Risk assessment for Listeria monocytogenes in hot-smoked fish in informal markets in Madina, Accra

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Published on February 12, 2014

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Presentation by K. Bomfeh, K. Tano-Debrah, F.K. Saalia and B. Bediako-Amoa at the 17th Faculty of Science Colloquium, University of Ghana, Accra, Ghana, 21 March 2012.

Risk assessment for Listeria monocytogenes in hotsmoked fish in informal markets in Madina, Accra K. Bomfeh, K. Tano-Debrah, F.K. Saalia and B. Bediako-Amoa Presented at the 17th Faculty of Science Colloquium, University of Ghana Accra, Ghana, 21 March 2012

BACKGROUND

• Listeria monocytogenes is a non-spore forming pathogenic bacterium that causes a highly fatal disease called listeriosis • L. monocytogenes is considered the leading cause of death among food-borne bacterial pathogens, with a fatality rate of 20-30%, and up to 75% in highly immunocompromised individuals Table 1: Fatality of L. monocytogenes infection (CDC, 2000) Pathogen Campylobacter spp. Illnesses 10,539 Deaths 99 Salmonella non-typhoidal 15,608 553 3.54 L. monocytogenes 2,298 499 21.71 Department of Nutrition and Food Science, Univ. of Ghana % Deaths 0.95

Foods frequently contaminated • Milk and milk products • Soft cheese • Processed meats, red meat • Vacuum packaged beef and poultry products • Lettuce • Coleslaw • Fried rice • Smoked fish • Salted fish Department of Nutrition and Food Science, Univ. of Ghana

RATIONALE • Human listeriosis is not documented in Ghana. However, the occurrence of the illness among herds of sheep has been documented • The pathogen has been isolated from fresh milk from informal markets, and from coleslaw from restaurants in some parts of Accra (Appiah, 2010; Dogbe 2010 both unpublished) • Fish has been implicated in listeriosis outbreaks elsewhere (Buchanan et al., 1994; Lindqvist and Westoo, 2000; FAO, 2000) Department of Nutrition and Food Science, Univ. of Ghana

RATIONALE • Ghana records high rates of fish consumption – Per capita fish consumption of 20-25kg, about twice the world average of 13kg – Fish purchases account for 22.4% of household food expenditures – Fish contributes 60% of total animal protein consumed in Ghana (BoG, 2008; Adu-Gyamfi, 2006; Oppey, 2003; Nketsia-Tabiri and Sefa-Dedeh, 2000; Steiner-Asiedu, 1991; Plahar et al., 1991) • Over 80% of fish landings are processed traditionally Department of Nutrition and Food Science, Univ. of Ghana

OBJECTIVES Main: Risk assessment of listeriosis associated with the consumption of traditionally processed fish in Ghana Specific: 1. To determine the presence and concentration of Listeria monocytogenes in traditionally hotsmoked fish • • • Mackerel: Scomber japonicus Tuna: Katsuwonus pelamis Herrings: Sardinella eba Department of Nutrition and Food Science, Univ. of Ghana

OBJECTIVES Specific: 2. To determine the exposure of consumers to the pathogen through consumption of the products 3. To determine the risk of illness following ingestion of the pathogen through consumption of traditionally processed fish Department of Nutrition and Food Science, Univ. of Ghana

METHODS

GENERAL STUDY DESIGN Hazard Identification Determination of the ability of an organism to cause harm Exposure Assessment Probability of ingesting hazard, and the likely quantities thereof Hazard Characterization Dose-response Assessment Risk Characterization Description of the (severity of the ) effect of the hazard following consumption Final quantitative or qualitative description of the nature of the risk Fig. 1: Codex Alimentarius Commission framework for risk assessment, 2003

HAZARD IDENTIFICATION • Literature review for information on – – – – – Nature of organism Occurrence and transmission Pathogenicity Outbreaks Risk assessments

EXPOSURE ASSESSMENT • Involved consumer survey and laboratory analysis of field samples Consumer Survey • Fish consumption patterns – Frequency of consumption – Quantities often consumed at an instance – Form in which consumed Laboratory analyses • Prevalence of Listeria monocytogenes (presence/absence) • Concentration of the pathogen (CFU/g)

EXPOSURE ASSESSMENT Consumer surveys • 150 consumers were interviewed with semistructured questionnaires on – – – – frequency of consumption of the products quantities often consumed at an instance form in which products are often consumed proxy estimation of the consumption pattern among the elderly, children, and pregnant women. • Total respondents: 600

