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PLOS ONE logoLink to PLOS ONE
. 2022 Dec 29;17(12):e0278199. doi: 10.1371/journal.pone.0278199

Longevity and mortality in cats: A single institution necropsy study of 3108 cases (1989–2019)

Michael S Kent 1,*, Sophie Karchemskiy 2,¤a, William T N Culp 1, Amandine T Lejeune 1, Patricia A Pesavento 3, Christine Toedebusch 1, Rachel Brady 2,¤b, Robert Rebhun 1
Editor: Silvia Sabattini4
PMCID: PMC9799304  PMID: 36580443

Abstract

Client-owned cats who underwent a post-mortem examination (n = 3,108) at a veterinary medical teaching hospital between 1989 and 2019 were studied to determine longevity and factors affecting mortality. Demographic factors, environmental factors, age, and causes of death were assessed. Sexes included 5.66% intact females, 39.86% spayed females, 6.95% intact males and 47.49% neutered males. 84.2% were mixed breed cats. Age at death was known for 2,974 cases with a median of 9.07 years. Cancer was the most common pathophysiologic cause of death (35.81%) and was identified in 41.3% of cats. When categorized by organ system, mortality was most attributed to multiorgan/systemic (21.72%). Renal histologic abnormalities were noted in 62.84% of cats but was considered the primary cause of death in only 13.06% of cats. Intact female and male cats had significantly shorter lifespans than their spayed or neutered counterparts. FeLV positive status was associated with decreased longevity (P<0.0001) while FIV status was not. This study reports on risk factors associated with mortality and highlights areas of research that may contribute to improved lifespan in cats.

Introduction

The process of aging and longevity is complex and highly variable among species. Studies designed to identify risk factors, or aging signatures, target multiple levels from molecular, genetics, behavior, ecology. Fundamental to any consideration of longevity in a single species is an understanding of the degenerative, infectious, and non-infectious causes of death.

There has been much recent interest in studies examining longevity and aging in domestic pets as they share their environment with the human population, have access to routine healthcare including prevention and treatment of disease. While common causes of mortality in dogs have recently been reported, comparatively little is known about mortality and longevity in domestic cats. Cats are one of the most common companion animals in the United States (US). While exact numbers are unknown, it is estimated that as many as 45 million US households have an average of 2 cats each, yielding a total of 90 million owned cats, although another survey indicated a smaller number of households at 37 million and a smaller population of cats in the US at 61 million [1, 2]. Additionally, there are an estimated 30 to 100 million unowned cats living in the US [35]. Several studies have looked at causes of death and to some degree factors that affect longevity in owned cats, but this topic remains largely unexplored [68].

Several studies have looked at individual risk factors for their impact on longevity including cardiovascular disease and body condition score, or specifically evaluated factors that affected survival in cats who tested positive for feline leukemia virus (FeLV) or feline immunodeficiency virus (FIV) infection. Large scale studies assessing overall longevity in cats and the causes of mortality are limited [68]. A 2015 study looked at a primary care database of cats in the UK and studied over 4,000 cats who had died [9]. That study determined the median longevity of cats to be 14.0 years with mixed breed cats living longer than pure bred cats. In that study, 91.7% were mixed breed cats, with just over half of the cats being female (50.7%) and the majority of cats being spayed or neutered (64.8%). The most frequently attributed causes of mortality in cats of all ages were trauma (12.2%), renal disorder (12.1%), non-specific illness (11.2%), cancer (10.8%) and mass lesion disorders (10.2%). Increased longevity was associated with being crossbred, having a lower bodyweight and being neutered. However, the cause of death was entered by the attending clinician, and it is not known whether these diagnoses were confirmed by biopsy or histopathology. Necropsy examinations can provide information as to the cause of death with greater accuracy than clinical diagnoses alone can. Further, in dogs it has been shown that clinical diagnoses were not consistently confirmed by necropsy, which often reveals alternate causes of death, or complex processes not understood without necropsy [10, 11].

We hypothesized that evaluation of a historical set of necropsy examinations combined with clinical annotations will provide information on longevity, identify causes of mortality and highlight risk factors affecting survival in cats in the US. We aimed to analyze this data by classifying death organ system and pathophysiological process to determine which mortally determining disease processes are most common in cats. By collecting information such as age of death and other factors including signalment, viral status, housing information, the presence of cancer, heart disease, and renal disease we also aimed to determine factors that may impact longevity.

Materials and methods

Case selection

The electronic medical record database of the UC Davis William R. Pritchard Veterinary Medical Teaching Hospital was searched for all cats undergoing necropsy examinations between January 1, 1989 and October 31, 2019. Client consent for all necropsy examinations were obtained verbally by the attending clinician or through a signed consent form, with the understanding that resulting data and collected tissues could be used for further research. Client-owned cats with a complete necropsy report were included in the study. Cats were excluded if they belonged to shelters, rescue or fostering organizations, research colonies, or were otherwise unowned or had unidentified owners. Client-owned cats who presented dead on arrival to the hospital without having been previous patients, and those submitted only for rabies testing were likewise excluded. Client-owned cats who were surrendered to the hospital prior to their death were included.

The following demographic information was collected for each cat included in the study: birthdate or estimated birthdate, date that necropsy was requested, sex, reproductive status, breed, coat color, name, and body weight. Method of death was classified as humane euthanasia vs. natural. Breeds were reported by the owner and classified according to The International Cat Association’s list of breeds. For those cats with multiple body weights recorded, the last reported weight or the most consistently reported weight was used. Body weights were assumed to be measured in kilograms if not otherwise stated, and estimated weights were not included. In some cases, weight was calculated based on an organ’s percentage of body weight reported at necropsy. Those classified as having been euthanized did not include those who were not resuscitated post-cardiac or respiratory arrest, regardless of whether they received a euthanasia injection. Patients who were placed on a ventilator post respiratory arrest prior to euthanasia were categorized as having been euthanized.

In addition to the above demographics, cats were also classified as “indoor only,” “outdoor only,” or “indoor-outdoor.” “Indoor only” cats were explicitly described as kept inside and included those with access to a balcony or those who escaped outdoors for a short time despite the clients’ intention to keep them indoors. “Outdoor only” cats were comprised of those explicitly identified as outdoor, including those with access to a barn or garage. “Indoor-outdoor” cats included those described as such, as well as indoor cats who escaped outside occasionally or for prolonged periods of time, indoor cats who had access to an outdoor enclosure or barn, and those who were primarily indoor or primarily outdoor. Otherwise, cats were classified as “unknown.” When this classification changed over a patient’s lifetime or was described inconsistently, the status with the greatest exposure to the outdoors reported within a year of death was recorded. If it was not known when this change occurred, the cats were categorized by their highest outdoor exposure.

The retroviral status was also collected from the medical record when available, specifically for feline leukemia virus (FeLV) and feline immunodeficiency virus (FIV). If a cat tested positive for FeLV or FIV on any test, such as ELISA antigen or antibody testing, immunohistochemistry, or polymerase chain reaction, the cat was classified as FeLV or FIV positive. Weakly positive test results were recorded as positive. If a previously FeLV positive cat reverted to a negative status, the negative result was recorded. Client-reported results were acceptable. When the retroviral status was not reported, it was classified as “unknown.”

