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Food quality and safety in Singapore: microbiology aspects

Food quality and safety in Singapore: microbiology aspects BACKGROUND: Singapore’s status as a first world island city-state which relies chiefly on food imports to meet the demand for consumption presents unique challenges in terms of microbial food safety and quality. Despite the efforts of the Ministry of Health in Singapore, in conjunction with the Agri-Food & Veterinary Authority of Singapore and the National Environment Agency actively collaborate together to promote safety in Singapore, foodborne diseases are still a major public health issue. OBJECTIVE: The aim of the review was to summarize the various foodborne diseases reported in Singapore in the past few years as well as to give an account of all the currently available microbiological findings indicating safety and quality of poultry, vegetables, fruits, and seafood sold in Singapore. Keywords: Singapore; Food safety; Food quality; Foodborne disease. Despite Singapore enjoying among the safest food in the world, Introduction foodborne diseases, as succinctly summarized by Kondakci and Yuk Despite constant advancements in technology and our knowledge of (2012), are still a major health burden. To minimize the risk of food- food safety, foodborne illness due to consumption of unwholesome borne illnesses, it is necessary to assess and estimate the extent of food remains a critical problem worldwide. One challenge in food the contribution of different food commodities to the foodborne safety is the prioritization of food commodities to be tested given the disease burden in Singapore. This review article aims to summarize limited time and resources (Batz et al., 2005). Considering the limita- and compile the currently published findings regarding the microbial tions, the ability to efficiently establish the relationship between the safety and quality of retail poultry, vegetables, fruits, and seafood in illness and the contaminated food is an important factor that can Singapore as well as give a summary of foodborne disease cases and promote food safety along the entire food supply chain. notable outbreaks in Singapore in the past few years. As an island city-state with scarce land for agriculture, Singapore relies predominantly on food imports to meet more than 90% of Foodborne Diseases in Singapore consumption (AVA, 2015a). Agri-Food & Veterinary Authority of Singapore (AVA) plays a very active approach in safeguarding public The Ministry of Health (MOH) in Singapore publishes communica- health by setting and enforcing food safety standards for all foods being ble diseases surveillance report on an annual basis and epidemiologi- imported from the point of production to retail in a series of compre- cal news bulletin articles on a quarterly basis. Information such as hensive monitoring, surveillance, and enforcement programmes. As number of cases and incidence rates of all reported cases of food-/ a result, residents of Singapore enjoy food of good quality, diversity, water-borne diseases in Singapore is available in the former while the affordability, and most importantly safety (Ludher, 2015). latter covers information on specific outbreaks in Singapore. © The Author 2017. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 2 Y. H. Zwe and H. G. Yuk Table 1. Annual incidence of reported food-/water-borne diseases in Singapore between 2006 and 2015.* Year No. of cases (Incidence rate/100 000 population) Campylobacteriosis Cholera Hepatitis A Hepatitis E Listeriosis Non-typhoidal Paratyphoid Shigellosis Typhoid salmonellosis 2006 236 (5.3) 0 (0.0) 146 (3.3) 31 (0.7) 9 (0.2) 380 (8.5) 23 (0.5) 19 (0.4) 60 (1.3) 2007 170 (3.7) 7 (0.2) 88 (1.9) 35 (0.8) 6 (0.1) 307 (6.7) 33 (0.6) 13 (0.3) 67 (1.2) 2008 176 (3.6) 1 (0.0) 107 (2.2) 54 (1.1) 5 (0.1) 718 (14.9) 29 (0.6) 29 (0.6) 84 (1.7) 2009 261 (5.2) 4 (0.1) 89 (1.8) 90 (1.8) —** 1144 (22.9) 28 (0.6) — 69 (1.4) 2010 320 (6.3) 4 (0.1) 68 (1.3) 112 (2.2) — 1480 (29.2) 38 (0.7) — 82 (1.6) 2011 372 (7.2) 2 (0.04) 57 (1.1) 95 (1.8) — 1374 (26.5) 30 (0.6) — 61 (1.2) 2012 443 (8.3) 1 (0.02) 94 (1.8) 99 (1.9) — 1499 (28.2) 51 (1.0) — 79 (1.5) 2013 397 (7.4) 2 (0.04) 77 (1.4) 53 (1.0) — 1735 (32.1) 17 (0.3) — 71 (1.3) 2014 435 (8.0) 2 (0.04) 67 (1.2) 63 (1.2) — 1883 (34.4) 17 (0.3) — 50 (0.9) 2015 420 (7.6) 3 (0.05) 45 (0.8) 58 (1.0) — 1988 (35.9) 24 (0.4) — 43 (0.8) *All data are obtained from the Ministry of Health Singapore (MOH, 2007–2016). **Data are not available. A report published by Kondakci and Yuk (2012) gave an over- In spite of that, a small-scale study conducted by Zheng et al. (2014) view of foodborne diseases in Singapore in the past decade from 2001 revealed that 10% (n  =  60) of raw duck wing samples purchased to 2010. The report found a significant rise in non-typhoidal salmo- from local supermarkets were contaminated with Salmonella spp. nellosis from an incidence rate/100 000 population of 3.9 at the start while Lim et al. (2015) reported 33.3% (n = 30) of raw duck wing of the decade to 