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Prevalence and antimicrobial resistance of Salmonella serotypes isolated from cats and dogs in Tripoli, Libya.
VetIt.1998.10744.4

Keywords

Antimicrobial resistance
Libya
pets
Salmonella
S. Kentucky

How to Cite

Elnageh, H. R., Hiblu, M. A., Abbassi, M. S., Abouzeed, Y. M., & Ahmed, M. O. (2021). Prevalence and antimicrobial resistance of Salmonella serotypes isolated from cats and dogs in Tripoli, Libya. Veterinaria Italiana, 57(2), 111–118. https://doi.org/10.12834/VetIt.1998.10744.4

Abstract

The prevalence of Salmonella in dogs and cats was investigated and analysed for serotyping, susceptibility to antimicrobial drugs and risk factors assessment. In total, 151 faecal samples from 103 and 48 healthy and nonhealthy (diarrheic) cats and dogs, respectively were examinated. Salmonellae were confirmed by laboratory and biomedical characteristics and further serotyped then subjected to antimicrobial susceptibility tests. Risk factors that are typically associated with the shedding of salmonellae were assessed using Fisher's exact tests. Salmonella was detected in 18% (n=27/151) of pets. Most of the positive samples 85%(n=23/27) were from healthy cats and 7.4% (n=2/27) from healthy dogs and 7.4% (n = 2/27) from a diarrhoeic cat and diarrhoeic dog. Only one sample from each diarrhoeic cat and diarrhoeic dog were positive for Salmonella. total, 25 salmonellae (93% of strains) were serotyped as S. Thompson mostly originated form healthy cats (n = 23/25). All were resistant to tetracycline and trimethoprim-sulfamethoxazole and expressed ed only resisted an overall intermediate susceptibility patterns to ciprofloxacin. Also, multidrug resistant S. Kentucky and S. Minnesota were identified from a diarrhoeic and an healthy dog, respectively. This is the first isolation report of Salmonella from cats and dogs in Libya. It indeed represents a public health concern wich requires further monitoring.

https://doi.org/10.12834/VetIt.1998.10744.4
VetIt.1998.10744.4

References

References

Afema J.A., Byarugaba D.K., Shah D.H., Atukwase E., Nambi M. & Sischo W.M. 2016. Potential Sources and Transmission of Salmonella and Antimicrobial Resistance in Kampala, Uganda. PLoS One, 11(3), e0152130. doi: 10.1371/journal.pone.0152130

Ahmed M.O., Almshawt N.F. & Elnageh H.R. 2017. Diarrheagenic Escherichia Coli O157 from Libya: Recent Perspectives and Challenges. J Public Health Afr, 8(1), 685.

Al-Gallas N., Abbassi M.S., Gharbi B., Manai M., Ben Fayala M.N., Bichihi R., Al-Gallas A. & Ben Aissa R. 2013. Occurrence of plasmid-mediated quinolone resistance determinants and rmtB gene in Salmonella enterica serovar enteritidis and Typhimurium isolated from food-animal products in Tunisia. Foodborne Pathog Dis, 10(9), 813-9.

Altayyar I.A., Elbreki M.F., Ali M.O. & Ali A.A.l. 2016. Prevalence and Antimicrobial Susceptibility Patterns of Salmonella spp Isolated from Gastroenteritis Patients, Southwestern, Libya. Int J Appl. Med Bio Res, 1 , 2-6.

Centers for Disease Control and Prevention (CDC). 2006. Human salmonellosis associated with animal-derived pet treats--United States and Canada, 2005. MMWR, 55(25), 702-705.

Centers for Disease Control and Prevention (CDC) 2008. Multistate outbreak of human Salmonella infections caused by contaminated dry dog food--United States, 2006-2007. MMWR, 57(19), 521-524.

Centers for Disease Control and Prevention (CDC) 2014. National Salmonella Surveillance Annual Report, 2012. Atlanta, Georgia, US Department of Health and Human Services, CDC, 2014.

Chipangura J.K., Eagar H., Kgoete M., Abernethy D. & Naidoo V. 2017. An investigation of antimicrobial usage patterns by small animal veterinarians in South Africa. Prev Vet Med,136, 29-38.

Clinical Laboratory Standard Institution (CLSI) 2015. M100-S25 performance standards for antimicrobial susceptibility testing. Twenty-fifth informational supplement.

