EXPOSURE ASSESSMENT OF SALMONELLA RELATED TO PORK HANDLING AND
CONSUMPTION AT HOUSEHOLDS IN HUNG YEN AND NGHE AN PROVINCES
Ngan Tran Thi1*, Sinh Dang Xuan1, Fred Unger2, Max Barot2, Hung Nguyen Viet2, Pham Van Hung3, Delia Grace2, Phuc Pham Duc1
ABSTRACT
Introduction: Along with poultry and eggs, pork meat represents one of the most significant risks of Salmonellosis. Pork accounts for 56% of the meat consumed daily in Vietnamese households and pork preparation and handling poses a major risk due to possible cross-contamination. The objective of this study is to conduct the exposure assessment by determination of Salmonella prevalence, concentration in market purchased pork and pork handling, and consumption at households in term of food safety in Hung Yen and Nghe An provinces.
Methods: A total of 217 pork samples were collected from pork shops in wet markets for Salmonella analysis between April 2014 and February 2015. A cross-sectional survey on pork
handling and consumption at households was also conducted using a structured questionnaire in 416 households in these two provinces.
Results: Overall Salmonella prevalence in market pork was 44.7% with an average concentration of 9 (<0.3 to >110) MPN/g. Most of consumers purchased pork at the market in the morning around 7:30 am with an average purchase amount of 0.45 (0.1-9.5) kg pork/
time. The methods used for storing raw pork before cooking were at room temperature (54.6%, 228/416) or in a refrigerator (41.8%, 174/416)) with an average duration of 0.6 and 2.4 hours, respectively. The percentages of household using the same knife or cutting board to prepare both raw and cooked pork were 80.5% and 74.5%, respectively.
1. Center of Public Health and Ecosystem Research (CENPHER), Hanoi School of Public Health 2. International Livestock Research Institute (ILRI)
3. Hanoi University of Agriculture (HUA)
Conclusion: These fi ndings highlight the high level of Salmonella in pork sold at informal retail markets. This study also shows that the behavior and practices of Vietnamese consumers can present a risk of Salmonella cross-contamination in the household that required the training and education programs on food safety practice of consumer.
Keywords: Pork, Salmonella, consumer, household, retail market.
INTRODUCTION
Food poisoning caused by Salmonella infection is a major public health risk in both developed and developing countries1. Global reports on Salmonella related infections show 93,8 million illnesses with 155,000 deaths annually2, including 22,8 million cases and 37,600 deaths yearly in Southeast Asia3. From 2010 to 2015, the Vietnam Food Administration has recorded an average of 176 food poisoning outbreaks and 5,590 cases per year, with microbiological origins accounting for 28.2% of these outbreaks4. In particular, Salmonella is listed as one of the leading causes microbial foodborne illness for human5.
Consuming foods derived from poultry and pork is a signifi cant source of salmonellosis of human foodborne illness worldwide6. In Vietnam, pork and pork products are the most popular animal food source in households.
Pork accounts for 56% of the total meat consumption in Vietnam at 29.1 kg per capita per year (in 2015)7. To prevent salmonellosis for Vietnamese consumers, Salmonella in the pork value chain needs to be further studied and focused on as a major food safety and public health issue.
To understand Salmonella contamination and food safety risks, this study aims to evaluate the Salmonella exposure by identifying Salmonella prevalence and concentration in market pork and documentthe practice of pork in purchasing, storing, handling and consumption at households in Hung Yen and Nghe An provinces.
MATERIALS AND METHODS
Study sites: This study was carried out in Hung Yen and Nghe An provinces, where pig production ranges from small-scale households to larger scale farms. In each province, three districts were selected based on typical pig production chain. In addition, these selected districts also represent for three difference contexts of rural, peri-urban, and urban areas.
Samples collection and analysis: This study is a part of current project (namely “PigRISK”) and only focused on the samples from market and households. At the market level, a total of 217 cut pork samples and eighty ground pork samples were collected in 18 communes in Hung Yen and Nghe An provinces. Each pork sample was taken by purchasing 3-4 separate pieces of lean pork from one carcass (total of 400-500 grams) following TCVN 4833-1:20028. Meanwhile ground pork was collected from 300-400 grams lean pork and grinded by the grinder machine at that shop.
