the gastrointestinal tract.²⁶^,⁹¹^,⁹⁸^,⁹⁹^,¹⁰²^,¹⁰³ Skin tumors are reported more frequently in Siberian hamsters than in Syrian hamsters and include squamous cell carcinoma, papilloma, fibrosarcoma, and atypical fibroma originating from skin ganglion cell–like cells.⁹²^,¹⁰⁴ Mammary tumors are also common in Siberian hamsters and tend to develop at a younger age compared with other tumors (eg, skin, lung, thyroid).⁹³^,⁹⁸^,¹⁰⁵ In European or black bellied hamsters (Cricetus cricetus (Linnaeus, 1758)), thymomas are among the few spontaneous tumors reported. ¹⁰⁶ Tables 31–33 summarize infectious agents that may be identified or may cause disease in hamsters.

Table 30.

Hamsters (M auratus): Neoplastic Conditions²⁶^,⁶⁹⁷^,⁷⁰²^,⁷¹⁶^,⁷³⁵^,⁷³⁶

System Organ/Tissue	Neoplastic Conditions
Endocrine	Adrenal cortical adenomas, most common tumor
Hematolymphoid	Lymphoma, multicentric
	Epitheliotropic T cell lymphoma (mycosis fungoides)
Integument	Mammary tumors in Djungarian (Siberian) hamsters
	Androgen-dependent atypical dermal fibromas of male Djungarian hamsters
Urogenital	Endometrial adenocarcinomas in aged Chinese hamsters

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Table 31.

Hamsters (M auratus): Viruses²⁶^,³²^,⁹¹^,⁶⁹³^,⁷¹⁵^,⁷³⁷^,⁷³⁸^,³⁹,⁹

Family and Genus	Agent	Comments
Polyomaviridae, Alphapolyomavirus	Mesocricetus auratus polyomavirus 1, hamster polyomavirus	Highly transmissible virus of Syrian hamsters. Spread via urine. Trichoepitheliomas develop in endemically infected colonies or when adults are infected. Causes multicentric lymphoma in naive young hamsters.⁷³⁹^,⁷⁴⁰
Arenaviridae, Mammarenavirus	LCMV	Syrian hamsters implicated as main source of zoonotic infections. Spread by infected saliva or urine via oronasal route or skin abrasions. Disease depends on age, strain and dose of virus, route of infection. Can be asymptomatic or see chronic wasting with vasculitis in multiple tissues.¹⁰⁰^,⁷⁴¹
Parvoviridae, unassigned	Hamster parvovirus	Subclinical in weanling and adult hamsters, but fetal or neonatal Syrian hamsters may have severe - lethal disease. Findings include incisor aplasia/discoloration/malformation, facial bone deformities, diarrhea, ataxia, stunted growth, domed calvaria, cerebellar hypoplasia, and multiorgan hemorrhage.⁷⁴²^,⁷⁴³
Paramyxoviridae, Respirovirus	Sendai virus	Rare, usually subclinical. Can cause mortality in newborn Syrian and Chinese hamsters. Lesions (if present) are in upper and lower respiratory tract.⁷⁴⁴

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Table 33.

Hamsters (M auratus): Eukaryotes: Fungi, Protists, Metazoan Parasites ²⁶^,³²^,⁹¹^,⁴⁴²^,⁶⁹³^,⁷¹⁵^,⁷³⁷^,⁷⁴⁵^,⁷⁵⁷

Protists	Comments
Cryptosporidium muris, C parvum	Small intestinal villus attenuation and crypt hyperplasia in aged or immune compromised.⁷⁵⁸
Giardia muris	Common but usually subclinical. Clinical disease in weanlings or aged. Chronic emaciation and diarrhea, with diffuse mural thickening of small and large intestine.⁷⁵⁹
Spironucleus muris	Common intestinal flagellate, usually subclinical⁷⁶⁰
Intestinal nematodes
Syphacia spp., Aspiculuris tetraptera, Dentostomella translucida	Syrian hamsters are susceptible to pinworms of other rodent species, usually subclinical.^761–763
Cestodes
Hymenolepis diminuta, Rodentolepis microstoma, R nana	Clinical signs possible with heavy infestation. H diminuta may cause catarrhal enteritis or chronic gastroenteritis and enterocolitis. H nana, associated with intestinal impaction and obstruction.¹⁰⁰^,⁷⁶⁴^,⁷⁶⁵
Arthropods
Demodex aurati, D criceti	Relatively common, usually subclinical in Syrian hamsters. Alopecia over back, neck and hindquarters with dry, scaling, non-pruritic skin.⁹³^,⁷⁶⁶^,⁷⁶⁷
Notoedres muris	Mange mite. Burrows in stratum corneum, produces scabby lesions on ears, face, feet and perianal skin.⁷⁶⁸

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Table 32.

