Molecular detection of Chlamydia spp. and risk factors in farmed siamese crocodile in the mid-northeastern provincial cluster of Thailand https://doi.org/10.12982/VIS.2022.018

Main Article Content

Rawikan Inchuai
Peerapol Sukon
Sompoth Weerakhun

Abstract

This study surveyed the prevalence of chlamydial infection among farms in the mid-northeastern provincial cluster of Thailand by PCR and phylogenetic analyses of the sequences. Samples from 94 crocodiles were collected from 17 farms in five provinces together with farm management data. Chlamydiaceae was found in 48.94% of the samples (46/94). Of the 17 pooled samples analyzed using 16S rRNA sequencing, four samples exhibited 99.3 to 99.5% nucleotide identity with Chlamydia psittaci, three samples exhibited 99.1 to 99.3% nucleotide identity with C. crocodili, and one sample exhibited similarity to both species. The risk factors related to chlamydial infection included the source of young crocodiles and the frequency of water changes. Chlamydial infection was higher in nonclinical crocodiles than in clinical or dead crocodiles (P=0.003). Pharyngitis, fibrinous pharyngitis, hepatitis, pneumonia, and hydropericardium were commonly found in chlamydial-positive cases of ill or dead crocodiles. C. psittaci and C. crocodili were found in both clinical and nonclinical crocodiles. C. psittaci is a well-known zoonotic pathogen. C. crocodili is a new species found in Siamese crocodiles in Thailand. In conclusion, the source of young crocodiles and frequency of water changes were identified as risk factors for chlamydial infection in crocodile farms. C. crocodili should be further investigated to better understand its implications for crocodile heath.

Article Details

How to Cite
Inchuai, R. ., Sukon, P. ., & Weerakhun, S. . (2022). Molecular detection of Chlamydia spp. and risk factors in farmed siamese crocodile in the mid-northeastern provincial cluster of Thailand: https://doi.org/10.12982/VIS.2022.018. Veterinary Integrative Sciences, 20(1), 231–245. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/255945
Section
Research Articles

References

tropics. Office of International Affairs, National Research Council, Washington, D.C.Bodetti, T. J., Jacobson, E., Wan, C., Hafner, L., Pospischil, A., Rose, K., Timms, P. (2002). Molecular Evidence to Support the Expansion of the Hostrange of Chlamydophila pneumoniae to Include Reptiles as Well as Humans, Horses, Koalas and Amphibians. Syst Appl Microbiol, 25(1), 146-152

Borel, N., Polkinghorne, A., Pospischil, A. (2018). A Review on Chlamydial Diseases in Animals: Still a Challenge for Pathologists? Vet Pathol, 55(3), 374–390.

Brien, M. L., Cherkiss, M. S., Parry, M. W., Mazzotti, F. J. (2008). Housing Crocodilians in Captivity: Considerations for Central America and Caribbean. Department of Wildlife Ecology and Conservation, Institute of Food and Agricultural Sciences Extension, University of Florida, Gainesville, Florida, United States of America.

Chaiwattanarungruengpaisan, S., Thongdee M., Anuntakarun S., Payungporn S., Arya N., Punchukrang A., Ramasoota P., Singhakaew S., Atithep T., Sariya L. (2021). A new species of Chlamydia isolated from Siamese crocodiles (Crocodylus siamensis). PLoS One, 16(5), e0252081.

Charruau, P., Pérez-Flores, J., Pérez-Juárez, J. G., Cedeño-Vázquez, J. R., Rosas-Carmona, R. (2012). Oral and cloacal microflora of wild crocodiles Crocodylus acutus and C. moreletii in the Mexican Caribbean. Dis Aquat Organ, 98(1), 27–39.

Cheong, H. C., Lee, C., Cheok, Y. Y., Tan, G., Looi, C. Y., Wong, W. F. (2019). Chlamydiaceae: Diseases in Primary Hosts and Zoonosis. Microorganisms. 7(5), 146.

