Abstract
Four species of Giardia out of nine have been identified in rodents based on molecular data: G. muris, G. microti, G. cricetidarum, and G. duodenalis. A total of seven G. duodenalis assemblages (A, B, C, D, E, F, G) have been identified in rodents to date. The zoonotic assemblages A and B are responsible for 74.88% (480/641) of the total identified genotypes in rodents by statistic. For sub-assemblage A in humans, AII is responsible for 71.02% (1397/1967) of the identified sub-assemblages, followed by AI with 26.39% (519/1967) and AIII with 1.17% (23/1967), indicating a significantly greater zoonotic potential for G. duodenalis infections in humans originating from animals. For sub-assemblages of type A in rodents, AI was identified in 86.89% (53/61), and AII in 4.92% (3/61). For assemblage B, 60.84% (390/641) were identified in rodents as having zoonotic potential to humans. In environmental samples, the zoonotic assemblages A and B were responsible for 83.81% (533/636) in water samples, 86.96% (140/161) in fresh produce samples, and 100% (8/8) in soil samples. The same zoonotic potential assemblage A or B simultaneously identified in humans, rodents, and environment samples had potential zoonotic transmission between humans and animals via a synanthropic environment. The infections and zoonotic potential for G. duodenalis were higher in farmed rodents and pet rodents than that in zoo, lab, and wild rodents. In conclusion, the role of rodents in zoonotic transmission of giardiasis should be noticed. In addition to rodents, dogs, cats, wild animals, and livestock could be involved in the zoonotic transmission cycle. This study aims to explore the current situation of giardiasis in rodents and seeks to delineate the role of rodents in the zoonotic transmission of giardiasis from the One Health perspective.
Keywords: Giardia duodenalis, Assemblages, Rodents, Zoonotic transmission
1. Introduction
Giardia spp. are important zoonotic protozoan pathogens that infect the intestines of a wide range of vertebrate hosts, including humans [1,2]. Giardia spp. are diplomonad flagellates found in a broad range of vertebrates. There are currently nine validated species (G. duodenalis, G. microti, G. muris, G. agilis, G. ardeae, G. psittaci, G. varani, G. peramelis, and G. cricetidarum) that have been identified based on the combination of cysts, trophozoite morphology, and host specificity [2]. Among these, G. duodenalis (synonyms G. lamblia and G. intestinalis) is commonly identified in humans and a wide range of livestock, wildlife, and companion animals [3,4].
Although asymptomatic infections can often occur, the main symptom for giardiasis (caused by G. duodenalis) is self-limiting diarrhea. It has also been associated with arthritis and irritable bowel syndrome in humans [2,3]. G. duodenalis is one of the most prevalent enteric parasites globally, with a high prevalence in both developing and developed countries [4]. G. duodenalis is known as a multispecies complex [5], with a total of eight genetically distinct assemblages (A–H). The zoonotic assemblages A and B are found in both humans and animals; host-adapted assemblages C and D occur primarily in dogs, E in ruminants, F in cats, G in rodents, and H in seals [2]. These assemblages likely represent different Giardia species, and this is supported by the apparent host specificity and distinct genetic polymorphism [5,6].
The ssu rRNA locus is a common marker for Giardia species differentiation; the conserved nature of that locus, however, makes genotyping results of G. duodenalis less reliable [6,7]. In addition to the ssu rRNA gene, β-giardin (bg), triosephosphate isomerase (tpi), elongation factor 1 alpha (ef1α), and glutamate dehydrogenase (gdh) genes are common markers for species differentiation and genotyping and subtyping of G. duodenalis [4,6], and even for whole-genome sequencing (WGS) applied to identification [8]. This generally involves sequence analysis of PCR products from these targets. Apparent host adaptation has been observed among the three classical sub-assemblages within assemblage A; sub-assemblage AI is mainly found in animals, sub-assemblage AII is mostly found in humans, while sub-assemblage AIII has been almost exclusively found in wild ruminants, especially deer [4,6]. Assemblage B is more polymorphic than assemblage A, with the generation of numerous subtypes at each of the three common genotyping loci. In contrast, the initial identification of sub-assemblages BIII and BIV based on the results of allozyme electrophoretic analysis is not supported by phylogenetic analysis [7,9]. Sequence polymorphism is apparently also present among assemblages C, D, and E isolates, although the utility of subtyping of these pathogens has not been demonstrated [[10], [11], [12], [13]]. Whole-genome sequencing and comparative genomics analysis have been used for high-resolution tracking of infection and contamination sources in giardiasis outbreaks [8,14]. Results of these comparative genomics analyses have confirmed the zoonotic transmission of assemblage B and sub-assemblage AI [14].
The life cycle of G. duodenalis comprises rapidly multiplying trophozoites and environmentally hardy cysts that are released in the feces and spread through the fecal-oral route [15]. The trophozoite is the vegetative form and replicates in the small intestine of the host, and the cyst is the environmentally stable stage of the parasite life cycle that facilitates the zoonotic transmission of cysts passed in the feces of one host into the environment to be ingested by the subsequent host, leading to waterborne or foodborne outbreaks [[16], [17], [18], [19]]. Several drugs have been approved for the treatment of giardiasis in humans; however, treatment failures are common with giardiasis and no vaccines are available [3,[19], [20], [21]].
Rodents are the most abundant and diversified order of mammals [22]. Since the Middle Ages, it has been recognized that rodents can contribute to human disease [[22], [23], [24], [25]]. In modern times, rodents are also recognized as carriers of many human pathogens with public health importance, and almost 10% of the global rodent population is either a carrier or a reservoir of pathogens with public health importance [[24], [25], [26]]. While much progress has been made in Giardia research, no retrospective analyses have been done on the epidemiology, diversity, or transmission routes of this parasite in rodents, and there has been no assessment of the potential risks posed to human and animal populations. This article aims to explore the current situation for giardiasis both in humans and rodents and attempts to examine the role of rodents in the zoonotic transmission of giardiasis from the One Health perspectives (human–animal–environment).