29.2 at the end. As shown in Table 1, in the new dec- samples being Salmonella positive (Table 2). The discrepancy in the ade starting 2011, the incidence rate of salmonellosis/100 000 popu- prevalence of Salmonella between the two studies could be attrib- lation has been on the rise every year from 26.5 in 2011 to 35.9 in uted to their small sample sizes. Combining the results from both 2015 (MOH, 2012, 2016). Other notable disease of interest reported studies, the overall prevalence of Salmonella spp. in duck wings in was campylobacteriosis which was largely caused by Campylobacter Singapore might be around 18% (n = 90). jejuni with an incidence rate/100 000 population of 1.2 in 2002 and Despite salmonellosis (typhoidal and non-typhoidal) accounting an average rate of 7.7 from 2011 to 2015 (MOH, 2016). for more than 66% of all food- and waterborne diseases reported in An epidemiological news bulletin article published in the last quar- Singapore from 2001 to 2010 (Kondakci and Yuk, 2012) and poul- ter of 2016 investigated the link between the Group B Streptococcus try being a well-known reservoir of Salmonella spp., there is a lack of (GBS) and the consumption of raw fish dishes. A joint investigation published information in the literature on prevalence of Salmonella between the MOH, National Environment Agency (NEA), and AVA spp. in various types of poultry and its role in contributing to the found a significant association between the GBS serotype III ST283 disease burden of salmonellosis in Singapore. More prevalence stud- infections and the consumption of the Chinese raw fish dish Yu Sheng ies involving different types of poultry such as chicken, quail, and (Tan et  al., 2016). Swift measures to ban the consumption of raw turkey in large enough sample sizes are needed to properly assess the freshwater fish in ready-to-eat (RTE) raw fish dishes and stepped up microbiological safety and quality of poultry in Singapore. measures to closely monitor the microbiological safety of salt water fish intended for raw consumption, were also reported. Fruits and Vegetables The Center for Science in the Public Interest (CSPI) reported that Poultry fresh produce (fruits, vegetables and their dishes) such as cucumber, Poultry production in 2016 is forecasted to be at 116.2 million tons; cilantro, cantaloupe, and peppers was the cause of most foodborne accounting for more than 36% of the forecasted total global meat illnesses in the United States with almost 20 000 illnesses over 629 production at 320.7 million tons with Asia at the helm followed outbreaks between 2004 and 2013 (CSPI, 2015). Moreover, vari- by North and South America according to the Food & Agriculture ous surveillance studies have previously described Salmonella spp., Organization (FAO) (Anonymous, 2016). These statistics suggest Escherichia coli O157:H7, Listeria monocytogenes, Staphylococcus that poultry is one of the most important food categories to be moni- aureus, Bacillus cereus, and Aeromonas spp. being isolated from tored for its wholesomeness and safety; especially with respect to fresh produce (Beuchat, 1996; Johnston et al., 2006; De Giusti et al., Salmonella contamination, since poultry has been associated with 2010). Salmonella outbreaks (Foley et  al., 2011). The Centers for Disease The amount of vegetables produced locally in Singapore only Control and Prevention (CDC) in the USA has reported a total of accounts for 8% of consumption (AVA, 2015c). Hence, a staggering 611 cases of human salmonellosis linked to live poultry in eight 92% of all vegetables consumed in Singapore are imported from multistate outbreaks spanning 45 states in the United States in 2016 countries such as Australia, China, and Malaysia. A  total of 388 alone (CDC, 2016). 364 tons of fruits such as watermelons, bananas and oranges were In Singapore, the definition of poultry encompasses domestic shipped to Singapore from countries such as Malaysia, China, and fowl or chickens, ducks, turkey, geese, quails, pigeons, etc. (AVA, the United States in the year 2012 (AVA, 2013, 2015c). Although no 2016). AVA has stringent regulations regarding the import of live major fresh produce-related foodborne outbreaks has been recently poultry into Singapore meant for slaughter and consumption to reported in Singapore, recent shift in tastes and preferences towards uphold the wholesomeness of the poultry consumed in Singapore. high fibre diets due to increased health consciousness (Good, 1998) Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 Food quality and safety: microbiology aspects 3 and the tendency to consume vegetables as RTE food warrants Singapore might be around 4% (n = 104). However, more compre- proper assessment of microbial safety and quality of fresh produce hensive studies covering more varieties of produce and presence of sold in Singapore. other significant pathogens like pathogenic E. coli and L. monocy- A study carried out by Seow et  al. (2012) characterizing the togenes are needed to paint a fuller picture of the microbial quality microbial quality of a total