Serogroups, and drug resistance of nontyphoidal Salmonella in symptomatic patients with community-acquired diarrhea and chicken meat samples in Tehran

Document Type : Full paper (Original article)

Authors

1 MSc in Microbiology, Department of Microbiology, Faculty of Medicine, Shahed University, Tehran, Iran

2 MSc Student in Microbiology, Department of Microbiology, Faculty of Basic Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran

3 MSc in Microbiology, Division of Microbiology, National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran

4 Molecular Microbiology Research Center, Faculty of Medicine, Shahed University, Tehran, Iran

5 Division of Microbiology, Professor Alborzi Clinical Microbiology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

6 Department of Medical Laboratory Sciences, School of Allied Medical Sciences, Tehran University of Medical Sciences, Tehran, Iran

7 Division of Microbiology, Anti-Microbial Resistance Research Center, Institute of Immunology and Infectious Diseases (IIID), Iran University of Medical Sciences, Tehran, Iran

8 MSc in Microbiology, Division of Microbiology, Anti-Microbial Resistance Research Center, Institute of Immunology and Infectious Diseases (IIID), Iran University of Medical Sciences, Tehran, Iran

9 Health Reference Laboratory, Health Reference Laboratory Research Center, Ministry of Health and Medical Education, Tehran, Iran

10 MSc in Microbiology, Department of Microbiology, Central Laboratory, Milad Hospital, Tehran, Iran

11 Pathology Laboratory, Mehr Hospital, Tehran, Iran

12 Center for Communicable Disease Control, Ministry of Health and Medical Education, Tehran, Iran

13 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

14 Pediatric Infections Research Center, Research Institute for Children’s Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran

10.22099/ijvr.2020.36912.5387

Abstract

Background: Salmonella is considered as a main cause of community-acquired diarrhea in humans, however, sources of the multi-drug resistant (MDR) strains and their link with the disease are not well known. Aims: This study aimed to investigate the frequency, serogroup diversity, and antimicrobial susceptibility patterns of Salmonella strains in poultry meat and stool samples of patients with community acquired diarrhea in Tehran. Methods: We compared the frequency of non-typhoidal Salmonella serogroups, the similarities of their resistance patterns to 10 antimicrobial compounds, the prevalence of extended spectrum β-lactamase (ESBL) and ampicillinase C (AmpC) genetic determinants, and class 1 and 2 integrons in 100 chicken meat and 400 stool samples of symptomatic patients in Tehran during June 2018 to March 2019. Results: Salmonella was isolated from 75% and 5.5% of the chicken meats and human stool samples, respectively. The chicken meat isolates mainly belonged to serogroup C (88%, 66/75), while the human stool isolates were mainly related to serogroup D (59.1%, 13/22). The MDR phenotype and the most common rates of resistance to antibiotics, including tetracycline, trimethoprim/sulfamethoxazole (TS) and azithromycin, were detected in 4.5% and 45.3%, 59% and 13.6%, 43% and 9.1%, 42% and 9.1% of the human stool and chicken meat samples, respectively. Carriage of blaCTX, blaSHV, and blaPER genes in the meat isolate with ESBL resistance phenotype and blaACC, blaFOX, and blaCMY-2 among the 7 meat strains with AmpC resistance phenotype was not confirmed using polymerase chain reaction (PCR). High prevalence of class 1 and 2 integrons was characterized and showed a correlation with resistance to TS and chloramphenicol. Conclusion: These findings showed a lack of association between chicken meats and human isolates due to discrepancy between the characterized serogroups and resistance phenotypes.