2. Search strategy and selection criteria
We searched PubMed, Web of Science, MEDLINE, ScienceDirect, China National Knowledge Infrastructure (CNKI), and WANGFANG DATA for publications written in both English and Chinese for epidemiology records of Giardia by using the search terms “Giarida” AND “Human,” OR “Giarida duodenalis” AND “Human” for human populations; “Giarida” AND “Rodent,” OR “Giarida duodenalis” AND “Rodent” for rodents populations; “Giarida duodenalis” AND “water,” OR “Giarida duodenalis” AND “vegetable,” OR “Giarida duodenalis” AND “soil” for environment samples. We restricted our search to updates published before October 10, 2022. The titles and abstracts of the literature were screened first, followed by the full articles, for inclusion in the epidemiology summary in this article. The literature from recent reviews was also used to find the original records. Additional key references were retrieved from the published personal databases of all coauthors. The raw data for occurrence and genotypes distributions of Giarida were showed in supplemental materials.
3. Molecular characteristics of Giardia in humans
Among the Giardia species, G. duodenalis is the only reported species that infects humans. There are many human populations that have been documented as having infections of G. duodenalis (Table 1). The pooled prevalence is 11.31% (5909/52254). For the locations, there were at least 53 countries that have reported G. duodenalis infections in humans, and the prevalence ranges from 0.42% (33/7805) [27] in humans in Romania to 62.22% (28/45) [28] for school children in Tanzania (Fig. 1).
Table 1.
The infections of Giardia duodenalis in different human populations.
| Populations | Locations | Total No. | Positive no. | Infection (%) | No. of genotyped | Assemblages | Sub-assemblage |
|---|---|---|---|---|---|---|---|
| Humans | |||||||
| Common humans | Brazil, Canada, Egypt, Ethiopia, Iran, Italy, Jamaica, Malaysia, New Zealand, Poland, Romania, Uganda, United Arab Emirates | 13,822 | 680 | 4.92% | 502 | A (311), B (175), E (2); F (1), A/B (12), B/E (1) | AI (63), AII (94) |
| Hospital patients | Bangladesh, Belgium, China, Turkey | 7661 | 425 | 5.55% | 349 | A (64), B (266), A/B (19) | AI (8), AII (36), AI/AII (1), AII/AIII (8) |
| Diarrheal patients | Canada, Egypt, Nepal, Netherlands, Spain, Vietnam | 4907 | 308 | 6.28% | 239 | A (66), B (142), B/E (9), A/B (22) | AI (7), AII (37) |
| Community | |||||||
| Communities and households peoples 1 | Argentina, Brazil, Ethiopia, Malaysia, Mongolia, Peru, South Africa, Thailand | 2230 | 329 | 14.75% | 136 | A (52), B (73), C (1), A/B (3), A/C or A/D (7) | AII (18), AII/AIII (1) |
| Poor communities people 2 | Australia, Bangladesh, Brazil, India, Thailand, Uganda, | 6434 | 1172 | 18.22% | 791 | A (317), B (393), A/B (61), D (4), C (3), A/C or A/D (13) | AI (45), AII (124), AIII (21), AII/AIII (10) |
| Children in Community | |||||||
| Common children 3 | Australia, Brazil, China, Cuba, Guinea-Bissau, Italy, Peru, Malaysia, Mexico, Mozambique, Sahrawi, Saudi Arabia, Spain, Tanzania, Thai-Myanmar border, Uganda | 7818 | 791 | 10.12% | 347 | A (160), B (154), E (15), A/B (17), F (1) | AI (31), AII (77) |
| Children in poor communities 4 | Brazil, Slovakia, Thailand, Uganda | 1578 | 235 | 14.89% | 146 | A (66), B (75), A/B (5) | AI (1), AII (44) |
| Children | |||||||
| Asymptomatic children | Mozambique, Portugal, Spain | 4764 | 1341 | 28.15% | 156 | A (20), B (132), A/B (4) | AI (1), AII (14), AII/AIII (6) |
| Symptomatic children 5 | Albania, China, Egypt, Ethiopia, Gabon, Mexico, Mozambique, Slovakia, Sweden | 2321 | 518 | 23.06% | 163 | A (55), B (100), A/B (9) | AI (1), AII (27), AII/AIII (1) |
| Peoples frequently connected with animals 6 | Côte d'Ivoire, Egypt, Germany, Ghana, Spain | 719 | 110 | 15.30% | 89 | A (75), B (7), A/B (7) | AI (60), AII (12) |
| Cases | |||||||
| Sporadic and outbreaks cases 7 | Africa, Argentina, Australia, Brazil, Canada, China, Côte d'Ivoire, Egypt, Ethiopia, Europe, France, India, Iran, Japan, Italy, Mexico, Nicaragua, New Zealand, Norway, Peru, Qatar, Turkey, Netherlands, Norway, Portugal, South Korea, Spain, Sweden, Uganda, United Kingdom, United States | 4703 | A (1887), B (2666), A/B (81), C (3); D (4); E (37), F (5), A/F (7); | ||||
| Total | 52,254 | 5909 | 11.31% | 7621 | A (3072), B (4174), A/B (263), E (54), D (8), C (7), F (6), B/E (10), A/F (7), A/C or A/D (20) | AI (519), AII (1397), AIII (23), AI/AII (1), AII/AIII (27) |
Communities and households peoples 1: Communities, Municipalities, Households, Asymptomatic immigrants.
Poor communities people 2: Poor communities people: Asymptomatic Indigenous People, Rural communities, Villages communities, Poor communities, Valley communities, Rural villages community, Amazonas communities.
Children 3: Children, kindergarten children, School children, Community children.
Children in poor communities 4: School children in rural community, Low-income families children, School children in villages; Children and adolescents in villages.
Symptomatic children 5: Children with acute gastroenteritis, Symptomatic children, Children with flatulence, Children with diarrhea, Symptomatic young children, Symptomatic school children.
Peoples frequently connected with animals 6: Animals owners, Farmers connected with animals, Zookeepers, Zookeepers and veterinarians.
