Log in

Hygienic status of beef butcher shop facilities and antibiotic resistance profile of Salmonella enterica in Ethiopia

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

The microbiological quality of meat is influenced by the conditions of hygiene prevailing during production and handling. Thus, this study aimed to assess the prevalence of Salmonella enterica and its antimicrobial resistance, load of hygiene indicator bacteria including E. coli (ECC), coliforms (CC), total coliform (TCC), Enterobacteriaceae (EB) and aerobic plate count (APC), and meat handler’s food safety knowledge and hygiene practices in butcher shops in two cities, Addis Ababa and Hawassa in Ethiopia, during 2020 and 2021. A total of 360 samples of beef carcasses (n = 120), knives (n = 60), chop** boards (n = 60), weighing balance (n = 60), and personnel’s hands (n = 60) were randomly collected for microbial analysis. Besides, 120 participants were selected to participate in a food safety knowledge and hygiene practices assessment. The S. enterica isolates were identified by agglutination test followed by qPCR targeting invA gene. Phenotypic antimicrobial resistance profiles of S. enterica were determined using disk diffusion assays as described in CLSI. The ECC, CC, TCC, EB, and APC populations were quantified by plating onto petrifilm plates. A structured questionnaire was used to determine food safety knowledge and hygiene practices of participants. Overall prevalence of S. enterica was 16.7% (95% CI, 8.3—26.7) and location seems to have no effect (p = 0.806). Only 20% of the S. enterica were resistant to ampicillin and tetracycline. However, the majority (80%) of S. enterica isolates were susceptible to the panel of 11 antimicrobials tested. The overall mean ± SD (log CFU/cm2) of ECC, CC, TCC, EB, and APC were 4.31 ± 1.15; 4.61 ± 1.33; 4.77 ± 1.32; 4.59 ± 1.38 and 5.87 ± 1.52, respectively. No significant difference (p = 0.123) in E. coli contamination was observed between samples of beef carcasses and chop** boards. The EB contamination showed no significant difference (p > 0.05) among sample sources. The APC contamination levels on beef carcass were significantly higher (p > 0.05) than other sample sources. A total of 56% (95% CI: 46.7 – 65.0) of the participants had poor knowledge and 65% (95% CI: 56.7 – 73.3) had poor hygiene practices towards food safety. This study highlighted the poor hygiene status of butcher facilities with a potential risk of beef safety. Thus, appropriate food safety control strategies and inspection is needed at retail establishments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Data Availability

The data supporting the findings of this study are presented within the manuscript and as supplementary material. The raw data generated during the current study are available from the corresponding author on reasonable request.

References

  1. Adjei VY, Mensah GI, Parry-Hanson Kunadu A, Tano-Debrah K, Ayi I, Addo KK (2022) Microbial Safety of Beef Along Beef Value Chains in the Ashaiman Municipality of Ghana. Front Vet Sci 9:813422. https://doi.org/10.3389/fvets.2022.813422

    Article  PubMed  PubMed Central  Google Scholar 

  2. Agüeria DA, Terni C, Baldovino VM, Civit D (2018) Food safety knowledge, practices and attitudes of fishery workers in Mar del Plata, Argentina. Food Control 91:5–11. https://doi.org/10.1016/j.foodcont.2018.03.028

    Article  Google Scholar 

  3. Al-Shabib NA, Mosilhey SH, Husain FM (2016) Cross-sectional study on food safety knowledge, attitude and practices of male food handlers employed in restaurants of King Saud University, Saudi Arabia. Food Control 59:212–217

    Article  Google Scholar 

  4. Alcaine SD, Warnick LD, Wiedmann M (2007) Antimicrobial resistance in nontyphoidal Salmonella. J Food Prot 70(3):780–790. https://doi.org/10.4315/0362-028X-70.3.780

    Article  CAS  PubMed  Google Scholar 

  5. Ali NH, Farooqui A, Khan A, Khan AY, Kazmi SU (2010) Microbial contamination of raw meat and its environment in retail shops in Karachi, Pakistan. The J Infect Dev Count 4(06):382–388. https://doi.org/10.3855/jidc.599

    Article  Google Scholar 

  6. Amistu K, Ermias B, Asrat A (2017) Consumer preference of raw beef (‘Kurt’) in Wolaita Sodo Town. Southern Ethiopia J Food Dairy Technol 5(4):7–13