Hamsters (M auratus): Bacteria²⁶^,³²^,⁹¹^,⁶⁹³^,⁷¹⁵^,⁷³⁷^,⁷⁴⁵^,⁶⁹⁷^,⁷¹,⁸

Genus and Species	Comments
Campylobacter jejuni	Usually asymptomatic, may be associated with enteritis and diarrhea. Zoonotic.⁷⁴⁶^,⁷⁴⁷
Clostridioides difficile	Highly susceptible to fatal disease. Dysbiosis due to disruption of intestinal microflora results in enterotoxemia. Antibiotics, stress, experimental manipulations, and high environmental contamination with spores have been associated with outbreaks. Sudden death, acute liquid diarrhea. Necrosis and hemorrhage of the cecum and colon with acute inflammation.⁷⁴⁶^,⁷⁴⁸^,⁷⁴⁹
Clostridium piliforme	Tyzzer’s disease. Epizootics in Syrian hamsters, most often weanlings. ⁷⁵⁰
Escherichia coli	Enteroinvasive and enteropathogenic strains associated with diarrhea and enteritis. Colitis and typhlitis also possible.⁷⁴⁶^,⁷⁵¹
Helicobacter spp.	Various species identified in hamsters, including H aurati, H cholecystus, H hepaticus, H bilis, and H typhlonicus; often subclinical; may affect gastrointestinal tract, liver, or gallbladder. Chronic helicobacter-associated gastritis in hamsters, may progress to carcinoma, and typhlocolitis can develop dysplastic changes.⁷⁵²^,⁷⁵³
Lawsonia intracellularis	Proliferative ileitis. Common and important disease in Syrian hamsters, high mortality in young (3–10 wk). Fetid watery diarrhea, anorexia, emaciation, and rectal prolapse; death a week after onset. Marked thickening of ileal wall with excessive epithelial hyperplasia, necrosis, and inflammation. Peritonitis also possible.¹⁰⁰^,⁷⁵⁴^,⁷⁵⁵
Salmonella spp.	Syrian hamsters are very susceptible. Epizootic with acute course and death. Salmonella enteritidis or S typhimurium. Main lesion is a septic phlebothrombosis in the lungs. Necrotizing foci frequently in the liver and spleen; can be associated with diarrhea. Zoonotic.⁷⁴⁶^,⁷⁵⁶
Staphylococcus aureus	Ubiquitous due to direct contact with humans. Abscesses and wound infections. Can be associated with suppurative submandibular or cervical lymphadenitis.¹⁰⁰

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NAKED MOLE-RATS

Naked mole rat: Order Rodentia, Suborder Hystricomorpha; Heterocephalus glaber

Naked mole-rats (NMRs; Heterocephalus glaber Rüppell, 1842) represent the only species in the genus Heterocephalus (family Bathyergidae). This burrowing, eusocial, and long-lived rodent is native to Eastern Africa, although captive colonies are found at many zoos and research institutions worldwide. NMRs are increasingly utilized in biomedical research as models for aging and carcinogenesis studies due to their unique physiology, resistance to cancer, and exceptionally long lifespan. NMRs are highly adapted to harsh subterranean living conditions and have many unusual anatomic and physiologic features (Table 34). NMRs and Damaraland mole-rats (Fukomys damarensis) are the only eusocial mammal species, further necessitating species-specific husbandry requirements.¹⁰⁷ In both free-ranging and managed captive colonies, the eusocial system typically results in a single breeding queen and a small group of breeding males, and the remainder of the colony members are workers.¹⁰⁸ Workers are sexually monomorphic and reproductively suppressed through hormonal cues. NMRs are inherently xenophobic and will kill burrow invaders, including other NMRs.¹⁰⁹ When a queen dies, violent upheavals ensue until a subsequent queen emerges, resulting in conspecific aggression, trauma, and death.¹¹⁰^,¹¹¹

Table 34.

Naked Mole-Rats: Anatomic and Physiologic Features⁶⁵^,¹²¹

System	Comments
General	Longest-lived rodent known,⁷⁶⁹ with negligible senescence,⁷⁷⁰ and sustained healthspan¹²²; genome stability and genes of long lifespan⁷⁷¹
	Sustained high levels of neuregulin-1⁷⁷²
	Oxidative stress tolerance⁷⁷³
	Cell injury resistance and repair related to transcription factor Nrf2⁷⁷⁴^,⁷⁷⁵
	Maintenance of juvenile traits (pedomorphy)⁷⁷⁶
	Cancer resistance. Multiple suggested mechanisms: contact inhibition due to high molecular weight hyaluronan¹¹⁶; decreased tumorigenicity of fibroblasts in vitro¹²⁸; Cdk2na (ARF) regulation and disruption of Eras decrease tumorigenicity of iPSCs⁷⁷⁷; and downregulation of Akt1 and Pik3ca⁷⁷⁸
Alimentary	Maxillary and mandibular incisors are external to the mouth
	Hindgut fermentation; large cecum with complex microbiota acts as heat sink⁷⁷⁹
	Cecotrophy¹²⁰
	Acquire all necessary water through diet
	No dietary requirement for vitamin D
Hematolymphoid	Extramedullary hematopoiesis common in spleen¹²⁶
	Thymus often present in adults
	High myeloid: lymphoid cell ratio⁷⁸⁰^,⁷⁸¹
	Lack of canonical NK cells⁷⁸⁰
	Robust phagocytosis and decreased apoptosis of macrophages⁷⁸²
	High RBC, HCT; high O2 affinity hemoglobin and myoglobin compared with mice, rats⁷⁸³^,⁷⁸⁴
Integument	Lack pelage; have facial vibrissae and tactile hairs along the body
	Thick epidermis; lack sweat glands; degenerate sebaceous glands
	Skin is very pliable due to high levels of high molecular weight hyaluronan ¹¹⁶
Musculoskeletal	Large broad heads with 25% total body muscle mass in masseter muscles.
	Body weight: 25–110 g in adults (average: 35 g).
	Largest colony member is the queen. Once established, new queen will grow rapidly in size, folliculogenesis commences.
Nervous	Lissencephalic⁷⁸⁵
	Neuroplasticity and independence of photoendocrine systems¹¹²
	Extreme tolerance to cerebral hypoxia⁷⁸⁶^,⁷⁸⁷
	Lack of cutaneous pain sensation with chemical stimuli and inflammation ⁷⁸⁸
Cardiovascular	Sustained cardiovascular health⁷⁸⁹
	Normal heart to body mass ratio 0.4%
Special senses
Auditory	Lack external ear pinnae; vestigial middle ear
Olfactory	Tolerance to ammonia fumes¹¹⁸ Small vomeronasal organ
Visual	Small, primitive eyes with rod-dominated retina
Respiratory	Primitive lungs with ectatic distal airways¹²⁶
Urogenital	No sexual dimorphism in workers. Hormonally suppressed with underdeveloped inactive gonads.
	Worker males normally have rare seminiferous tubules amongst abundant interstitial tissue; should not be misinterpreted as interstitial (Leydig) cell tumor.
	Unipapillate kidneys

