Microbiological Evaluation of Stuffed Mussels
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616 Journal of Food Protection, Vol. 71, No. 3, 2008, Pages 616–620 Copyright ᮊ, International Association for Food Protection Research Note Microbiological Evaluation of Stuffed Mussels DUYGU KIS¸LA* AND YASEMI˙NU¨ ZGU¨ N Department of Fishing and Fish Processing Technology, Ege University, Bornova,˙ Izmir, 35100, Turkey MS 07-436: Received 21 August 2007/Accepted 16 November 2007 ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/3/616/1681876/0362-028x-71_3_616.pdf by guest on 28 September 2021 Stuffed mussel is a traditional food, sold by street vendors in coastal parts of Turkey and other Mediterranean countries. In the present study, the microbiological quality of not only the stuffing mixture, but also the outer surface of the stuffed mussels was evaluated for 1 year, and the effect of the ambient temperatures on the prevalence and the count levels of the microorganisms were evaluated. Fifty samples (750 stuffed mussels in total) were collected periodically, and microbiological analyses were performed by standard procedures for aerobic plate count, coliforms, fecal coliforms, Enterobacteriaceae, Staph- ylococcus aureus, Bacillus cereus, and Vibrio spp. Aerobic plate counts above 5 log CFU/g were obtained in 16 and 72% of stuffing mixture samples at high and low ambient temperatures, respectively, and average aerobic plate counts of outer surface samples at high and low ambient temperatures were 3.21 and 4.34 log CFU/ml, respectively. The prevalence and the count levels of coliforms, fecal coliforms, Enterobacteriaceae, and Vibrio spp. (except for the prevalence of Vibrio spp. in stuffing mixture samples) in the samples at high ambient temperatures were considerably higher compared with those at low ambient temperatures (P Ͻ 0.05). High frequencies of pathogens S. aureus and B. cereus were found in stuffing mixture samples at high ambient temperatures, with averages of 2.84 and 2.94 log CFU/g, respectively (P Ͻ 0.05). The result of this investigation indicates that stuffed mussels as a street food may constitute a potential health hazard, especially at high ambient temperatures, depending on contamination level and lack of sanitary practices, and therefore, handling practices should require more attention and improvement. Stuffed mussel is a traditional food, sold by street ven- storage practices. Street fast foods are exposed to environ- dors in coastal parts of Turkey and other Mediterranean mental conditions, such as the presence of insects, flies, and countries. Mytilus galloprovincialis, known as the black dust. Furthermore, most street food vendors ignore good mussel in Turkey, is mostly used for preparation of stuffed food handling practices, exposing foods to unsafe condi- mussels. Although there are many seafood recipes under tions, such as cross-contamination, unhygienic storage, and the same name in some parts of the world, the preparation poor time–temperature conditions (12, 23, 25). Due to high of the stuffed mussels sold in Turkey is different from the levels of pathogenic bacteria, they have been implicated in others. In the production of stuffed mussels, mussel shells several outbreaks of foodborne diseases worldwide (4, 5, are cleaned well by scraping with a knife, and any beards 7, 10, 13, 15, 24, 33). are removed. A prepared mixture of rice, vegetable oil, salt, Generally, mobile street food sellers and stationary and spices is stuffed into each shell, including mussel flesh, food sellers sell the stuffed mussels on a table by the side- and shells are closed tightly before cooking by steaming. walks. The stuffed mussel sellers carry out their operations Vegetable oil is sprayed on the shells of stuffed mussels so in the ambient conditions for 6 to 8 h or more each day. they appear shiny before selling. Recently, there has been The consumer uses the mussel shell itself as a spoon to an increase in the selling of stuffed mussels in different take the stuffing out of the shell and scoop it to the mouth. food shops (delicatessens, restaurants, supermarkets) in In this case, the shell of the stuffed mussel is the critical Turkey. point for the potential health risk in addition to the stuffing Street food is defined by the Food and Agriculture Or- in the shell. Moreover, leftover stuffed mussels are gener- ganization (14) as ‘‘ready-to-eat foods and beverages pre- ally taken home at the end of the day and stored at ambient pared and/or sold by street vendors and hawkers, especially temperature, or sometimes in the refrigerator until the next in the street or other similar public places.’’ Familiarity, day. taste, low-cost, and convenience are some of the appealing To date, there are limited studies regarding the micro- factors that make street foods popular as food source, but biological quality of stuffed mussels sold in Turkey (9, 30), they may also present risks to people’s health (31). The and these studies did not take into consideration of the shell safety of street foods is affected by several common factors, of the stuffed mussel as a critical point for the potential from the quality of the raw materials to food handling and health risk. Because of lack of information on the incidence * Author for correspondence. Tel: ϩ90-232-3434000, Ext 5228; Fax: of foodborne diseases related to stuffed mussels and ab- ϩ90-232-3883685; E-mail: [email protected]. sence of microbiological standards for stuffed mussels, this J. Food Prot., Vol. 71, No. 3 MICROBIOLOGICAL QUALITY OF STUFFED MUSSELS 617 TABLE 1. Counts of microorganisms in stuffed mussel samples purchased at low and high ambient temperatures, in I˙zmir, Turkeya Low ambient temp High ambient temp Analysis SM (n ϭ 25) OS (n ϭ 25) SM (n ϭ 25) OS (n ϭ 25) APC 3.45 Ϯ 1.42 (1.30–7.18) 3.21 Ϯ 1.7 (0–6.85) 5.83 Ϯ 1.22 (3.62–7.4) 4.34 Ϯ 1.08 (2.53–6.59) Enterobacteriaceae 1.51 Ϯ 2.3 (1.3–7.08) 0.57 Ϯ 0.97 (1.18–3.9) 2.03 Ϯ 1.94 (1.30–5.79) 1.61 Ϯ 1.54 (1.23–4.26) S. aureus 0.44 Ϯ 1.11 (Ͻ2–4.36) 0.84 Ϯ 1.08 (Ͻ1–3.32) 2.84 Ϯ 2(Ͻ2–5.89) 3.11 Ϯ 0.89 (1.6–4.91) B. cereus 0.84 Ϯ 1.6 (Ͻ2–5.32) NA 2.94 Ϯ 1.84 (Ͻ2–5.28) NA a Values are arithmetic mean Ϯ standard deviation (range of values). SM, stuffing mixture (log CFU per gram); OS, outer surface (log CFU per milliliter); NA, not analyzed. Њ study was conducted to assess the microbiological quality cose agar (LAB-M, Lancashire, UK) after 24 h incubation at 37 C Downloaded from http://meridian.allenpress.com/jfp/article-pdf/71/3/616/1681876/0362-028x-71_3_616.pdf by guest on 28 September 2021 of stuffed mussel sold by street vendors in I˙zmir, Turkey. (17). Presumptive colonies were confirmed by oxidase test and Additionally, the effect of ambient temperatures on the anaerobic fermentation of glucose (using glucose salt agar) test. prevalence and the count levels of microorganisms in S. aureus was determined by surface plating 0.1 ml of dilutions Њ stuffed mussels was also investigated. on Baird-Parker agar (Oxoid) and incubating plates at 37 C for 48 h (2). Typical colonies were tested for coagulase production, MATERIALS AND METHODS confirmed by using coagulase rabbit plasma (Difco, Becton Dick- inson), and counted. For B. cereus determination, serial dilutions Stuffed mussels and sample collection. Fifty samples, 25 were surface plated on mannitol–egg yolk–polymyxin agar (Ox- of which at low ambient temperatures (autumn and winter months) oid) (2). The plates were incubated at 37ЊC for 24 h and reincu- and 25 of which at high ambient temperatures (spring and summer bated for another 24 h if there was no visible growth. All gram- months) were purchased from street vendors periodically in a year positive rods were confirmed by anaerobic fermentation of glucose in I˙zmir, Turkey. Each sample represents an average of the results (using modified Hugh Leifson’s medium), gelatin hydrolysis, and from 15 stuffed mussels purchased from three street vendors (5 nitrate reduction tests. Vibrio spp. enumeration was determined stuffed mussels from each street vendor; see below for sample by MPN method by considering turbidity of alkaline peptone wa- preparation) within a week; thus, 750 stuffed mussels in total were ter (3% NaCl, pH 8.6) tubes at 37ЊC for 16 to 18 h. A loopful collected in a year. Stuffed mussels were collected in the afternoon from alkaline peptone water tubes was then streaked onto thio- (roughly 5:00 p.m.) from mobile street vendors or stationary street sulfate–citrate–bile salt sucrose agar (Oxoid), and the plates were vendors with or without shelter, and then they were placed in incubated at 37ЊC for 24 h (8). Confirmation of Vibrio spp., ox- sterile plastic bags, surrounded with ice packs, and transported idase test, and anaerobic fermentation of glucose (using modified immediately to the laboratory. Hugh Leifson’s medium including 25 g NaCl/liter) test were car- Sample preparation. Five stuffed mussels from each street ried out. vendor were aseptically removed from the plastic bags and placed on a sterile filter paper. Both sides of outer surfaces of the stuffed pH analysis. A slurry was made combining distilled water mussels were swabbed using sterile swabs moistened with 0.1% and stuffing mixture sample at a ratio of 1:1. The mixture was peptone water (Difco, Becton Dickinson, Sparks, Md.), and then homogenized by stomacher for 1 min, and the pH was measured swabs were transferred into the test tubes containing 10 ml of with a microprocessor-based pH meter (model pH 211, Hanna 0.1% peptone water.