Dang, W., Zhang, W., Du, W. G. (2015). Incubation temperature affects the immune function of hatchling soft-shelled turtles, Pelodiscus sinensis. Sci Rep, 5, 10594.

Department for Environment and Water. (2020). Recommended Guidelines for the Captive Management of Crocodiles (Crocodylus johnstoni & C. porosus) in South Australia, Government of south Australia. [online]. https://www.environment.sa.gov.au/files/sharedassets/public/plants_and_animals/pa-gen-crocodileguidelines.pdf

Department of Fisheries. (2017). “Crocodile data in Thailand”. Ministry of Agriculture and Cooperatives, Thailand [online]. https://www4.fisheries.go.th/file_article/20170815143855_file.pdf

Donati, M., Laroucau, K., Guerrini, A., Balboni, A., Salvatore, D., Catelli, E., Lupini, C., Levi, A., Di Francesco, A. (2018). Chlamydiosis in Backyard Chickens (Gallus gallus) in Italy. Vector Borne Zoonotic Dis, 18(4), 222–225.

Ebani, V. V. (2017). Domestic reptiles as source of zoonotic bacteria: A mini review, Asian Pac J Trop Med, 10(8), 723–728.

Elwell, C., Mirrashidi, K., Engel, J. (2016). Chlamydia cell biology and pathogenesis. Nat Rev Microbiol, 14(6), 385–400.

Fayez, M.; Elmoslemany, A.; Alorabi, M.; Alkafafy, M.; Qasim, I.; Al-Marri, T.; Elsohaby, I. Seroprevalence and Risk Factors Associated with Chlamydia abortus Infection in Sheep and Goats in Eastern Saudi Arabia. Pathogens, 10, 489. Food and Agriculture Organization of the United Nations (FAO)., n.d. “Captive Breeding and The Management of Adult crocodiles” [online]. http://www.fao.org/3/T0226E/t0226e13.htm#cont1

Gregory, J. F., Deidre, K. F. (2014). Chapter 5 – Crocodilians (Crocodiles, Alligators, Caiman, Gharial). In: Miller, R.E., Fowler, M.E. (Eds.), Fowler’s Zoo and Wild Animal Medicine Volume 8, Elsevier Inc., United States, pp. 38–49.

Guo, W., Li, J., Kaltenboeck, B., Gong, J., Fan, W., Wang, C. (2016). Chlamydia gallinacea, not C. psittaci, is the endemic chlamydial species in chicken (Gallus gallus). Sci Rep 6, 19638.

Huchzermeyer, F. W. (2002). Diseases of farmed crocodiles and ostriches. Rev Sci Tech, 21(2), 265–76.

Huchzermeyer, F. W., Langelet, E., Putterill, J. F. (2008). An outbreak of chlamydiosis in farmed Indopacific crocodiles (Crocodylus porosus). J S Afr Vet Assoc, 79(2), 99–100.

Inchuai, R., Weerakun, S., Nguyen, H. N., Sukon, P. (2021). Global Prevalence of Chlamydial Infections in Reptiles: A Systematic Review and Meta-Analysis. Vector Borne Zoonotic Dis, 21(1), 32–39.

Inland Aquaculture Research and Development Regional. Center 5 (Surat Thani)., n.d. “Crocodile farming. Department of Fisheries”. Ministry of Agriculture and Cooperatives, Thailand. http://www.fisheries.go.th/if-suratthani/1crocodile.htm

Jelocnik, M. (2019). Chlamydiae from Down Under: The Curious Cases of Chlamydial Infections in Australia. Microorganisms, 7(12), 602.

Jerrett, I., Elliott, N., Tran-Nguyen, L. (2008). Chlamydial Infection in Farmed Crocodiles. Rural Industries Research and Development Corporation. Australian Government. Barton, Australian Capital Territory.