of 125 common fresh fruit and vegeta- and safety of fruits and vegetables in Singapore. ble items sold in Singapore showed that the highest mean aerobic The microbial quality of fruits sold in Singapore is relatively bet- mesophilic count and coliform counts were found in bean sprouts ter as compared to that of vegetables, with 4.0 and 1.1 log CFU/g among all tested items at 8 and 5.7 log CFU/g, respectively (Table 3). being the highest counts found in fruits (mango) for aerobic meso- RTE salad was found to have a mean aerobic mesophilic and coli- philic count and coliform count, respectively, as compared to 8.0 form count of 6.5 and 4.9 log CFU/g, respectively (Table 3). Neither and 5.7 log CFU/g in bean sprouts for the two parameters described E. coli O157:H7 nor Salmonella spp. was isolated from any of the above, respectively (Table 3) (Seow et al., 2012). Fruits are generally samples in the study. expected to have low microbial counts due to the fruits’ peel acting Two other separate studies by Lim et al. (2015) and Zheng et al. as a good biological barrier against microorganisms. Furthermore, (2014) reported a prevalence of Salmonella spp. in bean sprouts as fruits hang high on their trees, keeping them safe from contact with 6.7% (n = 30) and 3.3% (n = 60), respectively. Based on these previ- soil or irrigation water. Under such environments, the numbers of ous studies, the prevalence of Salmonella spp. in bean sprouts sold in microorganisms would be expected to be smaller than other produce Table 2. Prevalence of foodborne pathogens in various food items sold in Singapore. Sample No. of samples % (No.) of confirmed positive samples References Salmonella spp. Escherichia Vibrio spp. coli O157:H7 Poultry Duck wings 30 33.3 (10) —* — Lim et al. (2015) 60 10.0 (6) — — Zheng et al. (2014) Vegetables Carrot 12 0.0 (0) 0.0 (0) — Seow et al. (2012) Lettuce 13 0.0 (0) 0.0 (0) — Seow et al. (2012) Tomato 13 0.0 (0) 0.0 (0) — Seow et al. (2012) RTE salad 13 0.0 (0) 0.0 (0) — Seow et al. (2012) Bean sprouts 14 0.0 (0) 0.0 (0) — Seow et al. (2012) 30 6.7 (2) — — Lim et al. (2015) 60 3.3 (2) — — Zheng et al. (2014) Fruits Apple 14 0.0 (0) 0.0 (0) — Seow et al. (2012) Mango 10 0.0 (0) 0.0 (0) — Seow et al. (2012) Orange 11 0.0 (0) 0.0 (0) — Seow et al. (2012) Seafood Prawn 40 0.0 (0) — 2.5 (1) Huang et al. (2012) Shellfish 31 3.2 (1) — 0.0 (0) Huang et al. (2012) Fishball 32 0.0 (0) — 3.1 (1) Huang et al. (2012) 30 23.3 (7) — — Lim et al. (2015) *Not performed. Table 3. Aerobic mesophilic and coliform counts of various fruits and vegetables sold in Singapore (Seow, 2012). Name of sample Aerobic mesophilic count* Coliform count* n Mean Range n Mean Range Vegetables Carrot 16 4.8 2.6–6.9 12 2.7 1.4–4.9 Lettuce 17 5.8 3.4–7.0 13 4.2 1.6–5.5 Tomato 18 4.2 2.4–5.5 13 2.1 0.3–3.0 Bean sprouts 19 8.0 7.3–9.1 14 5.7 4.1–6.3 RTE salad 13 6.5 5.8–7.3 13 5.2 4.2–5.9 Fruits Apple 18 3.4 2.1–5.1 14 0.1 ND**–1.2 Mango 11 4.0 3.0–5.1 10 1.1 ND–2.5 Orange 13 3.4 1.6–4.4 11 0.9 ND–2.1 *All units are in log CFU/g.**Not detected. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 4 Y. H. Zwe and H. G. Yuk commodities. It was also suggested that the higher surface area of could be due to the different preparation procedures of fishball vegetables as compared to fruits made the former more susceptible (handmade or machine processed) and differences in the type of to bacterial contamination and adhesion (Aycicek et al., 2006). No market the samples were purchased from (wet markets or super- E. coli O157:H7 and Salmonella spp. contamination were found in markets). The overall prevalence of Salmonella spp. in fishball sold the 35 fruit items sampled in the study (Table 2). in Singapore might be around 11.3% (n = 62) based on these two studies. Seafood Conclusion Seafood is an important food source for a large segment of the world population and is widely consumed as a delicacy in many parts of Despite continuous efforts by the government to curb foodborne Asia (Huang et  al., 2012; Yaashikaa et  al., 2016). Seafood is sus- illnesses, it still remains as one of the most pressing public health ceptible to microbial contamination and pathogens may be present issues to be solved. Based on currently published data, a high overall in low levels at harvest while more may be introduced during han- prevalence of Salmonella spp. was found in duck wings (18%) fol- dling and processing. Risk of foodborne illness by consumption of lowed by fishballs (11%) and bean sprouts (4%) but no Salmonella seafood increases further if the food is mishandled by unsanitary spp. and E. coli O157:H7 were isolated from fruits and vegetables. practices where pathogens can multiply exponentially due to tem- Although some previous studies indicated that foods being sold in perature abuse conditions (Adams and Moss, 2000; Badrie et  al., Singapore are contaminated with some pathogenic bacteria, addi- 2006; Espiñeira et al., 2010; Bakr et al., 2011). tional prevalence and characterization work should be performed In Singapore, seafood is defined as including any variety of fishes, to