Generic Salmonella in Asymptomatic Adult Volunteers: Occurrence, Antibiogram, Extended-Spectrum β-Lactamase Production and Carbapenem Resistance

  • Chiamaka OKPALANWA University of Nigeria, Faculty of Pharmaceutical Sciences, Pharmaceutics Department, Nsukka
  • Madubuike U. ANYANWU Univeristy of Nigeria, Microbiology Unit, Department of Veterinary Pathology and Microbiology, Nsukka
  • Mumuni A. MOMOH University of Nigeria, Faculty of Pharmaceutical Sciences, Pharmaceutics Department, Nsukka
  • Petra O. NNAMANI University of Nigeria, Faculty of Pharmaceutical Sciences, Pharmaceutics Department, Nsukka
  • Anthony A. ATTAMA University of Nigeria, Faculty of Pharmaceutical Sciences, Pharmaceutics Department, Nsukka
Keywords: asymptomatic adult; carbapenem resistance; extended-spectrum β-lactamase production; extensive drug resistance; Salmonella

Abstract

This study was conducted to isolate generic Salmonella from stool of apparently-healthy/asymptomatic adult volunteers in Ankpa North-central Nigeria, and to determine antibacterial susceptibility, extended-spectrum β-lactamase production and carbapenem resistance. About a gram of stool was collected from 295 randomly-selected apparently-healthy/asymptomatic adult volunteers in Ankpa Kogi State, North-central Nigeria. Isolation of Salmonella was done by pre-enrichment with buffered peptone water, enrichment with Rapapport-Vassiliadis and sub-culturing on Salmonella-Shigella and MacConkey agar. Identification of the isolates to genus level was done using standard biochemical tests. Resistance of the isolates was determined by disc diffusion method. Production of ESBL was assessed by combination disc method while carbapenem resistance was determined using meropenem disc screening method. Nine (3.1%) out of 295 samples, gave positive growth of Salmonella. Of these 9 isolates, all were carbapenem (meropenem)-resistant and 1 (11.1%) was ESBL-producer. Among the isolates, all were resistant to ciprofloxacin, ofloxacin, norfloxacin, ampicillin, cefotaxime, ceftazidime, gentamicin and streptomycin, 5 (55.6%) to sulphamethoxazole-trimethoprim, 7 (77.8%) to amoxicillin-clavulanic acid and aztreonam, 6 (66.7%) to nitrofurantoin and 8 (88.9%) to tetracycline. All the isolates were resistant to ≥ 5 classes of antibacterial agents. Mean multiple antibacterial indexes of the isolates were 0.68 (range 0.79 - 1.00). Apparently-healthy/asymptomatic adults in Ankpa North-central Nigeria, are potential reservoirs and disseminators of multi- and extensive-drug resistant salmonellae.

Metrics

Metrics Loading ...

References

Abdallah HM, Alnaiemi N, Reuland EA, Wintermans BB, Koek A, Abdelwahab AM, … Vandenbroucke-Grauls CMJE (2017). Fecal carriage of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae in Egyptian patients with community-onset gastrointestinal complaints: a hospital-based cross-sectional study. Antimicrobial Resistance Infection Control 6:62.

Addis Z, Kebede N, Worku Z, Gezahegn H, Yirsaw A, Kassa T (2011). Prevalence and antimicrobial resistance of Salmonella isolated from lactating cows and in contact humans in dairy farms of Addis Ababa: a cross sectional study. BMC Infectious Diseases 11(1):222.

Adeolu M, Alnajar S, Naushad S, Gupta R (2016). Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. International Journal of Systemic and Evolutionary Microbiology 66(12):5575-5599.

Adikwu P, Umeh EU, Iheukwumere CC, Ogbonna IO, Awodi PS, Obande GA (2018).Variation in Salmonella typhi infection among local populations in Southern Benue, Nigeria. International Journal of Enteric Pathogens 6(4):89-94.

Akinyemi KO, Iwalokun BA, Alafe OO, Mudashiru SA, Fakorede C (2015). blaCTX-M-1 group extended-spectrum beta-lactamase-producing Salmonella typhi from hospitalized patients in Lagos Nigeria. Infection and Drug Resistance 8:99-106.

Anyanwu MU, Ugwu IC, Onah CU (2018). Occurrence and antibiogram of generic extended-spectrum cephalosporin-resistant and extended-spectrum β-lactamase-producing enterobacteria in horses. Macedonian Veterinary Reviews 41(2):123-132.

Anibijuwon II, Gbala ID, Adebisi OO (2018). Carbapenem-resistant Enterobacteriaceae among in-patients of tertiary hospitals in Southwest Nigeria. Notulae Scientia Biologicae 10(3):310-317.

