Circadian Rhythm of Salivary Immunoglobulin A and Associations with Cortisol as A Stress Biomarker in Captive Asian Elephants (Elephas maximus)
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals and Sample Collection
2.2. Enzyme Immunoassays
2.2.1. Immunoglobulin A
2.2.2. Cortisol
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Bansiddhi, P.; Brown, J.L.; Thitaram, C.; Punyapornwithaya, V.; Somgird, C.; Edwards, K.L.; Nganvongpanit, K. Changing trends in elephant camp management in northern Thailand and implications for welfare. PeerJ 2018, 6, e5996. [Google Scholar] [CrossRef] [Green Version]
- Möstl, E.; Palme, R. Hormones as indicators of stress. Domest. Anim. Endocrinol. 2002, 23, 67–74. [Google Scholar] [CrossRef]
- Matteri, R.L.; Carroll, J.A.; Dyer, C.J. Neuroendocrine responses to stress. In The biology of Animal Stress: Basic Principles and Implications for Animal Welfare; Moberg, G.P., Mench, J.A., Eds.; CABI Publishing: Wallingford, UK, 2000; pp. 43–76. [Google Scholar]
- Martin, P.A.; Crump, M.H. The adrenal gland. In McDonald’s Veterinary Endocrinology and Reproduction; Iowa State Press: Wiley, IA, USA, 2003; pp. 165–200. [Google Scholar]
- Menargues, A.; Urios, V.; Mauri, M. Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement. Anim. Welf. 2008, 17, 305–312. [Google Scholar]
- Millspaugh, J.J.; Washburn, B.E. Use of fecal glucocorticoid metabolite measures in conservation biology research: Considerations for application and interpretation. Gen. Comp. Endocrinol. 2004, 138, 189–199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sheriff, M.J.; Dantzer, B.; Delehanty, B.; Palme, R.; Boonstra, R. Measuring stress in wildlife: Techniques for quantifying glucocorticoids. Oecologia 2011, 166, 869–887. [Google Scholar] [CrossRef] [PubMed]
- Bansiddhi, P.; Nganvongpanit, K.; Brown, J.L.; Punyapornwithaya, V.; Pongsopawijit, P.; Thitaram, C. Management factors affecting physical health and welfare of tourist camp elephants in Thailand. PeerJ. 2019, 7, e6756. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bansiddhi, P.; Brown, J.L.; Khonmee, J.; Norkaew, T.; Nganvongpanit, K.; Punyapornwithaya, V.; Angkawanish, T.; Somgird, C.; Thitaram, C. Management factors affecting adrenal glucocorticoid activity of tourist camp elephants in Thailand and implications for elephant welfare. PLoS ONE 2019, 14, e0221537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Whitham, J.C.; Wielebnowski, N. New directions for zoo animal welfare science. Appl. Anim. Behav. Sci. 2013, 147, 247–260. [Google Scholar] [CrossRef]
- Yeates, J.W.; Main, D.C.J. Assessment of positive welfare: A review. Vet. J. 2008, 175, 293–300. [Google Scholar] [CrossRef]
- Staley, M.; Conners, M.G.; Hall, K.; Miller, L.J. Linking stress and immunity: Immunoglobulin A as a non-invasive physiological biomarker in animal welfare studies. Horm. Behav. 2018, 102, 55–68. [Google Scholar] [CrossRef]
- Tsujita, S.; Morimoto, K. Secretory IgA in saliva can be a useful stress marker. Environ. Health Prev. Med. 1999, 4, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Pressman, S.D.; Cohen, S. Does positive affect influence health? Psychol. Bull. 2005, 131, 925–971. [Google Scholar] [CrossRef] [PubMed]
