Quantitative Exposure Assessment to Vibrio cholerae through Consumption of Fresh Fish in Lusaka Province of Zambia
Keywords:
Cholera, Cross-contamination, Exposure Assessment, Fresh Fish, Vibrio cholera, Zambia.
Abstract
Fresh fish is one of the widely consumed sources of proteins in Zambia. Consumption of contaminated fresh fish has been linked to zoonotic transmission of diseases in humans as fresh fish harbors several spoilage bacteria and pathogens including V. cholerae which cause cholera in humans. This study aimed to conduct a quantitative exposure assessment to Vibrio cholerae through consumption of fresh fish in Lusaka Province of Zambia. We used Swift Quantitative Microbial Risk Assessment (sQMRA) model to estimate the risk of exposure. We obtained data from reviews of scientific literature, government reports, questionnaire survey, and expert opinions. We categorized fish consumers using three risk pathways; restaurants, households with low socioeconomic status, and households with high socio-economic status. Results revealed that at a serving portion of 100g in households with low socioeconomic status, a concentration of 50 cfu/g, and infectious dose 50 (ID50) of 106 cells, one person out of 2,251,898 population at risk would get ill, representing a probability of 4.4x10-7. At a serving portion of 200g in households with high socioeconomic status, a concentration of 330 cfu/g, and ID50 of 106 cells, 13 people out of 2,251,898 would get ill, representing a probability of 5.7x10-6. At an average serving portion of 200g in restaurants, a concentration of 50 cfu/g, and ID50 of 106 cells, 47 people would get ill, translating to a probability density of 2.02 x 10-5. These results indicate that the risk of exposure to Vibrio cholerae through the consumption of fresh fish among the population at risk in Lusaka Province of Zambia is extremely low through all risk pathways. Cross-contamination during preparation and consumption is the main source of exposure to the Vibrio cholerae. Therefore, improvement in good food safety handling and processing would further minimize the occurrence of foodborne illnesses.References
1. Ali M, Nelson AR, Lopez AL, Sack D. Updated Global Burden of Cholera in Endemic Countries. PLoS Negl Trop Dis. 2015; 9(6): e0003832.
doi:10.1371/journal.pntd.0003832.
2. Banerjee R, Bhabatosh D, Balakrish N, Surajit B. Dynamics in genome evolution of Vibrio cholera, volume23; https://doi.org/10.1016/j.meegid.2014.01.006
3. Reidl J, Klose KE. Vibrio cholerae and cholera: out of the water and into the host. Rontgenring 11, 97070 Wurzburg, Germany. FEMS Microbiol. Rev. 2002; 26: 125-139.
4. WHO. World Health Organization. Cholera, Weekly Epidemol Rec. 2010; 86:325-340.
5. Olu O, Babaniyi O, Songolo P, Matapo B, Chizema E, Kapin’a-kanyanga M, Musenga E, Walker O. 2013. Cholera epidemiology in Zambia from 2000 to 2010: Implications for improving cholera prevention and control strategies in the country, Lusaka, Zambia. East African Medical J. 2013; 10: 324.
6. MOH. Ministry of Health. Situational Report No. 122 Outbreak Name: Cholera Investigation start date: 4th October 2017; Lusaka, Zambia. 2018; 1–8.
7. WHO. World Health Organization. Zambia Global Task Force on Cholera Control, Cholera Country Profile: Lusaka, Zambia. 2011; 1-2
8. Chiyangi H, Muma JB, Malama S, Manyahi J, Abade A, Kwenda G, Matee MI. Identification and antimicrobial resistance patterns of bacterial enteropathogens from children aged 0–59 months at the University Teaching Hospital, Lusaka, Zambia: A prospective cross-sectional study 1–9.2017;
https://doi.org/10.1186/s12879-017-2232-0
9. Kobayashi T, Mudenda HB, Yamamoto H. The Survival of Vibrio cholerae in the Natural Environment of Zambia: Fish, the suspicious Gateway of Cholera Outbreak? Lusaka, Zambia. J. Int. Heal. 2010; 25: 33–39.