Balasubramanian R, Im J, Lee JS, Jeon HJ, Mogeni OD, Kim JH,… Marks F (2018). The global burden and epidemiology of invasive non-typhoidal Salmonella infections. Human Vaccines and Immunotherapeutics 15(6):1421-1426.

Beceiro A, Maharjan S, Gaulton T, Doumith M, Soares NC, Dhanji H,… Woodford N (2011). False extended-spectrum {beta}-lactamase phenotype in clinical isolates of Escherichia coli associated with increased expression of OXA-1 or TEM-1 penicillinases and loss of porins. Journal of Antimicrobial Chemotherapy 66(9):2006-2010.

Bockemuhl J (1976). Salmonellosis and shigellosis in Togo (West Africa), 1971-1973. I. Carrier rates in the rural population. Tropenmedizin und Parasitology 27(1):112-120.

Bockemuhl J (1977). Salmonellosis and shigellosis in Togo (West Africa), 1971-1973. Infections in the urban population of Lome.. Tropenmedizin und Parasitology 28(3):377-383.

Britto CD, Wong VK, Dougan G, Pollard AJ (2018). A systematic review of antimicrobial resistance in Salmonella enterica serovar Typhi, the etiological agent of typhoid. PLoS Neglected Tropical Diseases 12(10):e0006779.

Clinical and Laboratory Standards Institute (CLSI) (2018a). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. 11th ed. CLSI Standard M07. Wayne, PA: Clinical and Laboratory Standards Institute.

Clinical and Laboratory Standards Institute (CLSI) (2018b). Performance standard for antimicrobial susceptibility testing 28th ed. CLSI Standard M100, Wayne, PA: Clinical and Laboratory Standards Institute.

Crump JA, Heyderman RS (2015). A perspective on invasive Salmonella disease in Africa. Clinical Infectious Diseases 61(4):S235-S240.

Eze EA, Ocean EO, Eze EN (2015). Prevalence of beta-lactamases in Salmonella and Shigella in different hospitals in Anyigba Kogi State, Nigeria. African Journal of Microbiology Research 9(3):180-184.

Ejikeugwu C, Iroha I, Oguejiofor B, Orji Okoro L, Eluu S, Okafor C,, … Ezeador C (2017). Multidrug resistant metallo-β-lactamases (MBLs) positive Klebsiella species from cloacal swabs of poultry birds. Journal of Bacteriology and Parasitology 8:305.

Feglo PK, Frimpong EH, Essel-Ahun M (2004). Salmonellae carrier status of food vendors in Kumasi, Ghana. East African Medical Journal 81(7):358-361.

Fernández J, Guerra B, Rodicio MR (2018). Resistance to carbapenems in non-typhoidal Salmonella enterica serovars from humans, animals and food. Veterinary Science 5(2):40.

Hendriksen R. (2003). A global Salmonella surveillance and laboratory support project of the World Health Organization: Laboratory Protocols (Isolation of Salmonella), 4th Edition pp 253-278.

Jajere SM, Adamu NB, Atsanda NN, Onyilokwu SA, Gashua MM, Hambali IU, Mustapha FB (2015). Prevalence and antimicrobial resistance profiles of Salmonella isolates in apparently healthy slaughtered food animals at Maiduguri central abattoir Nigeria. Asian Pacific Journal of Tropical Diseases 5(12):996-1000.

Im J, Nichols C, Bjerregaard-Andersen M, Sow AG, Løfberg S, Tall A, … von Kalckreuth V (2016). Prevalence of Salmonella excretion in stool: a community survey in 2 sites, Guinea-Bissau and Senegal. Clinical Infectious Diseases 62(1):S50-S55.

Kariuki S, Gordon MA, Feasey N, Parry CM (2015). Antimicrobial resistance and management of invasive Salmonella disease. Vaccine 33(03):C21-C29.

Kemal J, Sibhat B, Menkir S, Terefe Y, Muktar Y (2015). Antimicrobial resistance patterns of Salmonella in Ethiopia: a review. African Journal of Microbiology Research 9(4):2249-2256.

Khan CMA (2014). The dynamic interactions between Salmonella and the microbiota, within the challenging giche of the gastrointestinal tract. International Scholarly Research Notes http: //dx.doi.org /10.1155/2014/846049.

Klemm EJ, Shakoor S, Page AJ, Qamar FN, Judge K, Saeed DK,…Hasan R. (2018). Emergence of an extensively drugresistant Salmonella enterica serovar Typhi clone harboring a promiscuous plasmid encoding resistance to fluoroquinolones and third-generation cephalosporins. mBio 9(1):e00105-18.

Krumperman PH (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied Environmental Microbiology 46(1):165-170.

