Salmonella Characterization in Poultry Eggs Sold in Farms and Markets in Relation to Handling and Biosecurity Practices in Ogun State, Nigeria
Abstract
:1. Introduction
2. Results
2.1. Prevalence and Diversity of Salmonella Isolates on Shells and in Contents of Eggs
2.2. Salmonella Serovar Resistance to Antimicrobials and Their Resistance Patterns
2.3. Biosecurity Practices in the Production and Handling of Eggs
3. Discussion
4. Materials and Methods
4.1. Study Location
4.2. Sample Collection
4.3. Isolation of Salmonella
4.4. Biochemical Identification of Salmonella
4.5. Antibiotic Sensitivity Testing
4.6. Procedure
4.7. Serotyping of Salmonella
4.8. Determination of Biosecurity Practices on Poultry Farms
4.9. Data Management and Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Idowu, F.; Junaid, K.; Paul, A.; Gabriel, O.; Paul, A.; Sati, N.; Maryam, M.; Jarlath, U. Antimicrobial screening of commercial eggs and determination of Tetracycline residue using two microbiological methods. Int. J. Poult. Sci. 2010, 9, 959–962. [Google Scholar] [CrossRef]
- Bettridge, J.M.; Lunch, S.E.; Brena, M.C.; Melese, K.; Dessie, T.; Terfa, Z.G.; Desta, T.; Rushton, S.; Hanotte, O.; Kaiser, P.; et al. Infection-interactions in Ethiopian village chickens. Prev. Vet. Med. 2014, 117, 358–366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Food and Agriculture Organization. Livestock and Livelihoods Spotlight NIGERIA: Cattle and Poutry Sectors. 2018. Available online: http://www.fao.org/3/CA2149EN/ca2149en.pdf (accessed on 22 November 2020).
- Food and Agricultural Organization (FAO). The Structure and Importance of the Commercial and Village Based Poultry Industry in Nigeria. 2006. Available online: http://www.fao.org/docs/eims/upload/214281/ReviewNigeria.pdf (accessed on 17 September 2020).
- Fagbamila, I.O.; Barco, L.; Mancin, M.; Kwaga, J.; Ngulukun, S.S.; Zavagnin, P.; Lettini, A.A.; Lorenzetto, M.; Abdu, P.A.; Kabir, J.; et al. Salmonella serovars and their distribution in Nigerian commercial chicken layer farms. PLoS ONE 2017, 12, e0173097. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.; Yin, Y.; Jones, M.B.; Zhang, Z.; Kaiser, B.L.D.; Dinsmore, B.A.; Fitzgerald, C.; Fields, P.I.; Deng, X. Salmonella serotype determination utilizing high-throughput genome sequencing data. J. Clin. Microbiol. 2015, 53, 1685–1692. [Google Scholar] [CrossRef] [Green Version]
- Ibrahim, G.M.; Morin, P.M. Salmonella serotyping using whole genome sequencing. Front. Microbiol. 2018, 9, 2993. [Google Scholar] [CrossRef] [Green Version]
- Herikstad, H.; Motarjemi, Y.; Tauxe, R.V. Salmonella surveillance: A global survey of public health serotyping. Epidemiol. Infect. 2002, 129, 1–8. [Google Scholar] [CrossRef]
- Orji, M.C.; Onuigbo, H.C.; Mbata, T.I. Serological survey of mycoplasmosis and pullorum disease in Plateau State of Nigeria. Int. J. Infect. Dis. 2005, 9, 86–89. [Google Scholar] [CrossRef] [Green Version]
- Crump, J.A.; Sjölund-Karlsson, M.; Gordon, M.A.; Parry, C.M. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella Infections. J. Clin. Microbiol. Rev. 2015, 28, 901–937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Glenn, L.M.; Lindsey, R.L.; Folster, J.P.; Pecic, G.; Boerlin, P.; Gilmour, M.W.; Harbottle, H.; Zhao, S.; McDermott, P.F.; Fedorka-Cray, P.J. Antimicrobial resistance genes in multidrug-resistant Salmonella enterica isolated from animals, retail meats, and humans in the United States and Canada. Microb. Drug Resist. 2013, 19, 175–184. [Google Scholar] [CrossRef] [Green Version]