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NMRs are stenothermic, regulating body temperature over a narrow range of ambient conditions, and thus require specific environmental temperature and humidity ranges in managed care.^112–114 Their large heads are adapted for excavating extensive burrow systems, with masseter muscles representing about 25% of their total body muscle mass. Their incisors are external to the mouth, enabling the lips to close while using the incisor teeth to dig through substrate. NMRs have long tubular bodies with short strong legs and no other external appendages, as ear pinnae are absent and males have internal testes. NMRs are not completely hairless and have facial vibrissae and tactile hairs along their bodies, enabling navigation in almost complete darkness.¹¹⁵ The epidermal layer is thick and devoid of sweat glands, and the skin very pliable, attributed in part to abundant high–molecular-weight hyaluronan in the epidermis and dermis, which allows them to pass other colony members in tight burrow tunnels.¹¹⁶ NMRs have small eyes and poor vision, relying on tactile hairs and olfaction for finding food and recognizing conspecifics.¹¹⁷ NMRs have been shown to have extreme tolerance to ammonia fumes; nevertheless, the olfactory system appears able to distinguish odors.¹¹⁸ The NMR vomeronasal organ is an order of magnitude smaller than that of mice, suggesting that pheromone signaling does not play a key role in reproductive suppression.¹¹⁹ NMRs are hindgut-fermenting herbivores with a simple monogastric stomach, a short small intestine, and a large cecum populated by a heterogenous population of microbes critical to efficient digestion.¹²⁰ Adult and weanling NMRs ingest cecotrophs for hydration and also to establish and/or maintain the appropriate cecal microflora.¹²⁰ Free-ranging NMRs consume tubers, geophytes, and corms of certain plants; captive diets aim to provide high levels of fiber, including fresh vegetables, particularly sweet potato, and small amounts of fruit and baby cereal.¹²¹

NMRs have an extremely long health span compared with other rodents and experience minimal clinical disease even in advanced age.¹²² Clinical pathology data on NMRs is scarce; thus, organ function assessments and clinicopathologic correlations to gross and microscopic lesions are not possible for many post-mortem cases. Nevertheless, increased surveillance of captive NMR populations has highlighted potential husbandry-related diseases and prompted new questions about the unique physiology, resilience, and proper captive management of this species. Standardized husbandry guidelines have been established for research and zoological settings to mitigate environmental, social, and nutritional causes of disease and to promote welfare and reproductive success.¹²¹ The eusocial structure and xenophobic nature of NMRs predispose to stress, conspecific trauma, and neonatal neglect, all of which represent key factors of morbidity and mortality in captive populations.¹¹⁴^,¹²³ Furthermore, individual colonies may vary in health and disease profiles due to genetic influences.¹²⁴ Recent studies of managed populations have identified several spontaneous conditions that should be considered in long-term studies involving NMR (Table 35). Neoplasia is rare in this species; however, reports of thorough post-mortem examinations to assess for pre-neoplastic and microscopic neoplastic processes are limited (Table 36).^125–127 Compared with other rodent species, NMRs seem far less susceptible to infectious diseases, with limited reports of infectious conditions (Table 37).¹²⁸^,¹²⁹ Comprehensive post-mortem examinations and continued surveillance for spontaneous diseases are critical to better understand factors affecting NMR health and welfare in both research and zoo populations.

Table 35.

Naked Mole-Rats: Non-infectious Non-neoplastic Conditions⁶⁵^,¹²⁶^,¹²⁹

System Organ/Tissue	Condition; Comments
Multisystem	Soft tissue mineralization (calcinosis cutis) or surrounding phalangeal joints (circumscripta), has been associated with (dietary) vitamin D toxicity⁷⁹⁰^,¹²⁶
	Transponder-related injuries
Alimentary
Teeth	Malocclusion, incisor overgrowth.
Esophagus, forestomach	Excessive (retained) keratin layers with prominent bacteria and fungi is associated with hyporexia or inanition
Intestines	“Bloat” (intestinal gas) can be common in neonates and weanlings.
	Dysbiosis; may lead to Clostridia spp. overgrowth and enteritis
	Necrotizing typhlocolitis with protozoal (ciliate) invasion
Liver	Hemosiderosis; can be severe in aged individuals; diet considered an important factor.
Liver	Hepatocellular megalocytosis and binucleation; incidental, increases with age (polyploidy is expected with ageing in various species).
Cardiovascular
Heart	Cardiomyocyte megalocytosis and lipofuscinosis common in aged individuals
	Lymphocytic myocarditis is rarely reported; unknown etiology
	Myocardial mineralization rare.
Arteries	Subintimal mineralization; Arteriosclerosis, thickened (proliferative) and/or degenerative (hyaline) changes of tunica media.
	Euthanasia solutions cause loss of detail in blood vessels.
Endocrine
Adrenal gland	Nodular cortical hyperplasia
	Cortical cell lipofuscinosis
Pancreas	Interstitial fibrosis
Integument	Conspecific trauma (fighting) cohoused animals; wounds can be severe and result in secondary infections and embolic spread to multiple tissues.
Musculoskeletal
Bone	Fractures due to conspecific trauma or habitat entrapment; amputations
Vertebra	Intervertebral disc disease and spondylosis
Nervous	Neurodegeneration, neuronal lipofuscinosis, and corpora amylacea in aged brain
Respiratory	Cartilage mineralization in trachea
Urogenital
Kidney	Renal tubule mineralization, very common
	Chronic progressive nephropathy; spectrum of lesions affecting the entire nephron, similar to disease found in old rats⁷⁹¹
Uterus	Queens may develop pyometra and endometritis

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Table 36.

