1887

Microbiology Society logo

Volume 168, Issue 10

Phenotypic and genotypic profiling reveals a high prevalence of methicillin-resistant isolated from hospitals, houseflies and adjacent informal food retailers in Botswana Free

Abstract

The increasing occurrence of methicillin-resistant (MRSA) in the environment, food and healthcare systems is a global public health concern. MRSA is reported to cause food poisoning, osteomyelitis and pyogenic infections of the skin, and consequently has been categorized as a high-priority pathogen by the World Health Organization. Here, we determined the presence of MRSA in clinical (=56), food (=150) and housefly samples (=970) collected from two hospitals in Botswana. Characterization based on phenotypic (antimicrobial resistance, biofilm production) and genotypic (antimicrobial resistance genes and integrons) profiles were performed on all isolates. Of the total samples tested, 64 were positive for MRSA following conventional culture methods and PCR amplification of the and genes for confirmation of presumptive MRSA isolates. The confirmed isolates included 71 % (95 % CI 83.2–59.6) from clinical, 9 % (95 % CI 14­–4.8) from food, and 1 % (95 % CI 1.6–0.4) collected from housefly samples. In total 89 % (=57) isolates in the current study showed a multidrug resistance phenotype, among these, resistance to β-lactams and glycoside antibiotic classes were predominant. Genotypic characterization showed the domination of the gene (95 %) followed by (63 %) and (19 %) whilst was only reported in 13 % of the isolates. Integrons were detected in 50 % (32/64) of the total MRSA isolates, and we report a high prevalence of gene, detected in 67 % (43/64) of the isolates followed by 38 % (24/64) whilst (3%) was the least detected genetic determinant. The genes and were not detected in a ll the tested MRSA isolates. We provide the first report on the prevalence of MRSA isolated from the clinical-food-vector nexus harbouring biofilm and genes, and antibiotic resistance profiles in Botswana. These results are significant for risk-assessment analysis and the development of improved MRSA infection prevention and control strategies.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): clinical , food , houseflies , MDR and MRSA
© 2022 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001213
2022-10-26
2024-04-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/168/10/mic001213.html?itemId=/content/journal/micro/10.1099/mic.0.001213&mimeType=html&fmt=ahah