- Agbaje, M.; Lettini, A.A.; Olufemi, O.E.; Longo, A.; Marafin, E.; Antonello, K.; Zavagnin, P.; Oluwasile, B.B.; Omoshaba, E.O.; Dipeolu, M.A. Antimicrobial Resistance Profiles of Salmonella serovars Isolated from Dressed Chicken Meat at Slaughter in Kaduna, Nigeria. Rev. Elev. Med. Vet. Pays Trop. 2019, 72. [Google Scholar] [CrossRef] [Green Version]
- European Food Safety Authority; European Centre for Disease Prevention and Control. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018. EFSA J. 2020, 18, e06007. [Google Scholar]
- Adesiji, Y.O.; Shivakumaraswamy, S.K.; Deekshit, V.K.; Kallappa, G.S.; Karunasagar, I. Molecular characterization of antimicrobial multi-drug resistance in non-typhoidal Salmonellae from chicken and clam in Mangalore, India. J. Biomed. Res. 2018, 32, 237–244. [Google Scholar]
- Al-Dawodi, R.; Farraj, M.A.; Essawi, T. Antimicrobial resistance in non-typhi Salmonella enterica isolated from humans and poultry in Palestine. J. Infect. Dev. Ctries. 2012, 6, 132–136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oluwasile, B.B.; Agbaje, M.; Ojo, O.E.; Dipeolu, M.A. Antibiotic usage pattern in selected poultry farms in Ogun State. Sokoto J. Vet. Sci. 2014, 12, 45–50. [Google Scholar] [CrossRef] [Green Version]
- Muhammad, M.; Muhammad, L.U.; Mani, A.U.; Ambali, A.G. A survey of chick mortality at hatching in three selected hatcheries in Jos, Central Nigeria. Int. J. Poult. Sci. 2009, 8, 656–659. [Google Scholar] [CrossRef]
- Fashae, K.; Ogunsola, F.; Aarestrup, F.M.; Henriken, R.S. Antimicrobial susceptibility and serovar of Salmonella from chickens and humans in Ibadan, Nigeria. J. Infect. Dev. Ctries. 2010, 4, 484–494. [Google Scholar] [CrossRef]
- Dias de Oliveira, S.; Siqueira-Flores, F.; Dos Santos, L.R.; Brandelli, A. Antimicrobial resistance in Salmonella Enteritidis strains isolated from broiler carcasses, food, human and poultry related samples. Int. J. Food Microbiol. 2005, 97, 297–305. [Google Scholar] [CrossRef] [PubMed]
- Adesiyun, A.; Webb, L.; Musai, L.; Louison, B.; Joseph, G.; Stewart-Johnson, A.; Samlal, S.; Rodrigo, S. Resistance to Antimicrobial Agents among Salmonella Isolates Recovered from Layer Farms and Eggs in the Caribbean Region. J. Food Prot. 2014, 77, 2153–2160. [Google Scholar] [CrossRef]
- Obi, C.N.; Igbokwe, A.J. Microbiological analyses of freshly laid and stored domestic poultry eggs in selected poultry farms in Umuahia, Abia State, Nigeria. Res. J. Biol. Sci. 2007, 2, 161–166. [Google Scholar] [CrossRef]
- Rouger, A.; Tresse, O.; Zagorec, M. Bacterial Contaminants of Poultry Meat: Sources, Species, and Dynamics. Microorganisms 2017, 5, 50. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, V.; Cardoso, M.J.; Magalhães, R.; Maia, R.; Neagu, C.; Dumitraşcu, L.; Teixeira, P. Occurrence of Salmonella spp. in eggs from backyard chicken flocks in Portugal and Romania—Results of a preliminary study. Food Control 2020, 113, 107180. [Google Scholar] [CrossRef]