Le Hello S, Bekhit A, Granier SA, Barua H, Beutlich J, Zając M,… Weill FX (2013). The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Frontiers in Microbiology 18(4):395.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG,… Monnet DL (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection 18(3):268-281.

Moudgil P, Bedi JS, Moudgil AD, Gill JPS, Aulakh RS (2017). Emerging issue of antibiotic resistance from food producing animals in India: Perspective and legal framework. Food Reviews International 34(5):447-462.

Nigerian Population Commission (NPC) (2007). Federal Republic of Nigeria (NPC/FRN). Special FRN, Gazette no 23 on the 2006 population census.

Ojo OE, Schwarz S, Michael GB (2016). Detection and characterization of extended-spectrum β-lactamase-producing Escherichia coli from chicken production chains in Nigeria. Veterinary Microbiology 15(194):62-68.

Olusanya O, Shonukan OO, Ogwo VA (1990). Childhood carriers of Salmonella and Shigella species in the rural area of Ile-Ife, Nigeria. Ethiopian Medical Journal 28(2):49-52.

Odugbemi T, Egri-Kwaji MT (1991). Screening of children for enteric bacterial pathogens in the outborn neonatal ward in Lagos, Nigeria. European Journal of Epidemiology 7(4):427-430.

Logan LK, Weinstein RA (2017). Epidemiology of carbapenem-resistant Enterobacteriaceae: The impact and evolution of a global menace. Journal of Infectious Diseases 215(S1):S28-36.

Lugito NPH, Cucunawangsi (2017). Antimicrobial resistance of Salmonella enterica serovars Typhi and Paratyphi isolates from a general hospital in Karawaci, Tangerang, Indonesia: A five-year review. International Journal of Microbiology https://doi.org/10.1155/2017/6215136.

Ramachandran A, Shanthi M, Sekar U (2017). Detection of blaCTX-M extended spectrum beta-lactamase producing Salmonella enterica serotype Typhi in a tertiary care centre. Journal of Clinical Diagnostic Research 11(9):DC21-DC24.

Rawat D, Nair D (2010). Extended-spectrum β-lactamases in Gram negative bacteria. Journal of Global Infectious Diseases 2(3):263-274.

Richardson NJ, Koornhof HJ (1965). Salmonellae and Shigellae in a group of Bantu school children in the eastern Transvaal Lowveld. South African Medical Journal 39(5):367-370.

Rotimi VO, Jamal W, Pal T, Sovenned A, Albert MJ (2008). Emergence of CTX-M-15 type extended-spectrum b-lactamase-producing Salmonella spp. in Kuwait and the United Arab Emirates. Journal of Medical Microbiology 57(7):881-886.

Smith SI, Alao F, Goodluck HT, Fowora M, Bamidele M, Omonigbehin E, Coker AO (2008). Prevalence of Salmonella typhi among food handlers from bukkas in Nigeria. British Journal of Biomedical Science 65(3):158-160.

Torkan S, Khamesipour F, Anyanwu MU (2015). Detection of virulence and antibacterial resistance genes in Salmonella isolates from diarrhoeic dogs in Iran. Revue de Medicine Veterinaire 166(7-8):221-228.

van Duijkeren E, Schink AK, Roberts MC, Wang Y, Schwarz S (2018). Mechanisms of bacterial resistance to antimicrobial agents. Microbiology Spectrum 6(1).

Whistler T, Sapchookul P, McCormick DW, Sangwichian O, Jorakate P, Makprasert S, … Gregory CJ (2018). Epidemiology and antimicrobial resistance of invasive non-typhoidal salmonellosis in rural Thailand from 2006-2014. PLoS Neglected Tropical Diseases 12(8):e0006718.

World Medical Association (WMA) (2013). World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. Journal of American Medical Association 310(20):2191-2194.

World Health Organization (WHO). Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25FebET_NM_WHO.pdf. 2017.

World Health Organization (WHO). Critically important antimicrobials for human medicine. 5th edition. http:// apps.who.int/iris/bitstream/handle/10665/255027/9789241512220eng.pdf;jsessionid=E6465D3C02939652305588FF323F0210?sequence=1.

Published
2019-09-30
How to Cite
OKPALANWA, C., ANYANWU, M. U., MOMOH, M. A., NNAMANI, P. O., & ATTAMA, A. A. (2019). Generic Salmonella in Asymptomatic Adult Volunteers: Occurrence, Antibiogram, Extended-Spectrum β-Lactamase Production and Carbapenem Resistance. Notulae Scientia Biologicae, 11(3), 383-390. https://doi.org/10.15835/nsb11310436
Section
Research articles

Most read articles by the same author(s)