10. Pal J, Shukla BN, Kumar AM, Verma OH, Pandey G, Amitha. A review on the role of fish in human nutrition with special emphasis on essential fatty acid, College of Fisheries NDUA & T Kumarganj Faizabad Uttar Pradesh, India. Int. J. Fisheries and Aquatic Stud. 2018; 6(2): 427-430
11. Senderovich Y, Izhaki I, Halpern M. Fish as Reservoirs and Vectors of Vibrio cholerae; Columbia University, United States of America. PLoS ONE. 2010; 5(1) 8607 5. https://doi.org/10.1371/journal.pone.0008607
12. Mizanda C. Investigation and Antimicrobial Susceptibility of Vibrio species isolated from the Tilapia Fish Marketed in Lusaka District, Zambia. 2019. The University of Zambia Thesis.
13. Acosta C, Galindo C, Kimario J, Senkoro K, Urassa H. Cholera outbreak in southern Tanzania: Risk factors and patterns of transmission. Emerg. Infect. Dis. 2001; 75: 83-587.
14. Forssmain B, Mannes T, Musto J, Baumann B, Frei U, Gottlieb T, Robertson G, Natoli JD, Shadbolt C, Biffin B, Gupta L. Vibrio cholera O1 E1 Tor cluster in Sydney linked to imported whitebait, New South Wales. Med. J. Aust. 2007; 187 (6): 345-347.doi:10.5694/j.1326-5377.2007.tb01278.x
15. Gama A, Kabwe P, Nanzaluka F, Langa N, Mutale LS, Mwanamoonga L, Moonga G, Chongwe G, Sinyange N. Cholera Outbreak in Chienge and Nchelenge Fishing Camps, Zambia, 2017. Health Press Zambia Bull. 2017; 2 (1): 12-19.
16. Murebwa-Chirambo R, Mwanza R, Mwinuna C, Mazaba ML, Mweene-Ndumba IMJ. Occurrence of cholera in Lukanga fishing camp, Kapiri-Mposhi district, Zambia. Health Press Zambia Bull. 2017;1(1).
17. Genschick S. Fish consumption in urban Lusaka: The need for aquaculture to improve targeting of the poor, Lusaka, Zambia. Aquac. 2018; 492: 280–289. https://doi.org/https://doi.org/10.1016/j.aquaculture.2018.03.052
18. FAO. Food and Agriculture Organization. Fishery country profile report: The republic of Zambia, general economic data, Lusaka, Zambia, FID/CP/ZAM. 2006; 1-10.
19. Evers EG, Chardon JE. A swift Quantitative Microbiological Risk Assessment (sQMRA) tool; BA Bilthoven, The Netherlands. J. Food Control. 2010; 21(3): 319-330.
20. CSO. Central Statistical Office living conditions monitoring survey. Retrieved from http://www.zamstats.gov.zm/report/Lcms/2006-2010. LCMS Report Final
21. CSO. Central Statistical Office. The 2015 Living conditions monitoring survey report, Lusaka, Zambia: CSO. 2016.
22. Dalusi L, Thomas J, Lugomela C, Ken MM, Sjoling. Toxigenic Vibrio cholerae identified in estuaries of Tanzania using PCR techniques, Dar es Salaam, Tanzania. 2015. doi: 10.1093/femsle/fnv009
23. Bronze MS, Greenfield RA. Biodefense Principles and Pathogens horizon bioscience. Norfolk England; FEMS Immunology & Medical Microbiology. 2005; 45(2): 351–352, DOI: 10.1016/j.femsim. 2005.06.002.
24. WHO. World Health Organization. Global task force on cholera control; assessing the outbreak response and improving preparedness. Geneva: World Health Organization. 2004
25. Cash RA, Music SI, Libonati JP, Craig JP, Pierce NF, Hornick RB. Response of man to infection with Vibrio cholerae. II. Protection from illness afforded by previous disease and vaccine. J. Infect. Dis. 1974; 130: 325–333.