further establish and determine the significance of this exposure crustaceans, aquatic mollusks, marine sponges, and any other form to the national disease burden. Meanwhile, continuous efforts are of aquatic life including their young and eggs harvested from brack- needed to educate food handlers and consumers on proper handling ish, marine, or fresh water (AVA, 2015b). Seafood-borne disease has and thorough cooking of food to prevent the risk of foodborne received increased attention ever since the 2009 Vibrio parahaemo- illnesses. lyticus outbreak associated with consumption of Indian Rojak from Conflict of interest statement. None declared. cross contamination with seafood resulting in many cases of illness, hospitalization, and two deaths (MOH, 2009). References A study on microbial quality of 116 seafood samples sold in Singapore reported that the mean aerobic mesophilic counts for Adams, M. R., Moss, M. O. (2000). Bacterial agents of foodborne illness. In Adams M. R., Moss M. O. (eds.), Food Microbiology, vol2. London: prawns, shellfish, and fishballs ranged between 4.6 and 6.6 log Royal Society of Chemistry. 184–271. CFU/g (Table 4). A significant finding from the study was that by Anonymous. (2016). Global poultry trends: poultry to boost global meat mar- comparing the bacterial load between the frozen shellfish and the ket share above 36 per cent. Retrieved from http://www.thepoultrysite. frozen-thawed shellfish, it was found that the thawing process com/articles/3645/global-poultry-trends-poultry-to-boost-global-meat- increased the bacterial load even when the process was carried market-share-above-36-per-cent/. out at refrigeration temperatures. It was suggested that the water AVA. (2013). Fruits & vegetables from the Philippines. Retrieved from http:// and nutrient released from the ruptured cells during freezing might www.ava.gov.sg/files/avavision/issues3-4_2013/food-security-fruits-vege- have encouraged the growth of organisms during the subsequent tables.html. thawing process. AVA. (2015a). AVA Annual Report 2014/2015. Retrieved 1 September 2016. Huang et al. (2012) reported the isolation of V. parahaemolyti- http://www.ava.gov.sg/files/annualreport/2015/ava-ar-2015.html, p. 30. AVA. (2015b). Bringing food into singapore & exporting: general classification cus from a sample of both shrimp meat and commercial fishball, of food & food products. Retrieved from http://www.ava.gov.sg/explore- establishing a prevalence of 2.5% (n  =  40) and 3.1% (n  =  32), by-sections/food/bringing-food-into-singapore-and-exporting/general- respectively. Salmonella spp. was isolated from one shellfish sam- classification-of-food-food-products ple, establishing a prevalence of 3.2% (n  =  31). However, in a AVA. (2015c). Singapore’s food supply: the food we eat. Retrieved from http:// separate study by Lim et al. (2015), Salmonella prevalence in fish- www.ava.gov.sg/explore-by-sections/food/singapore-food-supply/the- ball samples was found to be at 23.3% (n = 30). The discrepancy food-we-eat. AVA. (2016). Bringing food into Singapore & Exporting: commercial food imports. Retrieved from http://www.ava.gov.sg/explore-by-sections/food/ Table 4. Aerobic mesophilic count of various seafood in Singapore bringing-food-into-singapore-and-exporting/commercial-food-imports. (Huang et al., 2012). Aycicek, H., Oguz, U., Karci, K. (2006). Determination of total aerobic and indicator bacteria on some raw eaten vegetables from wholesalers in Name of sample Aerobic mesophilic count* Ankara, Turkey. International Journal of Hygiene and Environmental n Mean Range Health, 209, 197–201. Badrie, N., Gobin, A., Dookeran, S., Duncan, R. (2006). Consumer aware- Fresh prawn 31 6.1 5.2–7.7 ness and perception to food safety hazards in Trinidad, West Indies. Food Shrimp meat 10 5.8 5.0–6.5 Control, 17: 370–377. Frozen-thawed shellfish 23 6.6 4.7–7.2 Bakr, W. M., Hazzah, W. A., Abaza, A. F. (2011). Detection of Salmonella and Fresh shellfish 14 6.5 4.8–7.7 Vibrio species in some seafood in Alexandria. Journal of American Science, Frozen shellfish 6 4.6 3.9–5.0 7: 663–668. Handmade fishball 16 5.7 3.6–6.5 Batz, M. B., Doyle, M. P., Morris, G. Jr., Painter, J., Singh, R., Tauxe, R. V., Commercial fishball 16 4.7 ND**–6.8 Lo, F., Wong, D. (2005). Attributing illness to food. Emerging Infectious Diseases, 11: 993–999. *All units are in log CFU/g. Beuchat, L. R. (1996). Pathogenic microorganisms associated with fresh pro- **Not detected. duce. Journal of Food Protection, 59: 204–216. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 Food quality and safety: microbiology aspects 5 CDC. (2016). Eight multistate outbreaks of human Salmonella infections nella on duck meat, bean sprouts, and fishballs in Singapore. Journal of linked to live poultry in backyard flocks. Retrieved from https://www.cdc. Food Protection, 78: 1203–1207. gov/salmonella/live-poultry-05-16/index.html. Ludher, E. (2015). A case study of Singapore’s smart governance of food. CSPI. (2015). Fresh produce remains a leading cause of outbreaks. Retrieved Retrieved from http://www.clc.gov.sg/documents/books/Smart_food_gov- from https://cspinet.org/new/201512031.html. ernance_paper-SG_case_study_FINAL_Sept 28_3.pdf. De Giusti, M., Aurigemma, C., Marinelli, L., Tufi, D., De Medici, D., Di Pas- MOH. (2009). Update on food poisoning incidents (14 April). Retrieved from quale, S., Boccia, A. (2010). The evaluation of the microbial safety of fresh https://www.moh.gov.sg/content/moh_web/home/pressRoom/pressRoom- ready‐to‐eat vegetables produced by different technologies in Italy. Journal ItemRelease/2009/updates_on_food_poisoning_incidents_(14 April).html. of Applied Microbiology, 109: 996–1006. MOH. (2007). Communicable Disease Surveillance in Singapore 2006. https:// Espiñeira, M., Atanassova, M., Vieites, J. M., Santaclara, F. J. (2010). Valida- www.moh.gov.sg/content/moh_web/home/Publications/Reports/2007.html. tion of a method for the detection of five species, serogroups, biotypes and MOH. (2008). Communicable Disease Surveillance in Singapore 2007. virulence factors of Vibrio by multiplex PCR in fish and seafood. Food MOH. (2009). Communicable Disease Surveillance in Singapore 2008. Microbiology, 27: 122–131. MOH. (2010). Communicable Disease Surveillance in Singapore 2009. Foley, S. L., Nayak, R., Hanning, I. B., Johnson, T. J., Han, J., Ricke, S. C. MOH. (2011). Communicable Disease Surveillance in Singapore 2010. (2011). Population dynamics of Salmonella enterica serotypes in commer- MOH. (2012). Communicable Disease Surveillance in Singapore 2011. cial egg and poultry production. Applied and Environmental Microbiol- MOH. (2013). Communicable Disease Surveillance in Singapore 2012. ogy, 77: 4273–4279. MOH. (2014). Communicable Disease Surveillance in Singapore 2013. Good, D. L. (1998). Singapore—Market development reports: Singapore’s MOH. (2015). Communicable Disease Surveillance in Singapore 2014. food manufacturing industry. Retrieved from http://apps.fas.usda.gov/ MOH. (2016). Communicable Disease Surveillance in Singapore 2015. GainFiles/199812/25373133.pdf. Seow, J., Ágoston, R., Phua, L., Yuk, H. G. (2012). Microbiological quality of Huang, Y., Ghate, V., Phua, L., Yuk, H. G. (2012). Prevalence of Salmonella fresh vegetables and fruits sold in Singapore. Food Control, 25: 39–44. and Vibrio spp. in seafood products sold in Singapore. Journal of Food Tan, S., Foo, K., Koh, H. F., Lin, Y., Tow, C., Zhang, Y., Heng, D. (2016). Out- Protection, 75: 1320–1323. break of Group B Streptococcus Bacteraemia in Singapore. Epidemiologi- Johnston, L. M., Jaykus, L.-A., Moll, D., Anciso, J., Mora, B., Moe, C. L. (2006). cal News Bulletin, 42: 111–115. A field study of the microbiological quality of fresh produce of domestic and Yaashikaa, P., Saravanan, A., Kumar, P. S. (2016). Isolation and identification Mexican origin. International Journal of Food Microbiology, 112: 83–95. of Vibrio cholerae and Vibrio parahaemolyticus from prawn (Penaeus Kondakci, T., Yuk, H. (2012). Overview of foodborne outbreaks in the last monodon) seafood: Preservation strategies. Microbial Pathogenesis, 99: decade in Singapore: alarming increase in nontyphoidal salmonellosis. 5–13. Food and Beverage Asia. Pablo Publishing Pte Ltd., Singapore, 42–45. Zheng, Q., Mikš-Krajnik, M., Yang, Y., Xu, W., Yuk, H. G. (2014). Real-time Lim, H. S.  Y., Zheng, Q., Miks-Krajnik, M., Turner, M., Yuk, H. G. (2015). PCR method combined with immunomagnetic separation for detecting Evaluation of commercial kit based on loop-mediated isothermal ampli- healthy and heat-injured Salmonella Typhimurium on raw duck wings. fication for rapid detection of low levels of uninjured and injured Salmo- International Journal of Food Microbiology, 186: 6–13. 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Food quality and safety in Singapore: microbiology aspects

Food Quality and Safety , Volume Advance Article – May 4, 2017

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Abstract

BACKGROUND: Singapore’s status as a first world island city-state which relies chiefly on food imports to meet the demand for consumption presents unique challenges in terms of microbial food safety and quality. Despite the efforts of the Ministry of Health in Singapore, in conjunction with the Agri-Food & Veterinary Authority of Singapore and the National Environment Agency actively collaborate together to promote safety in Singapore, foodborne diseases are still a major public health issue. OBJECTIVE: The aim of the review was to summarize the various foodborne diseases reported in Singapore in the past few years as well as to give an account of all the currently available microbiological findings indicating safety and quality of poultry, vegetables, fruits, and seafood sold in Singapore. Keywords: Singapore; Food safety; Food quality; Foodborne disease. Despite Singapore enjoying among the safest food in the world, Introduction foodborne diseases, as succinctly summarized by Kondakci and Yuk Despite constant advancements in technology and our knowledge of (2012), are still a major health burden. To minimize the risk of food- food safety, foodborne illness due to