All samples were kept in cool boxes and transported to laboratory for analysis within 12 hours. Salmonella quantitative and qualitative tests were then conducted by following ISO 6579:20029 and the 3-tube MPN method10, respectively. All laboratory tested was done at the National Institute of Veterinary Research, Hanoi, Vietnam.
Consumer survey: A structured questionnaire using face-to-face interview was administered to 208 households in Hung Yen and 208 households in Nghe An. Key information on pork purchasing, storing, handling, cooking and consumption was collected.
Statistical analysis: Data from the questionnaires and laboratory results have been processed using MS Excel 2010. Chi-square was used to test the difference of two proportions.
Descriptive statistic was used to analyse data from the consumer’s survey. Statistical analysis was conducted using RStudio software (Version 3.3.0) at signifi cance level of 0.05.
RESULTS
Pork samples were collected from pork shops in markets which were categorized by size as center market (16-30 shops), village market (3-15 shops) or roadside vendor (1-2 shops).
Pork shops usually open from 5 a.m to 12 noon with an average of 80 kg (in Hung Yen) and 40 kg (in Nghe An) of pork sold per day. Some shops were just retail and others both retail and wholesale. From observation, about half of sampled pork shops at the markets were located in a compound area where other products (e.g.
vegetables, fruits or dried food stuff) were also being sold. Half of the sampled shops were located in specifi c areas for selling pork only.
From the household survey, most interviewed respondents were housewives who are mainly responsible for purchasing, preparing and cooking food in the household. All of the respondents were female with the average age of 43 (17-78) years old. The average number of household members was around 4, and 29%
of households have children under 5 years old.
Salmonella contamination in pork at markets
from each sample types at markets in Hung Yen and Nghe An provinces. Salmonella was found at a similar rate in cut pork in Nghe An(44.4%) and Hung Yen (45%). The proportion of Salmonella positives in ground pork in Nghe An (50%) was higher than that in Hung Yen (37.5%), however, this difference was not statistically signifi cant (x2=0.63, df=1, p=0.43). Overall, the prevalence of Salmonella in marketed pork in Nghe An (45.9%) was higher than that in Hung Yen (42.1%), but there was again no signifi cant difference between these two provinces (x2=0.29, df=1, p=0.59) (Chi-square).
Figure 1. Prevalence of Salmonella in marketed pork samples in each province
Quantitative results on Salmonella showed a higher rate of Salmonella MPN/g in cut pork in Nghe An (10.6 MPN/g) compared to Hung Yen (7.4 MPN/g), while in ground pork it was relatively similar (17.4 MPN/g in Hung Yen and 18.4 MPN/g in Nghe An). There was no different in Salmonella concentration in cut pork samples between the two provinces (p=0.06, t-test). Table 1 show in details the Salmonella concentration and frequency of
(*) The mean values of MPN/g were calculated within the range from 0.3 to 110 MPN/g
The prevalence of Salmonella in both cut and ground pork were similar in the different market types, even though there was higher Salmonella prevalence in cut pork compared to ground pork in central markets, it was not statistically signifi cant (x2 =0.25, df =1, p =0.62). In general, the Salmonella concentration in ground pork was higher than that in cut pork from all market types. The highest Salmonella MPN was in ground pork from vendors (30.5 MPN/g), while the average Salmonella MPN were lower in cut pork from center (8.2 MPN/g), village (11.3 MPN/g) and vendor markets (1.8 MPN/g). Among the three types of markets, village markets had the most pork purchased by consumers (74.9%), followed by central markets (17.6%).
Pork purchasing and storage habit
The purchasing and storage habits of consumers at the study sites are shown in Table 2. Most households buy fresh pork in the morning, around 7:30 a.m (from 4:30 a.m to 11:30 a.m). The average distance from households to the market was 0.45 km. The frequency
of purchasing pork was 2.8 times/week with an average of 0.4-0.5 kg pork on each occasion. Fresh pork was stored by 55% of households at room temperature and 43% in a refrigerator before cooking. About 2% of households sometimes cooked pork directly after buying from market. The average storage times at room temperature or in a refrigerator were 0.6 and 2.5 hours, respectively.