26. Novotny L, Dvorska L, Lorencova A, Beran V, Pavlik I. Fish: a potential source of bacterial pathogens for human beings, Brno, Czech Republic; Vet Med Czech. 2004; 49: 343-358.
27. Butler SM, Nelson EJ, Chowdhury N, Faruque SM, Stephen B, Calderwood AC. Cholera stool bacteria repress chemotaxis to increase infectivity; Boston, MA 02111, USA. Mol. Microbiol. 2006. https://doi.org/10.1111/j.1365-2958.2006.05096
28. Hornick RB, Music SI, Wenzel R, Cash RA, Libonati JP, Snyder MJ, Woodward T. The Broad Street Pump Revisited: Response of Volunteers to Ingested Cholera Vibrios. Bull. New York Acad. Med. 1971; 47(10): 1181-1191.
29. CSO. Central Statistical Office. Zambia in Figures-2018, Lusaka. 2018
30. WHO. World Health Organization. Prevention and control of cholera outbreaks: WHO Policy and Recommendations. 2019
31. CSO. Central Statistical Office Labour force Survey –Republic of Zambia. 2015.
32. Torres-vitela MAR, Castillo A, Finne G, Rodriguez-Garcia MAO, Martinez-Gonzales N E, Navarro-Hidalgol V. Incidence of Vibrio cholerae in Fresh Fish and Ceviche in Guadalajara, Mexico. 1997; 60: 237–241.
33. Hossain ZZ, Farhana I, Tulsiani SM, Begum A. Transmission and Toxigenic Potential of Vibrio cholerae in Hilsha Fish (Tenualosa ilisha) for Human Consumption in Bangladesh. Front. Microbiol. 2018; 9: 222,1–13.
https://doi.org/10.3389/fmicb.2018.00222
34. Traoré SG, Bonfoh B, Krabi R, Odermatt P, Utzinger J. Europe PMC Funders Group Risk of Vibrio Transmission Linked to the Consumption of Crustacean in Coastal Towns of Côte d’ Ivoire. 2016; 75: 1004–1011.
https://doi.org/10.4315/0362-028X.JFP-11-472.
35. Sperling L, Alter T, Huehn S. Prevalence and Antimicrobial Resistance of Vibrio spp. in Retail and Farm Shrimps in Ecuador. J. Food. Prot. 2015.
https://doi.org/10.4315/0362-028X.JFP-15-160.
36. Sudha S, Mridula C, Silvester R, Mohamed HA. Prevalence and antibiotic resistance of pathogenic Vibrios in shellfishes from Cochin market, Cochin 682 016, Kerala, India. Indian J. Geo-Marine Scie. 2014; 43(5): 815-824.
37. Vu TTT, Alter A, Huehn S. Prevalence of Vibrio spp. in Retail Seafood in Berlin, Germany. J. Food Prot. 2018; 81 (7): 1079-1086
38. Oumar T, Martikainen O, Anja S, Nicolas B, Kaisa H. Occurrence of Vibrio cholerae in fish and water from a reservoir and a neighboring channel in Ouagadougou, Burkina Faso. J. Infect. Dev. Countries. 2014; 8(10): 1334- 1338.
https://doi.org/10.3855/jidc.3946
39. Chitov T. Occurrence of potentially pathogenic Vibrio species in raw, processed, and ready-to-eat seafood and seafood products. 2009.
https://doi.org/oai:doaj.org/article:d22a 41b861646c3939b155dc337c7ab
40. Hossain ZZ, Farhana I, Tulsiani SM, Sultana R, Jensen PM, Begum A. Investigation of Household Transmission of Vibrio cholerae in Bangladesh. Poster session presented at American Society for Microbiology, Bostom, United States. 2016.