consumption of unwholesome borne illnesses, it is necessary to assess and estimate the extent of food remains a critical problem worldwide. One challenge in food the contribution of different food commodities to the foodborne safety is the prioritization of food commodities to be tested given the disease burden in Singapore. This review article aims to summarize limited time and resources (Batz et al., 2005). Considering the limita- and compile the currently published findings regarding the microbial tions, the ability to efficiently establish the relationship between the safety and quality of retail poultry, vegetables, fruits, and seafood in illness and the contaminated food is an important factor that can Singapore as well as give a summary of foodborne disease cases and promote food safety along the entire food supply chain. notable outbreaks in Singapore in the past few years. As an island city-state with scarce land for agriculture, Singapore relies predominantly on food imports to meet more than 90% of Foodborne Diseases in Singapore consumption (AVA, 2015a). Agri-Food & Veterinary Authority of Singapore (AVA) plays a very active approach in safeguarding public The Ministry of Health (MOH) in Singapore publishes communica- health by setting and enforcing food safety standards for all foods being ble diseases surveillance report on an annual basis and epidemiologi- imported from the point of production to retail in a series of compre- cal news bulletin articles on a quarterly basis. Information such as hensive monitoring, surveillance, and enforcement programmes. As number of cases and incidence rates of all reported cases of food-/ a result, residents of Singapore enjoy food of good quality, diversity, water-borne diseases in Singapore is available in the former while the affordability, and most importantly safety (Ludher, 2015). latter covers information on specific outbreaks in Singapore. © The Author 2017. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 2 Y. H. Zwe and H. G. Yuk Table 1. Annual incidence of reported food-/water-borne diseases in Singapore between 2006 and 2015.* Year No. of cases (Incidence rate/100 000 population) Campylobacteriosis Cholera Hepatitis A Hepatitis E Listeriosis Non-typhoidal Paratyphoid Shigellosis Typhoid salmonellosis 2006 236 (5.3) 0 (0.0) 146 (3.3) 31 (0.7) 9 (0.2) 380 (8.5) 23 (0.5) 19 (0.4) 60 (1.3) 2007 170 (3.7) 7 (0.2) 88 (1.9) 35 (0.8) 6 (0.1) 307 (6.7) 33 (0.6) 13 (0.3) 67 (1.2) 2008 176 (3.6) 1 (0.0) 107 (2.2) 54 (1.1) 5 (0.1) 718 (14.9) 29 (0.6) 29 (0.6) 84 (1.7) 2009 261 (5.2) 4 (0.1) 89 (1.8) 90 (1.8) —** 1144 (22.9) 28 (0.6) — 69 (1.4) 2010 320 (6.3) 4 (0.1) 68 (1.3) 112 (2.2) — 1480 (29.2) 38 (0.7) — 82 (1.6) 2011 372 (7.2) 2 (0.04) 57 (1.1) 95 (1.8) — 1374 (26.5) 30 (0.6) — 61 (1.2) 2012 443 (8.3) 1 (0.02) 94 (1.8) 99 (1.9) — 1499 (28.2) 51 (1.0) — 79 (1.5) 2013 397 (7.4) 2 (0.04) 77 (1.4) 53 (1.0) — 1735 (32.1) 17 (0.3) — 71 (1.3) 2014 435 (8.0) 2 (0.04) 67 (1.2) 63 (1.2) — 1883 (34.4) 17 (0.3) — 50 (0.9) 2015 420 (7.6) 3 (0.05) 45 (0.8) 58 (1.0) — 1988 (35.9) 24 (0.4) — 43 (0.8) *All data are obtained from the Ministry of Health Singapore (MOH, 2007–2016). **Data are not available. A report published by Kondakci and Yuk (2012) gave an over- In spite of that, a small-scale study conducted by Zheng et al. (2014) view of foodborne diseases in Singapore in the past decade from 2001 revealed that 10% (n  =  60) of raw duck wing samples purchased to 2010. The report found a significant rise in non-typhoidal salmo- from local supermarkets were contaminated with Salmonella spp. nellosis from an incidence rate/100 000 population of 3.9 at the start while Lim et al. (2015) reported 33.3% (n = 30) of raw duck wing of the decade to 29.2 at the end. As shown in Table 1, in the new dec- samples being Salmonella positive (Table 2). The discrepancy in the ade starting 2011, the incidence rate of salmonellosis/100 000 popu- prevalence of Salmonella between the two studies could be attrib- lation has been on the rise every year from 26.5 in 2011 to 35.9 in uted to their small sample sizes. Combining the results from both 2015 (MOH, 2012, 2016). Other notable disease of interest reported studies, the overall prevalence of Salmonella spp. in duck wings in was campylobacteriosis which was largely caused by Campylobacter Singapore might be around 18% (n = 90). jejuni with an incidence rate/100 000 population of 1.2 in 2002 and Despite salmonellosis (typhoidal and non-typhoidal) accounting an average rate of 7.7 from 2011 to 2015 (MOH, 2016). for more than 66% of all food- and waterborne diseases reported in An epidemiological news bulletin article published in the last quar- Singapore from 2001 to 2010 (Kondakci and Yuk, 2012) and poul- ter of 2016 investigated the link between the Group B Streptococcus try being a well-known reservoir of Salmonella spp., there is a lack of (GBS) and the consumption of raw fish dishes. A joint investigation published information in the literature on prevalence of Salmonella between the MOH, National Environment Agency (NEA), and AVA spp. in