Physiological changes in captive elephants in northern Thailand as a result of the COVID-19 tourism ban-muscle, liver, metabolic function, and body condition
Open accessAbstract
The international travel ban initiated in March 2020 due to the COVID-19 pandemic greatly affected how captive elephants were managed in Thailand. A lack of tourists and associated income meant elephants were chained longer with reduced food provisions, had fewer mahouts, and limited exercise like riding, which likely affected health and welfare. Fifty-eight elephants from six tourist camps were assigned a body condition score (BCS) and blood samples were collected monthly for 2 years during the travel ban to measure: (1) muscle enzymes [creatine kinase (CK), aspartate aminotransferase (AST)]; (2) liver enzymes [aspartate aminotransferase (AST), alkaline phosphatase (ALP), gamma-glutamyl transferase (GGT)]; (3) lipids [total cholesterol (TC), triglycerides (TG), low (LDL) and high (HDL) density lipoproteins]; and metabolic function [glucose, insulin, fructosamine]. Serum CK concentrations were lower at the end of the study, possibly due to no tourist activities like riding. Changes in liver function included increased AST and ALP, also possibly due to physical inactivity. Feeding less bananas and sugar cane was associated with fewer elephants in the obese category and lower TG concentrations. However, increases in glucose, insulin and fructosamine were observed as local people returned to feed elephants after lifting travel restrictions. In sum, changes in several health biomarkers were observed in association with restricted activities and food resources. Camps need better plans to meet the health and welfare needs of elephants during any future disruptions to the tourism industry, although reduced feeding of sweet treats appeared to have positive effects on body condition and metabolic function.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Akaike's Information Criterion in Generalized Estimating Equations
Pan, W. (2001) · Biometrics · doi:10.1111/j.0006-341x.2001.00120.x · Cited by 2,507 · see citing works
TheRPackagegeepackfor Generalized Estimating Equations
Halekoh, U., Højsgaard, S., & Yan, J. (2006) · Journal of Statistical Software · doi:10.18637/jss.v015.i02 · Cited by 1,921 · see citing works
Veterinary Hematology and Clinical Chemistry
Sharkey, L. C. (2004) · Veterinary Clinical Pathology · doi:10.1111/j.1939-165x.2004.tb00383.x · Cited by 950 · see citing works
Creatine kinase monitoring in sport medicine
Brancaccio, P., Maffulli, N., & Limongelli, F. M. (2007) · British Medical Bulletin · doi:10.1093/bmb/ldm014 · Cited by 944 · see citing works
Exercise-stimulated glucose uptake — regulation and implications for glycaemic control
Sylow, L., Kleinert, M., Richter, E. A., & Jensen, T. E. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.162 · Cited by 498 · see citing works
Rautou, P., Cazals-Hatem, D. L., Moreau, R., Francoz, C., Feldmann, G., Lebrec, D., Ogier‐Denis, É., Bédossa, P., Valla, D. C., & Durand, F. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.05.055 · Cited by 209 · see citing works
Serum Lactic Dehydrogenase in the Differential Diagnosis of Acute Hepatocellular Injury
Cassidy, W. M., & Reynolds, T. B. (1994) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-199409000-00008 · Cited by 169 · see citing works
A prospective study of the causes of notably raised aspartate aminotransferase of liver origin
Whitehead, M. W., Hawkes, N., Hainsworth, I. R., & Kingham, J. G. C. (1999) · Gut · doi:10.1136/gut.45.1.129 · Cited by 166 · see citing works