- Deinzer, R.; Kleineidam, C.; Stiller-Winkler, R.; Idel, H.; Bachg, D. Prolonged reduction of salivary immunoglobulin A (sIgA) after a major academic exam. Int. J. Psychophysiol. 2000, 37, 219–232. [Google Scholar] [CrossRef]
- Takatsuji, K.; Sugimoto, Y.; Ishizaki, S.; Ozaki, Y.; Matsuyama, E.; Yamaguchi, Y. The effects of examination stress on salivary cortisol, immunoglobulin A, and chromogranin A in nursing students. Biomed. Res. 2008, 29, 221–224. [Google Scholar] [CrossRef] [Green Version]
- Fan, Y.; Tang, Y.; Lu, Q.; Feng, S.; Yu, Q.; Sui, D.; Zhao, Q.; Ma, Y.; Li, S. Dynamic changes in salivary cortisol and secretory immunoglobulin A response to acute stress. Stress Health 2009, 25, 189–194. [Google Scholar] [CrossRef]
- Kikkawa, A.; Uchida, Y.; Nakade, T.; Taguchi, K. Salivary secretory IgA concentrations in beagle dogs. J. Vet. Med. Sci. 2003, 65, 689–693. [Google Scholar] [CrossRef] [Green Version]
- Svobodová, I.; Chaloupková, H.; Končel, R.; Bartoš, L.; Hradecká, L.; Jebavý, L. Cortisol and secretory immunoglobulin A response to stress in German shepherd dogs. PLoS ONE 2014, 9, e90820. [Google Scholar] [CrossRef]
- Svobodová, I.; Vápeník, P.; Pinc, L.; Bartoš, L. Testing German shepherd puppies to assess their chances of certification. Appl. Anim. Behav. Sci. 2008, 113, 139–149. [Google Scholar] [CrossRef]
- Muneta, Y.; Yoshikawa, T.; Minagawa, Y.; Shibahara, T.; Maeda, R.; Omata, Y. Salivary IgA as a useful non-invasive marker for restraint stress in pigs. J. Vet. Med. Sci. 2010, 72, 1295–1300. [Google Scholar] [CrossRef] [Green Version]
- Escribano, D.; Gutiérrez, A.M.; Tecles, F.; Cerón, J.J. Changes in saliva biomarkers of stress and immunity in domestic pigs exposed to a psychosocial stressor. Res. Vet. Sci. 2015, 102, 38–44. [Google Scholar] [CrossRef]
- Humphreys, A.F.; Tan, J.; Peng, R.; Benton, S.M.; Qin, X.; Worley, K.C.; Mikulski, R.L.; Chow, D.-C.; Palzkill, T.G.; Ling, P.D. Generation and characterization of antibodies against Asian elephant (Elephas maximus) IgG, IgM, and IgA. PLoS ONE 2015, 10, e0116318. [Google Scholar] [CrossRef] [PubMed]
- Edwards, K.L.; Bansiddhi, P.; Paris, S.; Galloway, M.; Brown, J.L. The development of an immunoassay to measure immunoglobulin A in Asian elephant feces, saliva, urine and serum as a potential biomarker of well-being. Conserv. Physiol. 2019, 7. [Google Scholar] [CrossRef] [PubMed]
- Hastings, M.H.; Maywood, E.S.; Brancaccio, M. Generation of circadian rhythms in the suprachiasmatic nucleus. Nat. Rev. Neurosci. 2018, 19, 453–469. [Google Scholar] [CrossRef] [PubMed]
- Logan, R.W.; McClung, C.A. Rhythms of life: Circadian disruption and brain disorders across the lifespan. Nat. Rev. Neurosci. 2019, 20, 49–65. [Google Scholar] [CrossRef]
- Shirakawa, T.; Mitome, M.; Oguchi, H. Circadian rhythms of S-IgA and cortisol in whole saliva—Compensatory mechanism of oral immune system for nocturnal fall of saliva. Pediatric. Dent. J. 2004, 14, 115–120. [Google Scholar] [CrossRef] [Green Version]