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Abd-Elghany, S; Sallam, K; Abd-Elkhalek, A and Tamura, T (2015). Occurrence, genetic characterization and antimicrobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol. Infect., 143: 997-1003.
Amini, K (2016). Prevalence of antibiotic resistance genes in Salmonella enteritidis isolated from animal and human and determining their antibiotic resistance patterns. J. Comp. Pathobiol. Iran., 12: 1733-1740.
Anonymous (2002). EN ISO 6579. Microbiology of food and animal feeding stuffs – Horizontal method for the detection of Salmonella spp. International Organization for Standardization, Geneva, Switzerland.
Britto, CD; Wong, VK; Dougan, G and Pollard, AJ (2018). A systematic review of antimicrobial resistance in Salmonella enterica serovar Typhi, the etiological agent of typhoid. PLoS Negl. Trop. Dis., 12: e0006779.
Chuma, T; Miyasako, D; Hesham, D; Takayama, T; Nakamoto, Y; Shahada, F; Akiba, M and Okamoto, K (2013). Chronological change of resistance to β-lactams in Salmonella enterica serovar Infantis isolated from broilers in Japan. Front Microbiol., 4: 113.
CLSI (2018). Performance standards for antimicrobial susceptibility testing. 28th Edn., Wayne, Pennsylvania. PP: 1-258.
Da Silva, N; Taniwaki, MH; Junqueira, VC; Silveira, N; Okazaki, MM and Gomes, RAR (2018). Microbiological examination methods of food and water: a laboratory manual. 2nd Edn., Taylor and Francis Group, UK, CRC Press. PP: 1-632.
Davis, JL; Smith, GW; Baynes, RE; Tell, LA; Webb, AI and Riviere, JE (2009). Update on drugs prohibited from extralabel use in food animals. J. Am. Vet. Med. Assoc., 235: 528-534.
Derakhshan, S; Najar Peerayeh, S; Fallah, F; Bakhshi, B; Rahbar, M and Ashrafi, A (2014). Detection of class 1, 2, and 3 integrons among Klebsiella pneumoniae isolated from children in Tehran hospitals. Arch. Pediatr. Infect. Dis., 2: 164-168.
European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC)(2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J., 16: e05500.
Farag, E; Garcell, HG; Ganesan, N; Ahmed, SNN; Al-Hajri, M; Al Thani, SMHJ; Al-Marri, SA; Ibrahim, E and Al-Romaihi, HE (2016). A retrospective epidemiological study on the incidence of salmonellosis in the State of Qatar during 2004-2012. Qatar Med. J., 2016: 3.
Fiett, J; Baraniak, A; Mrówka, A; Fleischer, M; Drulis-Kawa, Z; Naumiuk, Ł; Samet, A; Hryniewicz, W and Gniadkowski, M (2006). Molecular epidemiology of acquired-metallo-β-lactamase-producing bacteria in Poland. Antimicrob. Agents Chemother., 50: 880-886.
Firoozeh, F; Zahraei-Salehi, T and Shahcheraghi, F (2014). Molecular clonality and detection of class 1 integron in multidrug-resistant Salmonella enterica isolates from animal and human in Iran. Microb. Drug Resist., 20: 517-524.
Ford, L; Glass, K; Veitch, M; Wardell, R; Polkinghorne, B; Dobbins, T; Lal, A and Kirk, MD (2016). Increasing incidence of Salmonella in Australia, 2000-2013. PLoS One. 11: e0163989.
Gehring, R; Baynes, R and Riviere, J (2006). Application of risk assessment and management principles to the extralabel use of drugs in food-producing animals. J. Vet. Pharmacol. Ther., 29: 5-14.
Ghasemi, Y; Archin, T; Kargar, M and Mohkam, M (2013). A simple multiplex PCR for assessing prevalence of extended-spectrum β-lactamases producing Klebsiella pneumoniae in Intensive Care Units of a referral hospital in Shiraz, Iran. Asian Pac. J. Trop. Med., 6: 703-708.
