FLIES AS POTENTIAL CARRIERS FOR DISEASE IN PORK BUTCHERIES IN KAMPALA
DVM Martin Heilmann - Graduate fellow ILRI & PhD student at the Institute of Parasitology and Tropical Veterinary Medicine of Freie Universität Berlin
ILRI Nairobi seminar – 26 November 2014

Overview
Project description
Background
Objectives
Material and methods
Baseline
Intervention
Microbiological sampling
Results
Outlook
Discussion
Conclusion
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3
Project description
Background
Objectives
Material and methods
Baseline
Intervention
Microbiological sampling
Results
Outlook
Discussion
Conclusion

Background I – pigs and pork
The number of pigs in Uganda has increased rapidly [1]
Uganda has the highest per capita consumption of pork in East Africa
70% of pork is consumed in urban areas [2]
Road-side butcheries (known as pork joints) are very common
4
0
500
1000
1500
2000
2500
3000
1961
1963
1965
1967
1969
1971
1973
1975
1977
1979
1981
1983
1985
1987
1989
1991
1993
1995
1997
1999
2001
2003
2005
2007
2009
2011
2013
Pig numbers in thousands
Pigs in Uganda (FAOSTAT)

Background II – diarrhoea
5
Higher risk in low-income areas with poor sanitary conditions
Second most common cause of deaths in children under five [4]
Foodborne diseases a health concern worldwide [3]
Salmonellosis is one of the most common and globally distributed [5]
Disability-adjusted life year for diarrhea
per 100,000 inhabitants in 2004

Background III – flies
6
Synantrophic flies feed on human foodstuffs and waste
Potential to transmit pathogens causing diarrhoea and dysentery [6]

Natete zone, Kampala

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Project objectives
I.Flies' role as carrier for disease in pork joints
II.Butchers' and consumers' perception of flies
III.Prevalence of Salmonella ssp. in pork joints
IV.Impact of insecticide-treated nets on the number of flies in pork joints
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Project description
Background
Objectives
Material and methods
Baseline
Intervention
Microbiological sampling
Results
Outlook
Discussion
Conclusion

Material and methods - baseline
14
Random selection of 60 pork joints from geo-referenced survey conducted by J. Kungu in 2014 [7]
Interviews with 1 butcher and 4 customers
from each joint
Structured questionnaires
Socioeconomics
Market-related characteristics
Attitudes in preparing pork
and relishes (butchers)
Purchase and consumption
habits (customers)
Choice card example from butcher‘s questionnaire [8]

Material and methods - intervention
15
18 pork joints from baseline were netted
5 non-netted as controls
Net installation on wall or as window frame
Material: ZeroFly®, 270 mg Deltamethrin/m2
Monitoring for 3 months
Glue traps hung once per week for 48 consecutive hours
Phenotypic fly identification
Sample of nets collected monthly to test efficacy

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17

Material and methods – sampling
Sampling of Salmonella ssp. as indicator pathogen
Based on previous studies on food and animals in Kampala [5;11;12]
Sampling (ISO 6579:2002)
Raw and processed pork
Water
Fresh vegetables
Hands’ surface
Equipment
Flies’ midguts
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19
Project description
Background
Objectives
Material and methods
Baseline
Intervention
Microbiological sampling
Results
Outlook
Discussion
Conclusion

Results – baseline
20 Raw pork 53% Fried 30% Roasted 15%
Cooked 2%
Pork sold as
*
Sampled butchers' demographics:
Male-dominated (93%)
50% greater than middle school education
12% owners, 20% managers,
68% workers
87% cooked pork is
served with raw relishes
Flies present in 80% of butcheries
Other pest animals in 50%

Results – baseline retailers
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Attribute
Most total
Least
total
BW score
Standardized
BW score (mean)
Standard deviation
SQRT
(B/W)
Standardized ratio scale
Meat from the same day
175
7
168
0.700
1.139
5.00
100.00
Cleanliness of the butchery
153
7
146
0.608
0.769
4.68
93.50
Trust in the butcher
154
14
140
0.583
0.871
3.32
66.33
Color of the meat
128
51
77
0.321
0.929
1.58
31.68
The butcher is wearing a coat
63
20
43
0.179
0.928
1.77
35.50
Butchery close to main road
36
26
10
0.042
0.764
1.18
23.53
Price
12
30
-18
-0.075
0.514
0.63
12.65
Type of building structure
19
44
-25
-0.104
0.567
0.66
13.14
Bony meat
10
76
-66
-0.275
0.418
0.36
7.25
Presence of flies in the butchery
15
127
-112
-0.467
0.628
0.34
6.87
Fat layer of the meat
2
120
-118
-0.492
0.181
0.13
2.58
Pest animals in/around the butchery
5
127
-122
-0.508
0.279
0.20
3.97
Age of the animal
8
131
-123
-0.513
0.468
0.25
4.94
Importance of attributes within the best-worst scaling

-0.6
-0.4
-0.2
-1E-15
0.2
0.4
0.6
0.8
Average B-W score

Results – intervention
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0
5
10
15
20
25
30
35
40
45
50
13-Aug
20-Aug
27-Aug
03-Sep
10-Sep
17-Sep
24-Sep
01-Oct
08-Oct
15-Oct
22-Oct
29-Oct
05-Nov
12-Nov
19-Nov
Fly numbers
Fly monitoring
Control
Intervention
Linear (Control)
Linear (Intervention) 84% Trapped flies during Intervention (n=9532)
Musca
Chrysomya
OthersNetting installation

Results – microbiological sampling
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Pathogens on and in flies found in pretests:
E. coli
S. aureus
S. enteritidis
Klebsiella sp.
S. dysgalactiae
Coliforms
B. cereus
Proteus sp.