- Jibril, A.H.; Okeke, I.N.; Dalsgaard, A.; Kudirkiene, E.; Akinlabi, O.C.; Bello, M.B.; Olsen, J.E. Prevalence and risk factors of Salmonella in commercial poultry farms in Nigeria. PLoS ONE 2020, 15, e0238190. [Google Scholar] [CrossRef] [PubMed]
- Ogunleye, A.O.; Steve, A.; Carlson, S.A. Emergence of an SGI1-bearing Salmonella enterica serotype Kentucky isolated from septic poultry in Nigeria. J. Infect. Dev. Ctries. 2012, 6, 483–488. [Google Scholar] [CrossRef] [Green Version]
- Useh, N.M.; Ngbede, E.O.; Akange, N.; Thomas, M.; Foley, A.; Keena, M.C.; Nelson, E.; Christopher-Hennings, J.; Tomita, M.; Suzuki, H.; et al. Draft genome sequence of 37 Salmonella enterica strains isolated from poultry sources in Nigeria. Genome Announc. 2016, 4, e00315-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Le Hello, S.; Hendriksen, R.S.; Doublet, B.; Fisher, I.; Nielsen, E.M.; Whichard, J.M.; Bouchrif, B.; Fashae, K.; Granier, S.A.; Silva, N.J.-D.; et al. International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J. Infect. Dis. 2011, 204, 675–684. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Le Hello, S.; Harrois, D.; Bouchrif, B.; Sontag, L.; Elhani, D.; Guibert, V.; Zerouali, K.; Weill, F.X. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: A microbiological study. Lancet Infect. Dis. 2013, 13, 672–679. [Google Scholar] [CrossRef] [Green Version]
- Freitas, N.O.C.; Penha, F.R.A.C.; Barrow, P.; Berchieri, J.A. Sources of human non-typhoid salmonellosis: A review. Braz. J. Poult. Sci. 2010, 12, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Gast, R.K. Serotype-Specific and Serotype-Independent Strategies for Pre-harvest Control of Food-Borne Salmonella in Poultry. Avian Dis. 2007, 51, 817–828. [Google Scholar] [CrossRef]
- Sasanya, J.J.; Okeng, J.W.; Ejobi, F.; Muganwa, M. Use of sulfonamides in layers in Kampala district, Uganda and sulphonamide residues in commercial eggs. Afr. Health Sci. 2005, 5, 33–39. [Google Scholar]
- Smith, W.P.; Agbaje, M.; LeRoux-Pullen, L.; van Dyk, D.; Debusho, K.L.; Shittu, A.; Sirdar, M.M.; Fasanmi, O.G.; Adebowale, O.; Fasina, O.F. Implication of the knowledge and perceptions of veterinary students of antimicrobial resistance for future prescription of antimicrobials in animal health, South Africa. J. S. Afr. Vet. Assoc. 2019. [Google Scholar] [CrossRef] [Green Version]
- Fasina, F.O.; LeRoux-Pullen, L.; Smith, P.; Debusho, L.K.; Shittu, A.; Jajere, S.M.; Adebowale, O.; Odetokun, I.; Agbaje, M.; Fasina, M.M.; et al. Knowledge, Attitudes, and Perceptions Associated With Antimicrobial Stewardship Among Veterinary Students: A Multi-Country Survey From Nigeria, South Africa, and Sudan. Front. Public Health 2020, 8, 517964. [Google Scholar] [CrossRef]
- Makaya, P.V.; Matope, G.; Pfukenyi, D.M. Distribution of Salmonella serovars and antimicrobial susceptibility of Salmonella Enteritidis from poultry in Zimbabwe. Avian Pathol. 2012, 41, 221–226. [Google Scholar] [CrossRef]
- Adesiyun, A.; Offiah, N.; Seepersadsingh, N.; Rodrigo, S.; Lashley, V.; Musai, L. Antimicrobial resistance of Salmonella spp. and Escherichia coli isolated from table eggs. Food Control 2007, 18, 306–311. [Google Scholar] [CrossRef]
