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Given that this dataset spanned 37 years see below , humane euthanasia had to be performed under specific circumstances, per American Veterinary Medical Association definitions and guidelines, and with specific consideration to quality of life [ 39 ]. Humane euthanasia followed standard operating procedures at both facilities. Of the chimpanzees, were mother-reared, were nursery-reared, were wild-born or had an unknown captive rearing history, and 8 had missing data for this variable.
For classification purposes, mother-reared individuals were defined as those chimpanzees that were not separated from their mother for at least the first 2. Nursery-reared chimpanzees were individuals that were separated from the mother within the first month of life due to maternal rejection, illness, or injury.
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These individuals were cared for by humans, and were raised in an incubator with access to human infant formula until they were able to be independent. They were then placed in same-age peer groups until three years of age, at which point they were introduced into larger adult and sub-adult social groups [ 36 , 40 ].
We used hematology records from annual physical exams between and to obtain values for neutrophils and lymphocytes. Only data from annual physical exams were used for analyses; therefore, any values derived from sedations due to an injury or health issue were not included. Due to missing data for absolute values of neutrophils and lymphocytes, we used percent values to calculate neutrophil to lymphocyte ratios.
Therefore, the percent value of neutrophils was divided by the percent value of lymphocytes to obtain the NLR for each chimpanzee at each time point.
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Generally, each chimpanzee had one NLR data point per year corresponding to one annual physical exam per year across a year period. The year period corresponded to the 10 years prior to the year of the last annual physical exam that preceded either i death from natural causes or humane euthanasia, ii transfer to another facility, or iii the year of Where available, we also included NLRs taken at humane euthanasia. These averages did not include any NLR values taken at the point of euthanasia see below.
Not all chimpanzees had all 5 or 10 years of data.
Therefore, the total sample size for 5- and year NLR analyses was and individuals, respectively. Histograms and Q-Q plots showed that the data were positively skewed. Exploration of the data revealed five problematic outliers, which were removed from further analyses. We first wanted to examine the effects of age on NLR across the entire sample.
Therefore, to examine cross-sectional differences in NLR as a function of age, we used curve estimation to examine both linear and quadratic models for average 5-year and average year NLR. All relevant data are within the manuscript and its S1 Data. As shown in Fig 3 , mother-reared males had the highest average year NLR values. There were no other significant main or interaction effects. Individual chimpanzee NLR over 10 years as a function of sex a and rearing b.
Error bars represent standard error of the mean. As shown in Fig 5a , male chimpanzees and those with higher average NLR values died at younger ages. Additionally, mother-reared individuals who had the highest NLR values died at younger ages than nursery-reared individuals, whereas NLR was not related to age at death in wild-caught individuals. Across a large sample of chimpanzees from two separate colonies, longitudinal analyses showed that, within individuals, NLR did not change significantly over a year period.
However, cross-sectional analyses showed that NLR was influenced by sex, rearing, and age. Additionally, males had higher NLR values than females. Results from the current study partly support these results: male chimpanzees also showed higher NLR than females, and NLR was highest in chimpanzees between 25 and 30 years of age. In doing so, we found that mother-reared chimpanzees had higher NLR than nursery-reared and wild caught individuals, and there was a significant quadratic relationship between age and average 5- and year NLR in a cross-sectional analysis.
We also found that higher average 5-year NLR values predicted death at a younger age, and that NLR values at euthanasia were significantly higher than both average 5-year NLR and NLR values at the last physical exam prior to humane euthanasia. NLR showed a quadratic relationship with age, such that NLR was highest in chimpanzees between 25 and 35 years old, and was lower in both younger and older individuals.
This is in contrast with some findings in humans, which show that NLR increases linearly with old age in healthy populations, suggesting increased risk for inflammation [ 1 , 3 , 6 ]. The most parsimonious explanation for these data may be that chimpanzees with lower NLRs reach older ages precisely because they maintain better health, and thus, have lower NLR values.
Indeed, we found that those with higher NLR values died at a younger age. Perhaps those that have higher average NLRs throughout life [likely indicative of higher levels of inflammation and physiologic stress [ 41 ]] die at a younger age, whereas those with lower NLR values live into old age. Indeed, consistent with this explanation and the cross sectional and longitudinal NLR data in the current study, human longitudinal data show that lymphocyte counts decrease with age which would contribute to higher NLRs , whereas cross-sectional data show that lymphocyte counts are highest in the oldest age groups contributing to lower NLRs [ 42 ].
Given that the field of aging and aging theory lack reliable physiological measures of what constitutes good health and what predicts longevity [ 43 ], these data may point to the use of NLR as one possible indicator of health and longevity. Interestingly, within individuals, NLR did not increase over a year period, further suggesting that age-associated effects in the cross-sectional sample might be due to subject-specific differences rather than physiological aging.