Kabeya, H., Sato, S., Maruyama, S. (2015). Prevalence and Characterization of Chlamydia DNA in zoo animals in Japan. Microbiol Immunol, 59, 507–515

Lagae, S., Kalmar, I., Laroucau, K., Vorimore, F., Vanrompay, D. (2014). Emerging Chlamydia psittaci infections in chickens and examination of transmission to humans. J Med Microbiol, 63(Pt 3), 399–407.

Leslie, A.J., Spotila, J.R. (2000). Osmoregulation of the Nile crocodile, Crocodylus niloticus, in Lake St. Lucia, Kwazulu/Natal, South Africa. Comp. Biochem. Physiol A Mol Integr Physiol 126(3), 351–65.

Lin, M., Zeng, C., Li, Z., Ma, Y., Jia, X. (2019). Comparative analysis of the composition and function of fecal-gut bacteria in captive juvenile Crocodylus siamensis between healthy and anorexic individuals. Microbiologyopen, 8, e929.

Lovely, C. J., Leslie, A. J. (2008). Normal intestinal flora of wild Nile crocodiles (Crocodylus niloticus) in the Okavango Delta, Botswana. J S Afr Vet Assoc, 79(2), 67–70.

Manolis, S. C., Webb, G. J. W. (compilers). (2016). Best Management Practices for Crocodilian Farming. Version 1. IUCN-SSC Crocodile Specialist Group, Darwin, Australia.

Nevarez, J. (2009). Chapter 6-Crocodilians. In: Mitchell, M.A., Tully, T. N. (Eds.), Manual of Exotic Pet Practice. WB Saunders, 112–135.

Ochsenbein, A. F., Zinkernagel, R. M. (2000). Natural antibodies and complement link innate and acquired immunity. Immunol Today, 21(12), 624–630.

Panzetta, M. E., Valdivia, R. H., Saka, H. A. (2018). Chlamydia Persistence: A Survival Strategy to Evade Antimicrobial Effects in-vitro and in-vivo. Front Microbiol, 9, 3101.

Paungpin, W., Thongdee, M., Chaiwattanarungruengpaisan, S., Sariya, L., Sirimanapong, W., Kasantikul, T., Phonarknguen, R., Darakamas, P., Arya, N. (2021). Coinfection of Chlamydia spp. and herpesvirus in juvenile farmed Siamese crocodiles (Crocodylus siamensis) in Thailand, Vet World, 14(7), 1908-1914.

Paweenasakol, K., Chintrakulchai, P., Changbunjong, T. (2015). Biodiversity of benthic macroinvertebrates and surface water quality at Mahidol University, Nakhon Pathom Province. J Appl Anim Sci, 8(2), 43-56.Pu, W., Guo, G., Yang, N., Li, Q., Yin, F., Wang, P., Zheng, J., Zeng, J. (2019). Three species of Aeromonas (A. dhakensis, A. hydrophila and A. jandaei) isolated from freshwater crocodiles (Crocodylus siamensis) with pneumonia and septicemia. Lett Appl Microbiol, 68(3), 212–218.

Rios, F. M., Zimmerman, L. M. (2015). “Immunology of Reptiles”. John Wiley & Sons, Ltd. [online]. https://doi.org/10.1002/9780470015902.a0026260.

Robertson, T., Bibby, S., O’Rourke, D., Belfiore, T., Agnew-Crumpton, R., Noormohammadi, A.H. (2010). Identification of Chlamydial species in crocodiles and chickens by PCR-HRM curve analysis. Vet Microbiol, 145, 373–379. doi:10.1016/j.vetmic.2010.04.007

Rohde, G., Straube, E., Essig, A., Reinhold, P., Sachse, K. (2010). Chlamydial Zoonoses. Dtsch Arztebl Int, 107(10), 174–80.

Sachse, K., Bavoil, P. M., Kaltenboeck, B., Stephens, R. S., Kuo, C. C., Rosselló-Móra, R., Horn, M. (2015). Emendation of the family Chlamydiaceae: Proposal of a single genus, Chlamydia, to include all currently recognized species. Syst Appl Microbiol, 38(2), 99–103.