Morfeld, K. A., Meehan, C. L., Hogan, J. N., & Brown, J. L. (2016) · PLOS ONE · doi:10.1371/journal.pone.0155146 · Cited by 114 · see citing works
Self-citationCreatine kinase in the dog: A review
Aktaş, M. S., Auguste, D., Lefebvre, H. P., Toutain, P., & Braun, J. P. (1993) · Veterinary Research Communications · doi:10.1007/bf01839386 · Cited by 108 · see citing works
Severe acute liver damage in anorexia nervosa: two case reports
Caprio, C. D., Alfano, A., Senatore, I., Zarrella, L., Pasanisi, F., & Contaldo, F. (2006) · Nutrition · doi:10.1016/j.nut.2006.01.003 · Cited by 106 · see citing works
The diagnosis of equine insulin dysregulation
Bertin, F., & de Laat, M. A. (2017) · Equine Veterinary Journal · doi:10.1111/evj.12703 · Cited by 95 · see citing works
Effects of physical activity upon the liver
Shephard, R. J., & Johnson, N. A. (2014) · European Journal of Applied Physiology · doi:10.1007/s00421-014-3031-6 · Cited by 88 · see citing works
Rovira, S., Muñoz, A., & Benito, M. (2008) · Veterinární Medicína · doi:10.17221/1860-vetmed · Cited by 82 · see citing works
Pokharel, S. S., Seshagiri, P. B., & Sukumar, R. (2017) · Conservation Physiology · doi:10.1093/conphys/cox039 · Cited by 75 · see citing works
Stress and body condition are associated with climate and demography in Asian elephants
Mumby, H. S., Mar, K. U., Thitaram, C., Courtiol, A., Towiboon, P., Min-Oo, Z., Htut-Aung, Y., Brown, J. L., & Lummaa, V. (2015) · Conservation Physiology · doi:10.1093/conphys/cov030 · Cited by 72 · see citing works
Self-citationMagkos, F. (2009) · Progress in Lipid Research · doi:10.1016/j.plipres.2009.02.003 · Cited by 71 · see citing works
Liver function test abnormalities in anorexia nervosa—Cause or effect
Narayanan, V., Gaudiani, J. L., Harris, R. H., & Mehler, P. S. (2009) · International Journal of Eating Disorders · doi:10.1002/eat.20690 · Cited by 68 · see citing works
Ozawa, Y., SHIMIZU, T., & Shishiba, Y. (1998) · Internal Medicine · doi:10.2169/internalmedicine.37.32 · Cited by 64 · see citing works
Morfeld, K. A., Lehnhardt, J., Alligood, C. A., Bolling, J., & Brown, J. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093802 · Cited by 63 · see citing works
Self-citationElevation of liver function tests in severe anorexianervosa
Harris, R. H., Sasson, G., & Mehler, P. S. (2012) · International Journal of Eating Disorders · doi:10.1002/eat.22073 · Cited by 58 · see citing works
Norkaew, T., Brown, J. L., Bansiddhi, P., Somgird, C., Thitaram, C., Punyapornwithaya, V., Punturee, K., Vongchan, P., Somboon, N., & Khonmee, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204965 · Cited by 54 · see citing works
Self-citationKim, J., & Lee, J. (2015) · Physical Activity and Nutrition · doi:10.5717/jenb.2015.15061910 · Cited by 53 · see citing works
Changing trends in elephant camp management in northern Thailand and implications for welfare
Bansiddhi, P., Brown, J. L., Thitaram, C., Punyapornwithaya, V., Somgird, C., Edwards, K. L., & Nganvongpanit, K. (2018) · PeerJ · doi:10.7717/peerj.5996 · Cited by 52 · see citing works
Self-citationWelfare assessment and activities of captive elephants in Thailand
Bansiddhi, P., Brown, J. L., & Thitaram, C. (2020) · Animals · doi:10.3390/ani10060919 · Cited by 52 · see citing works
Self-citationTennant, B. C., & Sharon A. Center (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-370491-7.00013-1 · Cited by 47 · see citing works
Skrypnik, D., Ratajczak, M., Karolkiewicz, J., Mądry, E., Pupek‐Musialik, D., Hansdorfer-Korzon, R., Walkowiak, J., Jakubowski, H., & Bogdański, P. (2016) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2016.02.017 · Cited by 46 · see citing works