41. Lee HK, Abdul Halim H, Thong Kwai L, Chai LC. Assessment of Food Safety Knowledge, Attitude, Self-Reported Practices, and Microbiological Hand Hygiene of Food Handlers. Kuala Lumpur, Malaysia Int. J. Env. Res. Pub. Health. 2017; 14 (1): 55.
https://doi.org/10.3390/ijerph14010055
42. Tunung R, Margaret SP, Jeyaletchumi P, Chai LC, Zainazor TCT, Ghazali, FM. Prevalence and quantification of Vibrio in raw salad vegetables at retail level Prevalence and Quantification of Vibrio parahaemolyticus in Raw Salad Vegetables at Retail Level. J. Microbiol. Biotechnol. 2010; 20(2): 391-396.
https://doi.org/10.4014/jmb.0908.08009
43. Oliver JD, Kaper JB. Vibrio species. In Food Microbiology: fundamentals and frontiers (M.P. Doyle, ed.), 2nd Ed. ASM Press, Washington, DC, 263-300 2nd ED.ASM. 2001.
44. Manyori CI, Mumba C, Muma JB, Mwale MM, Munyeme M, Bwanga EK, Häsler B, Rich KM, Skjerve E. Quantitative risk assessment of developing salmonellosis through consumption of beef in Lusaka Province, Zambia. Food Control. 2017. doi:10.1016/j.foodcont.2016.10.027
45. Wachsmuth IK, Blake PA, Olsvik Ø. Vibrio cholerae and Cholera: Molecular to Global Perspectives. Washington D.C: ASM Press. 1994; 345–356.
46. Makukutu CA, Guthrie RK. The behavior of Vibrio cholerae in Hot Foods; Houston, Texas, USA. Am. Soc. Microbiol. 1996; 52: 824–831.
47. WHO. World Health Organization. Cholera –Zimbabwe: Emergencies preparedness response, Disease outbreak news: Update, 5 October 2018.
48. Wahed T. Knowledge of, attitudes toward, and preventive practices relating to cholera and oral cholera vaccine among urban high-risk groups: findings of a cross-sectional study in Dhaka, Bangladesh. BMC Public Heal. 2013; 13:242.
https://doi.org/doi: 10.1186/1471-2458-13-242
49. Schürmann D, Ebert N, Kampf D, Baumann B, Frei U, Suttorp N. Domestic Cholera in Germany Associated with Fresh Fish Imported from Nigeria. Eur. J. Clin. Microbiol. Infect. Dis. 2002; 21: 827–828. https://doi.org/10.1007/s10096-002-0832-z
50. WHO. World Health Organization. Microbiological aspects of the food hygiene; Report of a WHO Expert Committee with the participation of FAO, Geneva, Technical report series No. 598. 1976.
51. Sumner J. Food Safety Risks Associated with Prawns Consumed in Australia, Seafood CRC Project: 2009/787. 2011
52. PAOH. Pan American Health Organization. Veterinary Public Health Program, Risk of transmission of Cholera by food: Washington, DC, USA. 1991.
doi:10.1371/journal.pntd.0003832.
2. Banerjee R, Bhabatosh D, Balakrish N, Surajit B. Dynamics in genome evolution of Vibrio cholera, volume23; https://doi.org/10.1016/j.meegid.2014.01.006
3. Reidl J, Klose KE. Vibrio cholerae and cholera: out of the water and into the host. Rontgenring 11, 97070 Wurzburg, Germany. FEMS Microbiol. Rev. 2002; 26: 125-139.
4. WHO. World Health Organization. Cholera, Weekly Epidemol Rec. 2010; 86:325-340.
5. Olu O, Babaniyi O, Songolo P, Matapo B, Chizema E, Kapin’a-kanyanga M, Musenga E, Walker O. 2013. Cholera epidemiology in Zambia from 2000 to 2010: Implications for improving cholera prevention and control strategies in the country, Lusaka, Zambia. East African Medical J. 2013; 10: 324.
6. MOH. Ministry of Health. Situational Report No. 122 Outbreak Name: Cholera Investigation start date: 4th October 2017; Lusaka, Zambia. 2018; 1–8.
