MICROBIOTA BACTERIANA E ANTIBIOGRAMA DA CAVIDADE ORAL DE SERPENTES MANTIDAS SOB CUIDADOS HUMANOS

Authors

  • Samanta Arruda Quile de Oliveira Universidade de Sorocaba (UNISO)
  • Julia Mara Souza Eisenlohr Universidade de Sorocaba (UNISO) https://orcid.org/0009-0000-7414-2712
  • Mônica Rodrigues Alves Universidade de Sorocaba (UNISO)
  • Beatriz Fernandes de Camargo Universidade de Sorocaba (UNISO) https://orcid.org/0009-0006-4650-2235
  • Jéssica Parisi
  • Bianca Gianola Belline Silva Universidade de Sorocaba (UNISO) https://orcid.org/0000-0002-8979-8017
  • Rodrigo Hidalgo Friciello Teixeira Universidade de Sorocaba (UNISO). Parque Zoológico Municipal Quinzinho de Barros, Sorocaba, SP. Universidade Estadual Paulista (UNESP), Botucatu, SP. Programa de Pós-Graduação em Animais Selvagens da Universidade Paulista “Júlio de Mesquita Filho” (UNESP), Botucatu, SP https://orcid.org/0000-0001-8219-0845

DOI:

https://doi.org/10.35172/rvz.2025.v32.1689

Keywords:

antimicrobials, enterobacteria, bacterial isolation, reptiles, bacterial resistance, zoos

Abstract

Modern zoos play an essential role in biodiversity conservation, contributing to the management of wild species kept under human care. Snakes can harbor bacteria with zoonotic potential in their oral cavity, posing a risk to the health of reptiles as well as other animals and humans. This study aimed to evaluate the bacterial microbiota of the oral cavity of snakes from the families Boidae, Colubridae, and Dipsadidae kept at the Quinzinho de Barros Municipal Zoo, in Sorocaba/SP, Brazil. The research was conducted through the collection of oral cavity samples from 30 snakes using sterile swabs. The samples were cultured in MacConkey Agar and subjected to biochemical tests, Gram staining, and antibiograms for bacterial identification and evaluation of antimicrobial sensitivity. The results indicated the presence of various Gram-negative and Gram-positive bacteria, with Citrobacter freundii being the most prevalent species, followed by Klebsiella pneumoniae, Serratia spp., Salmonella spp., and Escherichia coli. Antimicrobial sensitivity tests demonstrated that Meropenem and Piperacillin were the most effective antibiotics, with sensitivity rates of 85.2%, while other drugs, such as ampicillin and cefotaxime, showed higher resistance, ranging from 40.7% to 59.3%. The techniques employed allowed mapping of the bacterial microbiota of the studied snakes' oral cavity and evaluation of antimicrobial resistance. These findings are fundamental for the development of sanitary management strategies and more effective treatments, reducing the risks of infections and bacterial resistance in snakes under human care.

References

D'Cruze N, Khan S, Carder G, Megson D, Coulthard E, Norrey J, et al. A global review of animal–visitor interactions in modern zoos and aquariums and their implications for wild animal welfare. Animals (Basel). 2019;9(6):332. D’Cruze, N., Khan, S., Carder, G., Megson, D., Coulthard, E., Norrey, J., & Groves, G. (2019). A Global Review of Animal–Visitor Interactions in Modern Zoos and Aquariums and Their Implications for Wild Animal Welfare. Animals, 9(6), 332. https://doi.org/10.3390/ani9060332

Brando S, Herrelko E. Wild animals in the city: Considering and connecting with animals in zoos and aquariums. The International Library of Environmental, Agricultural and Food Ethics. 2021. p. 341-360. https://doi.org/10.1007/978-3-030-63523-7_19

Duque FG, Ferreira CS, Laste VJ, Silva BL, Campacci MS, Pacheco BF. Zoológico e aquários: Sua importância contemporânea. Rev Bras Educ Ambient. 2021;16(5):8-26. https://doi.org/10.34024/revbea.2021.v16.11711

Hu X, Yang L, Zhang Y, Yang M, Li J, Fan Y, Guo P, Tian Z. Fecal and oral microbiome analysis of snakes from China reveals a novel natural emerging disease reservoir. Front Microbiol. 2024;11:14:1339188. https://doi.org/10.3389/fmicb.2023.1339188

Jacobson ER. Antibiotic therapy for reptiles. Current Veterinary Therapy XIII. Small Animal Practice 2000. p. 1168-1169.

Blaylock R, et al. Normal oral bacterial flora from some southern African snakes. Onderstepoort J Vet Res. 2001;68(3):175-182.