Sporadic and outbreaks positive cases 7: Only with the positive samples identification. Cases.
Fig. 1.
The infections and assemblages distributions of Giardia duodenalis in humans (A) and rodents (B).
The presence of diarrhea is a risk factor for G. duodenalis infections in previous investigations, as the pooled prevalence for diarrheal patients (6.28%, 308/4907) is significantly higher (P < 0.001) than that for common human populations (4.92%, 680/13822). Asymptomatic infections also seem common for G. duodenalis, as the pooled prevalence for the population of asymptomatic children (28.15%, 1342/4764) was higher than that for symptomatic children (23.06%, 518/2321) (Table 1).
Poor sanitation and hygiene are other risk factors for G. duodenalis infections identified in previous investigations. Undoubtedly, the pooled prevalence for people in poor communities (18.22%, 1172/6434) is significantly higher (P < 0.001) than that for common communities and households (14.75%, 329/2230). As for the children and G. duodenalis, the rate of infection in children in poor communities (14.89%, 235/1578) was significantly higher (P < 0.001) than that for more affluent children (10.12%, 791/7818) (Table 1).
Contact with animals is another risk factor for G. duodenalis infections identified in some previous investigations. The pooled prevalence for people frequently in contact with animals (15.30%, 110/719) is significantly higher (P < 0.001) than that for the overall human population (4.92%, 680/13822) (Table 1).
The pooled prevalence for children is generally higher than that for other populations, indicating that the age group is a significant factor for G. duodenalis infections. Many factors, including specimen size, host immune status, and diagnostic techniques, may also be responsible for the differences in G. duodenalis prevalence in different geographic areas (Table 1).
Among the positive samples, a total of 7621 samples (including 4703 sporadic or outbreak positive cases) were successfully genotyped by ssu rRNA or by bg, gdh or tpi genes. For G. duodenalis, a total of six assemblages (A, B, C, D, E, and F) and some mixed assemblages have been identified. The G. duodenalis assemblage B is dominant (54.77%, 4174/7621), followed by assemblage A (40.31%, 3072/7621) and mixed infections of assemblage A and B (3.45%, 263/7621).
For G. duodenalis assemblage A, genotype AII is the most common sub-assemblage identified in humans at 71.02% (1397/1967). For other subtypes within assemblage A, sub-assemblage AI was identified in 26.39% of cases (519/1967), AIII in 1.17% (23/1967), and mixed infections (AI/AII or AII/AIII) comprised 1.42% (28/1967) in animals in previous investigations.
In addition to the zoonotic assemblages A and B, assemblage E (0.71%, 54/7621) has been identified in humans, followed by D (0.10%, 8/7621), C (0.09%, 7/7621), F (0.08%, 6/7621), and some mixed infections of B/E (0.13%, 10/7621), A/F (0.09%, 7/7621), and A/C or A/D mixed genotypes (0.26%, 20/7621).
Unquestionable, the assemblages A and B are the dominant genotypes in humans, being responsible for 98.53% (7509/7621) of the identified genotypes. It is worth noting that assemblage E, although it was considered as ruminant-specific previously, has the potential for zoonotic transmission between humans and animals.
4. Molecular characteristics of Giardia in rodents
4.1. Prevalence of Giardia in rodents
To date, among the nine valid Giardia species, four have been identified in rodents based on molecular data: G. muris, G. microti, G. cricetidarum, and G. duodenalis (Table 2). G. microti and G. cricetidarum were the most prevalent in rodents, being identified in 55.73% (321/576) and 52.34% (56/107), respectively. The pooled prevalence in rodents of G. muris was 6.33% (43/679), and G. duodenalis was 20.23% (1019/5306).
Table 2.
The infections of Giardia duodenalis in different rodents.
| Host animals | Scientific name | Rodent types | Locations | Total No. | Positive no. | Infection (%) | No. of genotyped | Genetic locus | Assemblages | Sub-assemblage |
|---|---|---|---|---|---|---|---|---|---|---|
| Giardia muris | ||||||||||
| Hamsters | Farmed | USA | 1 | SSU rDNA | ||||||
| Mouse | Mus musculus | Lab | Australia | 3 | SSU rDNA | |||||
| Rat | Rattus spp. | Wild | Sweden | 2 | SSU rDNA | |||||
| mouse | Mus musculus | Wild | Sweden | 1 | SSU rDNA | |||||
| Swiss albino mice | Lab | Turkey | 1 | bg | ||||||
| Hamsters | Phodopus sungorus | Farmed | China | 87 | 3 | 3.45% | 3 | SSU rRN, bg, ef-1α | ||
| Berkenhout | Rattus norvegicus | Wild | China | 23 | 4 | 17.39% | 4 | SSU rRN, bg, ef-1α | ||
| Mice | Apodemus spp | Wild | Germany | 93 | 31 | 33.33% | 31 | SSU rDNA | ||
| Voles | Microtus spp | Wild | Germany | 175 | 2 | 1.14% | 2 | SSU rDNA | ||
| Voles | Myodes spp | Wild | Germany | 301 | 3 | 1.00% | 3 | SSU rDNA | ||