Crump J.A., Sjölund-Karlsson M., Gordon M.A. & Parry C.M. 2015. Epidemiology, Clinical Presentation, Laboratory Diagnosis, Antimicrobial Resistance, and Antimicrobial Management of Invasive Salmonella Infections. Clin Microbiol Rev, 28(4), 901-937.

Cuypers W.L., Jacobs J., Wong V., Klemm E.J., Deborggraeve S. & Van Puyvelde S. 2018. Fluoroquinolone resistance in Salmonella: insights by whole-genome sequencing. Microb Genom, 4(7), e000195

Damborg P., Broens E.M., Chomel B.B., Guenther S., Pasmans F., Wagenaar J.A., Weese J.S., Wieler L.H., Windahl U., Vanrompay D. & Guardabassi L. 2016. Bacterial Zoonoses Transmitted by Household Pets: State-of-the-Art and Future Perspectives for Targeted Research and Policy Actions. J Comp Pathol, 155(1 Suppl), S27-S40.

Damborg P., Morsing M.K., Petersen T., Bortolaia V. & Guardabassi L. 2015. CTX-M-1 and CTX-M-15-producing Escherichia coli in dog faeces from public gardens. Acta Vet Scand, 57, 83.

Dotto G., Menandro M.L., Mondin A., Martini M. & Pasotto D. 2017. First detection of Salmonella enterica serovar Napoli in kennel dogs in Italy. Vet Rec, 180(22), 544.

Elnageh H.R., Hiblu M.A., Abouzeed Y. & Ahmed M.O. 2017. Prevalence and antimicrobial resistance among enteric bacteria and Staphylococcus spp. isolated from pet-companion animals in Tripoli. First International Congress of Biochemistry & Microbiology Applied Technologies BMAT 2017, 3 - 5 November 2017.

European Committee on Antimicrobial Susceptibility Testing (EUCAST). 2019. Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0. http://www.eucast.org.

European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC). 2018. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016, EFSA Journal, 16 (2), 5182.

Ezenduka E.V. 2019. Screening of antimicrobial residues in poultry meat in Enugu metropolis, Enugu State, South East Nigeria. Vet Ital, 55(2), 143-148.

Fernández J., Guerra B. & Rodicio M.R. 2018. Resistance to Carbapenems in Non-Typhoidal Salmonella enterica Serovars from Humans, Animals and Food. Vet Sci, 5(2), E40.

Fisher I.S., Jourdan-Da Silva N., Hächler H., Weill F.X., Schmid H., Danan C., Kérouanton A., Lane C.R., Dionisi A.M. & Luzzi I. 2009. Human infections due to Salmonella Napoli: a multicountry, emerging enigma recognized by the Enter-net international surveillance network. Foodborne Pathog Dis, 6(5), 613-619.

Ghenghesh K.S., Rahouma A., Tawil K., Zorgani A. & Franka E. 2013. Antimicrobial resistance in Libya: 1970-2011. Libyan J Med, 27, 1-8.

Gossner C.M., Le Hello S., de Jong Bi, Rolfhamre P., Faensen D., Weill F.X. & Giesecke J. 2016. Around the World in 1,475 Salmonella Geo-serotypes. Emerg Infect Dis, 22(7), 1298–1302.

Graziani C., Luzzi I., Owczarek S., Dionisi A.M. & Busani L. 2015. Salmonella enterica Serovar Napoli Infection in Italy from 2000 to 2013: Spatial and Spatio-Temporal Analysis of Cases Distribution and the Effect of Human and Animal Density on the Risk of Infection. PLoS One, 10(11), e0142419.

Hackett T. & Lappin M.R. 2003. Prevalence of enteric pathogens in dogs of north-central Colorado. J Am Anim Hosp Assoc, 39, 52-56.

Halsby K.D., Walsh A.L., Campbell C., Hewitt K. & Morgan D. 2014. Healthy animals, healthy people: zoonosis risk from animal contact in pet shops, a systematic review of the literature. PLoS One,9(2), e89309.

Jia J., Frantz N., Khoo C., Gibson G.R., Rastall R.A. & McCartney A.L. 2010. Investigation of the faecal microbiota associated with canine chronic diarrhoea. FEMS Microbiol Ecol, 71(2), 304-312.

Kiflu B., Alemayehu H., Abdurahaman M., Negash Y. & Eguale T. 2017. Salmonella serotypes and their antimicrobial susceptibility in apparently healthy dogs in Addis Ababa, Ethiopia. BMC Vet Res, 13(1), 134.