References

  1. Patel K, Godden SM, Royster EE, Crooker BA, Johnson TJ et al. Prevalence, antibiotic resistance, virulence and genetic diversity of Staphylococcus aureus isolated from bulk tank milk samples of U.S. dairy herds. BMC Genomics 2021; 22:1–13 [View Article] [PubMed]
     [Google Scholar]
  2. Andrade-Figueiredo M, Leal-Balbino TC. Clonal diversity and epidemiological characteristics of Staphylococcus aureus: high prevalence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) associated with clinical isolates in Brazil. BMC Microbiol 2016; 16:1–9 [View Article] [PubMed]
     [Google Scholar]
  3. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 2019; 17:203–218 [View Article] [PubMed]
     [Google Scholar]
  4. Kourtis AP, Hatfield K, Baggs J, Mu Y, See I et al. Vital signs: epidemiology and recent trends in methicillin-resistant and in methicillin-susceptible Staphylococcus aureus bloodstream infections - United States. MMWR Morb Mortal Wkly Rep 2019; 68:214–219 [View Article] [PubMed]
     [Google Scholar]
  5. Garoy EY, Gebreab YB, Achila OO, Tekeste DG, Kesete R et al. Methicillin-resistant Staphylococcus aureus (MRSA): prevalence and antimicrobial sensitivity pattern among patients - A multicenter study in asmara, eritrea. Can J Infect Dis Med Microbiol 2019; 2019:
     [Google Scholar]
  6. Wangai FK, Masika MM, Maritim MC, Seaton RA. Methicillin-resistant Staphylococcus aureus (MRSA) in East Africa: red alert or red herring?. BMC Infect Dis 2019; 19:1–10 [View Article]
     [Google Scholar]
  7. Perovic O, Iyaloo S, Kularatne R, Lowman W, Bosman N et al. Prevalence and trends of Staphylococcus aureus bacteraemia in hospitalized patients in South Africa, 2010 to 2012: laboratory-based Surveillance mapping of antimicrobial resistance and molecular epidemiology. PLoS One 2015; 10:1–14 [View Article]
     [Google Scholar]
  8. Wood SM, Shah SS, Bafana M, Ratner AJ, Meaney PA et al. Epidemiology of methicillin-resistant Staphylococcus aureus bacteremia in Gaborone, Botswana. Infect Control Hosp Epidemiol 2009; 30:782–785 [View Article]
     [Google Scholar]
  9. Sato T, Usui M, Konishi N, Kai A, Matsui H et al. Closely related methicillin-resistant Staphylococcus aureus isolates from retail meat, cows with mastitis, and humans in Japan. PLoS One 2017; 12:1–11 [View Article]
     [Google Scholar]
  10. Weese JS, van Duijkeren E. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet Microbiol 2010; 140:418–429 [View Article]
     [Google Scholar]
  11. Ferreira JP, Anderson KL, Correa MT, Lyman R, Ruffin F et al. Transmission of MRSA between companion animals and infected human patients presenting to outpatient medical care facilities. PLoS One 2011; 6:e26978 [View Article]
     [Google Scholar]
  12. van Duijkeren E, Wolfhagen MJHM, Box ATA, Heck MEOC, Wannet WJB et al. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 2004; 10:2235–2237 [View Article]
     [Google Scholar]
  13. Juhász-Kaszanyitzky E, Jánosi S, Somogyi P, Dán A, Van Der Graaf-van Bloois L. MRSA transmission between cows and humans. Emerg Infect Dis 2007; 13:630–632 [View Article]
     [Google Scholar]
  14. Baptiste KE, Williams K, Willams NJ, Wattret A, Clegg PD et al. Methicillin-resistant staphylococci in companion animals. Emerg Infect Dis 2005; 11:1942–1944 [View Article]
     [Google Scholar]
  15. Pu S, Han F, Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol 2009; 75:265–267 [View Article]
     [Google Scholar]
  16. You Y, Song L, Nonyane BAS, Price LB, Silbergeld EK. Genomic differences between nasal Staphylococcus aureus from HOG slaughterhouse workers and their communities. PLoS One 2018; 13:e0193820 [View Article]
     [Google Scholar]
  17. Kyany’a C, Nyasinga J, Matano D, Oundo V, Wacira S et al. Phenotypic and genotypic characterization of clinical Staphylococcus aureus isolates from Kenya. BMC Microbiol 2019; 19:1–11 [View Article]
     [Google Scholar]
  18. Piddock LJV. Assess drug-resistance phenotypes, not just genotypes. Nat Microbiol 2016; 1:16120 [View Article]
     [Google Scholar]
  19. Islam MA, Parveen S, Rahman M, Huq M, Nabi A et al. Occurrence and characterization of methicillin resistant Staphylococcus aureus in processed raw foods and ready-to-eat foods in an urban setting of a developing country. Front Microbiol 2019; 10:1–7 [View Article]
     [Google Scholar]
  20. Loeto D, Matsheka MI, Gashe BA. Enterotoxigenic and antibiotic resistance determination of Staphylococcus aureus strains isolated from food handlers in Gaborone, Botswana. J Food Prot 2007; 70:2764–2768 [View Article]
