MICROBIAL RISK ASSESSMENT AND POTENTIAL ROLE IN MILK SAFETY

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GENERAL INTRODUCTION

The South African (SA) dairy industry is characterised by the primary sector (dealing with milk production at farms) and the secondary sector (consisting of milk processors). Within the secondary sector, a few large processors operate nationally in more than one region while smaller processors operate in specific areas, and a number of milk producers sell their own produce to retailers and consumers, known as producer-distributors (PDs) (MPO, 2016). Milk sold by PDs, also known as producer-distributor bulk milk (PDBM), is typically (i) raw milk for human consumption, (ii) raw milk received with the intention of processing and selling as pasteurised milk, and (iii) pasteurised milk received to be sold, that has been pasteurised elsewhere at an approved facility. Surveys carried out at national, provincial and district levels on milk produced and supplied by PDs have highlighted microbiological inadequacy, which can pose a public health risk (Lues et al., 2003; O’Ferrall-Berndt, 2003; Cawe, 2006; Lues et al., 2010; Caine et al., 2014).

MILK AND DAIRY PRODUCTION

Milk is the secretion of the mammae of the female mammal intended for nourishment of their young. It is obtained from dairy animals, with neither addition to it nor extraction from it, and is intended for further processing or consumption as liquid milk (Codex Alimentarius, 1999). According to the European Union (EU) legislation, raw milk is defined as milk produced by the secretion of the mammary gland of farmed animals that has not been heated to more than 40 °C or undergone any treatment that has an equivalent effect (Regulation (EC) No 853/2004). Humans have consumed milk from several farmed animals (cows, buffalos, goats, sheep, camels and horses) for centuries and it serves as a good source of carbohydrates (lactose), animal proteins, fats, vitamins and minerals (Haug et al., 2007). Cow or bovine milk is by far the most consumed (Haenlein, 2004; Haug et al., 2007). Therefore, in this study, the term ‘milk’ refers to cow/bovine milk. Milk is produced and marketed raw or heat-treated (pasteurised, sterilised or ultra-heat treated).

MILK PRODUCTION IN SOUTH AFRICA

The SA dairy industry is one of the largest in Africa, contributing about 0.54% of the world milk production (FAOSTAT, 2006; DAFF, 2014). It is the fourth largest agricultural industry in the country, producing an average of 3 million tonnes of milk per-year and representing 5.6% of the gross value of all agricultural production (Mkhabela and Mndeme, 2010; MPO, 2016). The number of milk producers has decreased by more than 50% (Table 2.1) from 3 665 in January 2008 to 1 683 in January 2016 (MPO, 2016). Within the stated period, Free State followed by Western Cape were the leading milk producing provinces in the country while Northern Cape and Limpopo provinces were the least. The biggest percentage decrease in producer numbers occurred in the Free State (69,5%). The Department of Agriculture, Forestry and Fisheries (DAFF) (2014) reports that coastal areas were more suitable for milk production because of mild temperatures, as well as good rainfall that ensures good quality natural and artificial pastures. The inland production areas are generally climatically less favourable for milk production (DAFF, 2014).

South African milk value chain

The SA milk value chain is characterised by the interconnection between the formal and informal market (Agenbag, 2008; DAFF, 2014). Figure 2.4 presents the structure of the SA milk and dairy value chain. The production of milk and dairy products in SA follows several stages and generally starts with animal feed production, followed by raw milk production at the farm, and further processing, either at a dairy company or at the farm itself. Spoilage and pathogenic organisms may enter at any stage along the dairy supply chain. E. coli pathotypes, particularly STEC O157, are one of the most commonly isolated pathogens in milk. Potential sources of STEC in milk can be water used for cleaning milking equipment or faecal contamination along the dairy value chain. Several studies in SA have isolated and detected STEC in water and cattle faeces (Ateba and Bezuidenhout, 2008; Aijuka et al., 2014; Iweriebor et al., 2015; Msolo, 2016).