    Google Scholar 

  7. Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA (2015) Global burden of invasive nontyphoidal Salmonella disease, 2010. Emerg Infect Dis 21(6):941. https://doi.org/10.3201/eid2106.140999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Asfaw T, Genetu D, Shenkute D, Shenkutie TT, Amare YE, Yitayew B (2023) High Levels of Multidrug-Resistant and Beta-Lactamase-Producing Bacteria in Meat and Meat Contact Surfaces, Debre Berhan Town, Ethiopia. Infect Drug Resistance:1965–1977. https://doi.org/10.2147/IDR.S405582

  9. Atlabachew T, Mamo J (2021) Microbiological quality of meat and swabs from contact surface in butcher shops in Debre Berhan, Ethiopia. J Food Qual 2021:1–11. https://doi.org/10.1155/2021/7520882

    Article  CAS  Google Scholar 

  10. Azage M, Kibret M (2017) The bacteriological quality, safety, and Antibiogram of salmonella isolates from fresh meat in retail shops of Bahir Dar City, Ethiopia. Int J Food Sci. https://doi.org/10.1155/2017/4317202

  11. Bahir MA, Errachidi I, Hemlali M, Sarhane B, Tantane A, Mohammed A, Filali-Maltouf A (2022) Knowledge, attitude, and practices (KAP) regarding meat safety and sanitation among carcass handlers operating and assessment of bacteriological quality of meat contact surfaces at the Marrakech slaughterhouse, Morocco. Int J Food Sci. https://doi.org/10.1155/2022/4881494

  12. Barbosa TM, Levy SB (2000) The impact of antibiotic use on resistance development and persistence. Drug Resist Updates 3(5):303–311. https://doi.org/10.1054/drup.2000.0167

    Article  Google Scholar 

  13. Barolia SK, Verma S, Verma BK (2011) Coliform contamination on different paper currency in Ajmer, Rajasthan, India. Univers J Environ Res Technol 1(4):552–556

    Google Scholar 

  14. Barros MDAF, Nero LA, Monteiro AA, Beloti V (2007) Identification of main contamination points by hygiene indicator microorganisms in beef processing plants. Food Sci Tech 27:856–862. https://doi.org/10.1590/S0101-20612007000400028

    Article  Google Scholar 

  15. Bersisa A, Tulu D, Negera C (2019) Investigation of bacteriological quality of meat from abattoir and butcher shops in Bishoftu, Central Ethiopia. Int J Microbiol. https://doi.org/10.1155/2019/6416803

  16. Beyi AF, Fite AT, Tora E, Tafese A, Genu T, Kaba T, Cox E (2017) Prevalence and antimicrobial susceptibility of Escherichia coli O157 in beef at butcher shops and restaurants in central Ethiopia. BMC Microbiol 17:1–6. https://doi.org/10.1186/s12866-017-0964-z

    Article  CAS  Google Scholar 

  17. Bonke R, Wacheck S, Bumann C, Thum C, Stüber E, König M, Fredriksson-Ahomaa M (2012) High prevalence of Salmonella enterica subsp. diarizonae in tonsils of sheep at slaughter. Food Res Int 45(2):880–884. https://doi.org/10.1016/j.foodres.2011.01.050

  18. Birhanu W, Weldegebriel S, Bassazin G, Mitku F, Birku L, Tadesse M (2017) Assesment of microbiological quality and meat handling practices in butcher shops and abattoir found in Gondar town Ethiopia. Int J Microbiol Res 8(2):59–68

    CAS  Google Scholar 

  19. Cai Y, Tao J, Jiao Y, Fei X, Zhou L, Wang Y, Jiao X (2016) Phenotypic characteristics and genotypic correlation between Salmonella isolates from a slaughterhouse and retail markets in Yangzhou, China. Int J Food Microbiol 222:56–64. https://doi.org/10.1016/j.ijfoodmicro.2016.01.020

    Article  CAS  PubMed  Google Scholar 

  20. Chen S, Zhao S, White DG, Schroeder CM, Lu R, Yang H, Meng J (2004) Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 70(1):1–7. https://doi.org/10.1128/AEM.70.1.1-7.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. CLSI (2020) Performance Standards for Antimicrobial Susceptibility Testing. 30th Ed. CLSI Supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute. vol 8. http://www.emeraldinsight.com/doi/10.1108/08876049410065598

  22. Cui M, **e M, Qu Z, Zhao S, Wang J, Wang Y, Wu C (2016) Prevalence and antimicrobial resistance of Salmonella isolated from an integrated broiler chicken supply chain in Qingdao, China. Food Control 62:270–276. https://doi.org/10.1016/j.foodcont.2015.10.036

