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

2

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

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0

500

1000

1500

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3000

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61

196

3

196

5

196

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196

9

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9

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200

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1

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3

Pig

num

bers

in thousa

nds

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

10

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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13

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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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 21

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 23

05

101520253035404550

13

-Aug

20-A

ug

27-A

ug

03-S

ep

10-S

ep

17-S

ep

24-S

ep

01

-Oct

08-O

ct

15-O

ct

22-O

ct

29-O

ct

05-N

ov

12-N

ov

19

-Nov

Fly

nu

mb

ers

Fly monitoring

Control Intervention

Linear (Control) Linear (Intervention)

84%

Trapped flies during Intervention (n=9532)

Musca Chrysomya Others

Netting installation

Results – microbiological sampling 24

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 25

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

26

Project description

Background

Objectives

Material and methods

Baseline

Intervention

Microbiological sampling

Results

Outlook

Discussion

Conclusion

Outlook 27

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 28

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 29

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 31

(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.