Pseudomonas aeruginosa from pet Chinese stripe-necked turtles (Ocadia sinensis) demonstrating antimicrobial and heavy metal resistance https://doi.org/10.12982/VIS.2022.059

Main Article Content

M.V.K.S. Wickramanayake
L.A.D.S. De Silva
Gang-Joon Heo

Abstract

Leading nosocomial pathogen Pseudomonas aeruginosa has increasingly been reported to be an opportunistic pathogen. In this study, a total of twenty P. aeruginosa isolates were isolated from 40 pet Chinese stripe-necked turtles and examined for their antimicrobial and heavy metal resistance properties. All isolates were multidrug resistance by scoring multiple antimicrobial resistance indices ≥0.2. In the disc distribution test, 100% resistance to ampicillin and oxacillin were detected. In addition to that, 14 (70%) isolate demonstrated amoxicillin resistance. Imipenem, fosfomycin, gentamycin, tobramycin and piperacillin resistance were detected in 40%, 15%, 20%, 10% and 5% of the isolates, respectively. The ESBLs gene that predominated in this study was blaSHV (55%), followed by blaTEM (50%), blaCTX (10%) and blaOXA (5%). The most frequent aminoglycoside resistance gene in this study was aac(6´)-Ib (40%). Class1 integron integrase gene intI1 and class 1 integron gene cassette gene aadA1 were detected in 45% and 35% of the isolates, respectively. All P. aeruginosa isolates demonstrated Cu and Cd resistance. CzcA and CopA genes were detected in 65% and 30% of the isolates, respectively. These findings reveal the presence of pet turtle-born P. aeruginosa can be a potential risk to public health and cannot be excluded as a non-nosocomial source of infections.

Downloads

Download data is not yet available.

Article Details

How to Cite
Wickramanayake, M. ., De Silva, L. ., & Heo, G.-J. . (2022). Pseudomonas aeruginosa from pet Chinese stripe-necked turtles (Ocadia sinensis) demonstrating antimicrobial and heavy metal resistance: https://doi.org/10.12982/VIS.2022.059. Veterinary Integrative Sciences, 20(3), 761–773. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/259793
Section
Research Articles

References

Anderson, M., 2008. Turtles for vets. Worms and germs blog. Available online: https://www.wormsandgermsblog.com/2008/04/articles/animals/information-sheets-forveterinarians/ (Accessed on February 1, 2020).

Bassetti, M., Vena, A., Croxatto, A., Righi, E., Guery, B., 2018. How to manage Pseudomonas aeruginosa infections. Drugs Context. 7, 212527.

Bédard, E., Charron, D., Lalancette, C., Déziel, E., Prévost, M., 2014. Recovery of Pseudomonas aeruginosa culturability following copper- and chlorine-induced stress. FEMS Microbiol. Lett. 356, 226–234.

Bluvias, J.E., K.L. Eckert, 2010. Marine turtle trauma response procedures: A husbandry manual. Wider Caribbean Sea Turtle Conservation Network (WIDECAST),Missouri.

Boerlin, P., Reid-Smith, R.J., 2008. Antimicrobial resistance: its emergence and transmission. Anim. Health Res. Rev. 9(2), 115-126.

Chellaiah, E.R., 2018. Cadmium (heavy metals) bioremediation by pseudomonas aeruginosa: a minireview. Appl. Water Sci. 8(6), 154.

Clifton, J.I., Peckham, D.J., 2010. Defining routes of airborne transmission of pseudomonas aeruginosa in people with cystic fibrosis. Expert Rev. Respir. Med. 4, 519-529.

CLSI, 2014. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement, Document No. M100-S24. Clinical and Laboratory Standards Institute, Pennsylvania.

Deng, Y., Wu, Y., Jiang, L., Tan, A., Zhang, R., Luo, L., 2016. Multi-drug resistance mediated by class 1 integrons in aeromonas isolated from farmed freshwater animals. Front Microbiol. 7, 935.

De Silva, B.C.J., Wimalasena, S.H.M.P., Hossain, S., Pathirana, H.N.K.S., Heo, G.J., 2017. Characterization of Quinolone Resistance of Pseudomonas aeruginosa Isolated from Pet Chinese Stripe-necked Turtles (Ocadia sinensis). Asian J. Anim. Vet. Adv. 12(3),152–160.