Overall, these results suggest that lower NLR values, which seem to be relatively stable over a year period, may be indicative of longer lifespans in chimpanzees. As such, average 5- and year NLR may serve as a tool aiding in identification of individuals that are at risk for early mortality.
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Although the NCCC colony had higher average NLRs than the Yerkes colony, the quadratic association between age and NLR was consistent between the two chimpanzee populations see Fig 1c and 1d suggesting that this is a consistent and repeatable finding. These results provide some support for the use of humane euthanasia in captive settings. This is particularly true for chimpanzees: because of their psychological complexity and phylogenetic proximity to humans, a higher level of ethical and moral justification is required for end-of-life decisions, including assessments of quality of life [ 44 , 45 ].
Indeed, elevated NLR may be used in quality of life programs similar to the one implemented at the NCCC to help identify which animals may be closer to their endpoints, prior to the need for euthanasia. Consistent with previous research showing the utility of NLR as a diagnostic tool in humans, NLR can be used as a tool to aid in diagnosing severe illness and trauma. In combination with a multitude of diagnostic criteria used to identify clinical illnesses, the utility of NLR may be in its use as a prognostic indicator of shorter lifespan and in identifying at-risk individuals.
For example, the leading cause of death in chimpanzees is cardiac disease, and research has shown that males are more likely to suffer from myocardial fibrosis and related sudden death [ 24 , 46 — 50 ]. Furthermore, many of these sudden deaths occur mid-life, between 25—30 years of age [ 47 , 48 , 50 ]. The finding that NLR was higher in males, and was highest in individuals between 25 and 35 years of age seems consistent with this cardiac death, sex, and age pattern. Interestingly, we also found that mother-reared chimpanzees had higher NLR values and died at younger ages than nursery-reared chimpanzees as well as wild-caught chimpanzees, but that effect is likely due to the confounding factor that wild-caught chimpanzees are significantly older than chimpanzees of other rearing types.
This finding is surprising: given the multitude of health consequences associated with nursery-rearing, we expected to find that nursery-reared individuals would have the highest NLR. Overall, if NLR indeed indicates increased inflammation and disease risk, this would suggest that mother-reared individuals, particularly mother-reared males between 25 and 35 years of age, have the highest risk for negative outcomes.
Unfortunately, we are currently unable to speculate about the mechanisms underlying this increased risk. Furthermore, caution should be exercised when interpreting these results, given that they are based on the use of a single immune parameter. Regardless, given the similarity between the patterns described above, NLR may prove a useful biomarker in identifying individuals at risk for sudden cardiac death.
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As such, there are likely a multitude of other factors, both genetic and environmental, affecting NLR. Because previous studies have found that NLR in humans is moderately heritable [ 4 ], we are currently examining the heritability of NLR in chimpanzees. Additionally, it is possible that individual differences in genetic or biological aging mechanisms may help to explain individual differences in NLR.
For example, there is significant variation between the biological as measured through changes in epigenetic methylation and chronological age of chimpanzees [ 51 ]. Animals that show a faster rate of biological aging may have shorter lifespans.
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Additionally, other measures or indicators of chronic physiological stress are likely correlated with NLR. For example, allostatic load, a measure of stress-induced physiological damage over the lifetime, is higher in wild-caught gorillas compared to their mother- and nursery-reared counterparts [ 52 , 53 ]. Given the lower NLR values of wild-caught chimpanzees in the current study although, again, this may be confounded with age , it is possible that chimpanzees with lower allostatic load also have lower NLR.
Additional research examining these variables would shed light on healthy aging in chimpanzees, a topic that is of increasing importance given the longer lifespans and aging populations of captive chimpanzees [ 25 , 30 ]. Regarding environmental factors, additional studies are currently underway that aim to examine the effects of chronic conditions, past experimental history, and body condition scores a proxy measure of BMI on NLR values.
In summary, although these findings reveal a complex relationship between NLR and individual chimpanzee characteristics, age, rearing, and sex explain only a modest amount of the total variance in average year NLR values. The current study builds on previous findings in chimpanzees by showing that i the oldest chimpanzees up to 58 years of age had lower NLR values, ii mother-reared males had the highest NLR values, and iii individuals with higher NLR values had shorter lifespans.
We believe that these older chimpanzees have longer lifespans precisely because of their lower NLR values; however, why some individuals have lower NLR values than others is a research question that we hope to continue exploring. Much more research is needed to understand the genetic and environmental factors that affect NLR, the relationships between NLR, lifespan, and clinical illness, as well as the use of NLR as a diagnostic and prognostic tool. Additionally, although the current study provides a preliminary reference for normal male and female NLR values [3.
The authors would like to thank Mary Ann Cree for assistance in obtaining archival Yerkes data, as well as Dr. Michele Mulholland and Mary Catherine Mareno for helpful comments during preparation of this paper. From there we never stopped talking, dating each other and falling deeper in love. For all the single people out there, especially introverted ones like us: do not be afraid to travel outside of your comfort zone.
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