- Heintz, M.R.; Santymire, R.M.; Parr, L.A.; Lonsdorf, E.V. Validation of a cortisol enzyme immunoassay and characterization of salivary cortisol circadian rhythm in chimpanzees (Pan troglodytes). Am. J. Primatol. 2011, 73, 903–908. [Google Scholar] [CrossRef]
- Brown, J.L.; Kersey, D.C.; Freeman, E.W.; Wagener, T. Assessment of diurnal urinary cortisol excretion in Asian and African elephants using different endocrine methods. Zoo Biol. 2010, 29, 274–283. [Google Scholar] [CrossRef]
- Menargues, A.; Urios, V.; Limiñana, R.; Mauri, M. Circadian rhythm of salivary cortisol in Asian elephants (Elephas maximus): A factor to consider during welfare assessment. J. Appl. Anim. Welf. Sci. 2012, 15, 383–390. [Google Scholar] [CrossRef] [Green Version]
- Casares, M.; Silván, G.; Carbonell, M.D.; Gerique, C.; Martinez-Fernandez, L.; Cáceres, S.; Illera, J.C. Circadian rhythm of salivary cortisol secretion in female zoo-kept African elephants (Loxodonta africana). Zoo Biol. 2016, 35, 65–69. [Google Scholar] [CrossRef]
- Hile, M.E.; Hintz, H.F.; Erb, H.N. Predicting Body Weight from Body Measurements in Asian Elephants (Elephas maximus). J. Zoo Wildl. Med. 1997, 28, 424–427. [Google Scholar]
- Ng, V.; Koh, D.; Fu, Q.; Chia, S.-E. Effects of storage time on stability of salivary immunoglobulin A and lysozyme. Clin. Chim. Acta 2003, 338, 131–134. [Google Scholar] [CrossRef] [PubMed]
- Team, R.C. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2017. [Google Scholar]
- Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D.; R. Core Team. nlme: Linear and Nonlinear Mixed Effects Models, R Package Version 3.1–143; 2019. Available online: https://cran.r-project.org/package=nlme (accessed on 12 December 2019).
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: New York, NY, USA, 2016. [Google Scholar]
- Bakdash, J.Z.; Marusich, L.R. Repeated Measures Correlation. Front. Psychol. 2017, 8, 456. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hucklebridge, F.; Clow, A.; Evans, P. The relationship between salivary secretory immunoglobulin A and cortisol: Neuroendocrine response to awakening and the diurnal cycle. Int. J. Psychophysiol. 1998, 31, 69–76. [Google Scholar] [CrossRef]
- Dimitriou, L. Circadian effects on the acute responses of salivary cortisol and IgA in well trained swimmers. Br. J. Sports Med. 2002, 36, 260–264. [Google Scholar] [CrossRef] [Green Version]
- Gleeson, M.; Cripps, A.W. Chapter 11—Ontogeny of mucosal immunity and aging. In Mucosal Immunology, 4th ed.; Mestecky, J., Strober, W., Russell, M.W., Kelsall, B.L., Cheroutre, H., Lambrecht, B.N., Eds.; Academic Press: Boston, MA, USA, 2015; pp. 161–185. ISBN 978-0-12-415847-4. [Google Scholar]
- Park, S.-J.; Tokura, H. Bright light exposure during the daytime affects circadian rhythms of urinary melatonin and salivary immunoglobulin A. Chronobiol. Int. 1999, 16, 359–371. [Google Scholar] [CrossRef]
- Mishra, K.P.; Yadav, A.P.; Ganju, L. Antarctic harsh environment as natural stress model: Impact on salivary immunoglobulins, transforming growth factor-β and cortisol level. Indian J. Clin. Biochem. 2012, 27, 357–362. [Google Scholar] [CrossRef] [Green Version]