The primary cause of death, main organ system affected, and pathophysiological process were assigned for each cat by one of the authors (MSK). The cause of death was determined based on necropsy findings. When the primary cause could not be established, it was recorded as undetermined. The organ system and pathophysiological process involved in the cause of death were classified based on a scheme modified from a previous study on dogs [12]. The 15 organ system classifications included: behavioral, cardiovascular, dermatologic, endocrine, gastrointestinal, genital, hematopoietic, hepato-biliary, musculoskeletal, neurologic, ophthalmologic, respiratory, urological, multiorgan/systemic, and undetermined. The multiorgan/systemic category included cases in which multiple organs were affected, with diseases such as non-localized lymphoma and feline infectious peritonitis or trauma affecting multiple organ systems. The 10 pathophysiological classifications were comprised of the following: congenital (including anomalous), degenerative, infectious, inflammatory (including immune-mediated), ischemic, metabolic, neoplastic, toxic, traumatic, vascular, and undetermined. The following findings were also recorded if present: cancer, renal and cardiac changes, and hyperthyroidism; the latter was defined as either a clinical history of hyperthyroidism or the presence of a thyroid adenoma or thyroid hyperplasia. The histologic diagnosis for cancer and renal disease was recorded, as well as whether the cancer or renal and cardiac changes led to a cat’s death. Renal changes were categorized by histological classifications including tubular/interstitial disease, glomerular disease, changes consistent with toxin exposure, end-stage renal disease, cancer, pyelonephritis, infarcts, polycystic kidney disease, changes consistent with feline infectious peritonitis, papillary necrosis, amyloidosis, the presence of renal calculi or nephroliths, tubular necrosis, congenital hypoplasia or aplasia and a miscellaneous category for those diagnoses that had one or two cases only. In cases where there were questions on wording of the interpretation or it was unclear in the necropsy report, a single boarded veterinary pathologist reviewed the stored histology samples to allow for classification. Tumors were categorized as being of epithelial, mesenchymal or round cell origin. A separate category was used for benign tumors, such as pituitary macroadenomas, that led to death or euthanasia for instance due to tissue compression, hemorrhage, quality of life, or other.

Statistical analyses

Data was recorded in a commercially available spreadsheet, and statistical analyses were conducted using a commercially available statistics program (Stata version 14.2, Stata Corporation, College Station Texas, USA). Descriptive statistics were performed to report demographic data, such as survival times, sex, and indoor/outdoor status, and to evaluate the frequency of FeLV or FIV infections, causes of death, cancer, renal and cardiac changes, and thyroid changes consistent with hyperthyroidism. Continuous data was assessed for normality by visualization of distributional plots and use of a Shapiro-Francia normality test. When continuous data was normally distributed, means and standard deviations were reported; otherwise, medians, interquartile ranges, and overall range were reported. Totals and percentages were used to describe categorical data. Differences in median survival times between categorical groups were assessed using either a t-test or ANOVA or a Mann-Whitney or Kruskal-Wallis test, depending on data normality and the number of categorical variables. For categorical variables where there were more than two possible outcomes, a Dunn’s test with Bonferroni corrections were done to look for differences between groups which were corrected for multiple comparisons. Analysis was done on all cats and then also for cats ≥ 1 year. Associations between categorical data were evaluated using a chi squared or Fisher’s exact test. To explore the effects of the categorical variables on age, regression analysis was performed. P values <0.05 were considered significant.

Results

A total of 3,511 cats were available for this study. A total of 3,108 cases with owner consent for complete necropsy were included and 403 cases were excluded based on the following reasons: 296 of the cats were not client-owned or an owner could not be identified; 75 cats were brought to the hospital already deceased and there was no previous patient-doctor relationship with any clinician at the hospital; 29 were research animals; 2 cats were presented to the pathology service for rabies testing only and a full necropsy examination was not performed; and one case in which a necropsy exam was requested, but the results were not recorded in the electronic medical record and could not be located. The dataset used in this study is available as S1 Dataset. The median number of necropsy examinations per year was 100 (range 50–137). The median number of individual cats seen each year at the hospital was 2288 (range 1870–3133). The median percentage of cats undergoing necropsy examination in comparison to the number of cats seen each year was 4.59% (range 1.81–6.16%) which significantly decreased over time during the study period, R2 0.57, F(1,29)– 38.23, P<0.0001 (S1 Fig).

Demographics

Included in the study were 176 (5.66%) intact females, 1,239 (39.86%) spayed females, 216 (6.95%) intact males and 1,476 (47.49%) neutered males. In one case, the sex was not recorded. There were 2,618 (84.2%) mixed breed and 490 (15.8%) purebred cats included in the study. A total of 26 different breeds of cats were examined. For 16 cats who were reported as purebred, their exact breed could not be defined according to the chosen classification system. For a complete breakdown of cat breeds see S1 Table. The median weight, available for 2,962 cats (%), was 4.0Kg (range 0.05–15.45Kg).

Age at time of death

Effect of method of death

In total, 512 (16.5%) cats died, and 2,596 (83.5%) cats were euthanized. Of the 2,974 cats with documented ages, the median age at death was 9.07 years (IQR 4.20–12.92 years; range 0.01–21.85 years). The median age of death for cats who died naturally was 8.27 years (IQR 3.84–12.25 years; range 0.01–21.24 years), while the median age at death for euthanized cats was 9.21 years (IQR 4.24–12.03 years; range 0.01–21.85 years). These were significantly different (p = 0.02). A total of 2,672 (89.85%) cats were ≥1 years of age at the time of death. The median overall survival for this group was 9.92 years (IQR 6–13.25; range 1.00–21.85 years). Age was not found to be normally distributed when looking at all cats or in the group of cats ≥ 1year of age at the time of death. A histogram of the age at death for both groups is shown in Fig 1.

Fig 1.

Fig 1

Distribution of age at death for cats (A) Histogram showing the ages of death for the 2,974 cats in the study for which their age was known. The line represents the median age of death at 9.07 years. (B) Histogram showing the ages of death for the 2,672 cats in the study for which their age was known and they were ≥ 1 year. The line represents the median age of death at 9.92 years.

Environmental, sex and viral infection status

Information regarding where the cat lived was available for 2,284 cats (73.49%). Of all cats, 1,023 (32.9%) cats were reported to live indoor only, 1,071 (34.5%) lived both indoor and outdoor and 190 (34.5%) lived outdoors exclusively. To determine if there was a relationship between sex of the cat and their environment, we further analyzed housing by sex. Of the intact female cats, 38 (42.22%) were indoor only, 40 (44.44%) were indoor outdoor and 12 (13.33%) were outdoor only. Amongst female spayed cats, 458 (49.09%) were indoor only, 411 (44.05%) were indoor outdoor and 64 (6.86%) were outdoor only. Within female cats, there was no difference in the distribution of where they lived between intact and spayed cats (p = 0.07).

For intact male cats, 47 (34.56%) were indoor only, 54 (39.71%) were indoor outdoor and 35 (25.74%) were outdoor only. For castrated male cats, 480 (42.67%) were indoor only, 566 (50.31%) were indoor outdoor and 79 (7.02) were outdoor only. The proportion of intact versus castrated male cats living in different environments was significantly different (p<0.0001).

To explore the possibility that cats with an outdoor exposure were at increased risk for developing potentially important infectious disease FeLV status and environment was looked at. The FeLV status was known for 1,626 (52.32%) of the cats, with 110 (3.5%) testing positive. Of the FeLV positive cats, 101 had an age of death available, with 89 ≥ 1 year of age. FIV status was known for 1,402 cats (45.11%), with 84 (5.99%) testing positive. Of the FIV positive cats, 78 had an age of death available, with 76 ≥1 year of age. Nine cats tested positive for both FeLV and FIV. 41 cats who tested positive for FeLV did not have a recorded FIV test, and 18 cats who tested positive for FIV did not have a recorded FeLV test. Intact male cats had a higher proportion of positive FeLV testing (15/21 (12.4%) compared to neutered males (51/811 (6.29%; p = 0.02). Three of the 81 (3.7%) intact females were FeLV positive while 41 of the 613 (6.69%) spayed female cats were FeLV positive; this difference was not statistically different (p = 0.22). Moreover, there was no effect of sex on the proportion of FIV positive cats. Eight of 94 (8.51%) intact males were FIV positive and 58 of 714 (8.12%) of neutered males were FIV positive (p = 0.09). Four of 64 (6.25%) intact female cats were FIV positive, while 14 of 530 (2.64%) spayed female cats were FIV (p = 0.12).