- Adesiyun, A.; Webb, L.; Musai, L.; Louison, B.; Joseph, G.; Stewart-Johnson, A.; Samlal, S.; Rodrigo, S. Survey of Salmonella contamination in chicken layer farms in three Caribbean countries. J. Food Prot. 2014, 77, 1471–1480. [Google Scholar] [CrossRef] [PubMed]
- Chousalkar, K.; Gole, V.; Caraguel, C.; Rault, J.L. Chasing Salmonella Typhimurium in free-range egg production system. Vet. Microbiol. 2016, 192, 67–72. [Google Scholar] [CrossRef] [PubMed]
- Sodagari, H.R.; Habib, I.; Whiddon, S.; Wang, P.; Mohammed, A.B.; Robertson, I.; Goodchild, S. Occurrence and Characterization of Salmonella Isolated from Table Egg Layer Farming Environments in Western Australia and Insights into Biosecurity and Egg Handling Practices. Pathogens 2020, 9, 56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lapuz, R.R.; Umali, D.V.; Suzuki, T.; Shirota, K.; Katoh, H. Comparison of the prevalence of Salmonella infection in layer hens from commercial layer farms with high and low rodent densities. Avian Dis. 2012, 56, 29–34. [Google Scholar] [CrossRef]
- Wales, A.; Breslin, M.; Carter, B.; Sayers, R.; Davies, R. A longitudinal study of environmental Salmonella contamination in caged and free-range layer flocks. Avian Pathol. 2007, 36, 187–197. [Google Scholar] [CrossRef]
- Trampel, D.W.; Holder, T.G.; Gast, R.K. Integrated farm management to prevent Salmonella Enteritidis contamination of eggs. J. Appl. Poult. Res. 2014, 23, 353–365. [Google Scholar] [CrossRef]
- Namata, H.; Welby, S.; Aerts, M.; Faes, C.; Abrahantes, J.C.; Imberechts, H.; Vermeersch, K.; Hooyberghs, J.; Méroc, E.; Mintiens, K. Identification of risk factors for the prevalence and persistence of Salmonella in Belgian broiler chicken flocks. Prev. Vet. Med. 2009, 90, 211–222. [Google Scholar] [CrossRef] [Green Version]
- Carrique-Mas, J.J.; Breslin, M.; Sayers, A.R.; McLaren, I.; Arnold, M.; Davies, R. Comparison of environmental sampling methods for detecting Salmonella in commercial laying flocks in the UK. Lett. Appl. Microbiol. 2008, 47, 514–519. [Google Scholar] [CrossRef] [PubMed]
- Adebowale, O.O.; Adeyemo, O.K.; Awoyomi, O.; Dada, R.; Adebowale, O. Antibiotic use and practices in commercial poultry laying hens in Ogun State Nigeria. Rev. Elev. Med. Vet. Pays Trop. 2016, 69, 41–45. [Google Scholar] [CrossRef] [Green Version]
- Grimont, P.A.D.; Weill, F.X. Antigenic Formulae of the Salmonella Serovars, 9th ed.; World Health Organization Collaborating Center for Reference and Research on Salmonella; Institut Pasteur: Paris, France, 2007; pp. 1–166. [Google Scholar]
Zone | Sources of Isolates | Identified Serovars | ||||
---|---|---|---|---|---|---|
Market (%) | Farm (%) | Shell (%) | Contents (%) | Market (n) | Farm (n) | |
Egba (n = 25) | 5/10 (50) | 2/15 (13.3) | 7/25 (28) | 0 | Agama (3), Colorado (1), Lattenkamp (1) | Kingston (1), Kentucky (1) |
Yewa (n = 25) | 4/10 (40) | 0/15 (0) | 4/25 (16) | 0 | Durham (2), Bradford (1), Derby (1) | - |
Ijebu (n = 25) | 1/10 (10) | 1/15 (6.7) | 2/25 (8) | 0 | Kentucky (1) | Carno (1) |
Remo (n = 25) | 0/10 (0) | 1/15 (6.7) | 0 | 1/25 (4) | - | Alachua (1) |
Total | 10/40 (25) * | 4/60 (6.7) | 13/100 (13) * | 1/100 (1) |
Serotypes | No of Isolates Tested | No (%) of Resistant Isolates | No (%) of Resistant to Antimicrobials | Antmicr Type Resist (n) | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