     [Google Scholar]
  21. Onwugamba FC, Fitzgerald JR, Rochon K, Guardabassi L, Alabi A et al. The role of “filth flies” in the spread of antimicrobial resistance. Travel Med Infect Dis 2018; 22:8–17 [View Article]
     [Google Scholar]
  22. Akter S, Sabuj AAM, Haque ZF, Kafi MA, Rahman MT et al. Detection of antibiotic-resistant bacteria and their resistance genes from houseflies. Vet World 2020; 13:266–274 [View Article]
     [Google Scholar]
  23. Dehkordi FS, Gandomi H, Basti AA, Misaghi A, Rahimi E. Phenotypic and genotypic characterization of antibiotic resistance of methicillin- resistant staphylococcus aureus isolated from hospital food; 2017:1–11
  24. Karmakar A, Dua P, Ghosh C. Biochemical and molecular analysis of Staphylococcus aureus clinical isolates from hospitalized patients. Can J Infect Dis Med Microbiol 2016; 2016:9041636 [View Article]
     [Google Scholar]
  25. Maurice Bilung L, Tahar AS, Kira R, Mohd Rozali AA, Apun K. High occurrence of Staphylococcus aureus isolated from fitness equipment from selected gymnasiums. J Environ Public Health 2018; 2018:4592830 [View Article]
     [Google Scholar]
  26. Abdolmaleki Z, Mashak Z, Safarpoor Dehkordi F. Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrob Resist Infect Control 2019; 8:1–14 [View Article]
     [Google Scholar]
  27. Pu S, Wang F, Ge B. Characterization of toxin genes and antimicrobial susceptibility of Staphylococcus aureus isolates from Louisiana retail meats. Foodborne Pathog Dis 2011; 8:299–306 [View Article]
     [Google Scholar]
  28. Uzunović S, Ibrahimagić A, Kamberović F, Rijnders MIA, Stobberingh EE. Molecular characterization of methicillin-susceptible and methicillin- resistant Staphylococcus aureus in food handlers in Bosnia and Herzegovina. TOIDJ 2013; 7:15–20 [View Article]
     [Google Scholar]
  29. CLSI - Clinical & Laboratory Standards Institute Performance standards for Antimicrobial Susceptibility Testing. An informational supplement for global application developed through the Clinical and Laboratory Standards Institute. Vol. 33, Clinical and Laboratory Standards Institute 2011 pp 1–35
     [Google Scholar]
  30. Mirzaee M, Peerayeh SN, Ghasemian A-M. Detection of icaABCD genes and biofilm formation in clinical isolates. Original article. Iran J Pathol 2014; 9:257–262
     [Google Scholar]
  31. Azab KSM, Abdel-Rahman MA, El-Sheikh HH, Azab E, Gobouri AA et al. Distribution of extended-spectrum β-lactamase (ESBL)-encoding genes among multidrug-resistant gram-negative pathogens collected from three different countries. Antibiotics 2021; 10:247 [View Article]
     [Google Scholar]
  32. Smith MS, Yang RK, Knapp CW, Niu Y, Peak N et al. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 2004; 70:7372–7377 [View Article]
     [Google Scholar]
  33. Shen H, Liu Y, Qu J, Cao B. Comparison of vanA gene mRNA levels between vancomycin-resistant Enterococci presenting the VanA or VanB phenotype with identical Tn1546-like elements. J Microbiol Immunol Infect 2016; 49:866–871 [View Article]
     [Google Scholar]
  34. Li L, Zhao X. Characterization of the resistance class 1 integrons in Staphylococcus aureus isolates from milk of lactating dairy cattle in Northwestern China. BMC Vet Res 2018; 14:1–7 [View Article]
     [Google Scholar]
  35. Yang X, Yu S, Wu Q, Zhang J, Wu S et al. Multilocus sequence typing and virulence-associated gene profile analysis of Staphylococcus aureus isolates from retail ready-to-eat food in China. Front Microbiol 2018; 9:1–8 [View Article]
     [Google Scholar]
  36. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
     [Google Scholar]
  37. Achek R, Hotzel H, Cantekin Z, Nabi I, Hamdi TM et al. Emerging of antimicrobial resistance in staphylococci isolated from clinical and food samples in Algeria. BMC Res Notes 2018; 11:1–7 [View Article]
     [Google Scholar]
  38. Pillsbury A, Chiew M, Bates J, Sheppeard V. An outbreak of staphylococcal food poisoning in a commercially catered buffet. Commun Dis Intell Q Rep 2013; 37:E144–E148
     [Google Scholar]
  39. Truong H, Shah SS, Ludmir J, Tawanana EO, Bafana M et al. Staphylococcus aureus skin and soft-tissue infections at a tertiary hospital in Botswana. Antimicrob Resist Infect Control 2011; 101:413–417 [View Article]
     [Google Scholar]
  40. Wang Y-T, Lin Y-T, Wan T-W, Wang D-Y, Lin H-Y et al. Distribution of antibiotic resistance genes among Staphylococcus species isolated from ready-to-eat foods. J Food Drug Anal 2019; 27:841–848 [View Article]
     [Google Scholar]