    Article  CAS  Google Scholar 

  23. Curiale MS, Sons T, Mclver D, McAllister JS, Halsey B, Roblee D, Fox TL (2002) ‘Official Method 991.14 Coliform and Escherichia Coli Counts in Foods’. Journal of AOAC International 74 (4): 635–48. http://edgeanalytical.com/wp-content/uploads/Food_AOAC-991.14.pdf

  24. da Cunha-Neto A, Carvalho LA, Carvalho RCT, dos Prazeres Rodrigues D, Mano SB, de Souza Figueiredo EE, & Conte-Junior CA (2018) Salmonella isolated from chicken carcasses from a slaughterhouse in the state of Mato Grosso, Brazil: antibiotic resistance profile, seroty**, and characterization by repetitive sequence-based PCR system. Poultry science, 97(4):1373–1381

  25. De Boeck E, Jacxsens EL, Bollaerts M, Uyttendaele M, Vlerick P (2016) Interplay between food safety climate, food safety management, and microbiology hygiene in farm butcheries and affiliated butcher shops. Food Control 65:78–91

    Article  Google Scholar 

  26. ESA (2019) Ethiopian National Standard on Beef_ Specification. ES 1111: 2019. 3rd Edition

  27. Figueiredo R, Card RM, Nunez-Garcia J, Mendonça N, da Silva GJ, Anjum MF (2018) Multidrug-Resistant Salmonella enterica Isolated from Food Animal and Foodstuff May Also Be Less Susceptible to Heavy Metals. Foodborne Pathog Dis 16(3):166–172. https://doi.org/10.1089/fpd.2017.2418

  28. Garedew L, Hagos Z, Addis Z, Tesfaye R, Zegeye B (2015) Prevalence and antimicrobial susceptibility patterns of Salmonella isolates in association with hygienic status from butcher shops in Gondar town, Ethiopia. Antimicrob Resist Infect Control 4:1–7. https://doi.org/10.1186/s13756-015-0062-7

    Article  Google Scholar 

  29. Gebeyehu DT, Tsegaye H (2022) Food safety knowledge and practice of abattoir and butcher shop workers: a health risk management perspective. One Health Outlook 4(1):14

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ghafir Y, China B, Dierick K, De Zutter L, Daube G (2008) Hygiene indicator microorganisms for selected pathogens on beef, pork, and poultry meats in Belgium. J Food Prot 71(1):35–45. https://doi.org/10.4315/0362-028X-71.1.35

    Article  CAS  PubMed  Google Scholar 

  31. Gyles CL (2007) Shiga toxin-producing Escherichia coli: an overview. J Animal Sci 85(suppl_13):E45-E62. https://doi.org/10.2527/jas.2006-508

  32. Haileselassie M, Taddele H, Adhana K, Kalayou S (2013) Food safety knowledge and practices of abattoir and butchery shops and the microbial profile of meat in Mekelle City, Ethiopia. Asian Pac J Trop Biomed 3(5):407–412. https://doi.org/10.1016/S2221-1691(13)60085-4

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hoffmann S, Devleesschauwer B, Aspinall W, Cooke R, Corrigan T, Havelaar A, Hald T (2017) Attribution of global foodborne disease to specific foods: Findings from a World Health Organization structured expert elicitation. PLoS ONE 12(9):e0183641. https://doi.org/10.1371/journal.pone.0183641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kawano K, Okada M, Haga T, Maeda K, Goto Y (2008) Relationship between pathogenicity for humans and stx genotype in Shiga toxin-producing Escherichia coli serotype O157. Eur J Clin Microbiol Infect Dis 27:227–232. https://doi.org/10.1007/s10096-007-0420-3

    Article  CAS  PubMed  Google Scholar 

  35. Kebede T, Afera B, Taddele H, Bsrat A (2014) Assessment of bacteriological quality of sold meat in the butcher shops of Adigrat, Tigray, Ethiopia. Appl J Hygiene 3(3):38–44. https://doi.org/10.5829/idosi.ajh.2014.3.3.8636

    Article  Google Scholar 

  36. Khan A, Rind R, Shoaib M, Kamboh AA, Mughal GA, Lakho SA, Yousaf A (2016) Isolation, identification and antibiogram of Escherichia coli from table eggs. J Anim Health Prod 4(1):1–5. https://doi.org/10.14737/journal.jahp/2016/4.1.1.5