Naked Mole-Rats: Neoplastic Conditions

System Organ/Tissue	Condition; Comments
Alimentary
Esophagus	Adenocarcinoma¹²⁷
Liver	Hepatocellular carcinoma¹²⁷
Endocrine
Stomach	Carcinoid¹²⁵
Chest/mediastinum	Neuroendocrine tumor (thyroid origin suspected)
Hemolymphoid
Multicentric	Lymphoma¹²⁷
Spleen and thymus	Lymphoproliferation (pre-neoplastic)¹²⁵
Integument
Mammary gland	Adenocarcinoma
Skin	Hemangioma¹²⁷
Subcutis (unknown gland)	Adenocarcinoma¹²⁵
Musculoskeletal
Vertebrae (sacrum)	Chordoma⁷⁹²
Urogenital
Kidney	Nephroblastoma (Wilm’s tumor)¹²⁷
	Atypical tubule profiles/adenoma¹²⁵
Uterus	Endometrial stromal tumor

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Table 37.

Naked Mole Rats: Infectious Agents¹²⁹^,¹²⁶^,⁷⁹³

Agent	Comments
Viruses	Not reported (Human Herpes Simplex Virus 1 Experimental)
Bacteria	Abscesses associated with skin wounds; Pasteurella, Pseudomonas, Staphylococcus implicated or isolated. Clostridial enteritis and dysbiosis (may be accompanied by mucosal invasion by ciliates).
Fungi	Yeasts, consistent with Candida spp in esophagus, forestomach, stomach
Protists	Ciliates consistent with Balantidium spp, and flagellates noted in intestine, are considered to be commensal, but may invade mucosa in compromised bowel.

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RABBITS

Rabbits: Order Lagomorpha, Family Leporidae, Oryctolagus cuniculus (Linnaeus, 1758)

All rabbits are in the Lagomorpha family Leporidae. The Eastern cottontail (Sylvilagus floridanus [Allen, 1890]), the ubiquitous wild rabbits populating suburban and rural America, and other Sylvilagus and Lepus species are uncommon in laboratory research but may serve as asymptomatic or clinical reservoirs for infectious agents. The domesticated European rabbit (Oryctolagus cuniculus [Linnaeus, 1758]) has been used in research for over 150 years, famously including Anichkov’s work on atherosclerosis and Pasteur’s attenuation of rabies virus for vaccination by serial passage in rabbits.²^,¹³⁰ There are more than 100 breeds of O cuniculus, with New Zealand White stocks being the most common in research and with the most available historical data. Rabbit size facilitates interventional studies, such as orthopedic and thoracic surgeries, that are impractical in smaller animals. They are generally docile, with fewer associated zoonotic, regulatory, financial, and ethical concerns than non-human primates.

The anatomic and physiologic features of the eyes, respiratory tract, reproductive tract, and cardiac conduction system of rabbits are favorable for certain areas of basic research and pre-clinical testing. The rabbit propensity to develop high-affinity antibodies, even to carbohydrates and other poorly antigenic substances, has made rabbit-derived antibodies useful in research and even human therapeutics (eg, rabbit anti-thymocyte globulin), and generation of rabbit monoclonal antibodies has become feasible.¹³¹ Experimental infection with Sylvilagus floridanus papillomavirus-1 (aka Shope papillomavirus) made rabbits, at the time, the only practical animal model available for papillomavirus research, including the development of human papillomavirus vaccines. Although inbred (including Watanabe heritable hyperlipidemic) and transgenic rabbits are uncommon compared with mice and rats, CRISPR/Cas9 gene editing has made genetically modified rabbits more feasible.^132–134 Tables 38–41 summarize research relevant features and conditions in laboratory rabbits. Tables 42–44 summarize infectious agents that may be identified or may cause disease in rabbits.

Table 39.