Bansiddhi, P., Brown, J. L., Khonmee, J., Norkaew, T., Nganvongpanit, K., Punyapornwithaya, V., Angkawanish, T., Somgird, C., & Thitaram, C. (2019) · PLoS ONE · doi:10.1371/journal.pone.0221537 · Cited by 46 · see citing works
Self-citationThe Liver and Hemorrhagic Shock
Helling, T. S. (2005) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2005.05.035 · Cited by 45 · see citing works
Associations of Serum Alkaline Phosphatase with Metabolic Syndrome and Mortality
Krishnamurthy, V. R., Baird, B. C., Wei, G., Greene, T., Raphael, K. L., & Beddhu, S. (2011) · The American Journal of Medicine · doi:10.1016/j.amjmed.2010.11.030 · Cited by 44 · see citing works
Sustained, Low-Intensity Exercise Achieved by a Dynamic Feeding System Decreases Body Fat in Ponies
de Laat, M. A., Hampson, B. A., Sillence, M. N., & Pollitt, C. C. (2016) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.14577 · Cited by 43 · see citing works
Exercise‐Induced Transient Hyperlipidemia in the Racehorse
Pösö, A. R., Viljanen‐Tarifa, E., Soveri, T., & Oksanen, H. E. (1989) · Zentralblatt für Veterinärmedizin Reihe A · doi:10.1111/j.1439-0442.1989.tb00771.x · Cited by 41 · see citing works
Mokuno, K., Riku, S., Sugimura, K., Takahashi, A., Kato, K., & Osugi, S. (1987) · Muscle & Nerve · doi:10.1002/mus.880100513 · Cited by 40 · see citing works
Valberg, S. J. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-370491-7.00015-5 · Cited by 37 · see citing works
Management factors affecting physical health and welfare of tourist camp elephants in Thailand
Bansiddhi, P., Nganvongpanit, K., Brown, J. L., Punyapornwithaya, V., Pongsopawijit, P., & Thitaram, C. (2019) · PeerJ · doi:10.7717/peerj.6756 · Cited by 32 · see citing works
Self-citationKhonmee, J., Norkaew, T., Brown, J. L., Bansiddhi, P., Somgird, C., Thitaram, C., Punyapornwithaya, V., Punturee, K., Vongchan, P., & Somboon, N. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210537 · Cited by 32 · see citing works
Self-citationCreatine Kinase Levels After Exercise
Kindermann, W. (2016) · Deutsches Ärzteblatt international · doi:10.3238/arztebl.2016.0344a · Cited by 31 · see citing works
Rambau, M. D., Fushai, F., & Baloyi, J. J. (2016) · South African Journal of Animal Science · doi:10.4314/sajas.v46i4.8 · Cited by 27 · see citing works
Brown, J. L., Bansiddhi, P., Khonmee, J., & Thitaram, C. (2020) · Animals · doi:10.3390/ani10040737 · Cited by 26 · see citing works
Self-citationNorkaew, T., Brown, J. L., Thitaram, C., Bansiddhi, P., Somgird, C., Punyapornwithaya, V., Punturee, K., Vongchan, P., Somboon, N., & Khonmee, J. (2019) · PLoS ONE · doi:10.1371/journal.pone.0218579 · Cited by 25 · see citing works
Self-citation[Rhabdomyolysis: clinical features, causes, complications and treatment].
Szumilak, D., Sułowicz, W., & Walatek, B. (1998) · PubMed · Cited by 24 · see citing works
Kosaruk, W., Brown, J. L., Plangsangmas, T., Towiboon, P., Punyapornwithaya, V., Silva-Fletcher, A., Thitaram, C., Khonmee, J., Edwards, K. L., & Somgird, C. (2020) · Animals · doi:10.3390/ani10101928 · Cited by 24 · see citing works
Self-citationPhysical activity, sedentary time, and liver enzymes in adolescents: the HELENA study
; on behalf of the HELENA Study Group, Ruiz, J. R., Labayen, I., Ortega, F. B., Moreno, L. A., Rodrı́guez, G., Breidenassel, C., Μanios, Y., Kafatos, A., Molnár, D., et al. (2014) · Pediatric Research · doi:10.1038/pr.2014.26 · Cited by 23 · see citing works
Effect of exercise on serum markers of muscle inflammation in Spanish Greyhounds
Lucas, V., Barrera, R., Duque, F. J., Ruiz, P., & Zaragoza, C. (2015) · American Journal of Veterinary Research · doi:10.2460/ajvr.76.7.637 · Cited by 23 · see citing works
Re-evaluation of the fructosamine reaction.
