Seasonal patterns of oxidative stress markers in captive Asian elephants in Thailand and relationships to elephant endotheliotropic herpesvirus shedding

Abstract

IntroductionOxidative stress refers to an imbalance between oxidant and antioxidant activity and accumulation of reactive oxygen species, which can have detrimental effects on animal health. Annual fluctuations in oxidative stress status can occur, increasing disease susceptibility during certain time periods. However, a full understanding of factors related to oxidative stress in Asian elephants and how to mitigate the negative consequences is lacking.MethodsThis study measured six serum oxidative stress markers [reactive oxygen species (ROS), malondialdehyde (MDA), 8-hydroxydeoxyguanosine (8-OHdG), albumin, glutathione peroxidase (GPx), and catalase] and two stress markers [serum cortisol and fecal glucocorticoid metabolites (fGCM)] in 23 captive Asian elephants in Thailand over a 12 months period to examine relationships with age and season.ResultsSeasonal variations were observed, with several markers exhibiting significantly higher concentrations in the summer (ROS, MDA, 8-OHdG, albumin) and lower values during the rainy/winter seasons (MDA, 8-OHdG, albumin, catalase). By contrast, GPx was the only marker to be highest during the rainy season. For the stress markers, higher fGCM concentrations were noted during the rainy season, which contrasts with earlier studies showing more activity in the winter (tourist season). Positive correlations were found between the temperature-humidity index and ROS, GPx, and fGCM, while a negative correlation was observed with serum albumin. Elephant endotheliotropic herpesvirus (EEHV) shedding events were associated with higher concentrations of ROS and MDA. A moderate negative correlation was observed between 8-OHdG and the PCR threshold cycle of EEHV shedding (Ct), indicating DNA damage may be involved in EEHV shedding in elephants.DiscussionResults revealed significant age and seasonal effects on several oxidative stress markers, indicating those factors should be considered in study design and data interpretation. There also may be physiological adaptations in oxidative stress conditions in relation to environmental changes that could impact health outcomes.

Physiological changes in captive elephants in northern Thailand as a result of the COVID-19 tourism ban—stress biomarkers

“…Serum MDA concentrations (1.3-3.8 μM) were similar to previous ranges [0.93-3.0 μM (44,45)], but showed a declining trend as the study progressed, with T01 (April 2020) being the highest and T07 (January-April 2020) the lowest. There was no obvious seasonal effect, which agrees with another study conducted during the same time period in Thai elephants (53), although a follow-up study did find somewhat lower concentrations during the rainy season (52). Polyunsaturated fatty acids are major substrates for lipid peroxidation (59,61,62), and MDA is an end-product produced by the decomposition of the lipid peroxidation process (61).…”

“…However, those months (November-February) also correspond to the high tourist season (5,6), so until now, it has been impossible to tease apart tourist activity versus climate conditions on adrenal activity. But this and another study (53) conducted during the COVID-19 lockdown strongly suggest that tourist activities are the most likely cause of increased fGCM excretion during the winter, high tourist season months. Thus, further studies are needed to better understand not only what tourist activities affect elephant health and welfare, but how.…”

“…Intra-and inter-assay coefficients of variation (CV) were 1.1 and 2.3%, respectively. Serum 8-OHdG was measured using a DetectX ® DNA Damage Enzyme Immunoassay Kit (Cat #K059-H5, Arbor Assays) validated for Asian elephants (52,53). Assay sensitivity was 0.072 ng/mL and intra-assay and inter-assay CVs were < 10 and 6.3%, respectively.…”

“…Reference categories were chosen based on specific questions as described previously (11,12), including Sex = male; Time = T01 (April 2020, the beginning of the travel ban); and Camp = F (the smallest camp). Differences in mean fGCM, oxidative stress markers, stress leukograms and H/L ratio among three seasons (summer: February 16-May 15; rainy: May 16-October 15; winter: October 16-February 15) (53,58,59) were analyzed by Tukey's post-hoc tests following GEE analyses.…”

“…The range in albeit at the higher end as the travel ban progressed. While there are limited studies on how tourist or logging activities impact stress hormone responses, there are indications that yearly patterns of GCs may be related more to work activities than environmental influences (52,53). In India, fGCM concentrations were higher in elephants involved in an intensive and crowded public festival, but not other tourist activities (61).…”