Table 2. Purchasing and storing pork at household
Information Hung Yen
(n=208)
Nghe An (n=208)
Overall (n=416) Pork purchasing (mean (min-max))
Time of purchasing (o’clock) 7.1 (4.5 – 11.5) 7.5 (4.5 – 11) 7.3 (4.5-11.5) Distance from home to
market (km) 0.4 (0-3) 0.5 (0-4) 0.45 (0-4)
Amount of pork purchased
(kg/time) 0.4 (0.1-9.5) 0.5 (0.1-6) 0.5 (0.1-9.5) Frequency of pork purchased
(time/week) 3.2 (0-7) 2.5 (0-7) 2.8 (0-7)
Storage condition of fresh pork At room (ambience)
temperature (%) 44.4 64.7 54.6
In fridge (less than 4oC) (%) 52.2 32.9 41.8 Cooking directly after
purchasing (%) 3.4 0.5 1.9
Storage duration at room
temperature (hour) 0.5 (0-4) 0.8 (0-4.5) 0.6 (0-4.5) Storage duration in fridge
(hour) 2.5 (0-6) 2.7 (0-24) 2.5 (0-24)
Pork preparation, cooking and consumption Several different methods were used to prepare fresh pork in the interviewed households before cooking. Pork was half-boiled (46.2%), washed with tap water (30.9%) or prepared
Content Central Village Vendor
(No.pos/n) (%) (Mean* (min-max)) (MPN/g)
(No.pos/n) (%)
(Mean (min-max)) (MPN/g)
(No.pos/n) (%)
(Mean (min-max)) (MPN/g) Sample type
Cut pork 53/116 (45.7) 8.2 (<0.3 – >110) 36/76
(47.4) 11.3 (<0.3 – >110) 8/25 (32.0) 1.8 (<0.3 – >110) Ground pork 23/57 (40.4) 14.1 (<0.3 – >110) 8/17 (47.1) 21.4 (<0.3 – >110) 2/6 (33.3) 30.5 (15 – 46) Frequency of buying pork of consumer in each market type (%)
Always 17.6 74.9 2.7
Sometimes 8.7 7.7 2.2
Rarely 6.7 2.4 0.7
Never 67.0 14.9 94.5
Table 1. The frequency of market types and Salmonella concentration result and frequency of pork purchasing by market types in Hung Yen and Nghe An
using lime, salt, or vinegar(7.8%) of. In Hung Yen hot water was used more frequently to treat fresh pork (62%) before cooking than in Nghe An, where washing of fresh pork with water was less frequent (51.2%). 65.4% of consumers washed their hands before cooking, but only 24% of consumers washed their hands between cooking different foods. During preparation of fresh pork and cooked pork, 80.5% and 74.5%
of households using the same knife and cutting board, respectively (Table 3).
Pork consumption by age and gender
Children from 2 to 5 years old and elders over 60 years old ate pork less often than other groups at 4.4 and 4.8 times per week, respectively. The frequency of pork consumption of children from 6 to 18 years old, and males and females from 19 to 60 years old was about 5 times per week. The estimated dietary pork (lean, fatty and mixture pork) consumed per member was 0.35 kg/week (95%CI: 0.32-0.38) (Table 3).
Table 3. Pork preparation, cooking and
consumption at households in Hung Yen and Nghe An
Information Hung Yen
(n=208)
Nghe An (n=208)
Overall (n=416) Process fresh pork before cooking
Wash fresh pork with water 13.0 51.2 30.9
Thaw frozen pork then wash with water 0.5 0.6 0.6 Wash with salted/lemon/vinegar water 3.8 12.4 7.8
Wash by using ozone machine 7.6 1.9 4.9
Immerse in hot water 62.0 28.4 46.2
Combine some of above methods 4.4 2.5 3.5
Washing hand before and after cooking Wash hands before preparing pork/other
food 62.5 68.3 65.4
Wash hands after cooking pork/other food 78.9 76.0 77.4
Wash hands before eating 57.2 70.7 63.9
Using knife and cutting board in kitchen Use the same knife for both raw and
cooked pork 76.9 84.1 80.5
Frequency of pork consumption (meal/week)
Children (2-5 years old) 4.4 4.5 4.4
Adolescent (6-18 years old) 5.7 4.5 5.1
Female adult (19-60 years old) 5.1 4.7 4.9
Male adult (19-60 years old) 5.3 4.4 4.9
Elder (over 60 years old) 5.0 4.4 4.8
Amount of pork consumption (Mean (95%CI)) Pork consumption** (kg/person/week) 0.36
(0.32-0.4) 0.34 (0.29-0.39)
0.35 (0.32-0.38) (**) The amount of pork consumption included lean, fatty, and mixture pork, and excluded bone, organ or other pork products
DISCUSSION
Our study found that 42.1% of cut pork and 45.9% of ground pork sold in markets was positive for Salmonella. These fi ndings are similar to previous studies in Vietnam (ranging from 33% to 69%)11-14, a range also comparable with recent fi ndings in northern Thailand (41%).15 However, these results are signifi cantly higher than developed countries, 8.1% (in Denmark)16, 2.6% (in Ireland)17 or 0.3 to 4.3%