Di Blasio, L., Santoro, R., Ferri, V., Battisti, C., Soccini, C., Egidi, A., Scalici, M., 2021. First successful reproduction of the Chinese striped-necked turtle Mauremys sinensis (Gray, 1834) in a European wetland. BioInvasions Records 10, 721–729.

Díaz, M.A., Cooper, R.K., Cloeckaert, A., Siebeling, R.J., 2006. Plasmid-mediated high-level gentamicin resistance among enteric bacteria isolated from pet turtles in louisiana.Appl. Environ. Microbiol. 72(1), 306-312.

Dieppois, G., Ducret, V., Caille, O., Perron, K., 2012. The transcriptional regulator CzcR modulates antibiotic resistance and quorum sensing in Pseudomonas aeruginosa.PLoS ONE. 7, e38148.

Di Ianni, F., Dodi, P.L., Cabassi, C.S., Pelizzone, I., Sala, A., Cavirani, S., Parmigiani, E.,Quintavalla, F., Taddei, S., 2015. Conjunctival flora of clinically normal and diseased turtles and tortoises. BMC Vet. Res. 11(91), 1-9.

Ebani, V.V., 2017. Domestic reptiles as source of zoonotic bacteria: a mini review. Asian Pac.J. Tropl. Med. 10, 723–728.

Gillings, M.R., Gaze, W.H., Pruden, A., Smalla, K., Tiedje, J.M., Zhu, Y.G., 2015. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9(6),1269–1279.

Grzimek, B.M., Hutchins, N., Schlager, Olendorf, D., 2003. Grzimek's Animal Life Encyclopedia, Volume 7: Reptiles, 2nd edition. Gale Group, Michigan, pp. 593.

Hossain, S., De Silva, B., Wimalasena, S., Pathirana, H., Heo, G., 2017. High prevalence of quinolone resistance genes in citrobacter freundii isolated from pet turtles. Asian J.Anim. Vet. Adv. 12(4), 212-217.

Jiang, H., Yu, T., Yang, Y., Yu, S., Wu, J., Lin, R., Li, Y., Fang, J. Zhu, C., 2020. Co-occurrence of antibiotic and heavy metal resistance and sequence type diversity of vibrio parahaemolyticus isolated from penaeus vannamei at freshwater farms, seawater farms, and markets in Zhejiang Province, China. Front. Microbiol. 11, 1294.

Kerr, K.G., Snelling, A.M., 2009. Pseudomonas aeruginosa: A formidable and ever-present adversary. J. Hosp. Infect. 73(4), 338-344.

Kim, J., Lim, Y.M., Rheem, I., Lee, Y., Lee, J.C., Seol, S.Y., Lee, Y.C., Cho, D.T., 2005. Ctx-m and shv-12 beta-lactamases are the most common extended-spectrum enzymes in clinical isolates of escherichia coli and klebsiella pneumoniae collected from 3 university hospitals within korea. FEMS Microbiol. Lett. 245(1), 93-98.

Krumperman, P.H., 1983. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl. Environ. Microbiol.46, 165–170.

Lupo, A., Haenni, M., Madec, J.Y., 2018. Antimicrobial resistance in Acinetobacter spp. and Pseudomonas spp. Microbiol. Spectr. 6, ARBA-0007-2017.

Mariana Ramos, F., Naiana Braga, F., Luciana Jatobá e Silva, P., Samira Teixeira Leal de, O., Renilde Cordeiro de, S., João José de Simoni, G., Mateus Matiuzzi da, C., Gisele Veneroni, G., 2018. The presence of plasmids in Aeromonas hydrophila and its relationship with antimicrobial and heavy metal-resistance profiles. Cienc. Rural.48(9), e20170813.

Mella, M.S., Sepúlveda, A.M., González, R.G., Bello, T.H., Domínguez, Y.M., Zemelman, Z.R., Ramírez, G.C., 2004. Aminoglucósidos-aminociclitoles: Características estructurales y nuevos aspectos sobre su resistencia. Revista Chilena de Infectología 21, 330–338.

Mirzaei, N., Rastegari, H., Kargar, M., 2013. Antibiotic resistance pattern among gram negative mercury resistant bacteria isolated from contaminated environments. Jundishapur J. Microbiol. 6, 8085.

