Çankaya Üniversitesi Fen-Edebiyat Fakültesi, Journal of Arts and Sciences Sayı: 12 / Aralık 2009

Comparison of the Microbiological Quality of Packed and Unpacked Ice Creams Sold in Bursa, Turkey

Gülben Erman Çağlayanlar1, Buket Kunduhoğlu2**, Nafi Çoksöyler3

In this study microbiological quality of packed (industrially produced, n=44) and unpacked (patisserie product, n=48) ice creams sold in Bursa, Turkey were compared. Total aerobic mesophilic bacteria (TAMB), yeast and mold counts in packed ice cream samples varied between 2.7x101–6.9x102, <10–1.0x101, and <10–2.0x101 cfu/g, respectively. Coliforms and Escherichia coli counts of the same samples were <10 cfu/g. In unpacked samples TAMB, coliforms, E. coli, yeast and mold counts ranged between 8.1x101–1.0x106, <10–2.4x103, <10–8.4x102, <10–1.5x105, and <10–1.2x103 cfu/g, respectively. Listeria monocytogenes, Staphylococcus aureus, and Salmonella spp. were not detected in any of the samples tested. All of packed samples conformed to Turkish Food Codex (TFC). In terms of TAMB, coliforms, E. coli, yeast and mold, percentage of the unpacked samples did not conform to TFC were 9.1%, 50.1%, 63.6%, 22.7% and 36.4%, respectively. Results showed that ice creams produced in patisseries in Bursa had poor microbiological quality. Application of the HACCP system for ice cream production should become legally mandatory to improve the product quality. Keywords. Microbiological quality, Plain ice cream, Flavored ice cream.

* Bu makale, birinci yazarın Yüksek Lisans tezinin bir bölümüdür ** Yazışmalardan sorumlu yazar / Corresponding author; E-mail: bkunduh@ogu.edu.tr

1 Graduate School of Natural and Applied Sciences, Eskisehir Osmangazi University, Eskisehir, Türkiye 2 Faculty of Science and Arts, Department of Biology, Eskisehir Osmangazi University, 26480 Eskisehir, Türkiye 3 Food Engineering Department, Faculty of Agriculture, University of Yüzüncü Yıl, 65080 Van, Türkiye


1996.7 ve %36. n=48) dondurma örneklerinin mikrobiyolojik kalitesi karşılaştırılmıştır.4’ü TAMB. Turkey Özet paketlenmemiş (pastanelerde üretilmiş. ve <10–1.1.0x101. and long storage period of ice cream. Çeşnili dondurma. <10–1. cones. Kanbakan and Çon. Bursa’da (Türkiye) satışa sunulan paketlenmiş (endüstriyel olarak üretilmiş. Marshall and Arbucle.7x101–6. Digrak and Özcelik. Other ingredients include flavoring matters and water. milk solids other than fat. 2000. 1994. maya ve küf sayısı. It is produced by freezing pasteurized mixture of milk. 2000). emulsifiers. Contamination of ice creams by pathogenic microorganisms at some processing steps resulted in several disease outbreaks in numerous countries of Asia. The microbiological quality of ice cream during retail marketing mainly depends upon the post production handling of the product. maya ve küf sayıları bakımından TGK kriterlerine uygun değildir. coli. <10–1.Comparison of the Microbiological Quality of Packed and Unpacked Ice Creams Sold in Bursa. 1991. 8. Dondurma üretiminde HACCP sistemi uygulamasının yasal olarak zorunlu kılınması ürün kalitesini arttıracaktır.. Ice cream is one of the major product of the dairy industry and continues to dominate the interest of large segments of the population. 2. a milk-based product. Anahtar kelimeler: Mikrobiyolojik kalite. 1996. 2000). almost neutral pH value (~pH 6–7).4x102. Türk Gıda Kodeksi’nin (TGK) kriterlerine uygundur. Bursa’daki pastanelerde üretilen dondurmaların mikrobiyolojik kalitesinin düşük olduğunu göstermiştir.. koliform... Djuretic et al. %50. <10–2. cream. n=44) ve Paketlenmiş dondurma örneklerindeki toplam aerobik mezofilik bakteri (TAMB). Europe. Aynı örneklerdeki koliform ve kob/g arasında değişmiştir. 1998. the open variety being distributed manually in scoops. Erol et al. Paketlenmemiş örneklerin sırasıyla %9. Sonuçlar. Paketlenmemiş örneklerdeki TAMB.4x103. Digrak et al.. Sade dondurma. transportation and storage.ye rastlanmamıştır. 1992. Staphylococcus aureus Ice cream. maya ve küf sayıları sırasıyla. sırasıyla Escherichia coli sayısı ise <10 kob/g olmuştur. coli. It is sold in packages or in open containers at retail outlets/ice cream parlors.0x106. Fruits.2x103 ve Salmonella spp. in addition to the efficiency and sanitary conditions during frozen storage. Paketlenmiş örneklerin tamamı. Test edilen örneklerin hiçbirinde Listeria monocytogenes. Bu çalışmada. 94 1.5x105.6. During production.1. candies and syrups are optionally added into ice cream for flavor enrichment. In previous studies. 1997). E. 2002. Evrensel and Gunes. <10–8. 1998. it may become contaminated with several microorganisms. %22..0x101 kob/g arasında değişmiştir. nuts. and North America (Chug.. koliform. Farrag and Marth. <10–2. sugars. Warke et al. is a good media for microbial growth due to high nutrient value. it is required to be microbiologically safe (Warke et al. 2005. %63. and stabilizers. E. Daniels et al. Introduction .1x101–1. or sundaes across the counter (Champagne et al.9x102. As most of the ice cream consumers are children of vulnerable age groups. high microbial loads in ice cream samples obtained from patisseries in Turkey have been reported (Coskun.