Results – Salmonella enteritidis
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Sample
Number
Positive
Prevalence
Raw pork
77
25
31%
Flies
55
16
29%
Tomatoes
77
6
8%
Cabbage
77
4
5%
Onions
77
2
3%
Roasted pork
77
1*
1%
Hands surface
77
0
0%
Equipment
77
0
0%
Water
15
0
0%
* S. gallinarum

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Project description
Background
Objectives
Material and methods
Baseline
Intervention
Microbiological sampling
Results
Outlook
Discussion
Conclusion

Outlook
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Sharing feedback with butchers
WTP with butchers from baseline
Post-sampling in netted butcheries
Molecularbiological analysis and antimicrobial resistance of Salmonella samples
Testing net efficacy
Sampling for environmental contamination
Further analysis, interpretation and writing

Discussion
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1.Most butchers are aware of flies in their pork joints and try to reduce them with limited success
2.Efficacy of insecticid treated nets depends strongly on local conditions and implementation
Butchers' and customers' acceptance for the net varies strongly
Proper use of insecticides requires users to know certain key facts in order to avoid resistances and environmental and health risks
3.Half of butchers obtain their pork from backyards or non-gazetted abattoirs
4.“We’re Africans – we don’t die of flies”

Some conclusions
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Salmonella is highly prevalent in flies and raw pork
Insecticide treated nets can reduce flies, but further research about (practicability of) implementation is necessary
Research disciplines combined like epidemiology, microbiology and economics to study the mechanisms under which pork in pork butcheries is produced, marketed and consumed could improve the understanding of how the growing pork joint industry impacts public health
Butchers are willing to learn and to invest in their business but there is still a major lack of awareness and understanding about food safety risks and public health

References
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(1)Uganda Bureau of Statistics 2009 & FAO 2014
(2)Roesel, K., Grace, D., Dione, M. M., Ouma, E. A., Pezo, D., Kungu, J., Ejobi, F., Clausen, P. H., 2013. Assessment of knowledge, attitudes and practices on pork safety among smallholder pig farmers in Uganda. Poster prepared for the First African Regional Conference of the International Association on Ecology and Health (Africa 2013 Ecohealth), Grand-Bassam, Côte d'Ivoire, 1-5 October 2013. Nairobi, Kenya: ILRI.
(3)Lukinmaa, S., Nakari, U. M., Eklund, M., Siitonen, A., 2004. Application of molecular genetic methods in diagnostics and epidemiology of food- borne bacterial pathogens. Acta Pathologica, Microbiologica et Immunologica Scandinavica, 112(11-12), 908-929.
(4)Liu, L., Johnson, H. L., Cousens, S., Perin, J., Scott, S., Lawn, J. E., Rudan, I., Campbell, H., Cibulskis, R., Li, M., Mathers, C., Black, R. E., 2012. Child Health Epidemiology Reference Group of WHO and UNICEF. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. The Lancet, 379(9832), 2151-2161.
(5)Bosco, K. J., Kaddu-Mulindwa, D. H. and Asiimwe, B. B., 2012. Antimicrobial Drug Resistance and Plasmid Profiles of Salmonella Isolates from Humans and Foods of Animal Origin in Uganda. Advances in Infectious Diseases, 2, 151-155.
(6)Förster, M., Klimpel, S., Mehlhorn, H., Sievert, K., Messler, S., Pfeffer, K., 2007. Pilot study of synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitology Research, 101, 243-246.
(7)Kungu, J. M., Dione, M. M., Ejobi, F., Ocaido, M., Roesel, K., Grace, D., 2014. Causal factors for taeniasis and Taenia solium cysticercosis associated with pork handling and consumption: a case study of Kampala district, Uganda. (submitted)
(8)Heilmann, M., Mtimet, N., Roesel, K., Grace, D., 2014 Assessing Ugandan pork butchers’ practices and their perception of customers’ preferences: A best-worst approach. (submitted)
(9)Molbak, K., 2005. Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clinical Infectious Diseases, 41(11), 1613-1620.
(10)Mian, L. S., Maag, H., Tacal, J. V., 2002. Isolation of Salmonella from muscoid flies at commercial animal establishments in San Bernardino County, California. Journal of Vector Ecology, 27(1), 82-85.
(11)Mugampoza, D., Byarugaba, G. W. B., Nyonyintono, A. and Nakitto, P., 2014. Occurrence of Escherichia coli and Salmonella spp. in street- vended foods and general hygienic and trading practices in Nakawa Division, Uganda
(12)G. W. Nasinyama, G. W., McEwen, S. A., Waltner-Toews, D., Gyles, C. L., Wilson, J., OpudaAsibo, J. and Poppe, C., 1998“Pre- valence, Characterisitics and Distribution of Non-Ty- phoidal Salmonella in Diarrhoea Patients and Slaughter Animals in Kampala District, Uganda,” Proceedings of the 4th World Congress Foodborne Infections and In- toxications, Berlin, 7-12 June 1998, pp. 433-444.