  37. Li Y, Yang Q, Cao C, Cui S, Wu Y, Yang H, Yang B (2020) Prevalence and characteristics of Salmonella isolates recovered from retail raw chickens in Shaanxi Province, China. Poultry Sci 99(11):6031–6044. https://doi.org/10.1016/j.psj.2020.07.038

    Article  CAS  Google Scholar 

  38. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, International Collaboration on Enteric Disease “Burden of Illness” Studies (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50(6):882-889.https://doi.org/10.1086/650733

  39. McAfee AJ, McSorley EM, Cuskelly GJ, Moss BW, Wallace JM, Bonham MP, Fearon AM (2010) Red meat consumption: An overview of the risks and benefits. Meat Sci 84(1):1–13. https://doi.org/10.1016/j.meatsci.2009.08.029

    Article  CAS  PubMed  Google Scholar 

  40. McEwen SA, Fedorka-Cray PJ (2002) Antimicrobial use and resistance in animals. Clin Infect Dis, 34(Supplement_3):S93-S106. https://doi.org/10.1086/340246

  41. Nidaullah H, Abirami N, Shamila-Syuhada AK, Chuah LO, Nurul H, Tan TP, Rusul G (2017) Prevalence of Salmonella in poultry processing environments in wet markets in Penang and Perlis, Malaysia. Vet World 10(3):286. https://doi.org/10.14202/vetworld.2017.286-292

  42. Park CJ, Li J, Zhang X, Gao F, Benton CS, Andam CP (2021) Diverse lineages of multidrug resistant clinical Salmonella enterica and a cryptic outbreak in New Hampshire, USA revealed from a year-long genomic surveillance. Infect Genet Evol 87:104645. https://doi.org/10.1016/j.meegid.104645

    Article  CAS  PubMed  Google Scholar 

  43. Pennington H (2010) Escherichia coli O157. Lancet 376(9750):1428–1435. https://doi.org/10.1016/S0140-6736(10)60963-4

    Article  CAS  PubMed  Google Scholar 

  44. Prendergast DM, Duggan SJ, Fanning S, Cormican M, Gonzales‐Barron U, Butler F, Duffy G (2008) Prevalence and numbers of Salmonella spp. and Enterobacteriaceae on pork cuts in abattoirs in the Republic of Ireland. J Appl Microbiol 105(4):1209–1219. https://doi.org/10.1111/j.1365-2672.2008.03854.x

  45. Redmond E, Griffith C (2006) Consumers of food products, domestic hygiene and public health. Understanding consumers of food products, 463–495. https://doi.org/10.1533/9781845692506.4.463

  46. Sallam KI, Mohammed MA, Hassan MA, Tamura T (2014) Prevalence, molecular identification and antimicrobial resistance profile of Salmonella serovars isolated from retail beef products in Mansoura. Egypt Food Control 38:209–214. https://doi.org/10.1016/j.foodcont.2013.10.027

    Article  CAS  Google Scholar 

  47. Serraino A, Bardasi L, Riu R, Pizzamiglio V, Liuzzo G, Galletti G, Merialdi G (2012) Visual evaluation of cattle cleanliness and correlation to carcass microbial contamination during slaughtering. Meat Sci 90(2):502–506. https://doi.org/10.1016/j.meatsci.2011.08.001

    Article  PubMed  Google Scholar 

  48. Soares LS, Almeida RC, Cerqueira ES, Carvalho JS, Nunes IL (2012) Knowledge, attitudes and practices in food safety and the presence of coagulase-positive staphylococci on hands of food handlers in the schools of Camaçari. Brazil Food control 27(1):206–213. https://doi.org/10.1016/j.foodcont.2012.03.016

    Article  Google Scholar 

  49. Tadesse G (2014) Prevalence of human Salmonellosis in Ethiopia: a systematic review and meta-analysis. BMC Infect Dis 14:1–10. https://doi.org/10.1186/1471-2334-14-88

    Article  Google Scholar 

  50. Teferi SC (2022) Food safety practice and its associated factors among meat handlers in North Shewa Zone, Oromia, Ethiopia. Int J Food Sci 2022. https://doi.org/10.1155/2022/5829352

  51. Teshome G, Habtam T (2022) Food safety knowledge and practice of abattoir and butcher shop workers: a health risk management perspective. One Health Outlook (Web) 4(1):1–14

    Google Scholar 

  52. Ukwuru MU, Gabriel A (2012) Cross contamination between food and money due to simultaneous handling. J Appll Sci Environ 3:42–48

