Microbiological Evaluation of Stuffed Mussels

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˙ Izmir, 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˙ Izmir, 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. Each stuffing mixture was aseptically re- Instruments, Germany). moved from the shells, mixed, and a 10-g portion was transferred into 90 ml of sterile 0.1% peptone water. The mixture then was Statistical analyses. The Mann-Whitney U test was used for homogenized by stomacher (IUL Instruments, Barcelona, Spain) statistical evaluations of the bacterial counts, and pH values at the for 1 min for all microbiological analysis except the Vibrio spp. level of P Ͻ 0.05. ␹2 tests were used to determine whether sta- count, for which a 10-g portion was added to 90 ml of sterile tistically significant differences (P Ͻ 0.05) existed between the 0.1% peptone water containing 3% NaCl. After serial dilutions in prevalence of coliforms, fecal coliforms, and Vibrio spp. at low 0.1% peptone water, the solutions were plated on the respective and high ambient temperatures (29). agar media for enumerations of aerobic plate count (APC), coliforms, fecal coliforms, Enterobacteriaceae, S. aureus, and B. ce- RESULTS AND DISCUSSION reus (only for stuffing mixture samples). Average minimum and maximum temperatures during Microbiological analyses. APC was determined by using analysis period ranged between 10.8 and 18.9ЊC at low am- pour plate method on plate count agar (PCA; Oxoid, Basingstoke, bient temperatures, and 17 and 27.1ЊC at high ambient tem- UK). Plates were incubated at 30ЊC for 48 h and enumerated (16). peratures, respectively (11). The results from microbiolog- Coliforms and fecal coliforms were enumerated by the three-tube ical analyses of stuffed mussels, including stuffing mixture most probable method (MPN) (16), for which lauryl sulfate broth and outer surface samples, at low and high ambient tem- (LSB; Oxoid) and EC broth (Merck, Darmstadt, Germany) were peratures are shown in Tables 1 and 2. Statistically signif- used, respectively. Confirmations of coliforms and fecal coliforms icant increases (P Ͻ 0.05) were determined in the preva- were performed by transferring gassing LSB tubes to brilliant ␹2 ϭ green bile 2% broth (Difco, Becton Dickinson) tubes, and streak- lence (coliforms—stuffing mixture 18.48, outer sur- 2 2 ing EC broth tubes onto eosin methylene blue agar (Difco, Becton face ␹ ϭ 20.5; fecal coliforms—stuffing mixture ␹ ϭ 12; Dickinson), respectively. Enterobacteriaceae count was deter- outer surface ␹2 ϭ 21.34; Vibrio spp.—outer surface ␹2 ϭ mined by double-layer pour plate method on violet red bile glu- 25.96), except for Vibrio spp. in stuffing mixture samples 618 KIS¸LA AND U¨ ZGU¨ N J. Food Prot., Vol. 71, No. 3

TABLE 2. Prevalence of coliforms, fecal coliforms, and Vibrio spp. 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)

Coliforms 7 (28) (Ͻ0.48 to Ͼ3.15) 5 (20) (ϽϪ0.52 to Ͼ2.15) 22 (88) (Ͻ0.48 to Ͼ3.15) 21 (84) (ϽϪ0.52 to Ͼ2.15) Fecal coliforms 4 (16) (Ͻ0.48 to Ͼ3.15) 2 (8) (ϽϪ0.52 to Ͼ2.15) 16 (64) (Ͻ0.48 to Ͼ3.15) 18 (72) (ϽϪ0.52 to Ͼ2.15) Vibrio spp. 4 (16) (Ͻ0.48 to Ͼ3.15) 3 (12) (ϽϪ0.52 to Ͼ2.15) 10 (40) (Ͻ0.48 to 2.3) 21 (84) (ϽϪ0.52 to Ͼ2.15) a Values are number (percentage) of positive samples (range of values). SM, stuffing mixture (log CFU per gram); OS, outer surface (log CFU per milliliter). 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 (P Ͼ 0.05, ␹2 ϭ 3.58) and the bacterial counts at high Nigeria, available data indicated that most of the street ambient temperatures. foods carried high levels of APCs, ranging between nearly 4 and 9 log CFU/g, and coliforms ranging between nearly APCs. The APC of ready-to-eat foods reflects the mi- 2 and 6 log MPN/g (12). The frequency of fecal contami- crobial content of the ingredients, effectiveness of process- nation (Ͼ0.48 log MPN/g) of street foods in Latin Amer- ing, and sanitary conditions during handling, preparation, ican cities ranged from 9.4 to 56.7% (1). In the study from and storage (20). Sixteen percent (4 of 25) and 72% (18 of Turkey, 52% of stuffing mixture samples were above 2 log 25) of stuffing mixture samples at low and high ambient MPN/g for coliforms, and 45% of stuffing mixture samples temperatures, respectively, were found higher than the per- were above 1.6 log MPN/g for fecal coliforms (30). Han- missible level (5 log CFU/g) for any cooked ready-to-eat ashiro et al. (15) reported that fecal coliforms (Ͼ0.48 log foods and delicatessen products (2, 12). Tatlısu (30) re- MPN/g) were detected in 55% of the street foods samples. ported that 63% of stuffing mixture samples exceeded the In the present study, it was observed that most of the permissible level for APC, whereas almost all the APCs of stuffed mussel vendors ignored good food handling, and stuffing mixture samples examined in the study carried out stuffed mussels were commonly exposed to aggravating en- by Ç olakog˘lu et al. (9) were higher than the permissible vironmental