A total of 1,296 cats had records of both their FeLV status and housing situation. Of the 592 cats that were indoor only, 27 (4.56%) were positive for FeLV infection. Of the 106 outdoor only cats for which FeLV status was known, 15 (14.15%) were positive, and for the 598 cats whose housing situation was indoor/outdoor, 36 (6.02%) were positive. These groups were statistically different overall (p = 0.002) with indoor only cats and cats that lived indoor/outdoor being having a lower proportion of infected cats then outdoor only cats (p = 0.0001 and p = 0.0006 respectively. There was no difference between cats that lived indoor only and those that lived indoor/outdoor (p = 0.15).

Similarly, 1,133 cats had records of their FIV status and housing situation. Of the 530 indoor only cats, 25 (4.72%) were positive for FIV, while 9 of 91 outdoor only cats, (9.90%) were positive for FIV. For the 512 cats who lived indoor/outdoor, 28 (5.47%) tested positive for FIV. These numbers were not statistically different (p = 0.13).

Causes of mortality

The most common organ system identified as the driver of mortality was the multiorgan/systemic category (21.72%), followed by the urological (13.93%), respiratory (11.42%), neurological (10.62%) and gastrointestinal systems (10.04%). In 45 (1.45%) cats, a primary organ system(s) could not be identified as the cause of death. The most common pathophysiologic cause of death was cancer (35.81%) followed by infectious causes (17.47%) and degenerative causes (11.97%). In 322 (10.36%) cases the main pathophysiologic cause of death was not identified. A complete list of the categorized causes of death by organ system and pathophysiology are presented in Tables 1 and 2, respectively.

Table 1. Cause of death by organ system, based on necropsy findings, for all cats and for cats ≥ 1 year of age.

All Cats Cats ≥1 year
Organ system cause of death Number Percent Number with Age Median Age (Years) IQR (Years) Range (Years) Number with Age Median Age (Years) IQR (Years) Range (Years)
Cardiovascular 299 9.62 280 8.41 4.31–12.02 0.04–21.13 264 8.73 5.00–12.15 1.00–21.13
Dermatologic 76 2.45 73 10.39 6.26–13.55 .51–18.41 69 10.44 7.77–13.61 1.53–18.41
Endocrine 173 5.57 165 12.65 9.67–15.01 1.02–21.85 165 12.65 9.67–15.01 1.02–21.85
Gastrointestinal 312 10.04 298 10.51 7.03–13.66 0.08–21.24 277 10.85 7.96–13.83 1.11–21.24
Genital 22 0.71 21 9.55 4.96–12.45 0.24–19.87 20 9.93 5.48–12.74 1.05–19.87
Hematopoetic 105 3.38 104 7.04 2.52–11.07 0.22–19.90 91 8.39 4.00–11.22 1.05–19.91
Hepato-billiary 158 5.08 151 8.52 5.48–11.72 0.02–21.44 146 8.67 6.02–11.81 1.35–21.44
Musculoskeletal 119 3.83 114 8.69 4.79–12.11 0.01–19.39 101 9.07 6.80–12.50 1.08–19.39
Neurological 330 10.62 324 8.24 3.66–12.66 0.06–20.66 290 9.07 5.16–13.02 1.00–20.66
Ophthalmologic 6 0.19 6 11.45 9.32–16.17 0.26–18.07 5 11.76 11.13–16.18 9.32–18.07
Respiratory 355 11.42 343 9.87 5.71–13.13 0.01–21.12 317 10.32 6.77–13.33 1.11–20.12
Systemic 675 21.72 643 6.25 1.38–11.53 0.05–20.44 508 8.75 4.00–12.39 1.01–20.44

Table 2. Cause of death by pathophysiologic process, based on necropsy findings, for all cats and for cats ≥ 1 year of age.

All Cats Cats ≥1 year
Pathophysiologic cause of death Number Percent Number with Age Median Age (Years) IQR (Years) Range (Years) Number with Age Median Age (Years) IQR (Years) Range (Years)
Anatomic/congenital 85 2.73 80 3.75 0.79–7.63 0.01–21.24 58 5.17 3.07–9.63 1.01–21.24
Degenerative 372 11.97 350 10.48 6.71–14.01 0.25–21.75 344 10.65 6.81–14.05 1.16–21.75
Infectious 543 17.47 523 3.45 0.79–8.64 0.01–19.85 362 6.26 3.04–10.64 1.01–19.85
Inflammatory 205 6.6 199 8.67 4.21–12.16 0.12–17.61 186 9.17 5.03–12.31 1.52–17.61
Ischemic 122 3.93 117 7.93 4.44–11.68 0.12–21.13 112 8.18 4.92–11.95 1.11–21.13
Metabolic 130 4.18 125 9.62 6.58–13.21 0.36–21.45 122 9.86 6.68–13.22 1.13–21.44
Neoplastic 1,113 35.81 1069 11.43 8.60–14.02 0.22–21.85 1054 11.58 8.76–14.04 1.01–21.85
Nutritional 2 0.06 2 2.49 0.53–4.44 0.53–4.44 1 4.44 NA 4.44
Toxic 69 2.22 66 5.01 1.95–8.01 0.51–16.58 58 5.72 2.69–10.03 1.00–16.58
Traumatic 145 4.67 130 3.35 1.03–9.04 0.11–18.07 99 5.60 2.16–10.04 1.02–18.07
Undetermined 322 10.36 313 7.35 3.23–11.64 0.01–20.69 276 8.00 4.55–12.04 1.02–20.69

Causes of death were further classified by disease process. The most common cause of death was cancer with 1,113 cases (35.81%). This was followed by renal failure, feline infectious peritonitis, and cardiac disease, with these processes leading to death in 336 (10.81%), 209 (6.72%) and 161 (5.18%) cats, respectively. These four causes of death accounted for 58.52% percent of all deaths. A complete listing of all causes of death for the cats in this study are listed in S2 Table.

Cancer

Cancer was identified in 1,283 (41.3%) cats. The identified cancer was the reported cause of death in 1,113 cats which was 35.81% of all cases and 86.75% of cases with cancer. In 170 cats diagnosed with cancer, their cancer was not the primary cause of death which represented 5.47% of all cases and 13.25% of cases with cancer. The number of solid tumors an individual cat was diagnosed with ranged from 0–5. Of the 1,283 cats diagnosed with cancer, 1122 (87.45%) were diagnosed with 1 cancer, 146 (11.38%) were diagnosed with 2 cancers, 12 (0.94%) were diagnosed with 3 cancers, 2 (0.16%) were diagnosed with 4 cancers and 1 (0.08%) was diagnosed with five distinct histologic types of cancer. Amongst the cats diagnosed with a single cancer, the most common type of cancer was round cell tumors (n = 479; 42.69%), followed by epithelial origin tumors (435; 38.77%) and mesenchymal origin tumors (177;15.078%). Thirty (2.67%) tumors were considered benign histologically but led to death, and one tumor was undifferentiated in a manner that prevented the cell of origin from being classified. A complete table of tumor categories broken down by the number of cancers for each cat is available in Table 3.

Table 3. Frequency of occurrence of tumor types and number of tumors seen in each cat.