| Subtotal | 679 | 43 | 6.33% | 51 | ||||||
| Giardia microti | ||||||||||
| Rats | Rattus norvegicus | Wild | US | 1 | SSU rRNA | |||||
| Deer mice | Peromyscus maniculatus | Wild | US | 1 | SSU rRNA | |||||
| Muskrat | Ondatra zibethicus | Wild | US | 3 | SSU rRN, tpi | |||||
| Mouse | Mus musculus | Wild | Sweden | 1 | SSU rDNA | |||||
| Günther's Voles | Microtus guentheri | Pet | Italy | 2 | SSU rRNA | |||||
| Milne Edwards | Eothenomys melanogaster | Wild | China | 7 | 7 | 100% | 7 | SSU rRNA | ||
| Mice | Apodemus spp | Wild | Germany | 93 | 7 | 7.53% | 7 | SU rRN, bg, gdh | ||
| Voles | Microtus spp | Wild | Germany | 175 | 134 | 76.57% | 134 | SU rRN, bg, gdh | ||
| Voles | Myodes spp | Wild | Germany | 301 | 173 | 57.48% | 173 | SU rRN, bg, gdh | ||
| Subtotal | 576 | 321 | 55.73% | 329 | ||||||
| Giardia cricetidarum | ||||||||||
| Hamsters | Phodopus campbelli | Farmed | China | 9 | 9 | 100% | 9 | SSU rRN, bg, ef-1α | ||
| Hamsters | Mesocricetus auratus | Farmed | China | 11 | 11 | 100% | 11 | SSU rRN, bg, ef-1α | ||
| Hamsters | Phodopus sungorus | Farmed | China | 87 | 36 | 41.38% | 36 | SSU rRN, bg, ef-1α | ||
| Subtotal | 107 | 56 | 52.34% | 56 | ||||||
| Giardia doudenalis | ||||||||||
| Alashan ground squirre | Spermophilus alaschanicus | Wild in the field | China | 99 | 2 | 2.02% | 2 | bg, gdh, tpi | B (2) | |
| Asian house rats | Rattus tanezumi | Wild in the field | China | 33 | 2 | 6.06% | 2 | bg, gdh, tpi | G (2) | |
| Bamboo rat | Rhizomys sinensis | Farmed | China | 480 | 52 | 10.83% | 52 | bg, gdh, tpi | B (52) | |
| Beaver | Castor canadensis | Wild in the field | Canada, United States | 32 | SSU rRNA, Tpi | A (18); B (14) | AI (1) | |||
| Beaver | Castor canadensis | Zoo | United States | 62 | 4 | 6.45% | 4 | TPI, ssrRNA, bg | B (4) | |
| Beaver | Castor fiber | Zoo | China | 3 | 1 | 33.33% | 1 | bg, gdh, tpi | B (1) | |
| Berkenhout | Rattus norvegicus | Wild in the field | China | 23 | 1 | 4.35% | SSU rRN, bg, ef-1α | |||
| Black rats | Rattus rattus | Wild in the field | Iran | 40 | 2 | 5.00% | 2 | tpi | B (1), G (1) | |
| Brown rats | Rattus norvegicus | Wild in the field | China，Iran | 208 | 12 | 5.77% | 12 | bg, gdh, tpi | G (12) | |
| Brown rats | Ruttus norvegicus | Lab | China | 355 | 33 | 9.30% | 33 | bg, gdh, tpi | G (33) | |
| Bush rat | Rattus fuscipes | Wild in the field | Australia | 12 | 1 | 8.33% | 1 | SSU rRNA, bg | C/F (1) | |
| Chinchilla | Chinchilla lanigera | Farmed | Brazil, Romania, Italy, Europe | 976 | 557 | 57.07% | 236 | bg, tpi, gdh, SSU rRNA, ITS | A (2); B (193); C (2), D (33), E (6) | AI (2) |
| Chinchilla | Chinchilla lanigera | Pet | Germany, Belgium, China, Czech Republic | 220 | 91 | 41.36% | 90 | bg, gdh, tpi | A (13) B (62), C (14), E (1) | AI (8), AII (3), AI/AII (2) |
| Chipmunk | Eutamias asiaticus | Pet | China | 279 | 24 | 8.60% | 24 | bg, gdh, tpi | A (13); G (11) | AI (13) |
| Coypus | Myocastor coypus | Farmed | China | 308 | 38 | 12.34% | 38 | bg, gdh, tpi | A (2); B (36) | AI (2) |
| Desmarest's hutia | Capromys pilorides | Pet | Europe | 1 | bg, tpi, SSU rRNA, ITS | B (1) | ||||
| Dolichotis | Dolichotis patagonum | Zoo | China | 15 | 6 | 40.00% | 6 | bg, gdh, tpi | A (3); B (1), E (2) | AI (3) |
| Groundhog | Wild | Canada | 2 | SSU rRNA | A (2) | |||||
| Guinea pig | Cavia porcellus | Lab | Australia | 3 | Allozymesb | A (3) | AI (3) | |||
| Guinea pig | Cavia porcellus | Pet | Sweden | 1 | bg, gdh, tpi | B (1) | ||||
| Guinea pig | Cavia porcellus | Farmed | Europe | 121 | 5 | 4.13% | bg, tpi, SSU rRNA, ITS | |||
| Hamsters | Phodopus sungorus | Farmed | China | 87 | 6 | 6.90% | SSU rRN, bg, ef-1α | |||
| Himalayan marmot | Marmota himalayana | Wild in the field | China, Gansu | 399 | 6 | 1.50% | 6 | bg, gdh, tpi | A (1); B (4), E (1) | |
| House mice | Mus musculus | Free living in community | China | 31 | 1 | 3.23% | 1 | bg, gdh, tpi | G (1) | |
| House mice | Mus musculus | Wild in the field | Iran | 40 | 1 | 2.50% | 1 | tpi | G (1) | |
| Mouse | Pseudomys albocinereus | Wild in the field | Australia | 2 | 1 | 50.00% | 1 | SSU rRNA, bg | E (1) | |
| Mouse | Apodemus spp. | Wild in the field | Germany | 82 | 1 | 1.22% | 1 | SU rRNA, bg, gdh | A (1) | |
| Mouse | Mus musculus | Wild in the field | Sweden | 1 | bg, gdh, tpi | A (1) | ||||
| Muskrat | Ondatra zibethicus | Wild in the field | United States | 5 | SSU rRN, tpi | B (5) | ||||
| Muskrat | Ondatra zibethicus | Wild in the field | Romania | 1 | 1 | 100% | 1 | gdh | C (1) | |
| Norway rats | Rattus norvegicus | Free living in community | Spain | 100 | 35 | 35.00% | gdh, tpi | |||
| Prairie dogs | Cynomys ludovicianus | Lab | USA | 60 | 29 | 48.33% | 29 | bg, gdh, tpi | A (19); B (6), A/B (4) | AI (16), AI/AII (3) |
| Prairie dogs | Cynomys ludovicanus | Pet | Thailand | 79 | 11 | 13.92% | 2 | ssu rRNA, tpi, gdh | A (1); B (1) | AI (1) |