EXPOSURE ASSESSMENT Laboratory analysis Primary Enrichment LEB, 37oC, 24h Secondary Enrichment Fraser, 37oC, 24-48h Plating on Oxford or Chromagar, 37oC, 24-28h

EXPOSURE ASSESSMENT • The likely number of L. monocytogenes ingested was calculated as N=CxQ [1] N = likely number of L. monocytogenes cells ingested C = CFU/g of L. monocytogenes in the fish product Q = serving size of fish product frequently consumed (Lindqvist and Westoo, 2000)

HAZARD CHARACTERIZATION • The Weibull-Gama model was used to determine the probability of illness (Lindqvist and Westoo, 2000; Bemrah et al., 1998; Farber et al.,1997) • Weibull-Gama dose-response model P = 1 – [ 1 + (Nb)/β ] – α P = probability of infection N = dose of L. monocytogenes α, β, b = model parameters α=0.25, b=2.14 β=1010.98 for high-risk population β=1015.26 for low risk population [2] N = C x Q [1]

RISK CHARACTERIZATION • Quantitative estimate of the risk of illness following consumption of contaminated fish ASSUMPTIONS • Fish were consumed as purchased OR were not heat-treated to an extent that guaranteed elimination of L. monocytogenes • All strains of L. monocytogenes in the fish products were virulent

RESULTS & DISCUSSION

Key Findings 1. Sanitary conditions of fish processing and handling were unsatisfactory 2. L. monocytogenes was detected in at least one sample of each product on informal markets 3. L. monocytogenes was detected in at least one sample from each step in processing except – – Fresh, frozen mackerel and herrings Hot-smoked tuna, mackerel and herrings sampled immediately after processing 4. Counts were low (102-103 CFU/g) 5. Low risk of ingestion and infection Department of Nutrition and Food Science, Univ. of Ghana

PROCESSING AND HANDLING Department of Nutrition and Food Science, Univ. of Ghana

Table 1: Average prevalence of Listeria monocytogenes in traditionally processed fish purchased from informal market Product Number of samples purchased Number of samples positive Prevalence of L. for L. monocytogenes monocytogenes (%) Smoked tuna 15 12 80 Smoked mackerel 15 14 93 Smoked herrings 15 10 67 Department of Nutrition and Food Science, Univ. of Ghana

16.00 16.00 14.00 14.00 12.00 x102 CFU/g 10.00 8.00 6.00 5.00 4.00 4.00 4.00 2.00 1.00 2.00 0.00 KA KO MO TU SA MA HR Type of fish Fig. 1: Average counts of L. monocytogenes in fish samples KA-kako (salted) KO-koobi (salted) MO-momoni (salted) TU-tuna MA-Mackerel HR-herrings DR-dried fish Department of Nutrition and Food Science, Univ. of Ghana DR

Fish contaminated with Lm on informal markets No Ingestion not likely Yes Fish eaten as is (without heating) No Lm survives in fish during cooking No Ingestion not likely Yes Risk of ingestion N = CxQ Yes Risk of ingestion N = CxQ Fig. 2: Event tree for risk of ingestion of Listeria monocytogenes through consumption of traditionally smoked fish purchased from informal markets Department of Nutrition and Food Science, Univ. of Ghana

Table 1: Likely numbers of L. monocytogenes ingested through consumption of contaminated TPF fish on informal markets in Ghana Product C (CFU/g) Q (g) N=CxQ Tuna 1.40x103 >200 ≥3.20x105 Mackerel 1.60x103 >200 ≥2.80x105 Herrings 4.00x102 151 6.04x104 C : average counts across five markets Q : Most frequently consumed quantities N=likely number of L. monocytogenes ingested P = 1 – [ 1 + (Nb)/β ] – α Department of Nutrition and Food Science, Univ. of Ghana

RISK ESTIMATION FOR LOW-SUSCEPTIBILITY CONSUMER • Dose required for illness = ≥ 109 cells (Buchanan et al., 1997; Schlech,1999) • Mean Lm CFU – Herrings – Mackerel – Tuna = 8.33x102 CFU/g = 2.90x103 CFU/g = 2.10x103 CFU/g Department of Nutrition and Food Science, Univ. of Ghana

1 5.0% 185.6 90.0% 317.8 5.0% 0.8 0.4 95% = 0.000318 Mean = 0.000248 0.2 500 450 400 350 300 250 200 150 0 100 Confidence 0.6 Probability of illness Values in Millionths Probability of illness among 18-49yrs from consuming smoked mackerel contaminated with L. monocytogenes Department of Nutrition and Food Science, Univ. of Ghana