Sakurai-Komada, N., Iso, H., Koike, K. A., Ikeda, A., Umesawa, M., Ikehara, S., Tsugane, S. (2014). Association between Chlamydophila pneumoniae infection and risk of coronary heart disease for Japanese: the JPHC study. Atherosclerosis, 233(2), 338–342.

Sariya, L., Kladmanee, K., Bhusri, B., Thaijongrak, P., Tonchiangsai, K., Chaichon, K., Ratanakorn, P. (2015). Molecular evidence for genetic distinctions between Chlamydiaceae detected in Siamese crocodiles (Crocodylus siamesis) and known Chlamydiaceae species. Jpn J Vet Res, 63(1), 5–14.

Santos, F., Leal, D. C., Raso, T. F., Souza, B. M. P. S., Cunha, R. M., Martinez, V. H. R., Barrouin-Melo, S. M., Franke, C. R. (2014). Risk factors associated with Chlamydia psittaci infection in psittacine birds. J Med Microbiol, 63, 458–463.Shilton, C. M., Jerrett, I. V., Davis, S., Walsh, S., Benedict, S., Iberg, S. R., Webb, G. J. W., Manolis, C., Hyndman, T. H., Phalen, D., Brown, G. P., Melville, L. (2016). Diagnosis investigation of new disease syndromes in farmed Australian saltwater crocodiles (Crocodylus porosus) reveals associations with herpesviral infection. J Vet Diagn Invest, 28(3), 279–290.

Staub, E., Marti, H., Biondi, R., Levi, A., Donati, M., Leonard, C.A., Ley, S. D., Pillonel, T., Greub, G., Seth-Smith, H. M. B., Borel, N. (2018). Novel Chlamydia species isolated from snakes are temperature-sensitive and exhibit decreased susceptibility to azithromycin. Sci Rep, 8(1), 5660.

Suksai, P., Onket, R., Wiriyarat, W., Sangkachai, N., Lekcharoen, P., Sariya, L. (2019). Occurrence of Chlamydia spp. in wild birds in Thailand. Asian Pac J Trop Med, 12(2), 67–71.

Suvarnabhumi Airport Fish Inspection Office. (2021). Export-Import of Aquatic Animals/Products at Suvarnabhumi airport on June 2021. Fish Quarantine and Inspection Division, Department of Fisheries, Ministry of Agriculture and Cooperatives, Thailand [online]. https://www4.fisheries.go.th/local/file_document/20210707174619_1_file.pdf

The Center of Food Security and Public Health [CFSPH]. (2017). Zoonotic Chlamydiae Maintained in Mammals. College of Veterinary Medicine, Iowa State University [online]. http://www.cfsph.iastate.edu/Factsheets/pdfs/chlamydiosis.pdf

The DEW Fauna Permit Unit., n.d. Recommended Guidelines for the Captive Management of Crocodiles (Crocodylus johnstoni & C. porosus) in South Australia, The Department for Environment and Water Government of south Australia [online]. https://www.environment.sa.gov.au/files/sharedassets/public/plants_and_animals/pa-gen-crocodileguidelines.pdf

Thongkamkoon, P., Tohmee, N., Morris, E. K., Inamnuay, L., Lombardini, E. D. (2018). Combined Fatal Systemic Chlamydia sp. and Aeromonas sobria Infection in Juvenile Siamese Crocodiles (Crocodylus siamensis). Vet Pathol, 55(5), 736–740.

Timms, P. (2009). Chlamydial infections in birds and animals. Australia and New Zealand Standard Diagnostic Procedure, 1–14.

Ujvari, B., Madsen, T. (2006). Age, parasites, and condition affect humoral immune response in tropical pythons. Behav Ecol, 17(1), 20–24.

Vlaholić, K., Dovč, A., Lasta, P. (2006). Zoonotic aspects of animal chlamydioses – a review. Vet Arh, 76, S259–S274.

Zimmerman, L.M., Vogel, L.A., Bowden, R. M. (2010). Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol, 213(5), 661–671.