Morita, Y., Tomida, J., Kawamura, Y., 2013. Responses of Pseudomonas aeruginosa to antimicrobials. Front. Microbiol. 4, 1–8.

Naguib, M.M., El-Gendy, A.O., Khairalla, A.S., 2018. Microbial diversity of operon genes and their potential rules in mercury bioremediation and resistance. The Open Biotechnol. J. 12(1), 56-77.

Nguyen, C.C., Hugie, C.N., Kile, M.L., Navab-Daneshmand, T., 2019. Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs:A review. Front Environ. Sci. Eng. 13(3), 46.

Osundiya, O., Oladele, R., Oduyebo, O., 2013. Multiple Antibiotic Resistance (MAR) indices of Pseudomonas and Klebsiella species isolates in Lagos University Teaching Hospital. African J. Clin. Exp. Microbiol. 14, 164–168.

Petitjean, M., Martak, D., Silvant, A., Bertrand, X., Valot, B., Hocquet, D., 2017. Genomic characterization of a local epidemic Pseudomonas aeruginosa reveals specific features of the widespread clone ST395. Microb. Genom. 3(10), e000129.

Qin, S., Xiao, W., Zhou, C., Pu, Q., Deng, X., Lan, L., Liang, H., Song, X., Wu, M., 2022. Pseudomonas aeruginosa: Pathogenesis, virulence factors, antibiotic resistance,interaction with host, technology advances and emerging therapeutics. Sig. Transduct Target Ther. 7(1), 199.

Radó, J., Kaszab, E., Petrovics, T., Pászti, J., Kriszt, B., Szoboszlay, S., 2017. Characterization of environmental Pseudomonas aeruginosa using multilocus sequence typing scheme. J. Med. Microbiol. 66, 1457–1466.

Ramsay, K.A., Wardell, S.J.T., Patrick, W.M., Brockway, B., Reid, D.W., Winstanley, C.,Lamont, I.L., 2019. Genomic and phenotypic comparison of environmental and patient-derived isolates of Pseudomonas aeruginosa suggest that antimicrobial resistance is rare within the environment. J Med. Microbiol. 68, 1591‐1595.

Schmidt, K.D., Tümmler, B., Römling, U., 1996. Comparative genome mapping of Pseudomonas aeruginosa PAO with P. aeruginosa C, which belongs to a major clone in cystic fibrosis patients and aquatic habitats. J. Bacteriol. 178, 85–93.

Singer, A.C., Shaw, H., Rhodes, V., Hart, A., 2016. Review of antimicrobial resistance in the environment and its relevance to environmental regulators. Front. Microbiol. 7,1–22.

Stam, F., Römkens, T.E., Hekker, T.A., Smulders, Y.M., 2003. Turtle-associated human salmonellosis. Clin. Infect. Dis. 37(11), e167-169.

Strateva, T., Yordanov, D., 2009. Pseudomonas aeruginosa - A phenomenon of bacterial resistance. J. Med. Microbiol. 58, 1133–1148.

Teitzel, G.M., Parsek, M.R., 2003. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69, 2313-2320.

Teixeira, B., Rodulfo, H., Carreño, N., Guzmán, M., Salazar, E., Dedonato, M., 2016. Aminoglycoside resistance genes in Pseudomonas aeruginosa isolates from cumana, Venezuela. Rev. Inst. Med. Trop. Sao Paulo. 58, 1–5.

Vaziri, F., Peerayeh, S.N., Nejad, Q.B., Farhadian, A., 2011. The prevalence of aminoglycoside-modifying enzyme genes (aac (6′)-I, aac (6′)-II, ant (2″)-I, aph (3′)-VI) in Pseudomonas aeruginosa. Clinics. 66, 1519–1522.

Viti, C., Marchi, E., Decorosi, F., Giovannetti, L., 2014. Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol. Rev. 38, 633–659.

Wendt, M., Heo, G.J., 2016. Multilocus sequence typing analysis of Pseudomonas aeruginosa isolated from pet Chinese stripe-necked turtles (Ocadia sinensis). Lab. Anim. Res.32, 208–216.

Zheng, W., Huyan, J., Tian, Z., Zhang, Y., Wen, X., 2020. Clinical class 1 integron-integrase gene – A promising indicator to monitor the abundance and elimination of antibiotic resistance genes in an urban wastewater treatment plant. Environ. Int. 135, 105372.