various types of poultry and its role in contributing to the found a significant association between the GBS serotype III ST283 disease burden of salmonellosis in Singapore. More prevalence stud- infections and the consumption of the Chinese raw fish dish Yu Sheng ies involving different types of poultry such as chicken, quail, and (Tan et  al., 2016). Swift measures to ban the consumption of raw turkey in large enough sample sizes are needed to properly assess the freshwater fish in ready-to-eat (RTE) raw fish dishes and stepped up microbiological safety and quality of poultry in Singapore. measures to closely monitor the microbiological safety of salt water fish intended for raw consumption, were also reported. Fruits and Vegetables The Center for Science in the Public Interest (CSPI) reported that Poultry fresh produce (fruits, vegetables and their dishes) such as cucumber, Poultry production in 2016 is forecasted to be at 116.2 million tons; cilantro, cantaloupe, and peppers was the cause of most foodborne accounting for more than 36% of the forecasted total global meat illnesses in the United States with almost 20 000 illnesses over 629 production at 320.7 million tons with Asia at the helm followed outbreaks between 2004 and 2013 (CSPI, 2015). Moreover, vari- by North and South America according to the Food & Agriculture ous surveillance studies have previously described Salmonella spp., Organization (FAO) (Anonymous, 2016). These statistics suggest Escherichia coli O157:H7, Listeria monocytogenes, Staphylococcus that poultry is one of the most important food categories to be moni- aureus, Bacillus cereus, and Aeromonas spp. being isolated from tored for its wholesomeness and safety; especially with respect to fresh produce (Beuchat, 1996; Johnston et al., 2006; De Giusti et al., Salmonella contamination, since poultry has been associated with 2010). Salmonella outbreaks (Foley et  al., 2011). The Centers for Disease The amount of vegetables produced locally in Singapore only Control and Prevention (CDC) in the USA has reported a total of accounts for 8% of consumption (AVA, 2015c). Hence, a staggering 611 cases of human salmonellosis linked to live poultry in eight 92% of all vegetables consumed in Singapore are imported from multistate outbreaks spanning 45 states in the United States in 2016 countries such as Australia, China, and Malaysia. A  total of 388 alone (CDC, 2016). 364 tons of fruits such as watermelons, bananas and oranges were In Singapore, the definition of poultry encompasses domestic shipped to Singapore from countries such as Malaysia, China, and fowl or chickens, ducks, turkey, geese, quails, pigeons, etc. (AVA, the United States in the year 2012 (AVA, 2013, 2015c). Although no 2016). AVA has stringent regulations regarding the import of live major fresh produce-related foodborne outbreaks has been recently poultry into Singapore meant for slaughter and consumption to reported in Singapore, recent shift in tastes and preferences towards uphold the wholesomeness of the poultry consumed in Singapore. high fibre diets due to increased health consciousness (Good, 1998) Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 Food quality and safety: microbiology aspects 3 and the tendency to consume vegetables as RTE food warrants Singapore might be around 4% (n = 104). However, more compre- proper assessment of microbial safety and quality of fresh produce hensive studies covering more varieties of produce and presence of sold in Singapore. other significant pathogens like pathogenic E. coli and L. monocy- A study carried out by Seow et  al. (2012) characterizing the togenes are needed to paint a fuller picture of the microbial quality microbial quality of a total of 125 common fresh fruit and vegeta- and safety of fruits and vegetables in Singapore. ble items sold in Singapore showed that the highest mean aerobic The microbial quality of fruits sold in Singapore is relatively bet- mesophilic count and coliform counts were found in bean sprouts ter as compared to that of vegetables, with 4.0 and 1.1 log CFU/g among all tested items at 8 and 5.7 log CFU/g, respectively (Table 3). being the highest counts found in fruits (mango) for aerobic meso- RTE salad was found to have a mean aerobic mesophilic and coli- philic count and coliform count, respectively, as compared to 8.0 form count of 6.5 and 4.9 log CFU/g, respectively (Table 3). Neither and 5.7 log CFU/g in bean sprouts for the two parameters described E. coli O157:H7 nor Salmonella spp. was isolated from any of the above, respectively (Table 3) (Seow et al., 2012). Fruits are generally samples in the study. expected to have low microbial counts due to the fruits’ peel acting Two other separate studies by Lim et al. (2015) and Zheng et al. as a good biological barrier against microorganisms. Furthermore, (2014) reported a prevalence of Salmonella spp. in bean sprouts as fruits hang high on their trees, keeping them safe from contact with 6.7% (n = 30) and 3.3% (n = 60), respectively. Based on these previ- soil or irrigation water. Under such