7. WHO. World Health Organization. Zambia Global Task Force on Cholera Control, Cholera Country Profile: Lusaka, Zambia. 2011; 1-2
8. Chiyangi H, Muma JB, Malama S, Manyahi J, Abade A, Kwenda G, Matee MI. Identification and antimicrobial resistance patterns of bacterial enteropathogens from children aged 0–59 months at the University Teaching Hospital, Lusaka, Zambia: A prospective cross-sectional study 1–9.2017;
https://doi.org/10.1186/s12879-017-2232-0
9. Kobayashi T, Mudenda HB, Yamamoto H. The Survival of Vibrio cholerae in the Natural Environment of Zambia: Fish, the suspicious Gateway of Cholera Outbreak? Lusaka, Zambia. J. Int. Heal. 2010; 25: 33–39.
10. Pal J, Shukla BN, Kumar AM, Verma OH, Pandey G, Amitha. A review on the role of fish in human nutrition with special emphasis on essential fatty acid, College of Fisheries NDUA & T Kumarganj Faizabad Uttar Pradesh, India. Int. J. Fisheries and Aquatic Stud. 2018; 6(2): 427-430
11. Senderovich Y, Izhaki I, Halpern M. Fish as Reservoirs and Vectors of Vibrio cholerae; Columbia University, United States of America. PLoS ONE. 2010; 5(1) 8607 5. https://doi.org/10.1371/journal.pone.0008607
12. Mizanda C. Investigation and Antimicrobial Susceptibility of Vibrio species isolated from the Tilapia Fish Marketed in Lusaka District, Zambia. 2019. The University of Zambia Thesis.
13. Acosta C, Galindo C, Kimario J, Senkoro K, Urassa H. Cholera outbreak in southern Tanzania: Risk factors and patterns of transmission. Emerg. Infect. Dis. 2001; 75: 83-587.
14. Forssmain B, Mannes T, Musto J, Baumann B, Frei U, Gottlieb T, Robertson G, Natoli JD, Shadbolt C, Biffin B, Gupta L. Vibrio cholera O1 E1 Tor cluster in Sydney linked to imported whitebait, New South Wales. Med. J. Aust. 2007; 187 (6): 345-347.doi:10.5694/j.1326-5377.2007.tb01278.x
15. Gama A, Kabwe P, Nanzaluka F, Langa N, Mutale LS, Mwanamoonga L, Moonga G, Chongwe G, Sinyange N. Cholera Outbreak in Chienge and Nchelenge Fishing Camps, Zambia, 2017. Health Press Zambia Bull. 2017; 2 (1): 12-19.
16. Murebwa-Chirambo R, Mwanza R, Mwinuna C, Mazaba ML, Mweene-Ndumba IMJ. Occurrence of cholera in Lukanga fishing camp, Kapiri-Mposhi district, Zambia. Health Press Zambia Bull. 2017;1(1).
17. Genschick S. Fish consumption in urban Lusaka: The need for aquaculture to improve targeting of the poor, Lusaka, Zambia. Aquac. 2018; 492: 280–289. https://doi.org/https://doi.org/10.1016/j.aquaculture.2018.03.052
18. FAO. Food and Agriculture Organization. Fishery country profile report: The republic of Zambia, general economic data, Lusaka, Zambia, FID/CP/ZAM. 2006; 1-10.
19. Evers EG, Chardon JE. A swift Quantitative Microbiological Risk Assessment (sQMRA) tool; BA Bilthoven, The Netherlands. J. Food Control. 2010; 21(3): 319-330.
20. CSO. Central Statistical Office living conditions monitoring survey. Retrieved from http://www.zamstats.gov.zm/report/Lcms/2006-2010. LCMS Report Final
21. CSO. Central Statistical Office. The 2015 Living conditions monitoring survey report, Lusaka, Zambia: CSO. 2016.
22. Dalusi L, Thomas J, Lugomela C, Ken MM, Sjoling. Toxigenic Vibrio cholerae identified in estuaries of Tanzania using PCR techniques, Dar es Salaam, Tanzania. 2015. doi: 10.1093/femsle/fnv009
23. Bronze MS, Greenfield RA. Biodefense Principles and Pathogens horizon bioscience. Norfolk England; FEMS Immunology & Medical Microbiology. 2005; 45(2): 351–352, DOI: 10.1016/j.femsim. 2005.06.002.