Lin W, Tsai T. Comparisons of the oral microbiota from seven species of wild venomous snakes in Taiwan using the high-throughput amplicon sequencing of the full-length 16S rRNA gene. Biology (Basel). 2023;12(9):1206. https://doi.org/10.3390/biology12091206

Hedley J, Whitehead ML, Munns C, Pellett S, Abou‐Zahr T, Calvo Carrasco D, et al. Antibiotic stewardship for reptiles. J Small Anim Pract. 2021. p. 829-839. https://doi.org/10.1111/jsap.13402

Ghosh T, Biswas M, Roy P, Guin C. Short review of different microflora from the oral cavity of snakes. Uttar Pradesh J Zool. 2017;37(1&2):30-34. https://doi.org/10.3390/biology12091206

Zancolli G, Mahsberg D, Sickel W, Keller A. Reptiles as reservoirs of bacterial infections: real threat or methodological bias? Microb Ecol. 2015;70(3):579-584. https://doi.org/10.1007/s00248-015-0618-3

Ferreira Junior RS, Siqueira AK, Campagner MV, Salerno T, Soares TCS, Lucheis SB, et al. Comparison of wildlife and captivity rattlesnakes (Crotalus durissus terrificus) microbiota. Pesq Vet Bras. 2009;29(12):999-1003. https://doi.org/10.1590/S0100-736X2009001200008

Maugeri G, Lychko I, Sobral R, Roque A. Identification and antibiotic-susceptibility profiling of infectious bacterial agents: a review of current and future trends. Biotechnol J. 2018;14:e1700750. https://doi.org/10.1002/biot.201700750

Cristina RT, Kocsis R, Dégi J, Muselin F, Dumitrescu E, Tirziu E, et al. Pathology and prevalence of antibiotic-resistant bacteria: a study of 398 pet reptiles. Animals (Basel). 2022;12(10):1279. https://doi.org/10.3390/ani12101279

Dipineto L, Russo TP, Calabria M, et al. Oral flora of Python regius kept as pets. Lett Appl Microbiol. 2014;8(5):462-465. https://doi.org/10.1111/lam.12214

Liu H, Zhao Z, Xue Y, Ding K, Xue Q. Fatal cases of Citrobacter freundii septicemia and encephalitis in sheep. J Vet Diagn Invest. 2018;30(2):245-248. https://doi.org/10.1177/1040638717731090

Su HY, Hussain B, Hsu BM, Lee KH, Mao YC, Chiang LC, et al. Bacterial community analysis identifies Klebsiella pneumoniae as a native symbiotic bacterium in the newborn Protobothrops mucrosquamatus. BMC Microbiol. 2023;23(1):213. https://doi.org/10.1186/s12866-023-02936-4

Hedley J. Anatomy and disorders of the oral cavity of reptiles and amphibians. Vet Clin North Am Exot Anim Pract. 2016;19(3):689-706. https://doi.org/10.1016/j.cvex.2016.04.002

Chinnadurai SK, Devoe RS. Selected infectious diseases of reptiles. Vet Clin North Am Exot Anim Pract. 2009;12(3):583–596. https://doi.org/10.1016/j.cvex.2009.06.008

Dai Y. Toxicity study of sulfonamides antibiotics. Front Sustain Dev. 2024;4(6):109-112. https://doi.org/10.54691/957gfp28

Liu L, Chen D, Liu L, Lan R, Hao S, Jin W, et al. Genetic diversity, multidrug resistance, and virulence of Citrobacter freundii from diarrheal patients and healthy individuals. Front Cell Infect Microbiol. 2018;10(8):233. https://doi.org/10.3389/fcimb.2018.00233

Liu L, Lan R, Liu L, Wang Y, Zhang Y, Wang Y, Xu J. Antimicrobial resistance and cytotoxicity of Citrobacter spp. in Maanshan Anhui Province, China. Front Microbiol. 2017;20(8):1357. https://doi.org/10.3389/fmicb.2017.01357

Hayder T, Aljanaby A. Antibiotics susceptibility patterns of Citrobacter freundii isolated from patients with urinary tract infection in Al-Najaf governorate – Iraq. Int J Res Pharm Sci. 2019; 10(2):1481-1488. https://doi.org/10.26452/ijrps.v10i2.722

Rahman A, Shamsuzzaman S, Dola N. Antimicrobial susceptibility pattern and virulence genes detection in Citrobacter freundii isolated from patients of a tertiary care hospital, Bangladesh. Int Arab J Antimicrob Agents. 2022; 12(2):1-7. https://doi.org/10.3823/865

Liu, L., Qin, L., Hao, S., Lan, R., Xu, B., Guo, Y., Jiang, R., Sun, H., Chen, X., LV, X., Xu, J., Zhao, C. Lineage, Antimicrobial Resistance and Virulence of Citrobacter spp. Pathogens. 2020; 9(3):195. https://doi.org/10.3390/pathogens9030195