Kirk M.D., Pires S.M., Black R.E., Caipo M., Crump J.A., Devleesschauwer B., Döpfer D., Fazil A., Fischer-Walker C.L., Hald T., Hall A.J., Keddy K.H., Lake R.J., Lanata C.F., Torgerson P.R., Havelaar A.H. & Angulo F.J. 2015. World Health Organization Estimates of the Global and Regional Disease Burden of 22 Foodborne Bacterial, Protozoal, and Viral Diseases, 2010: A Data Synthesis. PLoS Med, 12, e1001921.

Le Hello S., Hendriksen R.S., Doublet B., Fisher I., Nielsen E.M., Whichard J.M., Bouchrif B., Fashae K., Granier S.A., Jourdan-Da Silva N., Cloeckaert A., Threlfall E.J., Angulo F.J., Aarestrup F.M., Wain J. & Weill F.X. 2011. International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infect Dis, 204(5), 675-684.

Le Hello S., Harrois D., Bouchrif B., Sontag L., Elhani D., Guibert V., Zerouali K. & Weill F.X. 2013a. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis, 13(8),672-679.

Le Hello S., Bekhit A., Granier S.A., Barua H., Beutlich J., Zając M., Münch S., Sintchenko V., Bouchrif B., Fashae K., Pinsard J.L., Sontag L., Fabre L., Garnier M., Guibert V., Howard P., Hendriksen R.S., Christensen J.P., Biswas P.K., Cloeckaert A., Rabsch W., Wasyl D., Doublet B. & Weill F.X. 2013b. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol, 18, 395.

Leonard E.K., Pearl D.L., Finley R.L., Janecko N., Peregrine A.S., Reid-Smith R.J. & Weese J.S. 2011. Evaluation of pet-related management factors and the risk of Salmonella spp. carriage in pet dogs from volunteer households in Ontario (2005-2006). Zoonoses Public Health, 58(2), 140-149.

Lokken K.L., Walker G.T. & Tsolis R.M. 2016. Disseminated infections with antibiotic-resistant non-typhoidal Salmonella strains: contributions of host and pathogen factors. Pathog Dis, 74(8) ftw103. doi.org/10.1093/femspd/ftw103.

Majowicz S.E., Musto J., Scallan E., Angulo F.J., Kirk M., O'Brien S.J., Jones T.F., Fazil A. & Hoekstra R.M. 2010. International Collaboration on Enteric Disease 'Burden of Illness' Studies. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis, 50(6), 882-889.

Marks S.L., Rankin S.C., Byrne B.A. & Weese J.S. 2011. Enteropathogenic bacteria in dogs and cats: diagnosis, epidemiology, treatment, and control. J Vet Intern Med, 25(6),1195-1208.

Mulvey M.R., Boyd D.A., Finley R., Fakharuddin K., Langner S., Allen V, , Ang L., Bekal S., El Bailey S., Haldane D., Hoang L., Horsman G., Louis M., Robberts L. & Wylie J. 2013. Ciprofloxacin-resistant Salmonella enterica serovar Kentucky in Canada. Emerg Infect Dis, 19, 999–1001.

Nair A., Balasaravanan T., Malik S.V., Mohan V., Kumar M., Vergis J. & Rawool D.B. 2015. Isolation and identification of Salmonella from diarrheagenic infants and young animals, sewage waste and fresh vegetables. Vet World, 8(5), 669-673.

Parker C.T., Huynh S., Gorski L., Cooper K.K. & Miller W.G. 2015. Complete Genome Sequences of Two Outbreak Strains of Salmonella enterica subsp. enterica Serovar Thompson Associated with Cilantro. Genome Announc, 3(6), e01365-15.

Parry C.M. & Threlfall E.J. 2008. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis, 21(5), 531-538.

Phu Huong Lan N., Le Thi Phuong T., Nguyen Huu H., Thuy L., Mather A.E., Park S.E., Marks F., Thwaites G.E., Van Vinh Chau N., Thompson C.N. & Baker S. 2016. Invasive Non-typhoidal Salmonella Infections in Asia: Clinical Observations, Disease Outcome and Dominant Serovars from an Infectious Disease Hospital in Vietnam. PLoS Negl Trop Dis, 10(8), e0004857.