Rabbits: Anatomic and Physiologic Features²⁶^,¹³³^,⁸⁰²^–⁸⁰⁸

System	Comments
Alimentary	Do not vomit
Calcium absorption	Calcium absorption proportional to diet, not regulated by vitamin D
Cecotrophy	Mucus-covered soft feces (night feces) consumed directly from anus in early morning under control of adrenals and fusus coli.⁸⁰⁹ These provide B complex vitamins and proteins; inhibited by Elizabethan collars and similar devices.
Dentition/Teeth	Dental formula I2/1, C0/0, P3/2, M2-3/3. All teeth elodont; 2 pairs of maxillary incisors oriented rostral-caudal; caudal pair (peg teeth) occlude with mandibular incisors.
Hindgut fermentation	Hindgut fermentation; relatively large cecum (40% of ingesta) and colon with rapid gut transit times; rapid post-mortem autolysis.⁸¹⁰
Cardiovascular	⁸¹¹
Aorta and great vessels	Only 2 branches from aortic arch; (1) brachiocephalic trunk (innominate artery) giving rise to right subclavian and right and left common carotid arteries; and (2) left subclavian artery.⁸¹²
Blood collection	Marginal ear vein for intravenous injection; central auricular artery for blood collection; thrombi can lead to necrosis of ear pinnae.
Heart	Small heart weight: body weight (approximately 0.256); left: right ventricular ratio (3.66); right atrioventricular valve is bicuspid.
Hematolymphoid
Bone marrow and B cells	Bone marrow B cell lymphopoiesis ends at an early age; marrow source naïve B cells seed the appendix for further maturation. Rabbit ability to generate high affinity antibodies to poorly antigenic epitopes has been useful in antibody production.⁸¹³
GALT	Abundant GALT (gut associated lymphoid tissues) can be >50% of lymphoid mass in adult; includes sacculus rotundus, cecal tonsil, and appendix; appendix is major site of B lymphocyte somatic diversification, requires microflora.⁸¹⁴^,⁸¹³
Leukogram (WBC)	Lymphocytes are predominant circulating leukocyte. Major rabbit granulocyte is called heterophil because of staining, but functionally similar to neutrophil. Acute infections may not result in leukocytosis.^815–817
Spleen	Small spleen. Accessory spleens are common.
Nervous	Lissencephalic brain.⁸¹⁸^,⁸¹⁹
Musculoskeletal	High skeletal muscle to bone mass ratio; prone to skeletal fractures.
Respiratory	Obligate nose breathers.
Lung	Three lobes in left lung and 4 lobes in right. No respiratory bronchioles.
Trachea	No tracheal/bronchial submucosal glands.⁸²⁰
Special senses	⁸²¹
Urogenital/reproductive	Induced ovulation; pseudopregnancy common. Gestation 30–32 d; 4–10 kits/litter, up to 4–7 L/y; nesting important in maternal care and kit survival.
Kidneys	Unipapillate kidneys; insensitive to loop diuretics (eg, furosemide); urine is major route of calcium and magnesium excretion (FE_Ca = 45%), therefore urine is normally turbid with crystals or sediment.
Ovary	Prominent ovarian interstitial glands; should not be misdiagnosed as luteinization or luteoma.⁸²²
Placenta	Discoid labyrinthine hemochorial placentation
Uterus	Duplex uterus; 2 separate uterine horns, each with cervix opening into vagina; no uterine body.
Vagina	Simple columnar mucinous vaginal mucosa; only stratified squamous near the vestibule. No estrus cycle changes.
Males	No nipples. Penis and prepuce are caudal to the scrotum.⁸²³^,⁸²⁴

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Table 42.

Rabbits: Viruses²⁶^,⁴⁰⁰^,⁸²⁹^,⁸⁷³^,⁸⁷⁴

Family, Genus	Agent	Comments
Caliciviridae, Lagovirus	Rabbit hemorrhagic disease virus (RHDV)	Sudden death, epistaxis, pulmonary hemorrhage, acute hepatocellular necrosis, disseminated intravascular coagulation.⁸⁷⁵ RHDV2 epizootic in Sylvilagus and Lepus.
Caliciviridae, Lagovirus	Michigan rabbit calicivirus	Genetically distinct from, but clinically similar to RHDV; single outbreak in 2001.⁸⁷⁶
Reoviridae, Rotavirus	Rotavirus A	Enterocyte loss from small intestinal villous tips, with villous atrophy, blunting and fusion. Most common in young kits.
Herpesviridae, Simplexvirus	Herpes simplex virus	Acute necrotizing (meningo)encephalitis with large herpetic intranuclear inclusions. Anthroponosis from human.⁸⁷⁷
Herpesviridae, Simplexvirus	Leporid herpesvirus 4	Acute suppurative conjunctivitis, pulmonary and gastrointestinal hemorrhages, splenic necrosis, herpetic intranuclear inclusions and syncytia. Clinical resemblance to myxomatosis. Natural infections only in rabbits housed outdoors in Canada and Alaska.⁸⁷⁸
Poxviridae, Leporipoxvirus	Myxoma virus	High morbidity and mortality with coalescing wet (myxomatous) necrotizing subcutaneous lesions (particularly affecting head) and acute conjunctivitis. Arthropod vectors and fomite transmission. Sylvilagus spp. are asymptomatic wildlife reservoir.
Poxviridae, Leporipoxvirus	Rabbit (Shope) fibroma virus	Solid fibrotic subcutaneous nodules on head and legs; typical pox intracytoplasmic inclusions in atypical fibroblasts; lesions spontaneously regress. Transmission by direct contact and arthropods. Sylvilagus spp. are natural hosts.⁸⁶³
Poxviridae, Orthopoxvirus	“Rabbit pox virus”	Cutaneous pock lesions with proliferative margin and necrotic center; considered likely to be rabbit-adapted vaccinia. Experimental model for smallpox.
Papillomaviridae, Kappapapillomavirus	Sylvilagus floridanus papillomavirus-1 (cottontail rabbit PV [CRPV] or Shope PV)	Sylvilagus spp. are natural hosts; rare spontaneous disease; experimental infection of O. cuniculus to model human papillomavirus, approximately 25% progress to invasive squamous cells carcinoma.⁸⁷⁹ VX2 and VX7 carcinoma cell lines were established from carcinomas induced by SPV in domestic rabbits c1940.⁸⁸⁰
Papillomaviridae, Kappapapillomavirus	Oryctolagus cuniculus papillomavirus-1	White fleshy papillomas on ventral tongue (oral papillomatosis); self-limiting, usually in young animals.⁸⁸¹
Herpesviridae, Rhadinovirus	Leporid herpesvirus 1 (herpes cuniculi or virus III)	Apathogenic in O cuniculus, but can cause subclinical infections, contaminate cell cultures, or cause disease in other species.
	Leporid herpesvirus 2
	Leporid herpesvirus 3 (herpes sylvilagus virus)
Polyomaviridae unclassified	Rabbit kidney vacuolating virus
Paramyxoviridae, Respirovirus	Sendai virus	Apathogenic in O cuniculus, can cause subclinical infections or disease in other species.
Hepeviridae, Orthohepevirus	Hepatitis E virus	Apathogenic in O cuniculus; zoonotic⁸⁸²^,⁸⁸³

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Table 43.