conditions by the street vendors, such as soil, level, ranging from 4.99 to 7.32 log CFU/g. In the studies dust, insects, flies, etc. Furthermore, Karapınar and Tunçel from Nigeria and Philippines (3, 33), most of the counts (22) stated that the microbial load of spices, the basic in- from ready-to-eat foods and beverages purchased from gredient in the production of stuffed mussels, sold in I˙zmir street vendors were lower than the permissible level for was high, and they were contaminated with fecal coliforms. APC. On the other hand, the prevalence of samples unsuitable for human consumption, using a maximum APC Enterobacteriaceae counts. High Enterobacteriaceae (5 log CFU/g), ranged from 5.1 to 39.8% of different type count indicates the possible contamination from raw ma- of street foods sold in Trinidad and Tobago (24). In Johan- terial, dirty utensils, and equipments after the inadequate or nesburg, the quality and safety of street foods analyzed in unsuitable processing of food, and recontamination due to the study was considered acceptable based on relatively low the lack of unsanitary food practices (21). In the present bacterial counts and comparatively low incidences of food- study, Enterobacteriaceae was detected in 40% (10 of 25) borne pathogens (27). and 60% (15 of 25) of stuffing mixture samples, and 32% (8 of 25) and 60% (15 of 25) of outer surface samples at Coliform and fecal coliform counts. The presence of low and high ambient temperatures, respectively. The high- coliforms in ready-to-eat foods indicates unhygienic con- est count (7.08 log CFU/g) was observed in one stuffing ditions during processing, handling, and distribution or mixture sample at low ambient temperature. The average postprocessing contamination (20). As shown in Table 2, Enterobacteriaceae count of 2 log CFU/g for ready-to-eat coliforms were not detected in 72% (18 of 25) of stuffing street foods in Johannesburg was determined (26), whereas mixture samples and 80% (20 of 25) of outer surface sam- in another study carried out in the same city, the average ples at low ambient temperatures, whereas they were de- Enterobacteriaceae count of different type of selected street tected in most of the samples analyzed at high ambient foods from two street vendors was found between 1 and temperatures. Twenty percent (5 of 25) and 40% (10 of 25) 3.9 log CFU/g (27). High frequency of Enterobacteriaceae of stuffing mixture samples at low and high ambient tem- in the samples in the present study might have resulted from peratures, respectively, were found to be contaminated with lack of hygienic practices during preparation and handling coliforms higher than 2 log MPN/g, a permissible level for of stuffed mussels, and holding them at high ambient tem- delicatessen products (12). The presence of fecal coliforms peratures for over 6 h. indicates the lack of good hygienic practices and possible presence of enteric pathogens (21). Fecal contamination Pathogens. The presence of S. aureus indicates im- was detected in 40% (20 of 50) of each stuffing mixture proper handling and possible cross-contamination, and hu- and outer surface samples in the present study (Table 2). mans are the major source of this bacterium (18). B. cereus In total, 14% (7 of 50) of stuffing mixture samples analyzed is widely distributed in nature and is readily isolated from contained fecal coliforms greater than 3.15 log MPN/g. In soil, dust, and vegetation (18). Its presence in high counts J. Food Prot., Vol. 71, No. 3 MICROBIOLOGICAL QUALITY OF STUFFED MUSSELS 619 suggests a potential risk to the consumer due to the pro- ambient temperatures was very close to the permissible lev- duction of toxins associated with food poisoning (21). In el (32). the present study, the frequencies of contamination by coagulase-positive S. aureus were 30% (15 of 50) and 96% Vibrio spp. counts. As shown in Table 2, Vibrio spp. (43 of 50) of the samples analyzed at low and high ambient were detected in 16% (4 of 25) of stuffing mixture samples temperatures, respectively. It was mostly detected in the at low ambient temperatures, and in 40% (10 of 25) of the outer surface samples regardless the ambient temperatures. samples at high ambient temperatures. The difference was Ͼ B. cereus was detected in 28% (7 of 25) of stuffing mixture not statistically significant (P 0.05). This genus was de- samples at low ambient temperatures, whereas it was pres- tected at most in outer surface samples at high ambient ent in 76% (19 of 25) of stuffing mixture samples at high temperatures. Vibrio spp. are halophilic microorganisms, ambient temperatures. In a study carried out in Nigeria on which have been isolated from freshly caught seafood prod- Њ street food contamination, none of the samples from mobile ucts (16). If adequate heat (60 C/15 min) is applied to the food vendors was contaminated with S. aureus; those from seafood during the processing, it is enough to kill Vibrio 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 