  41. Bouamamaa L, Sorlozano A, Laglaoui A, Lebbadi M, Aarab A et al. Antibiotic resistance patterns of bacterial strains isolated from Periplaneta americana and Musca domestica in Tangier, Morocco. J Infect Dev Ctries 2010; 4:194–201 [View Article]
     [Google Scholar]
  42. Schaumburg F, Onwugamba FC, Akulenko R, Peters G, Mellmann A et al. A geospatial analysis of flies and the spread of antimicrobial resistant bacteria. Int J Med Microbiol 2016; 306:566–571 [View Article]
     [Google Scholar]
  43. Islam M, Sultana ZZ, Iqbal A, Ali M, Hossain A. Effect of in-house crowding on childhood hospital admissions for acute respiratory infection: a matched case-control study in Bangladesh. Int J Infect Dis 2021; 105:639–645 [View Article]
     [Google Scholar]
  44. Al-Zoubi MS, Al-Tayyar IA, Hussein E, Jabali AA, Khudairat S. Antimicrobial susceptibility pattern of Staphylococcus aureus isolated from clinical specimens in Northern area of Jordan. Iran J Microbiol 2015; 7:265–272
     [Google Scholar]
  45. Pekana A, Green E. Antimicrobial resistance profiles of Staphylococcus aureus isolated from meat carcasses and bovine milk in abattoirs and dairy farms of the Eastern Cape, South Africa. Int J Environ Res Public Health 2018; 15:E2223 [View Article]
     [Google Scholar]
  46. Al-Amery K, Elhariri M, Elsayed A, El-Moghazy G, Elhelw R et al. Vancomycin-resistant Staphylococcus aureus isolated from camel meat and slaughterhouse workers in Egypt. Antimicrob Resist Infect Control 2019; 8:1–8 [View Article]
     [Google Scholar]
  47. Wu Q, Sabokroo N, Wang Y, Hashemian M, Karamollahi S et al. Systematic review and meta-analysis of the epidemiology of vancomycin-resistance Staphylococcus aureus isolates. Antimicrob Resist Infect Control 2021; 10:101 [View Article]
     [Google Scholar]
  48. Rağbetli C, Parlak M, Bayram Y, Guducuoglu H, Ceylan N. Evaluation of antimicrobial resistance in Staphylococcus aureus isolates by years. Interdiscip Perspect Infect Dis 2016; 2016:9171395 [View Article]
     [Google Scholar]
  49. Harkins CP, Pichon B, Doumith M, Parkhill J, Westh H et al. Methicillin-resistant Staphylococcus aureus emerged long before the introduction of methicillin into clinical practice. Genome Biol 2017; 18:1–11 [View Article]
     [Google Scholar]
  50. Schroeder M, Brooks BD, Brooks AE. The complex relationship between virulence and antibiotic resistance. Genes (Basel) 2017; 8:E39 [View Article]
     [Google Scholar]
  51. Omidi M, Firoozeh F, Saffari M, Sedaghat H, Zibaei M et al. Ability of biofilm production and molecular analysis of spa and ica genes among clinical isolates of methicillin-resistant Staphylococcus aureus. BMC Res Notes 2020; 13:1–7 [View Article]
     [Google Scholar]
  52. Kim BR, Bae YM, Lee SY. Effect of environmental conditions on biofilm formation and related characteristics of Staphylococcus aureus. J Food Saf 2016; 36:412–422 [View Article]
     [Google Scholar]
  53. Algammal AM, Hetta HF, Batiha GE, Hozzein WN, El Kazzaz WM et al. Virulence-determinants and antibiotic-resistance genes of MDR-E. coli isolated from secondary infections following FMD-outbreak in cattle. Sci Rep 2020; 10:1–13 [View Article]
     [Google Scholar]
  54. Koosha RZ, Fooladi AAI, Hosseini HM, Aghdam EM. Prevalence of exfoliative toxin A and B genes in Staphylococcus aureus isolated from clinical specimens. J Infect Public Health 2014; 7:177–185 [View Article]
     [Google Scholar]
  55. Abimanyu N, Krishnan A, Murugesan S, Kaushik Subramanian G, Gurumurthy S et al. Use of triplex PCR, for rapid, PVL, MRSA, from methicillin-resistant coagulase negative staphylococci. J Clin Diagnostic Res 2013; 7:215–218 [View Article]
     [Google Scholar]
  56. Bukowski M, Wladyka B, Dubin G. Exfoliative toxins of Staphylococcus aureus. Toxins (Basel) 2010; 2:1148–1165 [View Article]
     [Google Scholar]
  57. Kleinwaks LP, Leung B, Sen B, Emery CL, Hamilton RJ et al. PVL toxin-producing methicillin-resistant sstaphylococcus aureus (MRSA) are predominant in a tertiary-care metropolitan teaching hospital; 2017; 32143–145
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001213
Loading
Phenotypic and genotypic profiling reveals a high prevalence of methicillin-resistant Staphylococcus aureus isolated from hospitals, houseflies and adjacent informal food retailers in Botswana
Microbiology 168, 001213 (2022); https://doi.org/10.1099/mic.0.001213
/content/journal/micro/10.1099/mic.0.001213
/content/journal/micro/10.1099/mic.0.001213
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error