- Kugler, J.; Hess, M.; Haake, D. Secretion of salivary immunoglobulin a in relation to age, saliva flow, mood states, secretion of albumin, cortisol, and catecholamines in saliva. J. Clin. Immunol. 1992, 12, 45–49. [Google Scholar] [CrossRef]
- Gleeson, M.; Cripps, A.W.; Clancy, R.L. Modifiers of the human mucosal immune system. Immunol. Cell Biol. 1995, 73, 397–404. [Google Scholar] [CrossRef]
- Evans, P.; Der, G.; Ford, G.; Hucklebridge, F.; Hunt, K.; Lambert, S. Social class, sex, and age differences in mucosal immunity in a large community sample. Brain Behav. Immun. 2000, 14, 41–48. [Google Scholar] [CrossRef] [Green Version]
- Corbett, L.; Muir, C.; Ludwa, I.A.; Yao, M.; Timmons, B.W.; Falk, B.; Klentrou, P. Correlates of mucosal immunity and upper respiratory tract infections in girls. J. Pediatric. Endocrinol. Metab. 2010, 23, 1–25. [Google Scholar] [CrossRef]
- Jafarzadeh, A.; Sadeghi, M.; Karam, G.A.; Vazirinejad, R. Salivary IgA and IgE levels in healthy subjects: Relation to age and gender. Braz. Oral Res. 2010, 24, 21–27. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; Chen, Y.; Zou, X.; Li, Q.; Li, H.; Shu, Y.; Li, X.; Li, W.; Han, L.; Ge, C. Salivary secretory immunoglobulin (SIgA) and lysozyme in malignant tumor patients. BioMed Res. Int. 2016, 2016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Orysiak, J.; Witek, K.; Zembron-Lacny, A.; Morawin, B.; Malczewska-Lenczowska, J.; Sitkowski, D. Mucosal immunity and upper respiratory tract infections during a 24-week competitive season in young ice hockey players. J. Sports Sci. 2017, 35, 1255–1263. [Google Scholar] [CrossRef] [PubMed]
- Escribano, D.; Campos, P.H.R.F.; Gutiérrez, A.M.; Le Floc’h, N.; Cerón, J.J.; Merlot, E. Effect of repeated administration of lipopolysaccharide on inflammatory and stress markers in saliva of growing pigs. Vet. J. 2014, 200, 393–397. [Google Scholar] [CrossRef] [PubMed]
- Iqbal, S.; Zebeli, Q.; Mansmann, D.A.; Dunn, S.M.; Ametaj, B.N. Oral administration of LPS and lipoteichoic acid prepartum modulated reactants of innate and humoral immunity in periparturient dairy cows. Innate Immun. 2014, 20, 390–400. [Google Scholar] [CrossRef] [PubMed]
- Hellhammer, D.H.; Wüst, S.; Kudielka, B.M. Salivary cortisol as a biomarker in stress research. Psychoneuroendocrinology 2009, 34, 163–171. [Google Scholar] [CrossRef] [PubMed]
- Gunnar, M.R.; Talge, N.M.; Herrera, A. Stressor paradigms in developmental studies: What does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology 2009, 34, 953–967. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Behringer, V.; Clauß, W.; Hachenburger, K.; Kuchar, A.; Möstl, E.; Selzer, D. Effect of giving birth on the cortisol level in a bonobo groups’ (Pan paniscus) saliva. Primates 2009, 50, 190–193. [Google Scholar] [CrossRef]
- Palme, R. Non-invasive measurement of glucocorticoids: Advances and problems. Physiol. Behav. 2019, 199, 229–243. [Google Scholar] [CrossRef]
- Skandakumar, S.; Stodulski, G.; Hau, J. Salivary IgA: A possible stress marker in dogs. Anim. Welf. 1995, 4, 339–350. [Google Scholar]