    Google Scholar 

  53. USDA-FSIS (2019) Isolation and Identification of Salmonella from Meat, Poultry, Pasteurized Egg, and Siluriformes (Fish) Products and Carcass and Environmental Sponges. Available online: https://s27415.pcdn.co/wp-content/uploads/2020/01/64ER20-7/Microbial/5-USDA-FSIS-4.10-Isolation-and-Identification-of-Salmonella.pdf

  54. Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, Dougan G (2015) Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter-and intracontinental transmission events. Nat Genet 47(6):632–639. https://doi.org/10.1038/ng.3281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wu Y, Jiang T, Bao D, Yue M, Jia H, Wu J, Ruan Z (2023) Global population structure and genomic surveillance framework of carbapenem-resistant Salmonella enterica. Drug Resist Updat 68:100953. https://doi.org/10.1016/j.drup.100953

    Article  CAS  PubMed  Google Scholar 

  56. Yang B, Qu D, Zhang X, Shen J, Cui S, Shi Y, Meng J (2010) Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China. Int J Food Microbiol 141(1–2):63–72. https://doi.org/10.1016/j.ijfoodmicro.2010.04.015

    Article  CAS  PubMed  Google Scholar 

  57. Zelalem A, Abegaz K, Kebede A, Terefe Y, Schwan CL, Vipham JL (2021) Food safety knowledge, attitudes, and hygienic practices of abattoir workers in Ethiopia: A cross-sectional study. Food Prot Trends 41(5):501–509. https://doi.org/10.4315/1541-9576-41.5.501

    Article  Google Scholar 

  58. Zelalem A, Sisay M, Vipham JL, Abegaz K, Kebede A, Terefe Y (2019) The prevalence and antimicrobial resistance profiles of bacterial isolates from meat and meat products in Ethiopia: a systematic review and meta-analysis. Int J Food Contamin 6(1):1–14. https://doi.org/10.1186/s40550-019-0071-z

    Article  Google Scholar 

  59. Zerabruk K, Retta N, Muleta D, Tefera AT (2019) Assessment of microbiological safety and quality of minced meat and meat contact surfaces in selected butcher shops of Addis Ababa, Ethiopia. J Food Qual. https://doi.org/10.1155/2019/3902690

Download references

Acknowledgements

The authors are grateful to staff of Animal Health institute, Haramaya University, Hawassa University and Kansas State University for supporting the microbial analysis of the study by providing consumables and laboratory services. The authors also would like extend their gratitude to butcher shop workers for their collaboration during the study time.

Funding

The authors were funded by the United States Agency for International Development (USAID) Bureau for Food Security under Agreement # AID-OAA-L-15–00003 as part of Feed the Future Innovation Lab for Livestock Systems. Any opinions, findings, conclusions, or recommendations expressed here are those of the authors alone.

Author information

Authors and Affiliations

Authors

Contributions

Andarge Zelalem participated in the experimental and project design, method development, validation, experimental activities, analyzing and interpreting the data, drafting and writing the manuscript. Kebede Abegaz and Jessie L. Vipham participated in experimental and project design, conceptualization, methodology, validation, fund acquisition, supervision, reviewing and editing the manuscript. Tafesse Koran, Abebe Olani, Abde Aliy, Zelalem Abera, Bahar Mummed, Meseret Chimdessa, Selam Fentahun and Carla L. Schwan participated in experimental design, experimental activities, analyzing and interpreting data. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Andarge Zelalem.

Ethics declarations

Competing interest

The authors declare that they have no competing interest.

Additional information

Responsible Editor: Luis Augusto Nero

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

• The S. enterica was recovered from beef with prevalence rate of 16.7% in butcher shops.

• Majority (80%) of the S. enterica isolates were susceptible to 11 antimicrobials tested.

• The mean ± SD (log CFU/cm2) of generic E. coli (4.31 ± 1.15) and Enterobacteriaceae (4.59 ± 1.38) indicates existence of meat safety risks.

• Among the sampled beef carcasses, 18.3% for E. coli and 15.0% for aerobic plate count were within the acceptable limit set by Ethiopian standards of beef specification

• 56% of the participants had poor knowledge towards food safety

• 65% of the participants had poor hygiene practices towards food safety

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 14 KB)

Supplementary file2 (DOCX 15 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zelalem, A., Koran, T., Abegaz, K. et al. Hygienic status of beef butcher shop facilities and antibiotic resistance profile of Salmonella enterica in Ethiopia. Braz J Microbiol 55, 1703–1714 (2024). https://doi.org/10.1007/s42770-024-01312-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-024-01312-2

Keywords

Navigation