Phillipou, G., Seaborn, C. J., & Phillips, P. J. (1988) · Clinical Chemistry · doi:10.1093/clinchem/34.8.1561 · Cited by 22 · see citing works
Khonmee, J., Brown, J. L., Rojanasthien, S., Aunsusin, A., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V., & Thitaram, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091633 · Cited by 22 · see citing works
Self-citationMorfeld, K. A., & Brown, J. L. (2017) · PLOS ONE · doi:10.1371/journal.pone.0188701 · Cited by 22 · see citing works
Self-citationMikota, S. K. (2006) · doi:10.1002/9780470344484.ch25 · Cited by 21 · see citing works
Cold Exposure-induced Rhabdomyolysis Demonstrated by Bone Scintigraphy
Lim, S. T., Sohn, M., & Jeong, H. (2008) · Clinical Nuclear Medicine · doi:10.1097/rlu.0b013e31816a78f8 · Cited by 17 · see citing works
Khonmee, J., Brown, J. L., Rojanasthien, S., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V., & Thitaram, C. (2014) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2014.02.008 · Cited by 17 · see citing works
Self-citationDierenfeld, E. S., Han, Y. A. M., Mar, K. U., Aung, A., Soe, A. T., Lummaa, V., & Lahdenperä, M. (2020) · Animals · doi:10.3390/ani10040725 · Cited by 16 · see citing works
Supanta, J., Brown, J. L., Bansiddhi, P., Thitaram, C., Punyapornwithaya, V., & Khonmee, J. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.1038855 · Cited by 14 · see citing works
Self-citationCorrelation between the High Density Lipoprotein and its Subtypes in Coronary Heart Disease
Gao, F., Ya-juan, R., Shen, X., Bian, Y., Chuan-shi, X., & Li, H. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000445552 · Cited by 13 · see citing works
Li, ., Hua, S., Chen, G., Strizich, G., Kuniholm, M. H., Shan, Z., Talavera, G. A., Castañeda, S. F., Gellman, M. D., Cai, J., et al. (2020) · Liver International · doi:10.1111/liv.14514 · Cited by 12 · see citing works
A survey of stereotypic behaviors in tourist camp elephants in Chiang Mai, Thailand
Fuktong, S., Yuttasaen, P., Punyapornwithaya, V., Brown, J. L., Thitaram, C., Luevitoonvechakij, N., & Bansiddhi, P. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105456 · Cited by 12 · see citing works
Self-citationChemical characteristic and cholesterol level of local sheep with intensive fattening
Hatta, M., Priyanto, R., Mas, M. S., & Prahesti, K. I. (2019) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/247/1/012025 · Cited by 10 · see citing works
Lipid and Lipoprotein Profiles Modification in Athletic Horses After Repeated Jumping Events
Assenza, A., Arfuso, F., Zanghì, E., Fazio, F., Bruschetta, D., & Piccione, G. G. (2016) · Journal of Equine Veterinary Science · doi:10.1016/j.jevs.2016.05.001 · Cited by 9 · see citing works
Starvation-induced Liver Enzyme Elevation after Initiation of Feeding
Nishioka, H., Yoshizaki, A., Imai, Y., & Higashibeppu, N. (2018) · Internal Medicine · doi:10.2169/internalmedicine.1663-18 · Cited by 8 · see citing works
Seasonal variation of health in Asian elephants
dos Santos, D. J. F., Berger, V., Cristofari, R., Htut, W., Nyein, U. K., Aung, H. H., Reichert, S., & Lummaa, V. (2020) · Conservation Physiology · doi:10.1093/conphys/coaa119 · Cited by 8 · see citing works
Spinella, G., Valentini, S., Musella, V., Bortolotti, E., & Lopedote, M. (2021) · Animals · doi:10.3390/ani11071879 · Cited by 8 · see citing works
Sakata, M., Takaki, A., Oyama, A., Adachi, T., Wada, N., Takeuchi, Y., Yasunaka, T., ONISHI, H., Shiraha, H., & Okada, H. (2020) · The Kurume Medical Journal · doi:10.2739/kurumemedj.ms6723011 · Cited by 8 · see citing works
Serum Chemistry of Southern Populations of Black Bears (Ursus americanus)
Hellgren, E. C., Maehr, D. S., & Doan-Crider, D. L. (1997) · The American Midland Naturalist · doi:10.2307/2426758 · Cited by 7 · see citing works
Zhang, Y., Zheng, P., Shi, J., Ma, Y., Chen, Z., Wang, T., & Jia, G. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.163250 · Cited by 6 · see citing works
Age related variation of health markers in Asian elephants
Reichert, S., Berger, V., dos Santos, D. J. F., Lahdenperä, M., Nyein, U. K., Htut, W., & Lummaa, V. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111629 · Cited by 4 · see citing works
Yang, Y., Tummaruk, P., Angkawanish, T., Langkaphin, W., & Chatdarong, K. (2023) · Animals · doi:10.3390/ani13071133 · Cited by 4 · see citing works
THE EFFECTS OF PHYSICAL EXERCISE ON PLASMA LIPID AND PROTEIN PROFILE IN RACE HORSES
Özcan, M., Arslan, M., Çötelioğlu, Ü., & Bakırel, U. (2002) · DergiPark (Istanbul University) · doi:10.16988/iuvfd.38394 · Cited by 3 · see citing works
[Effects of freezing and hypoxia on serum creatine kinase activity in rats].