AMP | CHL | CIP | FFN | GEN | KAN | NAL | STR | SMX | TET | TMP | ||||
Agama | 3 | 1 (33.30) | - | - | - | - | - | - | - | - | 1 | - | - | 1 |
Alachua | 1 | 1 (100) | - | - | 1 | - | - | - | - | - | - | - | - | 1 |
Bradford | 1 | 1 (100) | - | - | 1 | - | - | - | - | - | 1 | - | - | 2 |
Carno | 1 | 1 (100) | - | - | - | - | 1 | - | - | 1 | 1 | - | 1 | 4 |
Colorado | 1 | 0 (0) | - | - | - | - | - | - | - | - | - | - | - | |
Derby | 1 | 1 (100) | - | - | 1 | - | - | - | - | - | 1 | 1 | - | 3 |
Durham | 2 | 1 (50) | - | - | - | - | - | - | - | - | 1 | - | - | 1 |
Kentucky | 2 | 2 (100) | - | - | 2 | - | 1 | - | 2 | 1 | 1 | 1 | - | 6 |
Kingston | 1 | 1 (100) | - | - | - | - | - | - | - | - | 1 | 1 | - | 2 |
Lattenkamp | 1 | 1 (100) | - | - | - | - | - | - | - | - | 1 | - | - | 1 |
Total | 14 | 10 (71.4) * | 0 | 0 | 5 (50) | 0 | 2 (20) | 0 | 2 (20) | 2 (20) | 8 (80) | 3 (30) | 1 (10) |
Zones | No. (%) of Isolates | Salmonella Serovars (n) | Resistance Pattern |
---|---|---|---|
Egba | 7 (50) | Agama (2), Lattenkamp (1), Kingston (1) | SMX (4) |
Kentucky (1) | SMX-GEN-TET-STR-CIP-NAL (1) | ||
Yewa | 4 (28.6) | Durham (1) | SMX (1) |
Bradford (1) | SMX-CIP (1) | ||
Derby (1) | SMX-TET-CIP (1) | ||
Ijebu | 2 (14.3) | Kentucky (1) | CIP-NAL (1) |
Carno (1) | SMX-GEN-STR-TMP (1) | ||
Remo | 1 (7.1) | Alachua (1) | CIP (1) |
Items | Response | Frequency | Percentage | Χ2 (p-Value) |
---|---|---|---|---|
Husbandry system | Cage | 44 | 73.3 | 25.9 (<0.0001) |
Deep litter | 16 | 26.6 | ||
Presence of other farms <500 m away | Yes | 48 | 80.0 | 42.8 (<0.0001) |
No | 12 | 20.0 | ||
Presence of wild birds and rodents around the farm | Yes | 53 | 88.0 | 68.7 (<0.0001) |
No | 7 | 12.0 | ||
Sanitation | ||||
Wearing protective clothing | Yes | 13 | 21.6 | 38.3 (<0.0001) |
No | 47 | 78.3 | ||
Sharing of tools with other farms | Yes | 32 | 53.3 | 0.52 (0.47) |
No | 28 | 46.6 | ||
Cleaning of eggs before sale | Yes | 0 | 0.0 | 119.0 (<0.0001) |
No | 60 | 100.0 | ||
Inclusion of antibiotics in feed | Yes | 12 | 20.0 | 42.8 (<0.0001) |
No | 48 | 80.0 | ||
Traffic control | Farm premises | 41 | 68.3 | 16.0 (0.0001) |
Point of sale of eggs | Off-farm premises | 19 | 31.6 |
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Agbaje, M.; Ayo-Ajayi, P.; Kehinde, O.; Omoshaba, E.; Dipeolu, M.; Fasina, F.O. Salmonella Characterization in Poultry Eggs Sold in Farms and Markets in Relation to Handling and Biosecurity Practices in Ogun State, Nigeria. Antibiotics 2021, 10, 773. https://doi.org/10.3390/antibiotics10070773
Agbaje M, Ayo-Ajayi P, Kehinde O, Omoshaba E, Dipeolu M, Fasina FO. Salmonella Characterization in Poultry Eggs Sold in Farms and Markets in Relation to Handling and Biosecurity Practices in Ogun State, Nigeria. Antibiotics. 2021; 10(7):773. https://doi.org/10.3390/antibiotics10070773
Chicago/Turabian StyleAgbaje, Michael, Patience Ayo-Ajayi, Olugbenga Kehinde, Ezekiel Omoshaba, Morenike Dipeolu, and Folorunso O. Fasina. 2021. "Salmonella Characterization in Poultry Eggs Sold in Farms and Markets in Relation to Handling and Biosecurity Practices in Ogun State, Nigeria" Antibiotics 10, no. 7: 773. https://doi.org/10.3390/antibiotics10070773