Rabbits: Bacteria²⁶^,⁸²⁹^,⁸⁸⁴

Agent	Comments
Pasteurella multocida capsular type A or D	Snuffles. Suppurative inflammation or abscessation of upper/lower respiratory tract, genital tract, central nervous system, middle/inner ear, subcutis, eye, joints; also chronic atrophic rhinitis. Historically probably the most clinically significant infectious disease of rabbits, but uncommon in modern laboratory facilities. Vertical transmission and asymptomatic carriers. Zoonotic.
Bordetella bronchiseptica	Suppurative rhinitis and bronchopneumonia, milder than P multocida, may be subclinical. Co-infections with P multocida or Pneumocystis oryctolagi.
Clostridium spiroforme (C perfringens, Clostridioides difficile)	Necrotizing and hemorrhagic typhlitis (+/−colitis) with edema and loss of crypt and surface epithelium; coiled gram positive (beads on a string) bacteria (C spiroforme) are numerous in fecal smears; ‘normal’ flora; disease results from dysbiosis secondary to low roughage/high energy diets, stress and/or antibiotics, causing enterotoxemia with acute anorexia, diarrhea, dehydration, and depression; frequent mortality without early aggressive intervention.⁸⁸⁵
Clostridium piliforme	Tyzzer’s disease. Necrosis with intracellular stacks of straight filamentous gram negative bacteria in liver, cecum, and/or heart.
Pseudomonas aeruginosa	Blue fur disease. Moist dermatitis of the dewlap/neck; staining of the fur by bacterial pyocyanin. Characteristic smell.
Lawsonia intracellularis	Proliferative crypt epithelium with lack of goblet cells; argyrophilic bacteria in enterocyte cytoplasm.⁸⁸⁶^,⁸⁸⁷
Filobacterium rodentium	Basophilic and argyrophilic bacteria within and parallel to cilia; peribronchiolar lymphoid cuffing. Subclinical infections common. Inter-species transmission to rats and mice is controversial.
Staphylococcus aureus	Embolic suppurative inflammation or abscessation in the respiratory tract, genital tract, central nervous system, middle/inner ear, subcutis. Gangrenous mastitis (blue bag) in nursing does. Generalized septicemia in newborn or nursing kits. Opportunistic infection of pododermatitis lesions, indwelling medical devices. Zoonotic.
Treponema paraluiscuniculi	Rabbit syphilis. Ulcerative lesions of the penis/prepuce, vulva/vagina, and nares/muzzle; lymphohistiocytic infiltrates and argyrophilic spirochetes. Venereal transmission. No systemic spread (unlike human syphilis). Not zoonotic, largely eliminated from research colonies.

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Table 38.

Rabbits: Taxonomy, Genetics, Nomenclature, and Common Strains/Stocks²⁶^,^794–798

Strain or Stock	Comments
New Zealand White (:NZW^*)	Albino. Most common in research.
Dutch Belted (:DB)	Smaller body size than NZW, melanin pigmentation (non-albino)⁷⁹⁹
Watanabe Heritable Hyperlipidemic (WHHL/Kbe)	Developed at Kobe University in 1973. Spontaneous in-frame 12 bp deletion in low density lipoprotein receptor (LDLR) gene, functional inactivation; model for familial hypercholesterolemia with elevated total cholesterol (500–900 mg/dL), LDLs, and triglycerides and reduced HDLs. ⁸⁰⁰^,⁸⁰¹ WHHLMI/Kusm (myocardial infarction) substrain.
Audiogenic (EIII/JC)	Audiogenic seizures (ep/ep). Derived from parent III/J strain at the Jackson Laboratory by Fox in 1961, then to NCI

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^#‘/’ After strain/root abbreviation indicates inbred and is followed by the source laboratory code.

^*‘:’ Before stock abbreviation indicates outbred and is preceded by the source laboratory code.

Table 40.