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DECLARATION
ABSTRACT
DEDICATION
ACKNOWLEDGEMENTS
CHAPTER ONE: GENERAL INTRODUCTION
CHAPTER TWO: LITERATURE REVIEW
2.1. INTRODUCTION
2.2. MILK AND DAIRY PRODUCTION
2.3. MILK PRODUCTION IN SOUTH AFRICA
2.3.1. South African milk value chain
2.3.1.1. Milk from the formal value chain
2.3.1.2. Milk from the informal value chain
2.3.2. Producer-distributor bulk milk (PDBM)
2.3.2.1. Production, processing and sale of PDBM
2.3.2.2. Consumption patterns of PDBM
2.3.2.3. PDBM contamination routes
2.4. FOOD SAFETY IN DAIRY
2.4.1. Important milk-borne microbial contaminants
2.4.1.1. Spoilage microbiota
2.4.1.2. Pathogenic microbiota
2.5. ESCHERICHIA COLI
2.5.1. Pathogenic (diarrheagenic) E. coli
2.5.2. STEC
2.5.2.1. Detection of STEC in food
2.5.2.2. Sources and routes of STEC in milk
2.5.2.3. Epidemiology and clinical manifestation of STEC infection
2.5.2.4. Pathogenicity of STEC
2.5.2.5. Treatment of STEC infections and its control
2.5.2.6. STEC O157 and non O157 in dairy
2.6. ANTIBIOTIC RESISTANCE IN MILKBORNE MICROORGANISMS
2.6.1. Important types/classes of resistance
2.6.2. Occurrence of antibiotic resistant E. coli in dairy
2.7. MICROBIAL RISK ASSESSMENT AND POTENTIAL ROLE IN MILK SAFETY
2.7.1. Hazard identification
2.7.2. Hazard characterisation
2.7.3. Exposure assessment
2.7.4. Risk characterisation
2.8. CONCLUSIONS AND KNOWLEDGE GAPS
2.9. HYPOTHESES AND OBJECTIVES
2.9.1. Hypotheses
2.9.2. Objectives
CHAPTER THREE: CHARACTERISATION OF E. COLI AND OTHER ENTEROBACTERIACEAE IN PRODUCER-DISTRIBUTOR BULK MILK
3.1. ABSTRACT
3.2. INTRODUCTION
3.3. MATERIALS AND METHODS
3.3.1. Milk sample collection
3.3.2. Antibiotic residue and phosphatase test
3.3.3. Microbiological analyses
3.3.4. Identification and characterisation of the bacterial isolates
3.3.5. Antimicrobial susceptibility testing of E. coli isolates
3.3.6. Serotyping
3.3.7. Detection of virulence genes in E. coli
3.3.8. Presumptive detection of shigatoxin O157:H7 E. coli
3.3.9. Statistical analysis.
3.4. RESULTS AND DISCUSSION
3.4.1. Total plate count, coliforms and E. coli counts in retail PDBM
3.4.2. Identification and characterisation of bacterial species
3.4.3. Characterisation of E. coli
3.4.4. Hierarchical cluster analysis
3.5. CONCLUSION
CHAPTER FOUR: EXTENDED-SPECTRUM β-LACTAMASE, SHIGATOXIN AND HAEMOLYSIS CAPACITY OF O157 AND NON-O157 E. COLI SEROTYPES FROM PRODUCER-DISTRIBUTOR BULK MILK
4.1. ABSTRACT
4.2. INTRODUCTION
4.3. MATERIALS AND METHODS
4.3.1. E. coli strains
4.3.2. Screening for β-lactamase producing E. coli
4.3.3. Extraction of genomic DNA
4.3.4. Haemolysis on blood agar
4.3.5. E. coli O157:H7 and virulence gene determination
4.3.6. GTG5 Repetitive extragenic palindromic (REP)-PCR fingerprinting of the E. coli isolates.
4.3.7. O-Serotyping
4.4. RESULTS
4.4.1. Virulence genes and ESBLs in E. coli
4.4.2. Serotyping (O-gene cluster and restriction analysis)
4.4.3. Cluster analysis of E. coli serotypes in terms of phenotypic and genotypic relationship
4.5. DISCUSSION
4.6. CONCLUSION
CHAPTER FIVE: QUANTITATIVE RISK ASSESSMENT FOR SHIGATOXIN PRODUCING E.COLIN BULK MILK SOLD DIRECTLY FROM PRODUCER TO CONSUMER
5.1. ABSTRACT
5.2. INTRODUCTION
5.3. MATERIALS AND METHODS
5.3.1. Hazard identification
5.3.2. Hazard characterisation
5.3.3. Exposure assessment
5.3.3.1. Field survey
5.3.3.2. Overview of PDBM pathway to consumer and exposure model
5.3.3.3. Estimation of STEC concentration in PDBM
5.3.3.4. Producer-distributor storage
5.3.3.5. Transport from PD to home and consumer handling
5.3.3.6. Consumption habits at home and exposure to STEC
5.3.4. Dose response
5.3.5. Simulation and analysis
5.4. RESULTS
5.4.1. Concentration of STEC in raw and pasteurised PDBM
5.4.2. Exposure assessment
5.4.3. Risk characterisation
5.4.4. Effect of model parameters on the risk of HUS
5.4.5. Possible PDBM handling scenarios
5.5. DISCUSSION
5.6. CONCLUSION
CHAPTER SIX: GENERAL DISCUSSION
6.1. METHODOLOGICAL CONSIDERATIONS
6.2. CHARACTERISATION OF E. COLI AND OTHER ENTEROBACTERIACEAE SPECIES
6.3. QUANTITATIVE MICROBIAL RISK ASSESSMENT FOR STEC IN PDBM.
6.4. POTENTIAL FOR FUTURE STUDY
CHAPTER SEVEN: CONCLUSIONS AND RECOMMENDATIONS
CHAPTER EIGHT: REFERENCES
CHAPTER NINE: PUBLICATIONS
9.1. REFEREED JOURNAL ARTICLES
9.2. PRESENTATIONS.
9.2.1. Oral
9.2.2. Posters