Harish, B and Menezes, G (2011). Antimicrobial resistance in typhoidal Salmonellae. Indian J. Med. Microbiol., 29: 223-229.
Hendriksen, RS; Joensen, KG; Lukwesa-Musyani, C; Kalondaa, A; Leekitcharoenphon, P; Nakazwe, R; Aarestrup, FM; Hasman, H and Mwansa, JC (2013). Extremely drug-resistant Salmonella enterica serovar Senftenberg infections in patients in Zambia. J. Clin. Microbiol., 51: 284-286.
Hugas, M and Beloeil, P (2014). Controlling Salmonella along the food chain in the European Union-progress over the last ten years. Eurosurveillance. 19: 20804.
Hur, J; Kim, JH; Park, JH; Lee, YJ and Lee, JH (2011). Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. Vet. J., 189: 306-311.
Jeon, HY; Seo, KW; Kim, YB; Kim, DK; Kim, SW and Lee, YJ (2018). Characteristics of third-generation cephalosporin-resistant Salmonella from retail chicken meat produced by integrated broiler operations. Poult. Sci., 98: 1766-1774.
Jørgensen, RL; Nielsen, JB; Friis-Møller, A; Fjeldsøe-Nielsen, H and Schønning, K (2010). Prevalence and molecular characterization of clinical isolates of Escherichia coli expressing an AmpC phenotype. J. Antimicrob. Chem., 65: 460-464.
Kaur, J (2013). Increasing antimicrobial resistance and narrowing therapeutics in typhoidal Salmonellae. J. Clin. Diagn. Res., 7: 576.
Klemm, EJ; Shakoor, S; Page, AJ; Qamar, FN; Judge, K; Saeed, DK; Wong, VK; Dallman, TJ; Nair, S and Baker, S (2018a). Emergence of an extensively drug-resistant Salmonella enterica serovar Typhi clone harboring a promiscuous plasmid encoding resistance to fluoroquinolones and third-generation cephalosporins. mBio. 9: e00105-00118.
Konaté, A; Guessennd, N; Kouadio, F; Dembélé, R and Kagambèga, A (2019). Epidemiology and resistance phenotypes of Salmonella spp. strains responsible for gastroenteritis in children less than five years of age in Ouagadougou, Burkina Faso. Arch. Clin. Microbiol., 10: 90.
Kretzschmar, M; Mangen, MJJ; Pinheiro, P; Jahn, B; Fevre, EM; Longhi, S; Lai, T; Havelaar, AH; Stein, C and Cassini, A (2012). New methodology for estimating the burden of infectious diseases in Europe. PLoS Med., 9: e1001205.
Le Hello, S; Harrois, D; Bouchrif, B; Sontag, L; Elhani, D; Guibert, V; Zerouali, K and Weill, FX (2013). Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect. Dis., 13: 672-679.
Manyi-Loh, C; Mamphweli, S; Meyer, E and Okoh, A (2018). Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules. 23: 795.
Mietzner, TA; Carroll, KC; Hobden, JA; Miller, S; Morse, SA; Mitchell, TG; Sakanari, JA; McKerrow, JH and Detrick, B (2016). Jawetz, Melnick & Adelberg’s medical microbiology. 27th Edn., Chapter 15, Enteric Gram-Negative Rods (Enterobacteriaceae). McGraw-Hill Education. PP: 231-238.
Mikoleit, M (2010). Laboratory protocol: biochemical identification of Salmonella and Shigella using an abbreviated panel of tests. Geneva, Switzerland: WHO Global Foodborne Infections Network. http:// antimicrobialresistance.dk/CustomerData/Files/Folders/6-pdf-protocols/63_18-05-isolation-of-salm-220610.pdf.
Miriagou, V; Carattoli, A and Fanning, S (2006). Antimicrobial resistance islands: resistance gene clusters in Salmonella chromosome and plasmids. Microbes Infect., 8: 1923-1930.
Monstein, HJ; ÖStholm-Balkhed, Å; Nilsson, MV; Nilsson, M; Dornbusch, K and Nilsson, LE (2007). Multiplex PCR amplification assay for the detection of blaSHV, blaTEM and blaCTX-M genes in Enterobacteriaceae. APMIS. 115: 1400-1408.