  Number of Cats Mesenchymal Multiple Mesenchymal Epithelial Multiple Epithelial Round cell Multiple Round cell Benign Unclassified
Mesenchymal 177 NA 15 1 23 2 1 1
Multiple Mesenchymal NA 1 0 0 0 0 1 0
Epithelial 15 0 435 NA 67 4 7 0
Multiple Epithelial 1 0 NA 21 3 1 0 0
Round cell 25 0 67 3 479 NA 4 1
Multiple Round 2 0 4 1 NA 29 0 0
Benign 1 0 7 1 5 0 30 0
Unclassified 0 0 0 0 1 0 0 1
Total Path Diagnosis 221 3 528 27 578 36 43 3
Total Cats 1283 215 1 523 23 573 29 42 2
Cats with one tumor 1122 177 NA 435 NA 479 NA 30 1
Cats with two tumors 146 32 0 80 18 88 24 10 0
Cats with 3 tumors 12 4 1 7 3 7 1 1 1
Cats with 4 Tumors 2 1 0 1 1 0 1 1 0
Cats with 5 tumors 1 1 0 0 1 0 1 0 0

Renal disease

A total of 1953 (62.84%) cats were found to have histologic evidence of renal disease on necropsy examination. Renal disease was considered the cause of death in 406 cats, (13.16% of total cases and 20.8% of cases with renal disease), whereas the majority of affected cats (1,547 or 49.8% of all cases and 79.2% of those with renal pathology) died of another cause or causes. Of the cats with renal disease, the majority had a single pathological process (1,517; 77.7%). Multiple renal pathologies were diagnosed in a minority of cats, with two independent renal lesions found in 386 cats (19.8%), three in 46 cats (2.3%), and four in 4 cats (0.2%). Most (1,207, 61.8%) cats with renal disease were classified as having tubular/interstitial disease. In 875 cases (44.8%), tubular/interstitial disease was the only histopathological renal finding while in another 325 cases multiple processes such as glomerular, pelvic or other portions of the nephron in addition to tubular/interstitial disease were identified. For a complete breakdown of kidney disease in these cats see Table 4. This table also shows which cats had multiple renal pathologies and which type of kidney disease occurred together in a single cat.

Table 4. Renal disease processes as determined on necropsy examination in cats.

  Number of cats TI Gl Toxic End Stage Cancer Pyelo Misc Infarct Poly FIP Papillary Necrosis Am Calculi, nephroliths tubular necrosis Cong
TI 875 7 7 3 22 33 2 163 9 0 32 14 37 41 4
GI   7 43 0 0 1 2 0 3 0 0 0 0 0 0 0
Toxic 7 0 32 0 0 0 0 5 0 0 0 0 1 0 0
End Stage   3 0 0 131 1 16 1 15 0 0 1 1 10 12 0
Cancer 22 1 0 1 64 2 0 10 0 0 0 0 0 2 1
Pyelo   33 2 0 16 2 94 0 15 2 1 8 2 12 5 0
Misc 2 0 0 1 0 0 32 2 0 0 0 0 0 0 2
Infarct   163 3 5 15 10 15 2 109 0 2 8 0 13 8 0
Poly 9 0 0 0 0 2 0 0 9 0 1 0 0 1 0
FIP   0 0 0 0 0 1 0 2 0 75 0 0 0 0 0
Papillary Necrosis 32 0 0 1 0 8 0 8 1 0 5 0 3 2 0
Am   14 0 0 1 0 2 0 0 0 0 0 6 0 0 0
Calculi, nephroliths 37 0 1 10 0 12 0 13 0 0 3 0 9 2 0
Tubular necrosis   41 0 0 12 2 5 0 8 1 0 2 0 2 28 1
Cong 4 0 0 0 1 0 2 0 0 0 0 0 0 1 5
Number of pathological diagnosis   1249 56 45 191 103 192 39 353 22 78 60 23 87 102 13
Number of cats 1953 1207 55 41 184 98 170 39 317 19 78 46 23 66 88 12
Cats with one pathological diagnosis 1517 875 43 32 131 64 94 32 109 9 75 5 6 9 28 5
Cats with two pathological diagnosis 386 293 11 6 47 29 56 7 173 8 3 29 17 39 48 6
Cats with three pathological diagnosis 46 36 1 2 5 5 18 0 34 1 0 10 0 15 10 1
Cats with four pathological diagnosis 4 3 0 1 1 0 2 0 1 1 0 2 0 3 2 0

Table 4 abbreviations: TI = Tubular/Interstitial Disease; GD = Glomerular Disease; Pyleo = Pyelonephritis; Misc = Miscellaneous; Poly = Polycystic; AM = Amyloidosis; Cong = Congenital hypoplasia/aplasia

Cardiac disease

A total of 867 (27.90%) cats were found to have some form of cardiac pathology with it being attributed as the cause of death in 224 (25.84%) of those cases. The most common cardiac abnormality noted was hypertrophic cardiomyopathy (392 cases with it being identified as the cause of death in 145 cases). This was followed by endocardiosis with 85 cases (where it was identified as the main driver of mortality in 13 cases), myocarditis with 59 cases (where it cause death in 8 cases), and myocardial fibrosis (where it was identified as the cause of death in 8 cases).

Hyperthyroidism

Hyperthyroidism was diagnosed in 521 of 3108 cats (16.8%). Of these 521 cases, 461 were mixed breed (17.61% of mixed breed cats) and 60 were purebred cats (12.24% of purebred cats); thus, a significantly higher proportion of mixed breed cats had hyperthyroidism (p = 0.004). 11.1% of outdoor only cats were diagnosed with hyperthyroidism which was significantly lower than indoor cats (18.9%) or indoor/outdoor cats (19.1%) diagnosed with hyperthyroidism (p = 0.03).

Factors affecting longevity

Effect of sex

The median age of death for intact female cats was 1.05 years (IQR 0.45–4.73 years; range 0.01–21.15 years) while the median age of death for spayed female cats was 10.28 years (IQR 6.27–13.59 years; range 0.22–21.85 years); these were significantly different (p<0.0001). The median age of death for an intact male cat was 0.79 years (IQR 0.38–3.08 years; range 0.01–19.05 years), while the median age of death for castrated males was 9.55 years (IQR 5.30–12.83 years; range 0.18–21.19 years). These differences were also significantly different (p = 0.0001). The median lifespan of intact female cats ≥ 1 year of age was 4.68 years (IQR 2.03–10.36 years; range 1.01–21.15 years) while the median lifespan of spayed females in this age group was 10.48 years (IQR 6.97–13.68; range 1.01–21.85 years). These were significantly different (P = 0.0001). Of those who died at ≥ 1 year of age, the median lifespan of intact male cats was 3.67 years (IQR 1.96–8.70; range 1.01–19.05 years) while the median lifespan of male neutered cats was 9.84 years (IQR 6.06–13.04 years). These were significantly different (P = 0.0001), with data presented in Fig 2.

Fig 2. Spay and neuter status affects longevity in cats.

Fig 2

(A) Box plot showing age at time of death for all cats where age was known categorized by sex. (B) Box plot showing age at time of death for all cats ≥ 1 year where age was known categorized by sex. F = Intact Female, FS = Female spayed, M = Intact male and MN = male neutered.

Effect of environment/housing

The median age at death for indoor only cats was 9.43 years (IQR 4.8–13.11 years, range 0.11–21.85 years) while the median age at death for indoor outdoor cats was 9.82 years (IQR 5.3–13.13 years, range 0.06–21.19 years) and the median age for outdoor cats was 7.25 years (IQR 1.78–11.92 years, range 0.12–20.64 years). These were statistically different (p = 0.0001) with outdoor cats having a shorter lifespan than either indoor only cats (p = 0.0001) or cats that lived indoor/outdoor (p<0.0001). There was no difference in the age of death between indoor only cats and those that lived indoor/outdoor. For cats ≥1 year of age, the median age of death for indoor cats was 9.98 years (IQR 6.14–13.46 years, range 1.01–21.85 years) while the median age of death for indoor outdoor cats was 10.09 years (IQR 6.29–13.35 years; range 1.00–21.19 years) and the median age of death for outdoor cats was 9.80 years (IQR 4.07–12.92 years). These differences were not statistically different (p = 0.11).