Liu, J., Zhang, Z., Yang, Z., Li, F., Yan, P., & Liu, Y. (1996) · PubMed · Cited by 3 · see citing works
Physiological response of exercise as modulation of lipid profile in young adults
Sugiharto, S., Merawati, D., Susanto, H., Taufiq, A., Pranoto, A., & Angga, P. D. (2023) · Comparative Exercise Physiology · doi:10.3920/cep220056 · Cited by 3 · see citing works
Veterinary Laboratory Medicine (Clinical Biochemistry and Haematology), Morag G. Kerr
Duncan, N. M. (1991) · Journal of the South African Veterinary Association · doi:10.4102/jsava.v62i1.1574 · Cited by 2 · see citing works
Why is HDL‐cholesterol good cholesterol?
Stanley, J. C. (2008) · Lipid Technology · doi:10.1002/lite.200800039 · Cited by 1 · see citing works
Association between physical activity and serum liver aminotransferases in Southwestern Iran
Badiei, S., Hashemi, S. J., Masjedizadeh, A., Sayyah, J., Mohammadi, Z., Hariri, S., Hashemi, F., Rahimi, Z., Danehchin, L., Abolnezhadian, F., et al. (2022) · Journal of Research in Medical Sciences · doi:10.4103/jrms.jrms_835_21 · Cited by 1 · see citing works
Flagged first, then by citations
3 of the 74 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Ghimire, R., Brown, J. L., Thitaram, C., & Bansiddhi, P. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1370909 · Cited by 8 · see citing works
“…(49), but during an international travel ban in Thailand during the Covid-19 pandemic, the highest concentrations were in the rainy season, suggesting it is tourist activities that are the most likely cause of increased glucocorticoid excretion during the winter, high tourist season months (114).”
BackgroundSelf-citationSupanta, J., Brown, J. L., Bansiddhi, P., Thitaram, C., Punyapornwithaya, V., Punturee, K., Towiboon, P., Somboon, N., & Khonmee, J. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1351361 · Cited by 4 · see citing works
Self-citationMetabolic profiles of captive Asian elephants (Elephas maximus) in Lao PDR and Thailand
Pérez, A. B. L., Brown, J. L., Punyapornwithaya, V., Thitaram, C., Pongsumpan, J., Supanta, J., Tocharoennirattisai, W., & Khonmee, J. (2025) · PLoS ONE · doi:10.1371/journal.pone.0334550
Self-citationSaengthong, A., Brown, J. L., Towiboon, P., Punturee, K., Buddhasiri, S., Nganvongpanit, K., Punyapornwithaya, V., Tocharoennirattisai, W., & Khonmee, J. (2026) · PLoS ONE · doi:10.1371/journal.pone.0344383
Self-citation
- Authors
- Supanta, J., Brown, J. L., Bansiddhi, P., Thitaram, C., Punyapornwithaya, V., Punturee, K., Somboon, N., Towiboon, P., & Khonmee, J.
- Affiliations
- Chiang Mai University (TH)
- Smithsonian Conservation Biology Institute (US)
- Corresponding author
- Khonmee, Jaruwan
- ORCID
- Venue
- Frontiers in Veterinary Science
- Publisher
- Frontiers Media SA
- Published
- 2023-12-21
- Volume
- 10
- Pages
- 1303537-1303537
- ISSN
- 2297-1769 (ISSN-L)
- PMC
- PMC10764436
- OpenAlex
- W4390056188
- Cited by
- 4
- References
- 74
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Veterinary Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Smithsonian Institution
- Chiang Mai University
- Smithsonian Conservation Biology Institute
- Faculty of Veterinary Medicine, Chiang Mai University (R000032244)
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Health Sciences › Veterinary › Equine › Veterinary Equine Medical Research
- Physical Sciences › Environmental Science › Ecology › Wildlife Ecology and Conservation
- Keywords
- captive elephants, elephant welfare, body condition score, muscle enzymes, creatine kinase, aspartate aminotransferase, liver enzymes, serum lipids, glucose, insulin, fructosamine, physical inactivity, tourism disruption
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
