Urinary markers of oxidative stress respond to infection and late-life in wild chimpanzees

Abstract

Oxidative stress (OS) plays a marked role in aging and results from a variety of stressors, making it a powerful measure of health and a way to examine costs associated with life history investments within and across species. However, few urinary OS markers have been examined under field conditions, particularly in primates, and their utility to non-invasively monitor the costs of acute stressors versus the long-term damage associated with aging is poorly understood. In this study, we examined variation in 5 urinary markers of oxidative damage and protection under 5 validation paradigms for 37 wild, chimpanzees living in the Kibale National Park, Uganda. We used 924 urine samples to examine responses to acute immune challenge (respiratory illness or severe wounding), as well as mixed-longitudinal and intra-individual variation with age. DNA damage (8-OHdG) correlated positively with all other markers of damage (F-isoprostanes, MDA-TBARS, and neopterin) but did not correlate with protection (total antioxidant capacity). Within individuals, all markers of damage responded to at least one if not both types of acute infection. While OS is expected to increase with age, this was not generally true in chimpanzees. However, significant changes in oxidative damage were detected within past-prime individuals and those close to death. Our results indicate that OS can be measured using field-collected urine and integrates short-and long-term aspects of health. They further suggest that more data are needed from long-lived, wild animals to illuminate if common age-related increases in inflammation and OS damage are typical or recently aberrant in humans.

Urinary neopterin of wild chimpanzees indicates that cell-mediated immune activity varies by age, sex, and female reproductive status

“…First, we included the time of day at which the sample was collected. While some prior studies of genus Pan do not report a diurnal effect on neopterin excretion 43 , 48 , such an effect has been observed in humans 65 and in Kanyawara chimpanzees 50 , with a peak in the early morning and low levels in the afternoon. In addition, to control for seasonal variation in neopterin levels 66 , we included the date of sample collection.…”

“…Among sanctuary chimpanzees, older males exhibited greater risk of inflammatory diseases with advanced age than did females 55 . Yet, in wild chimpanzees at Kanyawara, there were no sex differences in urinary neopterin concentrations 50 , nor did reproductive status predict observations of respiratory illness among females 53 . There is, however, evidence of pregnancy-related immunomodulation in wild chimpanzees, as late-term pregnant females at Ngogo and Kanyawara shed more gastrointestinal parasites than other females 52 and in Taï National Park, Côte d’Ivoire, were more likely to test positive for malaria 56 .…”

“…To avoid overestimating the effects of sample dilution, we excluded all samples with an SG below 1.003 (N = 8 samples) and above 1.050 (N = 8 samples). Furthermore, to avoid the confounding effects of severe acute immune challenge on neopterin levels 43 , 48 , 50 , we excluded samples collected during an outbreak of respiratory disease 63 and from individuals otherwise exhibiting clinical signs of acute disease and injury (N = 72 samples), leaving 502 samples for statistical analyses. Final sample sizes for each age and sex class, as well as mean sample sizes for individual chimpanzees, are presented in Supplementary Table S1 .…”

“…If inflammaging results primarily from recent lifestyle shifts (e.g., decreased physical activity), the increased proinflammatory markers observed in aging members of industrialized human populations and captive nonhuman primates should not be present in wild primate populations. In support of this hypothesis, a recent study of the Kanyawara chimpanzee community, also located in Kibale, found that urinary neopterin levels did not increase across the life course 50 . However, among three past-prime individuals who died during the study period, neopterin increased as the time to death decreased 50 .…”

“…In support of this hypothesis, a recent study of the Kanyawara chimpanzee community, also located in Kibale, found that urinary neopterin levels did not increase across the life course 50 . However, among three past-prime individuals who died during the study period, neopterin increased as the time to death decreased 50 . Furthermore, data on infectious agent abundances suggest that wild chimpanzees experience notable immunosenescence, as older individuals exhibit infections at higher frequencies and burdens.…”