- Jarillo-Luna, R.A.; Rivera-Aguilar, V.; Pacheco-Yépez, J.; Godínez-Victoria, M.; Oros-Pantoja, R.; Miliar-García, A.; Campos-Rodríguez, R. Nasal IgA secretion in a murine model of acute stress. The possible role of catecholamines. J. Neuroimmunol. 2015, 278, 223–231. [Google Scholar] [CrossRef] [PubMed]
Parameter | Day | Time (hours) | Min-Max | ||||
---|---|---|---|---|---|---|---|
(ng/mL) | 06:00 | 10:00 | 14:00 | 18:00 | 22:00 | (ng/mL) | |
sIgA | 1 | 60.61 ± 3.99 | 53.40 ± 5.63 | 43.69 ± 4.00 | 55.52 ± 6.62 | 55.04 ± 6.38 | 22.80–83.70 |
2 | 85.13 ± 11.4 | 61.62 ± 6.88 | 71.33 ± 7.27 | 51.89 ± 6.82 | 79.13 ± 7.75 | 19.87–150.18 | |
3 | 70.36 ± 8.68 | 42.85 ± 6.03 | 58.05 ± 5.4 | 39.17 ± 6.17 | 49.17 ± 4.92 | 13.71–96.19 | |
Overall | 72.09 ± 5.07 a | 52.96 ± 3.69 b | 56.67 ± 3.57 a,b | 48.64 ± 3.76 b | 61.75 ± 4.29 a,b | 13.71–150.18 | |
Cortisol | 1 | 0.82 ± 0.09 | 0.76 ± 0.10 | 0.86 ± 0.15 | 0.71 ± 0.31 | 0.55 ± 0.15 | 0.12–3.17 |
2 | 0.87 ± 0.17 | 0.56 ± 0.14 | 0.52 ± 0.05 | 0.34 ± 0.10 | 0.48 ± 0.18 | 0.08–2.01 | |
3 | 0.63 ± 0.06 | 0.49 ± 0.14 | 0.41 ± 0.10 | 0.28 ± 0.05 | 0.23 ± 0.06 | 0.10–1.26 | |
Overall | 0.79 ± 0.07 a | 0.61 ± 0.07 a,b | 0.59 ± 0.08 a,b | 0.46 ± 0.12 a,b | 0.45 ± 0.09 b | 0.08–3.17 |
Parameter | Time (hours) | Min-Max | ||||
---|---|---|---|---|---|---|
(ng/mL) | 06:00 | 10:00 | 14:00 | 18:00 | 22:00 | (ng/mL) |
sIgA | ||||||
Male | 65.88 ± 8.55 | 52.77 ± 8.34 | 59.83 ± 7.11 | 46.06 ± 6.91 | 60.93 ± 6.45 | 13.71–125.12 |
Female | 78.74 ± 8.84 | 53.15 ± 3.58 | 52.72 ± 4.77 | 51.62 ± 6.15 | 62.7 ± 8.7 | 14.88–150.18 |
Cortisol | ||||||
Male | 0.83 ± 0.13 | 0.69 ± 0.12 | 0.5 ± 0.08 | 0.37 ± 0.07 | 0.42 ± 0.14 | 0.08–2.01 |
Female | 0.73 ± 0.10 | 0.52 ± 0.11 | 0.71 ± 0.15 | 0.61 ± 0.29 | 0.44 ± 0.12 | 0.1–3.17 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Plangsangmas, T.; Brown, J.L.; Thitaram, C.; Silva-Fletcher, A.; Edwards, K.L.; Punyapornwithaya, V.; Towiboon, P.; Somgird, C. Circadian Rhythm of Salivary Immunoglobulin A and Associations with Cortisol as A Stress Biomarker in Captive Asian Elephants (Elephas maximus). Animals 2020, 10, 157. https://doi.org/10.3390/ani10010157
Plangsangmas T, Brown JL, Thitaram C, Silva-Fletcher A, Edwards KL, Punyapornwithaya V, Towiboon P, Somgird C. Circadian Rhythm of Salivary Immunoglobulin A and Associations with Cortisol as A Stress Biomarker in Captive Asian Elephants (Elephas maximus). Animals. 2020; 10(1):157. https://doi.org/10.3390/ani10010157
Chicago/Turabian StylePlangsangmas, Tithipong, Janine L. Brown, Chatchote Thitaram, Ayona Silva-Fletcher, Katie L. Edwards, Veerasak Punyapornwithaya, Patcharapa Towiboon, and Chaleamchat Somgird. 2020. "Circadian Rhythm of Salivary Immunoglobulin A and Associations with Cortisol as A Stress Biomarker in Captive Asian Elephants (Elephas maximus)" Animals 10, no. 1: 157. https://doi.org/10.3390/ani10010157
APA StylePlangsangmas, T., Brown, J. L., Thitaram, C., Silva-Fletcher, A., Edwards, K. L., Punyapornwithaya, V., Towiboon, P., & Somgird, C. (2020). Circadian Rhythm of Salivary Immunoglobulin A and Associations with Cortisol as A Stress Biomarker in Captive Asian Elephants (Elephas maximus). Animals, 10(1), 157. https://doi.org/10.3390/ani10010157