Effect of FeLV/FIV infection

The median age of death for an FeLV positive cat amongst cats of all ages was 3.89 years (IQR 1.64–7.58 years; range 0.22–15.25 years) while the median age of death for an FeLV negative cat was 8.70 years (IQR 4.03–12.17 years; range 0.12–21.85 years). These ages were significantly different (P<0.0001). When examining cats ≥1 year of age (N = 89), the median age of death for an FeLV positive cat was 4.28 years (IQR 2.35–8.61 years; range 1.05–15.25 years) while for FeLV negative cats >1 year of age was 9.42 years (IQR 5.83–12.65 years; range 1.01–21.85 years), which were significantly different (P = 0.0001). The median age of death for FIV positive cats was 9.19 years (IQR 6.45–13.15 years; range 0.22–15.25 years), while the median age of death for an FIV negative cat was 8.65 years (IQR 4.16–12.15 years; range 0.35–20.44 years). Unlike FeLV, FIV status did not affect median survival time when all cats were included (p = 0.08). For cats ≥ 1 year of age, the median age at death for an FIV positive cat was 9.38 (IQR 6.70–13.40; range 1.22–20.44) while the median age of death for an FIV negative cat was 9.26 years (IQR 5.59–12.55 years; range 1.01–21.85 years). These ages were also not statistically different (p = 0.42).

Multivariate analysis of demographics

To explore the effects that the cat’s environment, breed, FeLV and FIV status, sex and spay/neuter status had on age of death, linear regression analysis was done. The overall model was significant at F (8,1067) = 17.80, p<0.0001 with an R2 = 0.12. Being FeLV positive (p<0.001) and being intact (p<0.0001) were associated with a decreased survival time. However, being a spayed female (p<0.0001) and being a neutered male (p<0.0001) were associated with an increased survival time. Environmental status, FIV status, and breed status did not have significant effects on the model.

Organ system and pathophysiologic effect on cause of death

Age at the time of death was calculated for each of the different organ systems for all cats and for those cats ≥ 1 year of age. Those with endocrine organ disease had the highest median age at death at 12.65 (IQR 9.67–15.01 years, range 1.02–21.85 years) years for all cats. The data for all organ systems is presented in Table 1. Age at time of death was also calculated for each pathophysiologic process for all cats and for cats ≥ 1 year of age. Cats dying of cancer were the oldest with a median age of death being 11.43 (IQR 8.60–14.02 years; range 0.22–21.85 years) years for all cats and 11.58 (IQR 8.76–14.04 years; range 1.01–21.85 years) years for cats ≥ 1 year of age. The data for all pathophysiologic processes are presented in Table 2.

There were a total of 1914 cats with histologic evidence of renal disease. The median survival overall was 10.35 years (IQR 6.28–13.72 years; range 0.01–21.85 years). Cats who died of their renal disease had a median age of death of 9.41 (IQR 5.50–13.46 years; range 0.11–21.75 years) while those who were classified with less significant renal disease and died of another cause had a median age at death of 10.52 years (IQR 6.61–13.78 years; range 0.01–21.85 years). These ages of death were statistically different (p<0.01). There were 832 cats who had signs of cardiac pathology on their necropsy examination. Cats who died of cardiac disease had a median age of death at 8.42 years (IQR 4.68–12.07 years; range 0.10–21.13 years), while those who had cardiac pathology found but died of other causes had a median age of death at 10.84 years (IQR 6.01–14.02 years; range 0.11–21.75 years). The age at death was statistically different between the two groups (p<0.0001). Those cats who had no signs of cardiac disease on their necropsy lived a median of 8.70 years (IQR 3.56–12.59 years; range 0.01–21.85 years). Of cats with a known age of death diagnosed with cancer (n = 1914), the median age of death was 11.75 years (IQR 8.78–14.31 years; range 0.22–21.85 years). Cats who died of their cancer had a median age of death of 11.46 years (IQR 8.61–14.04 years; range 0.22–21.85 years), cats who were diagnosed with cancer but died of other causes had a median age at death of 13.13 years (IQR 10.19–15.76 years, range 1.11–21.75 years). These ages were statistically different (p<0.001).

Effect of spay or neuter status on longevity by cause of death

Intact reproductive status was found to result in a decreased longevity, and therefore, this was further explored by characterizing the cause of death by pathophysiological process and by organ system. When looking at all female cats, intact cats died at a significantly younger age for all pathophysiological processes except the degenerative, ischemic, metabolic, neoplastic, and toxic causes. Nutritional causes could not be explored as only two cases in total were identified (one female spayed cat and intact male cat). Of note, there were no categories where the median age of death for intact female cats was ≥ the median age of spayed female cats. When looking at female cats ≥1 year of age, in addition to the above-mentioned categories the congenital and inflammatory categories no longer had statistically different ages at the time of death. When evaluating male cats, neutered males also had a survival advantage over intact males in all categories except ischemic, metabolic and neoplastic causes of death. Again, there were no categories where the median age of death was higher for intact males compared to neutered male cats. When looking at male cats ≥1 year of age, in addition to the above-mentioned categories the degenerative, inflammatory and metabolic categories were no longer statistically different. This data is presented in Table 5.