Results of this study may help (a) to compare microbiological quality of industrially produced-packed ice cream with ice cream produced in patisseries and sold unpacked. there are only a few studies about industrially produced ice cream sold in retail stores in Turkey (Bostan and Akin... 1994. 2006). 2. and Staphylococcus aureus. Patir et al. belonging to two different brands) were purchased from retail stores and 48 open ice cream samples were purchased from 3 different patisseries (from June to August 2003) in Bursa city. Yaman et al. monocytogenes. 2005. 2005). Nafi ÇOKSÖYLER 1999. violet red bile agar (VRBA. ice 95 Enumeration and isolation methods .. using overlay method). Also. VRBA and CCA plates were incubated at 37 ºC for 24 h. Korel et al.. 1997. it was observed that most of the ice cream samples obtained from patisseries did not conform to TFC (2001) in mentioned studies. Industrial ice cream producers and patisseries were represented by the letters A and B for the former and C-E for the latter groups. Kivanc et al. yeast extract-glucose-chloramphenicol agar (YEGCA). yeast and mold. PCSMA plates were incubated at 35 ºC for 48 h. cocoa.. (b) to understand the difference in the microbiological qualities between flavored and plain ice creams. fruits.. Samples were divided into two categories: plain and flavored (with nuts.1. Materials and Methods 2. 2. for enumeration of total aerobic mesophilic bacteria (TAMB). Escherichia coli. respectively.). and BPA plates were incubated at 37 ºC for 48 h.1. Korel et al. and (c) to understand whether there is any improvement in the microbiological quality of ice cream offered for public consumption by making comparisons with previous researches. Buket KUNDUHOĞLU. This study has been carried out in Bursa to determine the microbiological quality of ice cream offered for public consumption. and Baird-Parker agar (BPA).Gülben ERMAN ÇAĞLAYANLAR. To isolate L. The samples were transported in a freezer bag and analyzed within 3 h after collection. Nevertheless. Producers and stores were chosen randomly. Materials Ice cream samples A total of 44 industrially produced ice cream samples (packed. chromocult coliform agar (CCA). coliform bacteria. Sezgin et al. 2002.1. Methods Ten g of ice cream sample were diluted with 90 ml sterile peptone water in a conical flask containing glass beads. chocolate etc. 2006. Three serial dilutions were plated in duplicates onto plate count skim milk agar (PCSMA). Ozcan and Kurdal. YEGCA plates were incubated at 30 ºC for 48–72 h. 1997.