stationary vendors, without shelter, had the highest fre- spp. present in the raw material (16). In the present study, quency of contamination by S. aureus (26.3%) and B. ce- detection of Vibrio spp. in the samples regardless of tem- reus (32.9%) (33). In a study carried out in Gaborone, the perature indicated that there might be inadequate cooking B. cereus contamination rate for street food samples was process and/or cross-contamination between the raw mate- 65%, ranging from a not-detectable level to levels as high rial and the finished product by the means of utensils used as 9.1 log CFU/g (28). B. cereus was detected in 17% and by the street vendors. Ͻ S. aureus in 3% of the selected street food samples in South Statistically significant difference (P 0.05) was ob- Africa (27). Hanashiro et al. (15) reported that B. cereus served between the pH values of the samples at low and was present in 12.5% of the popular street foods in Brazil high ambient temperatures. The range of pH values of stuff- in counts above 3 log CFU/g, and S. aureus was found in ing mixture at low ambient temperatures was between 6.34 Ϯ 2.5% of the samples in counts above 3 log CFU/g. In the and 7.06 (average 6.77 0.18) and between 5.83 and 6.98 Ϯ study carried out by Ç olakog˘lu et al. (9), S. aureus counts (average 6.41 0.37) for high ambient temperatures (data of stuffing mixture samples ranged from 1 to 4 log CFU/g. not shown). The range of pH values was suitable for the Spices and rice, the main added materials in the production growth of most of the microorganisms implicated in food- of stuffed mussel, may be contaminated with spore-forming borne diseases (21) regardless the ambient temperatures. (B. cereus, Clostridium perfringens), non–spore-forming Based on the high bacterial levels and the prevalence (Salmonella, Escherichia, Shigella) bacteria and molds ca- of foodborne pathogens (especially at high ambient tem- pable of synthesizing mycotoxins (19). Although the temperatures), the quality and the safety of the stuffed mussels perature used in cooking the stuffed mussels is always high analyzed in the present study was shown to be unacceptable to kill most vegetative cells, the resistant spores may sur- for human consumption. This investigation also indicated vive and the number of the spore-formers increases when that the outer surface of the stuffed mussels in addition to foods are held at ambient temperature for several hours. It the stuffing mixture might constitute a potential health haz- was found that when rice and related foods were held at ard, depending on the contamination level and lack of san- room temperature for4horlonger, high numbers of bac- itary practices, because the shell is used as a spoon by the teria developed during this interval (6, 13). Since the consumers. As a control measure, it could be suggested that stuffed mussels are generally prepared in bulk and dis- street vendors might sell the stuffed mussels in a cooler, played for a whole day (more than 6 h) for sale at ambient especially at high ambient temperatures. Primarily, it is im- temperature, the presence and the counts of S. aureus and portant that there is a need to enforce regulations on sani- B. cereus besides the other bacterial counts in the samples, tary practices during preparation and sale of stuffed mussels at high ambient temperatures were found considerably through the education of the street vendors (covering their higher than those counts at low ambient temperatures (Ta- heads, wearing aprons, avoiding handling stuffed mussels ble 1). The present study indicated that the major source of and money simultaneously, or handling stuffed mussels S. aureus was probably the food handlers, because at the with bare hands, etc.), employing the hazard analysis crit- point of sale, regular contact was observed with the stuffed ical control point system as a strategy to prevent contami- mussels by both the street vendors and buyers. Presence of nation. B. cereus in the samples was ascribed to its presence in the ACKNOWLEDGMENT spices and/or rice in spore form that survived during cooking and germinated during holding. According to the mi- The financial support of Ege University, Science and Technology crobial criteria in Turkish Food Codex for ready-to-eat and Research Center is gratefully acknowledged. delicatessen foods, B. cereus and S. aureus counts should REFERENCES not be above 3 log CFU/g and 2 log CFU/g, respectively (32). In the present study, the average S. aureus count of 1. Almeida, C. R., D. M. T. Schuch, D. S. Gelli, J. A. S. Cuellar, A. stuffing mixture at high ambient temperatures was above V. R. Diez, and J. A. Escamilla. 1996. Microbial contamination of street foods sold in Latin America and socioeconomic characteristics the microbial criteria stated in Turkish Food Codex, but it of their vendors and consumers. PAHO/WHO/INPPAZ, OPS/HCP/ was below the permissible level at low ambient tempera- HCV/FOS/96.22. tures. 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