Makavchik S, Borisova M. Antibiotic resistance of Klebsiella pneumoniae and practical significance for veterinary medicine. Leg Reg Vet Med. 2023; 1:26-30. https://doi.org/10.52419/issn2782-6252.2023.1.26

Harada K, Shimizu T, Mukai Y, Kuwajima K, Sato T, Usui M, Tamura Y, Kimura Y, Miyamoto T, Tsuyuki Y, Ohki A, Kataoka Y. Phenotypic and molecular characterization of antimicrobial resistance in Klebsiella spp. isolates from companion animals in Japan: clonal dissemination of multidrug-resistant extended-spectrum β-lactamase-producing Klebsiella pneumoniae. Front Microbiol. 2016; 7:1021. https://doi.org/10.3389/fmicb.2016.01021

Sebola D, Oguttu J, Kock M, Qekwana D. Antimicrobial resistance patterns of Acinetobacter baumannii and Klebsiella pneumoniae isolated from dogs presented at a veterinary academic hospital in South Africa. Vet World. 2023;16:1880-1888. https://doi.org/10.14202/vetworld.2023.1880-1888

Kowalczyk J, Czokajło I, Gańko M, Śmiałek M, Koncicki A. Identification and antimicrobial resistance in Klebsiella spp. isolates from turkeys in Poland between 2019 and 2022. Animals (Basel). 2022; 2(22):3157. https://doi.org/10.3390/ani12223157

Abdullah A, Nadhom B, Al-Ammiri H. Isolation and identification of Serratia marcescens from bovine mastitis infections in Iraq and their susceptibility to antibiotics. J Entomol Zool Stud. 2017;5:489-492. https://doi.org/10.13140/RG.2.2.25863.83362

Allen J, Doidge N, Bushell R, Browning G, Marenda M. Healthcare-associated infections caused by chlorhexidine-tolerant Serratia marcescens carrying a promiscuous IncHI2 multi-drug resistance plasmid in a veterinary hospital. PLoS One. 2022; 17(3):e0264848. https://doi.org/10.1371/journal.pone.0264848

Cota J, Carvalho A, Dias I, Reisinho A, Bernardo F, Oliveira M. Salmonella spp. in pet reptiles in Portugal: prevalence and chlorhexidine gluconate antimicrobial efficacy. Antibiotics (Basel). 2021; 10(3):324. https://doi.org/10.3390/antibiotics10030324

Abatcha M, Zakaria Z, Kaur D, Thong K. Prevalence and antimicrobial susceptibility of Salmonella spp. isolated from snakes in Peninsular Malaysia. J Vet Adv. 2013;3:306-312.

Dégi J, Herman V, Radulov I, Morariu F, Florea T, Imre K. Surveys on pet-reptile-associated multi-drug-resistant Salmonella spp. in the Timișoara Metropolitan Region—Western Romania. Antibiotics (Basel). 2023; 12(7):1203. https://doi.org/10.3390/antibiotics12071203

Marín C, Lorenzo-Rebenaque L, Laso O, Villora-Gonzalez J, Vega S. Pet reptiles: a potential source of transmission of multidrug-resistant Salmonella. Front Vet Sci. 2021;7. https://doi.org/10.3389/fvets.2020.613718

Xia Y, Li H, Shen Y. Antimicrobial drug resistance in Salmonella enteritidis isolated from edible snakes with pneumonia and its pathogenicity in chickens. Front Vet Sci. 2020; 7:613718. https://doi.org/10.3389/fvets.2020.00463

Tang P, Divers S, Sanchez S. Antimicrobial susceptibility patterns for aerobic bacteria isolated from reptilian samples submitted to a veterinary diagnostic laboratory: 129 cases (2005-2016). J Am Vet Med Assoc. 2020;257(3):305-312. https://doi.org/10.2460/javma.257.3.305

Mao Y, Liu P, Hung D, Lai W, Huang S, Hung Y, et al. Bacteriology of Naja atra snakebite wound and its implications for antibiotic therapy. Am J Trop Med Hyg. 2016;94(5):1129-1135. https://doi.org/10.4269/ajtmh.15-0667

Published

2025-09-27

How to Cite

1.
Arruda Quile de Oliveira S, Mara Souza Eisenlohr J, Rodrigues Alves M, Fernandes de Camargo B, Parisi J, Gianola Belline Silva B, et al. MICROBIOTA BACTERIANA E ANTIBIOGRAMA DA CAVIDADE ORAL DE SERPENTES MANTIDAS SOB CUIDADOS HUMANOS. RVZ [Internet]. 2025 Sep. 27 [cited 2025 Dec. 5];32:1-11. Available from: https://rvz.emnuvens.com.br/rvz/article/view/1689

Issue

Section

Original Articles

Most read articles by the same author(s)