Reimschuessel R., Grabenstein M., Guag J., Nemser S.M., Song K., Qiu J., Clothier K.A., Byrne B.A., Marks S.L., Cadmus K., Pabilonia K., Sanchez S., Rajeev S., Ensley S., Frana T.S., Jergens A.E., Chappell K.H., Thakur S., Byrum B., Cui J., Zhang Y., Erdman M.M., Rankin S.C., Daly R., Das S., Ruesch L., Lawhon S.D., Zhang S., Baszler T., Diaz-Campos D., Hartmann F. & Okwumabua O. 2017. Multilaboratory Survey To Evaluate Salmonella Prevalence in Diarrheic and Nondiarrheic Dogs and Cats in the United States between 2012 and 2014. J Clin Microbiol, 55(5), 1350-1368.

Rickert-Hartman R. & Folster J.P. 2014. Ciprofloxacin-resistant Salmonella enterica serotype Kentucky sequence type 198. Emerg Infect Dis, 20(5), 910-911.

Seiffert S.N., Perreten V., Johannes S., Droz S., Bodmer T. & Endimiani A. 2014. OXA-48 carbapenemase-producing Salmonella enterica serovar Kentucky isolate of sequence type 198 in a patient transferred from Libya to Switzerland. Antimicrob Agents Chemother, 58(4), 2446-2449.

Selmi M., Stefanelli S., Bilei S., Tolli R., Bertolotti L., Marconi P., Giurlani S., De Lucia P.G., Ruggeri G. & Pagani A. 2011. Contaminated commercial dehydrated food as source of multiple Salmonella serotypes outbreak in a municipal kennel in Tuscany. Vet Ital, 47(2), 183-190.

Sjölund-Karlsson M., Folster J.P., Pecic G., Joyce K., Medalla F., Rickert R. & Whichard J.M. 2009. Emergence of plasmid-mediated quinolone resistance among non-typhi Salmonella enterica isolates from humans in the United States. Antimicrob. Agents Chemother, 53, 2142–2144.

Srisanga S., Angkititrakul S., Sringam P., Le Ho P.T., T Vo A.T. & Chuanchuen R. 2017 Phenotypic and genotypic antimicrobial resistance and virulence genes of Salmonella enterica isolated from pet dogs and cats. J Vet Sci, 18(3), 273-281.

Stavisky J., Radford A.D., Gaskell R., Dawson S., German A., Parsons B., Clegg S., Newman J. & Pinchbeck G. 2011. A case-control study of pathogen and lifestyle risk factors for diarrhoea in dogs. Prev Vet Med, 199(2-4), 185-192.

Stiver S.L., Frazier K.S., Mauel M.J. & Styer E.L. 2003. Septicemic salmonellosis in two cats fed a raw-meat diet. J Am Anim Hosp Assoc, 39, 538–542.

Stull J.W., Brophy J. & Weese J.S. 2015. Reducing the risk of pet-associated zoonotic infections. CMAJ, 187(10), 736-743.

Tadesse G., Tessema T.S., Beyene G. & Aseffa A. 2018. Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: A systematic review and meta-analysis. PLoS One, 13(2), e0192575.

Uche I.V., MacLennan C.A. & Saul A. 2017. A Systematic Review of the Incidence, Risk Factors and Case Fatality Rates of Invasive Nontyphoidal Salmonella (iNTS) Disease in Africa (1966 to 2014). PLoS Negl Trop Dis, 11(1), e0005118.

Van Immerseel F., Pasmans F., De Buck J., Rychlik I., Hradecka H., Collard J.M., Wildemauwe C., Heyndrickx M., Ducatelle R. & Haesebrouck F. 2004. Cats as a risk for transmission of antimicrobial drug-resistant Salmonella. Emerg Infect Dis, 10(12), 2169-2174.

Westermarck E. 2016. Chronic Diarrhea in Dogs: What Do We Actually Know About It? Top Companion Anim Med, 31(2), 78-84.

Westrell T., Monnet D.L., Gossner C., Heuer O. & Takkinen J. 2014. Drug-resistant Salmonella enterica serotype Kentucky in Europe. Lancet Infect Dis, 14(4), 270-271.

World Health Organization (WHO) 2018. Salmonella (non-typhoidal) www.who.int/mediacentre/factsheets/fs139/en/.

World Health Organization & Food and Agriculture Organization of the United Nations. (‎2016)‎. Interventions for the control of non-typhoidal Salmonella spp. in beef and pork: meeting report and systematic review. World Health Organization. https://apps.who.int/iris/handle/10665/249529

World Organisation for Animal Health (OIE). 2008. Salmonellosis – Chapter 2.9.9. In OIE Terrestrial Manual. Paris, OIE.