environments, the numbers of ous studies, the prevalence of Salmonella spp. in bean sprouts sold in microorganisms would be expected to be smaller than other produce Table 2. Prevalence of foodborne pathogens in various food items sold in Singapore. Sample No. of samples % (No.) of confirmed positive samples References Salmonella spp. Escherichia Vibrio spp. coli O157:H7 Poultry Duck wings 30 33.3 (10) —* — Lim et al. (2015) 60 10.0 (6) — — Zheng et al. (2014) Vegetables Carrot 12 0.0 (0) 0.0 (0) — Seow et al. (2012) Lettuce 13 0.0 (0) 0.0 (0) — Seow et al. (2012) Tomato 13 0.0 (0) 0.0 (0) — Seow et al. (2012) RTE salad 13 0.0 (0) 0.0 (0) — Seow et al. (2012) Bean sprouts 14 0.0 (0) 0.0 (0) — Seow et al. (2012) 30 6.7 (2) — — Lim et al. (2015) 60 3.3 (2) — — Zheng et al. (2014) Fruits Apple 14 0.0 (0) 0.0 (0) — Seow et al. (2012) Mango 10 0.0 (0) 0.0 (0) — Seow et al. (2012) Orange 11 0.0 (0) 0.0 (0) — Seow et al. (2012) Seafood Prawn 40 0.0 (0) — 2.5 (1) Huang et al. (2012) Shellfish 31 3.2 (1) — 0.0 (0) Huang et al. (2012) Fishball 32 0.0 (0) — 3.1 (1) Huang et al. (2012) 30 23.3 (7) — — Lim et al. (2015) *Not performed. Table 3. Aerobic mesophilic and coliform counts of various fruits and vegetables sold in Singapore (Seow, 2012). Name of sample Aerobic mesophilic count* Coliform count* n Mean Range n Mean Range Vegetables Carrot 16 4.8 2.6–6.9 12 2.7 1.4–4.9 Lettuce 17 5.8 3.4–7.0 13 4.2 1.6–5.5 Tomato 18 4.2 2.4–5.5 13 2.1 0.3–3.0 Bean sprouts 19 8.0 7.3–9.1 14 5.7 4.1–6.3 RTE salad 13 6.5 5.8–7.3 13 5.2 4.2–5.9 Fruits Apple 18 3.4 2.1–5.1 14 0.1 ND**–1.2 Mango 11 4.0 3.0–5.1 10 1.1 ND–2.5 Orange 13 3.4 1.6–4.4 11 0.9 ND–2.1 *All units are in log CFU/g.**Not detected. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqs/fyx016/3798234 by Ed 'DeepDyve' Gillespie user on 04 May 2018 4 Y. H. Zwe and H. G. Yuk commodities. It was also suggested that the higher surface area of could be due to the different preparation procedures of fishball vegetables as compared to fruits made the former more susceptible (handmade or machine processed) and differences in the type of to bacterial contamination and adhesion (Aycicek et al., 2006). No market the samples were purchased from (wet markets or super- E. coli O157:H7 and Salmonella spp. contamination were found in markets). The overall prevalence of Salmonella spp. in fishball sold the 35 fruit items sampled in the study (Table 2). in Singapore might be around 11.3% (n = 62) based on these two studies. Seafood Conclusion Seafood is an important food source for a large segment of the world population and is widely consumed as a delicacy in many parts of Despite continuous efforts by the government to curb foodborne Asia (Huang et  al., 2012; Yaashikaa et  al., 2016). Seafood is sus- illnesses, it still remains as one of the most pressing public health ceptible to microbial contamination and pathogens may be present issues to be solved. Based on currently published data, a high overall in low levels at harvest while more may be introduced during han- prevalence of Salmonella spp. was found in duck wings (18%) fol- dling and processing. Risk of foodborne illness by consumption of lowed by fishballs (11%) and bean sprouts (4%) but no Salmonella seafood increases further if the food is mishandled by unsanitary spp. and E. coli O157:H7 were isolated from fruits and vegetables. practices where pathogens can multiply exponentially due to tem- Although some previous studies indicated that foods being sold in perature abuse conditions (Adams and Moss, 2000; Badrie et  al., Singapore are contaminated with some pathogenic bacteria, addi- 2006; Espiñeira et al., 2010; Bakr et al., 2011). tional prevalence and characterization work should be performed In Singapore, seafood is defined as including any variety of fishes, to further establish and determine the significance of this exposure crustaceans, aquatic mollusks, marine sponges, and any other form to the national disease burden. Meanwhile, continuous efforts are of aquatic life including their young and eggs harvested from brack- needed to educate food handlers and consumers on proper handling ish, marine, or fresh water (AVA, 2015b). Seafood-borne disease has and thorough cooking of food to prevent the risk of foodborne received increased attention ever since the 2009 Vibrio parahaemo- illnesses. lyticus outbreak associated with consumption of Indian Rojak from Conflict of interest statement. None declared. cross contamination with seafood resulting in many cases of illness, hospitalization, and two deaths (MOH, 2009). References A study on microbial quality of 116 seafood samples sold in Singapore reported that the mean aerobic mesophilic counts for Adams, M. R., Moss, M. O. (2000). Bacterial agents of foodborne illness. In Adams M. R., Moss M. O. (eds.), Food Microbiology, vol2. London: prawns, shellfish, and fishballs ranged between 4.6 and 6.6 log Royal Society of Chemistry. 184–271. CFU/g (Table 4). 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Food Quality and SafetyOxford University Press

Published: May 4, 2017

References