Rabbits: Non-infectious Non-neoplastic Conditions²⁶^,⁷⁹⁷^,⁸⁰²^,⁸²⁵^–⁸³¹^,⁸³²

System Organ/Tissue	Condition; Comments
Multisystemic	Soft tissue mineralization (eg, aortic media); vitamin D toxicity or unbalanced dietary calcium, phosphorus, or magnesium levels.
Alimentary	⁸³³
Teeth	Incisor malocclusion and overgrowth, associated with mandibular prognathism, which is a heritable trait; elodont molars also can over grow.
Stomach	Trichobezoar (hairball); low fiber diet, lack of enrichment, stereotypy; can be incidental.
	Gastric ulcer. Stress or NSAIDs; may bleed.⁸³⁴
Intestines	Mucoid enteropathy. High energy/low roughage (fiber) diets, stress. Dysbiosis with acidosis of cecal contents; most common in recently weaned kits. Production of copious clear or feces-stained mucus; florid goblet cell hyperplasia/metaplasia in colon with minimal inflammation. ⁸³⁵
Liver	Hepatic lipidosis. Obesity, stress, pregnancy, with negative energy balance; may occur focally with liver lobe torsion.
Cardiovascular
Heart	Xylazine and detomidine cardiotoxicity. Cardiomyocyte loss and fibrous replacement⁸³⁶^,⁸³⁷
	Euthanasia solutions cause loss of detail in blood vessels (especially pulmonary arteries) and perivascular tissues with hypereosinophilia and fluid exudation; occurs when label dose is exceeded.⁸³⁸
Endocrine
Adrenal gland	Hyperplastic adrenal cortical nodules; nodules of well-differentiated cortical cells, usually encapsulated, near or next to the adrenal gland; incidental.
Parathyroid gland	Kursteiner’s cysts; developmental; variably sized cyst within or adjacent to parathyroid with pale proteinaceous fluid contents and single cuboidal ciliated epithelial lining; incidental.
Pituitary	Rathke’s pouch cysts; developmental origins; variably sized cyst between pars intermedia and pars distalis with similar features of Kursteiner’s cyst; incidental.
Integument
Skin	Conspecific trauma (fighting). Lacerations (bites), particularly of the genitals or ear pinna (including amputations); often between adult bucks; may occur when does reject kits.
	Pododermatitis (sore hocks). Unclean cages, sharp flooring surfaces, inadequate drainage of wastes; ulcerative skin lesions over the plantar tarsals and metatarsals; Staphylococcus aureus may be cultured but is likely opportunistic.
Musculoskeletal
	Hip dysplasia. Inadequate nesting boxes; shallow femoral acetabulum with flattened femoral head; femur may luxate; secondary arthritis may be present.⁸³⁹
	Fractures. Inadequate restraint or caging defects; spinal (L4-L7) and tibial fractures most common; spinal fractures may result in paraplegia or paraparesis.⁸⁴⁰^,⁸⁴¹
	Splayleg. Polygenic; inability to adduct all limbs.
Nervous
Sciatic nerve	Iatrogenic injury from intramuscular injections in caudal thigh (particularly ketamine). Necrosis, hemorrhage, and histiocytic inflammation of the nerve and tissues; Wallerian degeneration; self-mutilation of ipsilateral digits. Injections should be given in the dorsal lumbar (epaxial) muscles.⁸⁴²^,⁸⁴³
Brain	Hydrocephalus. Autosomal recessive (hy/hy); vitamin A deficiency or toxicity. Dilated lateral ventricles with variable doming of the dorsal skull.⁸⁴⁴
Respiratory
Lung	Spontaneous emphysema (destruction of alveolar septa). Age-related.⁶⁴⁹^,⁸³⁸
Special senses	⁸³³ ^, ⁸⁴⁵ ^, ⁸⁴⁶
Eye	Glaucoma. Autosomal recessive with incomplete penetrance in NZW (bu/bu); malformation of the drainage angle (goniodysgenesis); buphthalmia. Candidate genes include MYOC and PITX1.⁸⁴⁷
	Cataract. Autosomal dominant with incomplete penetrance or autosomal recessive.⁸⁴⁸
Urogenital	^849–853
Uterus	Endometrial venous aneurysms. Usually nonpregnant multiparous does; aneurysmal dilatation of endometrial vein(s), may form an intraluminal mass; may cause vaginal bleeding.⁸⁵⁴
Perineum	Urine scald (hutch burn). Poor husbandry and cage hygiene; moist exudative dermatitis of ventral abdomen.
Urine	Red urine due to excretion of dietary porphyrins may be mistaken for hematuria/hemoglobinuria/myoglobinuria.
Bladder/kidney	Urolithiasis (stones). Dietary; usually soft stones composed of calcium carbonate and triple magnesium phosphate.
Kidney	Bowman's space cysts. Idiopathic, genetic.⁸⁵⁵
	Tiletamine nephrotoxicity.⁸⁵⁶

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Table 41.

Rabbits: Neoplastic Conditions²⁶^,⁸²⁹^,⁸³¹^,^857–859^,⁸³²

System Organ/Tissue	Condition; Comments
Endocrine
Pituitary	Acidophil adenoma of pars distalis (prolactinoma). Frequent secondary mammary hyperplasia/neoplasia.⁸⁶⁰
Hematolymphoid
Multicentric	Lymphoma. Second most common malignancy of rabbits. Often multiorgan, kidneys and stomach most common; variable lymphoid organ involvement.⁸⁶¹
Thymus	Thymoma. Uncommon, possible paraneoplastic autoimmune disease.
Integument
Skin	Trichoblastoma. Most common non-viral skin tumor.⁸⁶²^,⁸⁶³ Anaplastic sarcoma, histiocytic sarcoma.⁸⁶⁴
Mammary gland	Adenocarcinoma most common. Adenoma, fibroadenoma.⁸⁶⁵
Urogenital	⁸⁵⁰
Uterus	Endometrial adenocarcinoma is the most commonly reported tumor in rabbits. Increased incidence with age; unaffected by exogenous steroid hormones. Frequent pulmonary metastases. Incidence in NZW is not well documented.⁸⁴⁹^,⁸⁶⁶
	Deciduosarcoma. Unique tumor of rabbits; iatrogenic induction by estrogen exposure; rarely a spontaneous condition. Can occur in the spleen of males and females, with frequent pulmonary metastases. Induced tumors may regress with estrogen withdrawal.⁸⁶⁷^,⁸⁶⁸
Testis	Interstitial (Leydig) and granular cell tumors. Overlapping histologic features, but cytology and transmission electron microscopy distinguish.^869–872
Kidney	Renal lymphoma. Nephroblastoma (Wilm’s tumor).

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Table 44.