| Prairie dogs | Cynomys ludovicanus | Wild in the field | Canada | 1 | SSU rRNA | A (1) | ||||
| Patagonian cavy | Docilchotis patagonum | Zoo | Croatia | 1 | 1 | 100% | 1 | bg, tpi, gdh, SSU rRNA, ITS | B (1) | |
| Prevost's squirrel | Callosciurus prevosti | Zoo | Croatia | 1 | 1 | 100% | 1 | bg, tpi, SSU rRNA, ITS | B (1) | |
| Rat | Rattus spp. | Lab | Australia | 2 | Allozymesb | G (2) | ||||
| Rat | Rattus spp. | Wild in the field | Sweden | 8 | bg, gdh, tpi | G (8) | ||||
| Rat | Rattus spp. | Free living in community | Spain | 64 | 9 | 14.06% | 9 | bg, gdh, tpi | G (9) | |
| Rodents | // | Wild in the field | Brazil | 136 | 4 | 2.94% | 4 | gdh, tpi | A (4) | AI (4) |
| urban rodents | / | Free living in community | Malaysia | 134 | 4 | 2.99% | 1 | tpi | B (1) | |
| Voles | Myodes spp. | Wild in the field | Germany | 301 | 4 | 1.33% | 4 | SU rRN, bg, gdh | A (2), B (2) | |
| Wild rodent | // | Wild in the field | Spain | 284 | 73 | 25.70% | 20 | bg, gdh, tpi | B (1); G (19) | |
| Subtotal | 5306 | 1019 | 20.23% | 641 | A (86), B (390), G (99), D (33), C (17), E (11), A/B (4); C/F (1) | AI (53), AII (3), AI/AII (5) | ||||
There were also other Giardia species identified in rodents based only on morphology, including the natural intestinal G. muris (9.3%, 19/204) in rodents in Iran [29] and 19.2% (10/52) in another study [30]; Giardia sp. was identified in captive rats (Rattus norvegicus) in Brazil zoos with 42.86% (3/7) [31]; Giardia sp. was identified in Syrian hamsters (Mesocricetus auratus) by morphology and histology of intestinal tissues [32].
4.2. Molecular characteristics of G. duodenalis by rodents species
The pooled prevalence of G. duodenalis was 20.23% (1019/5306) in rodents by molecular identification. For the locations, there were at least 16 countries that reported rodent infections of G. duodenalis, and the infection rates ranged from 1.31% (5/383) [33,34] in chinchillas in Germany to 66.25% (53/80) [35] for chinchillas in Belgium, and 100% (2/2) [36] for squirrels in Croatia [37] (Fig. 1).
Among the G. duodenalis-positive samples identified in rodents, only 641 samples were successfully genotyped by ssu rRNA, bg, gdh or tpi genes. A total of seven assemblages were identified in rodents: A (86), B (390), G (99), D (33), C (17), E (11), A/B (4), and C/F (1). Assemblage B was predominant (60.84%, 390/641), followed by assemblage G (15.44%, 99/641), assemblage A (13.42%, 86/614), assemblage D (5.15%, 33/641), assemblage C (2.65%, 17/641), assemblage E (1.72%, 11/641), and some mixed infections (assemblage A/B (0.62%, 4/641) and assemblage C/F (0.16%, 1/641)).
For different rodent species, the prevalence of G. duodenalis varied from 1.00% (3/301) in voles (Myodes spp.) to 57.07% (557/976) in chinchillas (Chinchilla lanigera) (Table 2). Among the genotypes, the G. duodenalis zoonotic assemblages B (n = 390) were frequently identified in most rodent species, and the G. duodenalis zoonotic assemblages A (n = 86) and rodent host-specific G (n = 99) were both commonly identified in rodents (Table 2).
For subtypes of assemblage A in rodents, sub-genotype AI is the most common sub-assemblage, identified in 86.89% (53/61) in rodents. Sub-assemblage AII, previously identified in humans, was responsible for 4.92% (3/61), and mixed (AI/AII) infections are also common at 8.20% (5/61).
For the other assemblage distributions, assemblage C (n = 17) has been reported in chinchillas (Chinchilla lanigera) in Italy [38], and muskrats (Ondatra zibethicus) in Romania [36]. Assemblage D (n = 33) was only reported in chinchillas in one study in Romania [39]. Assemblage E (n = 11) was reported in mice (Pseudomys albocinereus) in Australia [40], chinchillas (Chinchilla lanigera) in Romania [39], and Himalayan marmots (Marmota himalayana) and maras (Dolichotis patagonum) in China [41,42]. The mixed of assemblage C and F was identified in wild bush rats (Rattus fuscipes) in Australia [40].
5. Molecular characteristics of G. duodenalis in environmental samples
The environmental factors involved in the G. duodenalis transmission are cysts contaminating water, soil, or fresh produce (Table 3). For water samples, the pooled prevalence of G. duodenalis was 48.83% (812/1663), with the highest record in recreational lakes in China at 98.08% (51/52) [43] and 100% (10/10) in untreated water in Egypt [44]. Among the positive samples, only 636 were successfully genotyped by ssu rRNA, bg, gdh, or tpi genes. There were five kinds of G. duodenalis assemblages identified in water samples, namely A, B, D, E, and G, and some mixed infections A/B and A/E. The zoonotic assemblage A was dominant (72.01%, 458/636), followed by assemblage B (11.79%, 75/636), assemblage E (3.30%, 21/636), assemblage D (0.31%, 2/636), and mixed infections A/B (1.89%, 12/636) and A/E (2.20%, 14/636).
Table 3.