24. WHO. World Health Organization. Global task force on cholera control; assessing the outbreak response and improving preparedness. Geneva: World Health Organization. 2004
25. Cash RA, Music SI, Libonati JP, Craig JP, Pierce NF, Hornick RB. Response of man to infection with Vibrio cholerae. II. Protection from illness afforded by previous disease and vaccine. J. Infect. Dis. 1974; 130: 325–333.
26. Novotny L, Dvorska L, Lorencova A, Beran V, Pavlik I. Fish: a potential source of bacterial pathogens for human beings, Brno, Czech Republic; Vet Med Czech. 2004; 49: 343-358.
27. Butler SM, Nelson EJ, Chowdhury N, Faruque SM, Stephen B, Calderwood AC. Cholera stool bacteria repress chemotaxis to increase infectivity; Boston, MA 02111, USA. Mol. Microbiol. 2006. https://doi.org/10.1111/j.1365-2958.2006.05096
28. Hornick RB, Music SI, Wenzel R, Cash RA, Libonati JP, Snyder MJ, Woodward T. The Broad Street Pump Revisited: Response of Volunteers to Ingested Cholera Vibrios. Bull. New York Acad. Med. 1971; 47(10): 1181-1191.
29. CSO. Central Statistical Office. Zambia in Figures-2018, Lusaka. 2018
30. WHO. World Health Organization. Prevention and control of cholera outbreaks: WHO Policy and Recommendations. 2019
31. CSO. Central Statistical Office Labour force Survey –Republic of Zambia. 2015.
32. Torres-vitela MAR, Castillo A, Finne G, Rodriguez-Garcia MAO, Martinez-Gonzales N E, Navarro-Hidalgol V. Incidence of Vibrio cholerae in Fresh Fish and Ceviche in Guadalajara, Mexico. 1997; 60: 237–241.
33. Hossain ZZ, Farhana I, Tulsiani SM, Begum A. Transmission and Toxigenic Potential of Vibrio cholerae in Hilsha Fish (Tenualosa ilisha) for Human Consumption in Bangladesh. Front. Microbiol. 2018; 9: 222,1–13.
https://doi.org/10.3389/fmicb.2018.00222
34. Traoré SG, Bonfoh B, Krabi R, Odermatt P, Utzinger J. Europe PMC Funders Group Risk of Vibrio Transmission Linked to the Consumption of Crustacean in Coastal Towns of Côte d’ Ivoire. 2016; 75: 1004–1011.
https://doi.org/10.4315/0362-028X.JFP-11-472.
35. Sperling L, Alter T, Huehn S. Prevalence and Antimicrobial Resistance of Vibrio spp. in Retail and Farm Shrimps in Ecuador. J. Food. Prot. 2015.
https://doi.org/10.4315/0362-028X.JFP-15-160.
36. Sudha S, Mridula C, Silvester R, Mohamed HA. Prevalence and antibiotic resistance of pathogenic Vibrios in shellfishes from Cochin market, Cochin 682 016, Kerala, India. Indian J. Geo-Marine Scie. 2014; 43(5): 815-824.
37. Vu TTT, Alter A, Huehn S. Prevalence of Vibrio spp. in Retail Seafood in Berlin, Germany. J. Food Prot. 2018; 81 (7): 1079-1086
38. Oumar T, Martikainen O, Anja S, Nicolas B, Kaisa H. Occurrence of Vibrio cholerae in fish and water from a reservoir and a neighboring channel in Ouagadougou, Burkina Faso. J. Infect. Dev. Countries. 2014; 8(10): 1334- 1338.
https://doi.org/10.3855/jidc.3946
39. Chitov T. Occurrence of potentially pathogenic Vibrio species in raw, processed, and ready-to-eat seafood and seafood products. 2009.
https://doi.org/oai:doaj.org/article:d22a 41b861646c3939b155dc337c7ab
40. Hossain ZZ, Farhana I, Tulsiani SM, Sultana R, Jensen PM, Begum A. Investigation of Household Transmission of Vibrio cholerae in Bangladesh. Poster session presented at American Society for Microbiology, Bostom, United States. 2016.