Rabbits: Eukaryotes: Fungi, Protists, Metazoan Parasites⁴⁴²^,⁸²⁵^,⁸²⁶^,⁸²⁹^,⁸⁸⁸

Agent	Comments
Fungi
Encephalitozoon cuniculi	Granulomatous (meningo)encephalitis, tubulointerstitial nephritis, hepatitis, myocarditis. Congenital cataracts and uveitis in dwarf breeds. Shed in urine with vertical transmission. Largely eliminated from research colonies. Formerly Nosema cuniculi/nosematosis. Zoonotic.
Pneumocystis oryctolagi	PCP in immune deficient animals.¹³³ Organisms are transiently visible in lungs of normal weanlings with no significant lesions.⁸⁸⁹
Trichophyton mentagrophytes, Microsporum canis	Dermatophytosis (ringworm). Pruritic crusty circular alopecia. Zoonotic.
Protozoa	⁸⁹⁰
Eimeria spp.	Intestinal coccidiosis. Variable inflammation with villous atrophy, blunting and fusion. Grouped as highly pathogenic (E flavescens, E intestinalis); intermediately pathogenic (E magna, E irresidua, E piriformis); and minimally pathogenic (E media, E perforans, E neoleporis).
E. stiedae	Hepatic coccidiosis. Proliferative lesions of the intra- and extra-hepatic biliary tree with intra-epithelial coccidia.
Nematodes
Passalurus ambiguus	Pinworm. Intraluminal worms and eggs in the cecum and colon, typically subclinical.
Baylisascaris procyonis visceral larva migrans (VLM)	Serpiginous necrotizing tracts, particularly within brain, with larval large ascarid(s). Rabbit is an aberrant host, infected by consuming raccoon feces in feed, hay, or bedding.
Cestodes
Cysticercus pisiformis	Mesenteric cysticerci, metacestode of Taenia pisiformis (dog-rabbit tapeworm). Infected by consuming carnivore feces, possibly in hay.⁸⁹¹
Arthropods
Psoroptes cuniculi	Ear mite. Pruritic and exudative otitis externa.
Cheyletiella parasitovorax	Walking dandruff. Non-pruritic alopecia, particularly between scapulae. Zoonotic.
Leporacarus gibbus	Uncommon fur mite, can cause alopecia, moist dermatitis, and pruritus.⁸⁹²

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SUMMARY AND CONCLUSIONS

Animal models continue to facilitate and accelerate meaningful science that positively impacts human and animal health. “All models are wrong, but some are useful” is often quoted from the statistician George Box,¹³⁵ and to paraphrase Santayana, those who do not learn from the history, genetics, and pathology of animal models should expect unfortunate and unnecessary errors.¹³⁶^,¹³⁷ Improved recognition of factors that influence or confound data and data interpretations will improve validity, utility, translatability, and reproducibility in research.

Acknowledgments

Alessandra Piersigilli was supported by the MSKCC NCI Cancer Center Support Grant P30 CA008748. The authors wish to thank Dr Jens H. Kuhn (NIH/NIAID/DCR/IRF-Frederick, Fort Detrick, Frederick, MD, USA) for critical manuscript review. Contributions: Mice and rats: C.F.B., T.K.C., A.P., D.K.M. Gerbils: A.P.B. Guinea pigs: T.K.C., T.L.S., C.B. Hamster: A.P.B. Naked Mole Rats: M.A.D. Rabbits: T.K.C. C.B. conceived the plan. All authors contributed to and reviewed the manuscript.

Potential conflicts of interest. All authors: No reported conflicts.

Contributor Information

Timothy K Cooper, Department of Comparative Medicine, Penn State Hershey Medical Center, Hershey, PA, USA.

David K Meyerholz, Department of Pathology, University of Iowa Roy J. and Lucille A. Carver College of Medicine, Iowa City, Iowa, USA.

Amanda P Beck, Department of Pathology, Yeshiva University Albert Einstein College of Medicine, Bronx, New York, USA.

Martha A Delaney, Zoological Pathology Program, University of Illinois at Urbana-Champaign College of Veterinary Medicine, Urbana-Champaign, Illinois, USA.

Alessandra Piersigilli, Laboratory of Comparative Pathology and the Genetically Modified Animal Phenotyping Service, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Teresa L Southard, Department of Biomedical Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York, USA.

Cory F Brayton, Department of Molecular and Comparative Pathobiology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

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PERMALINK

Research-Relevant Conditions and Pathology of Laboratory Mice, Rats, Gerbils, Guinea Pigs, Hamsters, Naked Mole Rats, and Rabbits

Timothy K Cooper

David K Meyerholz

Amanda P Beck

Martha A Delaney

Alessandra Piersigilli

Teresa L Southard

Cory F Brayton

Abstract

INTRODUCTION

MICE

Laboratory Mice: Order Rodentia, Suborder Myomorpha; Mus musculus ssp.

Table 1.

Table 4.

Table 5.

Table 7.

Table 2.

Table 3.

Table 6.

RATS

Laboratory Rats: Order Rodentia, Suborder Myomorpha; Rattus norvegicus

Table 8.

Table 10.

Table 11.

Table 14.

Table 9.

Table 12.

Table 13.

GERBILS

Mongolian Gerbils: Order Rodentia, Suborder Myomorpha; Meriones unguiculatus

Table 15.

Table 16.

Table 17.

Table 18.

Table 19.

GUINEA PIGS

Guinea Pig: Order Rodentia, Suborder Hystricomorpha; Cavia porcellus

Table 20.

Table 23.

Table 24.

Table 26.

Table 21.

Table 22.

Table 25.

HAMSTERS

Hamsters: Order Rodentia, Suborder Myomorpha

Table 27.

Table 28.

Table 29.

Table 30.

Table 31.

Table 33.

Table 32.

NAKED MOLE-RATS

Naked mole rat: Order Rodentia, Suborder Hystricomorpha; Heterocephalus glaber

Table 34.

Table 35.

Table 36.

Table 37.

RABBITS

Rabbits: Order Lagomorpha, Family Leporidae, Oryctolagus cuniculus (Linnaeus, 1758)

Table 39.

Table 42.

Table 43.

Table 38.

Table 40.

Table 41.

Table 44.

SUMMARY AND CONCLUSIONS

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