The infections of Giardia duodenalis in water sources, fresh produce, and soil.
| Location | Environment factors | Total No. | Positive No. | Infection rate (%) | No. of samples genotyped | Genetic locus | Assemblages | |
|---|---|---|---|---|---|---|---|---|
| Philippines | Lake stations | 36 | 6 | 16.67% | 6 | SSU rRNA | A (6) | |
| Philippines | Tributary rivers | 69 | 26 | 37.68% | 26 | SSU rRNA | A (24), B (2) | |
| China | Sewer wastewater | 386 | 319 | 82.64% | 202 | tpi | A (243), B (6), A/B (53) | AII (243) |
| Colombia | River Water | 55 | 26 | 47.27% | 26 | gdh | A (19), B (7) | AII (2) |
| Pakistan | Water Bodies | 600 | 160 | 26.67% | // | SSU rRNA | ||
| Norway | Sewage | 40 | 30 | 75.00% | 30 | SSU rRNA, bg, gdh | A (27), B (3) | AII (27) |
| Hungary | Raw, surface and sewage water | 36 | 13 | 36.11% | 12 | SSU rRNA, gdh | A (7), B (1), A/B (4) | AI (1), AII (4) |
| China | Wastewater | 40 | 32 | 80.00% | 32 | bg, gdh, tpi | A (31), B (1) | AII (31) |
| China | Combined sewer overflow | 40 | 33 | 82.50% | 33 | bg, gdh, tpi | A (31), B (1), G (1) | AII (31) |
| Spain | Treated wastewater | 96 | 12 | 12.50% | 12 | SSU rRNA, bg | A (5), A/E (7) | AI (2), AII (3) |
| Romania | Wastewater and Different Surface Water | 76 | 22 | 28.95% | 22 | gdh | A (9), D (1); E (12) | AII (9) |
| France | Wastewater | 36 | 25 | 69.44% | 25 | tpi | A (8), B (1), E (4), A/B (5), A/E (7) | |
| China | Raw urban wastewater | 48 | 23 | 47.92% | 23 | tpi | A (17), B (5), A/B (1) | AII (17) |
| China | Recreational lakes | 52 | 51 | 98.08% | 5 | SSU rRNA | A (3), B (1), D (1) | |
| Malaysia | Recreational lake water | 9 | 7 | 77.78% | 7 | SSU rRNA | A (7) | |
| USA, Canada, New Zealand | Raw surface water | 29 | tpi, WGS | A (6), B (21), A/B (2) | AI (6) | |||
| Canada | Raw surface water | 29 | SSU rRNA, bg, gdh, tpi, WGS | A (4), B (25) | ||||
| Brazil | Water | 10 | 3 | 30.00% | 1 | SSU rRNA, gdh, tpi | E (1) | |
| Egypt | Raw water | 10 | 10 | 100.00% | // | tpi, gdh | A (10) | AII (10) |
| Bangladesh | Water samples | 24 | 14 | 58.33% | 5 | tpi, bg | B (1), E (4) | |
| US | Sewage samples | 1 | SSU rRNA | A (1) | ||||
| Subtotal | 1663 | 812 | 48.83% | 636 | A (458), B (75), A/B (12), A/E (14), D (2), E (21), G (1) | AI (9), AII (377) | ||
| Italy | Ready-to-eat salads and berry fruits | 324 | 25 | 7.72% | 25 | bg | A (6), B (18), E (1) | |
| Pakistan | Vegetables | 200 | 16 | 8.00% | // | SSU rRNA | ||
| Brazil | Vegetables | 11 | 2 | 18.18% | 2 | bg, gdh | B (2) | |
| Brazil | Fresh Leafy Vegetables | 128 | 16 | 12.50% | 16 | gdh | A (16) | AII (16) |
| Brazil | Vegetables | 260 | 19 | 7.31% | 11 | gdh | A (9), B (1), E (1) | AI (9) |
| Brazil | Vegetables | 62 | 16 | 25.81% | 2 | SSU rRNA, gdh, tpi | E (2) | |
| India | Fresh produce | 284 | 13 | 4.58% | 2 | SSU rRNA, tpi, gdh | A (1), D (1) | |
| Italy | Ready-to-eat packaged salad | 648 | 4 | 0.62% | 4 | tpi | A (4) | |
| Syria | Salad vegetables | 128 | 17 | 13.28% | 17 | bg | B (17) | |
| Canada | Ready-to-eat packaged leafy greens | 544 | 10 | 1.84% | 9 | SSU rRNA | A (2), B (7) | |
| Spain | Green leafy vegetables | 129 | 30 | 23.26% | // | qPCR | ||
| Morocco | Leafy green | 152 | 4 | 2.63% | // | qPCR | ||
| Iraq | Vegetables and fruits | 230 | 4 | 1.74% | // | SSU rRNA | ||
| China | Street markets vegetables | 642 | 73 | 11.37% | 73 | SSU rRNA | B (72), E (1) | |
| Mozambique | Fresh Horticultural Products | 321 | 12 | 3.74% | // | bg | ||
| Subtotal | 4063 | 261 | 6.42% | 161 | A (38), B (117), E (5), D (1) | AI (9), AII (16) | ||
| Brazil | Soil | 10 | 2 | 20.00% | // | SSU rRNA, gdh, tpi | ||
| Pakistan | Soil | 400 | 71 | 17.75% | // | SSU rRNA | ||
| Colombia | Soil | 50 | 8 | 16.00% | 8 | gdh | A (4), B (4) | AII (1) |
| Subtotal | 460 | 81 | 17.61% | 8 | A (4) B (4) | AII (1) | ||
For the fresh produce, G. duodenalis was identified in green leafy vegetables, street market vegetables, ready-to-eat packaged leafy greens and fresh horticultural products, ready-to-eat salads, and fruits (Table 3). The pooled prevalence of G. duodenalis infection in fresh produce was 6.42% (261/4063). Among the positive samples, only 161 were successfully genotyped by ssu rRNA, bg or gdh genes, with assemblage A, B, D, and E being identified. Among these, the zoonotic assemblage B was dominant (72.67%, 117/161), followed by assemblage B (23.60%, 38/161), assemblage E (3.11%, 5/161), and assemblage D (0.62%, 1/161).