(in Belgium)16-18. The Salmonella prevalence in marketed pork in Vietnam in the past decades has remained at a high level11-14. Furthermore, the average Salmonella concentration on pork sold in markets was 9 (< 0.3 to >110) MPN/g which might refl ect the typical condition of selling meat at wet markets without any cooling facilities. Ambient temperature at retail levels are be ideal for the bacterial multiplication19. A recent study in Hung Yen of Salmonella in pork also reported at the same range of concentration (0.3 to 15 MPN/g)11, and higher compared to fi ndings in a study in Irish retail pork (2009) (between <0.03 and 2.10 MPN/g)17 and in Belgium (-2.64±1.76 log CFU/g)18. These high levels of contamination require an improvement in the hygiene conditions and practices along the pork value chain, especially at the pork market, to limit cross contamination and multiplication
Consumers usually buy fresh pork in the morning, around 7:30 am, daily at wet markets which accounts for 80% of the pork market in Vietnam20. Minimarts or supermarkets with the cold chain facilities to distribute fresh pork are not commonly available in these two provinces.
The time of selling and purchasing fresh pork lasted from 5:00 a.m to 11:30 a.m with the ambiance temperature ranging from 17 to 30oC21. This presents a major risk for bacterial growth and proliferation19. It is obvious that the longer the pork is unsold, the higher risk of contamination and concentration of Salmonella in fresh pork22. In addition, consumers appear to store fresh pork at room temperature before cooking for about 0.6 hours (range 0 - 4.5), and the risks of this should be emphasized in food handling education programs. In reality Salmonella contamination might never be eliminated, but substantial reduction of levels by improving processing, handling and work practices at pork shops, will reduce human morbidity. Emphasis is need on reducing time and temperatures in the pork shops. Cooking pork is also a crucial point which can lead to cross contamination via kitchen equipment23,24. In our study, the practice of immersing fresh pork in boiling hot water before cooking could help to reduce Salmonella contamination. However, the proportion of households that used the same knife and/or cutting board to prepare raw and cooked pork was more than 70%. This presents a major risk factor of transferring bacteria from raw food or contaminated surfaces to the cooked pork or clean food utensils. Previous studies simulating the cross contamination of Salmonella in kitchens reported a high rate of transference of Salmonella to boiled pork by using the same cutting board, knife and hand25, and long survival (at least 4 hours) of Salmonella on a cutting
board’s surface26. This underlines the necessity for proper sanitization of kitchen equipment and hygienic preparation of raw produce and cooked equipment as well as promoting personal hygiene practices in the household kitchen.
In conclusion, this study shows the high prevalence and concentration of Salmonella in market pork and potential risks of households practices (storage and preparation or cooking) which might lead to human salmonellosis cases. However, there is little data available on transference of salmonellosis to consumers;
only a WHO report showing a 1% (0.2 - 7%) yearly salmonellosis incidence for Asian countries, including Vietnam27. This study provides valuable information for risk communication, food safety education and intervention activities to the informal pork value chain to improve pork safety in Vietnam.
Future studies into pork safety, including salmonellosis quantitative microbial risk assessment are important to adequately manage this public health problem in Vietnam.
DECLARATION OF CONFLICTING INTERESTS
The authors declared no potential confl icts of interest with respect to the research, authorship, and/or publication of this article.
ACKNOWLEDGEMENTS
This study was a component of the on-going project: “Reducing the disease risks and improving food safety in smallholder pig value chains in Vietnam” (PigRISK), and funded by the Australian Centre for International Agriculture Research (ACIAR), the Consultative Group on International Agricultural Research (CGIAR), and Research Program Agriculture for Nutrition and Health (A4NH).
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