Noda, T; Murakami, K; Ishiguro, Y and Asai, T (2010). Chicken meat is an infection source of Salmonella serovar Infantis for humans in Japan. Foodborne Pathog. Dis., 7: 727-735.
Pérez-Pérez, FJ and Hanson, ND (2002). Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J. Clin. Microbiol., 40: 2153-2162.
Popoff, MY (1997). Antigenic formulas of the Salmonella serovars. WHO Collaborating Center for Reference and Research on Salmonella. https://www.pasteur.fr/sites/ default/files/veng_0.pdf.
Popoff, M and Le Minor, L (2001). Antigenic formulas of the Salmonella serovars, WHO Collaborating Centre for Reference and Research on Salmonella. World Health Organization, Geneva, Switzerland.
Raeisi, E and Ghiamirad, M (2015). Survey on prevalence of Salmonella serogroups and antibiotics susceptibility pattern in chicken meat in Ardabil, Iran. J. Ardabil Univer. Med. Sci., 15: 320-329.
Ramadan, F; Unni, A; Hablas, R and Rizk, M (1992). Salmonella-induced enteritis. Clinical, serotypes and treatment. J. Egypt. Public Health Assoc., 67: 357-367.
Soltan Dallal, MM and Moezardalan, K (2004). Aeromonas spp associated with children’s diarrhoea in Tehran: a case-control study. Ann. Trop. Paediatr., 24: 45-51.
Stanaway, JD; Reiner, RC; Blacker, BF; Goldberg, EM; Khalil, IA; Troeger, CE; Andrews, JR; Bhutta, ZA; Crump, JA and Im, J (2019). The global burden of typhoid and paratyphoid fevers: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect. Dis., 19: 369-381.
Tajbakhsh, M; Avini, MY; Alikhajeh, J; Tajeddin, E; Rahbar, M; Eslami, P; Alebouyeh, M and Zali, MR (2016). Emergence of blaCTX-M-15, blaTEM-169 and blaPER-1 extended-spectrum β-lactamase genes among different Salmonella enterica serovars from human faecal samples. Infect Dis. (London)., 48: 550-556.
Threlfall, EJ (2010). Salmonella. In: Topley & Wilson’s microbiology and microbial infections. (Systemic Bacteriology) 10th Edn., Vol. 2, Hoboken, NJ, John Wiley & Sons, Ltd.
Tibaijuka, B; Molla, B; Hildebrandt, G and Kleer, J (2003). Occurrence of Salmonellae in retail raw chicken products in Ethiopia. Berl. Munch Tierarztl Wochenschr., 116: 55-58.
Travers, K and Michael, B (2002). Morbidity of infections caused by antimicrobial-resistant bacteria. Clin. Infect. Dis., 34: S131-S134.
Wang, W; Peng, Z; Baloch, Z; Hu, Y; Xu, J; Zhang, W;
Fanning, S and Li, F
(2017). Genomic characterization of an extensively-drug resistance Salmonella enterica serotype Indiana strain harboring blaNDM-1 gene isolated from a chicken carcass in China. Microbiol. Res., 204: 48-54.
White, DG; Hudson, C; Maurer, JJ; Ayers, S; Zhao, S; Lee, MD; Bolton, L; Foley, T and Sherwood, J (2000). Characterization of chloramphenicol and florfenicol resistance in Escherichia coli associated with bovine diarrhea. J. Clin. Microbiol., 38: 4593-4598.
WHO (2010). Laboratory Protocol. In: Isolation of Salmonella spp. from food and animal faeces. 5th Edn., June 2010. PP: 4-8, 13.
Wong, MHY; Zeng, L; Liu, JH and Chen, S (2013). Characterization of Salmonella food isolates with concurrent resistance to ceftriaxone and ciprofloxacin. Foodborne Pathog. Dis., 10: 42-46.
Zdrodowska, B; Liedtke, K and Radkowski, M (2014). Post-harvest Salmonella spp. prevalence in turkey carcasses in processing plant in the northeast part of Poland. Pol. J. Vet. Sci., 17: 181-183.
Zeng, YB; Xiong, LG; Tan, MF; Li, HQ; Yan, H; Zhang, L; Yin, DF; Kang, ZF; Wei, QP and Luo, LG (2019). Prevalence and antimicrobial resistance of Salmonella in pork, chicken, and duck from retail markets of China. Foodborne Pathog. Dis., 16: 339-345.