For the soil, only three studies have reported infections of G. duodenalis in soil samples. The pooled prevalence was 17.61% (81/460) [[45], [46], [47]]. Among the positive samples, only eight samples were successfully genotyped by ssu rRNA or gdh genes, including assemblage A (50.0%, 4/8) and B (50.0%, 4/8) [47]. There were also some other negative results reported for G. duodenalis infections in soil samples, such as in Brazil [48,49], Egypt [44], and Mongolia [50].
Both G. duodenalis sub-genotypes AI and AII were identified in environmental factors (Table 3). Sub-assemblage AI has mostly been seen in animals in previous investigations, and AII in humans.
6. Ecological significance from a one health perspective for giardiasis transmission
6.1. Possible waterborne or foodborne zoonotic transmission
Giardia duodenalis causes large numbers of gastrointestinal illnesses in humans, and there have been over 300 reported outbreaks of giardiasis in the world since 1954, most of which were related to contaminated water [16,17,51]. The largest drinking water outbreak of giardiasis was reported in Portland, Oregon, USA in 1955, with 50,000 infected individuals [17]. More recently, important waterborne giardiasis extensive outbreaks have been documented in Bergen, Norway, in 2004, with over 2500 individuals becoming infected (1500 patients were laboratory diagnosed) caused by drinking water contaminated with Giardia cysts in sewage pipes due to leakage from one particular septic tank [52,53].
In North America, there were two outbreaks (83 laboratory confirmed cases were documented in the first outbreak, and 124 laboratory confirmed cases were identified during the second outbreak) at five-year intervals that occurred in the same community with a population of 4200 in the mountains of British Columbia, Canada [54]. In November 1981, an outbreak of waterborne giardiasis occurred at a popular ski resort in Colorado, United States [55]. Many waterborne giardiasis outbreaks have been documented, and giardiasis outbreaks are usually associated with drinking water or recreational water exposure [16].
Very few foodborne outbreaks have been documented [17], and only 38 foodborne outbreaks of giardiasis have been reported [56]. In many of the outbreak investigations, the food type or source was frequently undetermined. However, a variety of foods have been implicated, with fresh produce the most common food type and infected food handlers the most common source [56].
For sporadic cases, numerous risk factors have been identified, including direct and indirect fecal contact, male–male sexual contact, and international travel; these factors have very high odds ratios, but on a population basis, additional risk factors with lower odds ratios are still important because of their high prevalence. These include daycare exposure, swimming in or drinking from natural water bodies, and even chronic gastrointestinal conditions or the use of antibiotics [19,57].
Numerous studies of the relative importance of genotypes A (usually AII) and B have been reported, but the results of these studies do not clearly identify a difference in epidemiology. In contrast, there is accumulating evidence that genotype AI is primarily a zoonotic infection [19]. These studies have also identified the common concurrence of both assemblages A and B in drinking water-associated outbreaks of giardiasis [7,14].
6.2. Zoonotic potential of G. duodenalis from rodents
From a One Health perspective, the human–animal–environment has been identified as being involved in the G. duodenalis transmission. For humans, the zoonotic assemblages A, B, and mixed infections have been identified in 98.53% (7509/7621) of the human samples. The animal host-specific C, D, E, F, and mixed infections were identified in 0.98% (75/7621) of cases, and the mixed genotypes were identified in 0.49% (37/7621).
For rodents, the zoonotic assemblages A, B and mixed infections were identified in 74.88% (480/641) of rodents samples. The rodent host-specific assemblage G was identified in 15.44% (99/641); the dog host-specific assemblages C and D were identified in 7.80% (50/641); the ruminant host-specific assemblage E was identified in 1.72% (11/641), and one dog/cat host-specific assemblage C/F (0.16%, 1/641) was identified.
For the environmental samples, the zoonotic assemblages A, B, and mixed infections were identified in 85.69% (545/636) in water samples; the ruminant host-specific assemblage E was identified in 3.30% (21/636); the dog host-specific assemblage D was identified in 0.31% (2/636); the rodent host-specific assemblage G was identified in 0.16% (1/636), and there were 14 assemblage A/E mixed infections (2.20%, 14/636). The zoonotic assemblages A, B, and mixed infections were identified in 96.27% (155/161) in fresh produce samples; the ruminant host-specific assemblage E was identified in 3.11% (5/161); the dog host-specific assemblage D was identified in 0.62% (1/161). The zoonotic assemblages A (n = 4) and B (n = 4) were identified in 100% (8/8) of reported soil samples.
G. duodenalis assemblages A and B are the major zoonotic assemblages, and assemblage E has also been reported in humans; C and D are occasionally reported in humans, while G has not been reported in humans to date (Table 4). The animal host-specific assemblages C, D, E, and F identified in rodents indicated that the dogs, cats, wild animals, and some farm animals could be involved in the G. duodenalis zoonotic transmission cycle. The rodents could also serve as the reservoir for G. duodenalis transmission between different animals.
Table 4.
Distributions of different Giardia duodenalis assemblages in humans and rodents.