41. Lee HK, Abdul Halim H, Thong Kwai L, Chai LC. Assessment of Food Safety Knowledge, Attitude, Self-Reported Practices, and Microbiological Hand Hygiene of Food Handlers. Kuala Lumpur, Malaysia Int. J. Env. Res. Pub. Health. 2017; 14 (1): 55.
https://doi.org/10.3390/ijerph14010055
42. Tunung R, Margaret SP, Jeyaletchumi P, Chai LC, Zainazor TCT, Ghazali, FM. Prevalence and quantification of Vibrio in raw salad vegetables at retail level Prevalence and Quantification of Vibrio parahaemolyticus in Raw Salad Vegetables at Retail Level. J. Microbiol. Biotechnol. 2010; 20(2): 391-396.
https://doi.org/10.4014/jmb.0908.08009
43. Oliver JD, Kaper JB. Vibrio species. In Food Microbiology: fundamentals and frontiers (M.P. Doyle, ed.), 2nd Ed. ASM Press, Washington, DC, 263-300 2nd ED.ASM. 2001.
44. Manyori CI, Mumba C, Muma JB, Mwale MM, Munyeme M, Bwanga EK, Häsler B, Rich KM, Skjerve E. Quantitative risk assessment of developing salmonellosis through consumption of beef in Lusaka Province, Zambia. Food Control. 2017. doi:10.1016/j.foodcont.2016.10.027
45. Wachsmuth IK, Blake PA, Olsvik Ø. Vibrio cholerae and Cholera: Molecular to Global Perspectives. Washington D.C: ASM Press. 1994; 345–356.
46. Makukutu CA, Guthrie RK. The behavior of Vibrio cholerae in Hot Foods; Houston, Texas, USA. Am. Soc. Microbiol. 1996; 52: 824–831.
47. WHO. World Health Organization. Cholera –Zimbabwe: Emergencies preparedness response, Disease outbreak news: Update, 5 October 2018.
48. Wahed T. Knowledge of, attitudes toward, and preventive practices relating to cholera and oral cholera vaccine among urban high-risk groups: findings of a cross-sectional study in Dhaka, Bangladesh. BMC Public Heal. 2013; 13:242.
https://doi.org/doi: 10.1186/1471-2458-13-242
49. Schürmann D, Ebert N, Kampf D, Baumann B, Frei U, Suttorp N. Domestic Cholera in Germany Associated with Fresh Fish Imported from Nigeria. Eur. J. Clin. Microbiol. Infect. Dis. 2002; 21: 827–828. https://doi.org/10.1007/s10096-002-0832-z
50. WHO. World Health Organization. Microbiological aspects of the food hygiene; Report of a WHO Expert Committee with the participation of FAO, Geneva, Technical report series No. 598. 1976.
51. Sumner J. Food Safety Risks Associated with Prawns Consumed in Australia, Seafood CRC Project: 2009/787. 2011
52. PAOH. Pan American Health Organization. Veterinary Public Health Program, Risk of transmission of Cholera by food: Washington, DC, USA. 1991.
Published
2021-12-16
How to Cite
1.
Malata M, Muma J, Siamate J, Bumbangi F, Hang’ombe B, Mumba C. Quantitative Exposure Assessment to Vibrio cholerae through Consumption of Fresh Fish in Lusaka Province of Zambia. Journal of Agricultural and Biomedical Sciences [Internet]. 16Dec.2021 [cited 22Dec.2024];5(2). Available from: https://journals.unza.zm/index.php/JABS/article/view/667
Section
Veterinary Medicine
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