5.0% 1 5.56 83.5% 11.5% 10.00 0.8 0.4 0.2 95% = 1.088E-005 Mean = 8.012E-006 Probability of illness according to Weibull-Gamma / NA 18 16 14 12 10 8 6 4 0 2 Confidence 0.6 Probability of illness Values in Millionths Probability of illness among 18-49yrs from consumption of traditionally smoked herrings contaminated with L. monocytogenes Department of Nutrition and Food Science, Univ. of Ghana

5.0% 0.01 99.3 90.0% 169.8 5.0% 0.008 Confidence 0.006 0.002 95% = 0.000170 Mean = 0.000132 0.004 Tuna Probability of illness Values in Millionths Risk of illness among 18-49yr tuna consumers Department of Nutrition and Food Science, Univ. of Ghana 382.5 286.875 191.25 95.625 0 0

RISK ESTIMATION FOR LOW-SUSCEPTIBILITY CONSUMER 5.0% 100.0% 1 99.2 90.0% 0.0% 5.0% 0.0% 169.9 0.6 Tuna Herrings / NA 95% = 0.000318 Mean = 0.000248 95% = 0.000170 Mean = 0.000132 0.2 Mean = 8.012E-006 Mackerel / Quantity Consumed 0.4 397.58 Probability of illness Values in Millionths 298.185 198.79 99.395 0 0 Confidence 0.8 Comparison of probability of illness from consumption of tuna, mackerel and herrings Department of Nutrition and Food Science, Univ. of Ghana

RISK ESTIMATION FOR HIGH-SUSCEPTIBILITY CONSUMER • Dose required for illness = ≥ 104 cells (Buchanan et al., 1997; Schlech,1999) • Average Lm CFU – Herrings – Mackerel – Tuna = 8.33x102 CFU/g = 2.90x103 CFU/g = 2.10x103 CFU/g Department of Nutrition and Food Science, Univ. of Ghana

5.0% 100.0% 1 0.1993 90.0% 0.0% 5.0% 0.0% 0.2949 0.6 Tuna / Average 0.4 Herring / Average Mean = 0.3250 0.2 Mean = 0.2478 Mean = 0.0285 Mackerel / Average Probability of illness Comparison of probability of illness Department of Nutrition and Food Science, Univ. of Ghana 0.45 0.4 0.35 0.3 0.25 0.2 0.15 0.1 0.05 0 0 Confidence 0.8

HIGH-RISK vs. LOW-RISK GROUPS Department of Nutrition and Food Science, Univ. of Ghana

5.0% 90.0% 0.0% 0.0% 0.0000000 1 5.0% 100.0% 0.8 0.2 Mean = 0.0285 Mean = 8.012E-006 0.4 Probability of illness Values in Thousands Comparison of risk of illness from herrings: Low risk vs. High Risk Department of Nutrition and Food Science, Univ. of Ghana 0.000064 0.0000492 0.0000344 0.0000196 0.0000048 0 -0.00001 Confidence 0.6

EFFECT OF MITIGATION Department of Nutrition and Food Science, Univ. of Ghana

Tuna Mode of consumption AHI ADULT ELDERLY As is 1.00E-04 2.07E-01 Mitigation 6.90E-06 1.93E-02 Department of Nutrition and Food Science, Univ. of Ghana

1 5.0% 90.0% 0.0% 0.0% 4.9 9.0 5.0% 100.0% 0.8 Red: mitigation Blue: No mitigation 0.4 Probability of illness Values in Millionths Effect of mitigation on risk reduction among 18-49yrs, tuna Department of Nutrition and Food Science, Univ. of Ghana 245.75 222.5 199.25 176 152.75 Mean = 0.000132 129.5 106.25 83 59.75 36.5 13.25 0 Mean = 6.829E-006 0.2 -10 Confidence 0.6

CONCLUSIONS Exposure Assessment • Traditionally smoked tuna, mackerel and herrings on informal markets are potential vehicles for the transmission of L. monocytogenes • Depending on the kind of product and quantity consumed at an instance, consumers are exposed to ingesting 102 to 105 cells of L. monocytogenes

CONCLUSIONS Hazard Characterization and Dose-Response • Depending on dose ingested and susceptibility to infection, consumers have a 1 in 10 to 1 in 100,000,000 risk of illness Risk Characterization • Risk of ingestion and infection are generally low. However, individuals who either consume TPF from informal markets as is or do not heat-treat the products sufficiently increase their risks of ingestion and infection, and vice versa

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