Table 5. Cause of death in all cats and cats ≥1 year of age at the time of death categorized by organ system, sex and spay neuter status.
    All Cats Cats >1 Yr
Organ System Sex Number of Cats Median Age at Death (years) p value Number of Cats Median Age at Death (years) p value
Cardiovascular F 9 0.40 (IQR 0.12–0.79; Range 0.04–2.88) <0.0001 1 2.88 0.42
FS 90 9.59 (IQR 5.09–12.61; Range 0.36–18.94) 89 9.64 (IQR 5.45–12.61; Range 1.01–18.94)
M 15 3.72 (IQR 0.79–8.02; Range 0.24–15.18) 0.005 10 5.11 (IQR 3.72–8.28; Range 3.42–15.18) 0.38
MN 166 8.45 (IQR 4.96–12.13; Range 0.51–21.13) 164 8.47 (IQR 5.45–12.15; Range 1.33–21.13)
Dermatologic F 4 7.43 (IQR 2.77–11.75; Range 0.52–13.66) 0.51 3 9.84 (IQR 5.01–13.66; Range 5.01–13.66) 1.00
FS 35 11.93 (IQR 8.41–13.67; Range 0.51–18.41) 33 12.17 (IQR 8.94–13.67; Range 3.25–18.41)
M 2 1.10 (IQR 0.67–1.53; Range 0.67–1.53) 0.15 1 1.53 0.44
MN 32 10.04 (IQR 5.68–12.67; Range 2.63–17.76) 32 10.04 (IQR 5.68–12.67; Range 2.63–17.76)
Endocrine F 3 14.02 (IQR 1.02–21.15; Range 1.02–21.15) 1.0000 3 14.02 (IQR 1.02–21.15; Range 1.02–21.15) 1.00
FS 66 13.05 (IQR 9.32–15.18; Range 2.13–21.85) 66 13.05 (IQR 9.32–15.18; Range 2.13–21.85)
M 3 9.47 (IQR 9.41–14.51; Range 9.41–14.51) 1.0000 3 9.47 (IQR 9.41–14.51; Range 9.41–14.51) 1.00
MN 93 12.35 (IQR 9.91–15.01; Range 3.15–19.86) 93 12.35 (IQR 9.91–15.01; Range 3.15–19.86)
Gastrointestinal F 9 2.77 (IQR 0.23–9.77; Range 0.08–17.71) 0.04 5 9.77 (IQR 3.02–15.06; Range 2.77–17.71) 1.00
FS 139 10.85 (IQR 8.02–13.98; Range 0.66–21.24) 136 11.00 (IQR 8.35–14.09; Range 1.53–21.24)
M 15 1.21 (IQR 0.21–2.90; Range 0.13–15.87) <0.0001 8 2.59 (IQR 1.60–10.23; Range 1.21–15.87) 0.04
MN 135 10.65 (IQR 7.64–13.76; Range 0.55–19.85) 128 10.97 (IQR 8.15–13.80; Range 1.11–19.85)
Genital F 6 1.61 (IQR 1.05–2.08; Range 0.24–10.36) 0.005 5 1.73 (IQR 1.48–2.08; Range 1.05–10.36) 0.01
FS 13 12.15 (IQR 9.55–13.58; Range 4.96–19.87) 13 12.15 (IQR 9.55–13.58; Range 4.96–19.87)
M 1 6.00 1.0000 1 6.00 1.00
MN 1 9.35 1 9.35
Hematopoetic F 6 5.93 (IQR 1.27–12.54; Range 0.45–15.03) 1.0000 5 10.36 (IQR 1.50–12.54; Range 1.27–15.03) 1.00
FS 32 7.28 (IQR 3.05–11.11; Range 0.22–19.90) 30 7.80 (IQR 4.58–11.22; Range 1.05–19.90)
M 9 1.64 (IQR 0.82–8.36; Range 0.45–14.99) 0.16 5 8.36 (IQR 2.81–10.04; Range 1.64–14.99) 1.00
MN 57 7.46 (IQR 3.50–11.08; Range 0.62–18.04) 51 8.56 (IQR 4.10–11.14; Range 1.06–18.04)
Hepato-billiary F 8 4.13 (IQR 1.35–6.27; Range 0.02–11.01) 0.0200 6 4.45 (IQR 4.07–7.83; Range 2.58–11.01) 0.16
FS 74 8.56 (IQR 6.02–12.08; Range 0.88–21.44) 73 8.60 (IQR 6.02–12.08; Range 1.64–21.44)
M 5 5.48 (IQR 1.96–13.30; Range 0.36–14.44) 1.0000 4 9.39 (IQR 3.72–13.87; Range 1.96–14.44) 1.00
MN 64 8.83 (IQR 6.85–11.58; Range 0.51–17.62) 63 8.86 (IQR 6.88–11.65; Range 1.35–17.62)
Musculoskeletal F 6 0.29 (IQR 0.17–0.64; Range 0.02–5.20) 0.0001 1 5.20 0.59
FS 38 10.12 (IQR 7.56–13.72; Range 0.52–19.39) 37 10.35 (IQR 7.81–13.72; Range 2.02–19.39)
M 9 0.53 (IQR 041–2.93; Range 0.01–8.70) 0.0008 4 3.53 (IQR 2.36–6.41; Range 1.78–8.70) 0.13
MN 61 8.47 (IQR 6.60–12.12; Range 0.74–17.73) 59 8.99 (IQR 6.71–12.33; Range 1.08–17.73)
Neurological F 23 1.11 (IQR 0.53–2.69; Range 0.06–16.13) <0.0001 13 2.38 (IQR 1.52–4.73; Range 1.06–16.13) 0.0003
FS 127 9.18 (IQR 4.37–13.49; Range 0.34–20.49) 118 9.64 (IQR 5.54–13.78; Range 1.03–20.49)
M 15 0.91 (IQR 0.43–1.96; Range 0.27–8.90) <0.0001 6 2.81 (IQR 1.78–4.80; Range 1.00–8.90) 0.001
MN 159 9.04 (IQR 5.40–12.85; Range 0.18–20.66) 153 9.25 (IQR 5.90–12.96; Range 1.07–20.66)
Ophthalmologic F 1 0.26 0.35 0    
FS 4 11.45 (IQR 10.23–13.97; Range 9.32–16.18) 4 11.45 (IQR 10.23–13.97; Range 9.32–16.18)  
M 0     0    
MN 1 18.07   1 18.07  
Respiratory F 14 2.4 (IQR 0.62–5.35; Range 0.10–13.33) 0.0003 9 5.05 (IQR 3.02–11.73; Range 1.24–13.33) 0.05
FS 161 10.32 (IQR 7.32–13.41; Range 0.41–20.12) 156 10.60 (IQR 7.65–13.47; Range 1.58–20.12)
M 17 0.75 (IQR 0.14–2.24; Range 0.01–8.14) <0.0001 7 2.35 (IQR 2.08–7.25; Range 1.19–8.14) 0.001
MN 151 10.31 (IQR 6.34–13.33; Range 0.34–17.63) 145 10.81 (IQR 6.67–13.37; Range 1.11–8.14)
Multi-organ F 49 0.69 (IQR 0.48–2.77; Range 0.05–16.24) <0.0001 20 3.26 (IQR 2.11–8.30; Range 1.01–16.24) 0.0016
FS 225 9.30 (IQR 3.96–13.01; Range 0.28–19.75) 204 10.01 (IQR 5.88–13.35; Range 1.02–19.75)
M 83 0.69 (IQR 0.4 1.95; Range 0.11 19.05) <0.0001 29 2.66 (IQR 1.57–4.97; Range 1.03–19.05) 0.0002
MN 286 7.25 (IQR 2.57–11.95; Range 0.27–20.44) 255 8.55 (IQR 4.11–12.23; Range 1.02–20.44)
Undetermined F 5 0.12 (IQR 0.12–0.25; Range 0.01–1.20) 0.002 1 1.20 0.30
FS 18 10.24 (IQR 7.09–13.04; Range 4.53–17.47) 18 10.24 (IQR 7.09–13.04; Range 4.53–17.47)
M 6 0.12 (IQR 0.12–0.18; Range 0.09–15.30) 0.06 1 15.30 0.57
MN 11 10.19 (IQR 6.47–12.28; Range 4.02–19.70) 11 10.19 (IQR 6.47–12.28; Range 4.02–19.70)
Urological F 19 2.60 (IQR 0.75–12.40; Range 0.22–17.33) 0.001 13 9.56 (IQR 2.60–13.82; Range 1.39–17.33) 0.44
FS 173 11.58 (IQR 6.53–15.16; Range 0.71–21.75) 170 11.65 (IQR 6.69–15.28; Range 1.12–21.75)
M 12 0.92 (IQR 0.24–5.74; Range 0.11–13.84) 0.001 6 5.74 (IQR 1.80–8.93; Range 1.13–13.84) 0.38
MN 207 8.74 (IQR 5.88–12.63; Range 0.24–21.19) 199 9.07 (IQR 6.12–12. 76; Range 1.02–21.19)

When assessing the cause of death for female cats by organ system, being intact significantly shortened longevity for all organ systems except dermatologic, endocrine and hematopoietic systems. Again, in no organ system category was longevity greater for intact females than spayed females. When looking at female cats ≥1 year of age, the gastrointestinal system, hepatobiliary, musculoskeletal, respiratory and urological systems were no longer statistically different in addition to the systems listed above. Intact males had significantly shorter lifespans for all categories except dermatologic, endocrine, genital, hematopoietic, hepato-biliary and undetermined. The ophthalmic system could not be evaluated as only one neutered male fell into this category. When looking at male cats ≥ 1 year at time of death, the cardiovascular, musculoskeletal and urologic systems were no longer significant. This data is presented in Table 5.