| Assemblages | No. of genotyped | Major hosts | Reports in humans | Reports in rodents (Positive no.) |
|---|---|---|---|---|
| Assemblage A | 86 | Humans, non-human primates, ruminants, pigs, horses, canines, felines, rodents, marsupials, other mammals | Numerous | Chinchilla (1), Beaver (12), Chinchilla (7), Guinea pig (3), Chinchilla (2), Beaver (6), Chinchilla (5), Prairie dogs (19), Mouse (1), Voles (2), Chipmunk (13), Rodents (4), Coypus (2), Prairie dogs (1), Himalayan marmot (1), Dolichotis (3), Mouse (1), Prairie dogs (1), Groundhog (2) |
| AI | 66 | Livestocks | Few | Chinchilla (1), Chinchilla (7), Guinea pig (3), Chinchilla (2), Beaver (6), Chinchilla (5), Prairie dogs (19), Chipmunk (13), Rodents (4), Coypus (2), Prairie dogs (1), Dolichotis (3) |
| AII | 8 | Humans | Numerous | Chinchilla (5), Prairie dogs (3) |
| Assemblage B | 390 | Humans, non-human primates, horses, rabbits, marsupials, chinchillas, beavers | Numerous | Beaver (7), Muskrat (5), Beaver (4), Guinea pig (1), Prevost's squirrel (1), Patagonian cavy (1), Chinchilla (10), Chinchilla (3), Chinchilla (29), Desmarest's hutia (1), Chinchilla (10), Wild rodent (1), Beaver (1), Beaver (7), Chinchilla (33), Prairie dogs (6), Chinchilla (151), Chinchilla (1), Voles (2), Bamboo rat (52), urban rodents (1), Chinchilla (18), Coypus (36), Black rats (1), Prairie dogs (1), Himalayan marmot (4), Alashan ground squirre (2), Dolichotis (1) |
| Assemblage C | 17 | Canines | Few | Chinchilla (16); Muskrat (1) |
| Assemblage D | 33 | Canines | Few | Chinchilla (33) |
| Assemblage E | 11 | Ruminants, pigs | Some | Mouse (1); Chinchilla (7); Himalayan marmot (1); Dolichotis (2) |
| Assemblage G | 99 | Mice, rats | None | Rat (2), Rat (8), Wild rodent (19), Brown rats (11), Asian house rats (2), House mice (1), Chipmunk (11), Brown rats (33), Rat (9), House mice (1), brown rats (1), Black rats (1) |
For rodents, there are six feeding types, namely wild in the field, free living in the community, pets, farmed, zoo, and lab (Table 5). The rodents of the farm feeding type had the highest prevalence of G. duodenalis infections with 33.37% (658/1972), followed by pet rodents with 21.80% (126/578), zoo rodents with 15.85% (13/82), lab rodents with 14.94% (62/415), free living in community rodents with 14.89% (49/329), and the lowest in wild rodents at 6.69% (111/1660).
Table 5.
Distributions of Giardia duodenalis in rodents of different feeding types.
| Rodents feeding types | Total No. | Positive no. | Infection (%) | No. of genotyped | Assemblages(no.) | Sub-assemblage A | Zoonotic potential (%) |
|---|---|---|---|---|---|---|---|
| Wild in the field | 1660 | 111 | 6.69% | 106 | A (30); B (29); C (1); E (2); G (43), C/F (1) | AI (5) | 53.15% |
| Free living in community | 329 | 49 | 14.89% | 11 | B (1); G (10) | // | 9.09% |
| Pet | 578 | 126 | 21.80% | 118 | A (27); B (65); G (11), C (14), E (1) | AI (22), AII (3), AI/AII (2) | 77.97% |
| Farm | 1972 | 658 | 33.37% | 326 | A (4); B (281); C (2); D (33); E (6) | AI (4) | 87.42% |
| Zoo | 82 | 13 | 15.85% | 13 | A (3); B (8); E (2) | AI (3) | 84.62% |
| Lab | 415 | 62 | 14.94% | 67 | A (22); B (6); G (35); A/B (4) | AI (19), AI/AII (3) | 41.79% |
| Total | 5036 | 1019 | 20.23% | 641 | A (86), B (390), A/B (4); G (99), C (17); D (33); E (11); C/F (1) | AI (53), AII (3), AI/AII (5) | 74.26% |
For the zoonotic potential assemblages in the different rodent feeding types, the highest was in farm rodents (87.4%) followed by zoo rodents (84.6%), pet rodents (77.97%), wild in the field rodents (53.15%), lab rodents (41.79%), and the lowest in the free living in the community rodents (9.09%). In summary, the farmed rodents and pet rodents had a higher prevalence and potential for G. duodenalis zoonotic transmission between rodents and animals (Table 5).
There are also some biases for the published literature, as only studies with positive results or those reporting the highly zoonotic potential for G. duodenalis assemblages were easy to have published.
7. Conclusions
From the One Health perspective, G. duodenalis zoonotic assemblages (A and B) have been simultaneously identified in humans, animals, and environment factors involved in zoonotic transmission. The role of rodents in the zoonotic transmission of giardiasis should be taken into consideration from the One Health perspective owing to the fact that rodents are both in close contact with humans and different types of environments. Among the total of seven G. duodenalis assemblages identified in rodents, assemblages A and B were responsible for the majority of infections, indicating their higher zoonotic potential. Rodents played an essential role in the zoonotic transmission of giardiasis. In addition to rodents, dogs, cats, wild animals, and some farm animals could be involved in the zoonotic transmission cycle. Therefore, giardiasis can only be effectively controlled by implementing the One Health approach. Further studies are required to investigate G. duodenalis among the diverse human population, livestock, pet animals, and rodents in various ecosystems, and researchers should pursue a multidisciplinary One Health approach with contributions from zoologists, ecologists, veterinarians, and public health experts to understand rodent-related G. duodenalis and possible transmission routes.
Funding
This work was partially supported by the National Natural Science Foundation of China (32102698), the Outstanding Talents of Henan Agricultural University (30501055), the Henan Postdoctoral Scientific Research Initiation Project (282851), and the Leading Talents of Thousand Talents Program of Central China (19CZ0122).
Declaration of Competing Interest
The authors declare no competing interests.
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.onehlt.2023.100500.
Appendix A. Supplementary data
Table S1: Occurrence and genotypes of Giardia duodenalis genotypes in humans.
Table 2S: Occurrence of Giardia spp. in rodents.
Table 3S: Occurrence and genotypes of Giardia doudenalis in rodents.
Table 4S: Occurrence and genotypes of Giardia duodenalis in environmental samples.
Supplemental material_References.
Data availability
The data that has been used is confidential.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Table S1: Occurrence and genotypes of Giardia duodenalis genotypes in humans.
Table 2S: Occurrence of Giardia spp. in rodents.
Table 3S: Occurrence and genotypes of Giardia doudenalis in rodents.
Table 4S: Occurrence and genotypes of Giardia duodenalis in environmental samples.
Supplemental material_References.
Data Availability Statement
The data that has been used is confidential.