Discussion

The study reviewed 3,108 cat necropsy examinations and their associated medical records to gain insights on longevity and what factors affect longevity in cats. The study was designed to include only client-owned animals to limit biased results that may be introduced from a broader population; including non-client owned animals would have had limited correlative data, less likely reflecting the population of owned cats who we were interested in studying. Of interest was the finding that the proportion of cats undergoing a necropsy examination has decreased over time. This is similar to what was found in dogs undergoing necropsy examinations at the same institution during much of the time period of the current study [10, 11]. With a declining proportion of cats that die or are euthanized it is possible to miss changes in disease patterns or the emergence of new diseases, although this was beyond the scope of this study. Using a necropsy cohort allows for a more objective and perhaps more accurate diagnosis of disease and cause of death than from clinical data alone, which is why this population was chosen for study [10, 11].

This study found that a greater proportion of intact males lived in an outdoor environment compared to neutered males. This was not true for intact versus spayed female cats. Interestingly the proportion of FeLV positive cats was higher among intact males than among castrated males, with no significant differences in FeLV status found between intact and spayed females. This could be related to the increased exposure risk from living in an outdoor environment as well as behavioral differences between neutered and intact males. In contrast, FIV status and differences in environmental housing did not have a statistically significant relationship for either sex. The longer lifespan of cats who were FIV positive compared to those who were FeLV positive together with the possibility that cats known to be FIV positive may have been more likely to be kept indoors may account for this.

When looking at causes of death and morbidity based on histological findings it is important to realize that even though considered a gold standard histopathology may not be able to precisely determine a cause of death. For example, in inflammatory diseases confidence in how much a mild or moderate inflammatory response leads to a particular disease process or co-morbidity can be difficult to determine in most organ systems. The most common organ system found to be the cause of death was the multiorgan/systemic category. This was followed by the urological system. The most common pathophysiologic cause of death was cancer followed by infectious disease. When looking at classification of disease, the most common cause of death was cancer followed by renal disease, feline infectious peritonitis and cardiac disease. These four causes of death accounted for 58.52% percent of all deaths indicating the importance of these four disease categories on feline mortality and longevity and highlighting areas of future research that need to be performed to impact both quality and quantity of life.

Cancer was identified in 41.3% of cats on their necropsy examinations, with 86.75% dying of their cancer. Interestingly we found that while the majority of cats had a single cancer identified (87.45%), 2 to 5 distinct cancers were noted in the remaining cats. The most common category of cancer was round cell tumors.

Renal disease was also found to have a significant contribution to both morbidity and mortality; 62.84% of cats had some form of renal pathology identified with 20.79% of these cases having their death attributed to renal disease. The majority of these cats were diagnosed with tubular/interstitial disease with nearly 39% of the cats in this study having histopathological evidence of this disease process, which is consistent with other reports [13]. Again here it is important to note that while the majority of deaths were not directly attributable to their renal disease it is difficult to say if they contributed to either loss of quality of life or other co-morbidities that may have limited their longevity.

Cardiac disease also had a significant impact on cats, with 27.90% of cats found to have some form of cardiac pathology and 25.84% of these cats dying from it. Hypertrophic cardiomyopathy in cats has been evaluated in a large multicenter study, which included this institution. That study found cardiovascular-related death in 27.9% of 1008 cats diagnosed with this condition [6].

In a study looking at causes of death in cats living in free roaming colonies in the city of Milan, Italy the most common causes of death included inflammatory diseases (which included infectious causes), organ failure and trauma [14]. It is not surprising that the results in this study differed given that these animals were unowned and faced different pressures than owned cats. Feline infectious peritonitis was still prominent cause of death in these cats with 13/186 (7%) cats dying of this disease, which was quite similar to the 6.72% of cats in our study who died of this.

The median age of death was 9.07 years among all cats and 9.92 years among cats who lived to ≥ 1 year of age. To better control for the effect that death at a young age might introduce, statistical analysis was performed for both the entire group of cats and for those ≥ 1 year of age. One year was chosen as the age for a cat to become an adult based on several studies that used this age; however, we acknowledge there is no real defined age for when a kitten becomes an adult cat [15, 16]. The longevity found in our study is shorter than what another study reported for cats in England, which might relate to this being a necropsy-based population or that of a referral institution [9].

To try to determine what environmental and demographic factors affected a cat’s longevity, regression analysis was performed. Being FeLV positive decreased age at death (p<0.001), being intact, male or female combined, decreased age at death (p<0.0001), while being a spayed female (p<0.0001) and being a neutered male (p<0.0001) increased longevity significantly. Environmental housing status, FIV status, or being purebred versus mixed breed did not have significant effects on the model.

We found that intact animals had a decreased longevity when compared to spayed or neutered animals. This held true across the board for all organ systems and pathophysiologic processes, although not all of these differences were found to be statistically different. Interestingly, a study by Hamilton et al. from 1969 that examined cats from a different university teaching hospital found that being intact negatively impacted longevity for both male and female cats [17].

In most mammalian species females on average live longer than males [18, 19], which was also found in this study. While the exact causes for this are not known, it has been linked to epigenetic changes. Interestingly, Sugrue et al. found that castrated male sheep had decelerated aging compared to their intact counterparts. This was at least in part due to the removal of androgens [20]. This could help explain the differences in longevity seen between intact and neutered male cats but does not explain the differences in longevity seen between intact and spayed female cats.

We were unable to determine the age at time of spay for female cats and/or if they had any litters, as this information was not explicitly recorded in the majority of records. There is mixed evidence in humans that reproduction, particularly at a younger age, decreases longevity, but this could not be correlated in cats since this information was not available for most cases [21].

One limitation of this study is that the cases come from a veterinary medical teaching hospital collection, with a majority of cases being referral or emergency in nature. This may have selected for a less healthy population with a shorter longevity than might have been found in the general population of owned cats, such as those presenting to primary care practices [9]. By using cases from a veterinary medical teaching hospital with a referral base bias may have been introduced because of an inconsistent catchment area, referral of patients thought to have a better prognosis, or referral of those cats owned by people of a higher economic status. Other limitations include missing or incomplete data for several factors including the age and environmental data for some cats.

Conclusions

This study determined longevity in a population of cats undergoing a necropsy examination at a veterinary medical teaching hospital over a period of 30 years. The most common disease process found was cancer. Renal disease also was found in a large portion of the cases. As other studies have also found, intact males and females had a significantly shorter longevity than their castrated or spayed counterparts.

Supporting information

S1 Fig. Proportion of cats undergoing necropsy examination by year.

Graph showing the proportion of cats undergoing necropsy by year from 1989–2019. In addition, the regression line showing a decrease in the proportion of cats undergoing a necropsy along with the 95% confidence intervals represented by the shaded area is shown.

(TIF)

S1 Table. Table showing breeds of cats in the study along with their ages at time of death.

(DOCX)

S2 Table. Table with the main cause of death of client owned cats in this study.

(DOCX)

S1 Dataset. The entire dataset of cats analyzed in this study.

This file contains the dataset used for the study. A code book is available at the bottom of the file.

(XLSX)

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

Center for Companion Animal Health, University of California Davis School of Veterinary Medicine. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Silvia Sabattini

26 Sep 2022

PONE-D-22-19408Longevity and mortality in cats: A single institution necropsy study of 3108 cases (1989-2019)PLOS ONE

Dear Dr. Kent,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Nov 10 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Silvia Sabattini

Academic Editor

PLOS ONE

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When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

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2. We understand that the electronic medical record database of the UC Davis William R. Pritchard Veterinary Medical Teaching Hospital was accessed to evaluate the records of all cats undergoing necropsy examinations. Please clarify whether the authors had access to personal identifying information from the cat owners.

3. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match.

When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

4. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability.

Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized.

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We will update your Data Availability statement to reflect the information you provide in your cover letter.

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7. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The authors did an outstanding epidemiological study on the main causes of death in cats, reviewing more than 3000 necropsies in detail, and putting the data in correct correlation and statistics. This paper deserves publication as it’s important the scientific contribution given to the veterinary community.

Just very few corrections to the manuscript are reported.

Line 96 – There’s a typo in the word “Research”.

Line 96 – “With a complete” instead of “completed”.

Line 273 – Typo

Line 297 – Please rephrase the period.

Line 318 – is “at” a typo?

Line 334 – What kind of macroscopic or histopathological findings were present in cardiac disease bearing animals? Could you please rephrase the entire period, because it doesn’t sound fluid in reading. Thanks.

Line 510-513 – This was not mentioned in the results (as previous comment requested). Can you please add more specific details of the cardiac pathologies found?

Table 3 and 4 - These tables are really difficult to understand. My suggestion would be to make them in a clear way, or delete them at all.

Reviewer #2: The manuscript is very good and the topic very interesting.

The manuscript is well written, the study is well designed and based on several well exposed exposed data. Results are very interesting and well commented in the discussion.

The manuscript is a little bit long, but I suggest to maintain this lenght because the manuscript is not boring: it is simply very complete.

It is maybe the first time in my life that I really have no critics to do.

I have a simple suggestion to improve the study: practically no data are present in literature concerning causes of death in pet animals. A recent paper, published on "Animals", analysed the causes of death in colony cats. It would be interesting to insert, in the present manuscript, few sentences comapring the causes of death of owned cat with those of free cats

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

**********

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PLoS One. 2022 Dec 29;17(12):e0278199. doi: 10.1371/journal.pone.0278199.r002

Author response to Decision Letter 0


5 Oct 2022

Dear editor and reviewers;

Thank you very much for the effort and time put into reviewing our manuscript. We have done our best to address the issues raised and look forward to your re-review of the manuscript.

Please find answers to all the comment integrated into the text below.

Respectfully submitted,

Michael Kent, DVM, DACVIM (Oncology), DACVR (Radiation Oncology), ECVDI (RO-Add on)

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

I have reviewed the files and believe that I have followed the guidelines for this.

2. We understand that the electronic medical record database of the UC Davis William R. Pritchard Veterinary Medical Teaching Hospital was accessed to evaluate the records of all cats undergoing necropsy examinations. Please clarify whether the authors had access to personal identifying information from the cat owners.

As the faculty and students at our institution we have access to all records and all information that is in the EMR, although owner information beyond contact information is not stored in our EMR. For the purposes of this study this limited owner information that is collected was not accessed. All owner’s given verbal or written consent for necropsy examination and are informed that the results are stored for research as our tissue samples (which were not accessed for this study).

3. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match.

When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

These were the same funder but I have expanded this to include all the information in the financial disclosure section.

4. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability.

Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized.

We have made a new supplemental file with the data set used in this study to ensure full access to the data.

5. Please upload a copy of Supplemental Table 1 and Table 2 which you refer to in your text on page 10 and 16.

These have been uploaded along with the revised manuscript.

6. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information.

These have been placed at the end after the reference list.

7. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

The reference list has been reviewed. No paper that we have cited has been retracted.

Reviewer #1: The authors did an outstanding epidemiological study on the main causes of death in cats, reviewing more than 3000 necropsies in detail, and putting the data in correct correlation and statistics. This paper deserves publication as it’s important the scientific contribution given to the veterinary community.

We appreciate your opinion on our work and its value. Thank you.

Just very few corrections to the manuscript are reported.

Line 96 – There’s a typo in the word “Research”.

Corrected – thank you

Line 96 – “With a complete” instead of “completed”.

Change made as requested.

Line 273 – Typo

Change made as requested.

Line 297 – Please rephrase the period.

Rephrased.

Line 318 – is “at” a typo?

Yes it was – thank you for finding this.

Line 334 – What kind of macroscopic or histopathological findings were present in cardiac disease bearing animals? Could you please rephrase the entire period, because it doesn’t sound fluid in reading. Thanks.

We have edited the sentence as suggested and added the following to the manuscript in the results section.

A total of 867 (27.90%) cats were found to have some form of cardiac pathology with it being attributed as the cause of death in 224 (25.84%) of those cases. The most common cardiac abnormality noted was hypertrophic cardiomyopathy (392 cases with it being identified as the cause of death in 145 cases). This was followed by endocardiosis with 85 cases (where it was identified as the main driver of mortality in 13 cases), myocarditis with 59 cases (where it cause death in 8 cases), and myocardial fibrosis (where it was identified as the cause of death in 8 cases).

Line 510-513 – This was not mentioned in the results (as previous comment requested). Can you please add more specific details of the cardiac pathologies found?

Please see above comment where this information was added.

Table 3 and 4 - These tables are really difficult to understand. My suggestion would be to make them in a clear way, or delete them at all.

We have tried to better explain the table but do feel the information is valuable for determining how often multiple cancers or types of renal disease were present. We have made the following changes to the table lead in and titles to help better explain the data in the tables:

A complete table of tumor categories broken down by the number of cancers for each cat is available in Table 3.

Table 3: Frequency of occurrence of tumor types and number of tumors seen in each cat.

For a complete breakdown of kidney disease in these cats see Table 4. This table also shows which cats had multiple renal pathologies and which type of kidney disease occurred together in a single cat.

Reviewer #2: The manuscript is very good and the topic very interesting.

The manuscript is well written, the study is well designed and based on several well exposed exposed data. Results are very interesting and well commented in the discussion.

The manuscript is a little bit long, but I suggest to maintain this length because the manuscript is not boring: it is simply very complete.

It is maybe the first time in my life that I really have no critics to do.

Thank you for your review of our work and we value and appreciate your opinion.

I have a simple suggestion to improve the study: practically no data are present in literature concerning causes of death in pet animals. A recent paper, published on "Animals", analysed the causes of death in colony cats. It would be interesting to insert, in the present manuscript, few sentences comparing the causes of death of owned cat with those of free cats

We were unaware of this study – thank you for bringing it to our attention. We have added the following to the manuscript in the discussion section:

In a study looking at causes of death in cats living in free roaming colonies in the city of Milan, Italy the most common causes of death included inflammatory diseases (which included infectious causes), organ failure and trauma[14]. It is not surprising that the results in this study differed given that these animals were unowned and faced different pressures than owned cats. Feline infectious peritonitis was still prominent cause of death in these cats with 13/186 (7%) cats dying of this disease, which was quite similar to the 6.72% of cats in our study who died of this.

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 1

Silvia Sabattini

14 Nov 2022

Longevity and mortality in cats: A single institution necropsy study of 3108 cases (1989-2019)

PONE-D-22-19408R1

Dear Dr. Kent,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Silvia Sabattini

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: (No Response)

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: (No Response)

Reviewer #2: Authors accepted all comments and did related corrections

The manuscript is now improved and, on my opinion, suitable for publication

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

**********

Acceptance letter

Silvia Sabattini

21 Nov 2022

PONE-D-22-19408R1

Longevity and mortality in cats: A single institution necropsy study of 3108 cases (1989-2019)

Dear Dr. Kent:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Silvia Sabattini

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Fig. Proportion of cats undergoing necropsy examination by year.

    Graph showing the proportion of cats undergoing necropsy by year from 1989–2019. In addition, the regression line showing a decrease in the proportion of cats undergoing a necropsy along with the 95% confidence intervals represented by the shaded area is shown.

    (TIF)

    S1 Table. Table showing breeds of cats in the study along with their ages at time of death.

    (DOCX)

    S2 Table. Table with the main cause of death of client owned cats in this study.

    (DOCX)

    S1 Dataset. The entire dataset of cats analyzed in this study.

    This file contains the dataset used for the study. A code book is available at the bottom of the file.

    (XLSX)

    Attachment

    Submitted filename: Response to Reviewers.docx

    Data Availability Statement

    All relevant data are within the paper and its Supporting Information files.


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