coliform bacteria. respectively.1x104 cfu/g. Differences between the log10 values were statistically compared by the Pearson’s correlation coefficient analysis. samples that do not comply with TFC (2001) are evaluated. TAMB. type of product (plain ice cream/flavored ice cream). 1992). TAMB. respectively. in their study. respectively. and 103 and 2x104 cfu/ml. was carried out by a two-step enrichment procedure in lactose broth and selenite cystine broth (37 ºC for 24 h). Evaluations conducted according to manufacturing type (manufactured industrially-packed type/ manufactured in patisseries-unpacked type). an inoculum from the LEB was plated onto Palcam Listeria selective agar and the plates were then incubated at 30 ºC for 24–48 h. (2004) investigated the microbiological quality of 72 ice creams from 12 different factories in Kathmandu.1. 96 . and Staphylococcus spp. After 48 h incubation at 30 ºC. aureus. and between 4 and 42 cfu/ml. and different producers (factory/ patisserie) are provided in Tables 1 to 3.0x102 and 2. respectively. (2002) reported higher TAMB and coliform counts in packed ice cream than that found in this study. Suspected colonies were then identified using standard bacteriological procedures (Ice Cream Standard. They could not isolate E. 3. Results and Discussion Findings obtained from the microbiological analysis of ice cream samples are categorized into three groups. and brilliant green agar. Statistical analysis Plate-count data were transformed into logarithms before statistical treatment. and coliform counts of packed samples ranged between 1. from the samples tested. bismuth sulfite agar.8 x 103 and 5. and Salmonella spp. and 0 and 9. In our study. Germany.7x103 cfu/g.3x107 cfu/ml. TAMB and coliform counts ranged between 2. They isolated only one Salmonella spp. coli. All plating and enrichment media were purchased from Merck.Comparison of the Microbiological Quality of Packed and Unpacked Ice Creams Sold in Bursa. <10 and 1. In their study. the microbiological load of the industrially produced and packed ice cream samples were lower compared to the findings of Bostan and Akin (2002). varied between 103 and 1.6 x 104 cfu/ml. Microbiological quality of packed and unpacked ice creams The microbiological qualities of packed and unpacked ice cream are shown in Table 1. yeast-mold. Turkey cream samples (25 g) were added into Fraser Listeria selective enrichment broth (LEB). Statistical analysis was carried out using the SPSS software. 3. Detection of Salmonella spp. In Table 4. S.52x108 cfu/ ml. 103 and 1. ��������������������������������� Joshi���������������������������� et al.3 MPN/g. followed by streaking on Salmonella-Shigella agar. M-E-Elahi et al.

4. (2006).Gülben ERMAN ÇAĞLAYANLAR. 22. ��� ElSharef et al..5x10 cfu/g (Kivanc et al.. 103 to 1. 1994.. 1998.. Korel et al. (2000) isolated L. El-Sharef et al. and 29% by Patir et al. coli was found in 29.. Evrensel and Gunes. Some researchers reported S. Kanbakan et al. (2000). Erol et al. were not detected in any of the 92 ice cream samples tested.5x105 <10 – 1. Kivanc et al. 2005.0x101 Total (n = 92) 2. Erol et al.. ����������������������������������� (2005) reported isolation rates of Salmonella spp. and the counts varied between 10 and 8. Ozcan and Kurdal.2x103 Minimum number of microorganisms Maximum number of microorganisms The range of TAMB counts in the patisserie sample was 8. monocytogenes. (1998). The ratio of samples containing E. 6% by El-Sharef et al. coli from 2% of coliform-containing samples (0. Warke et al.4x103 cfu/g). (2006).0x101 <10 – 2.0x106 <10 – 2. (2006) stated that coliform counts in 71% of ice cream samples were higher than the limits permitted (>10 cfu/g) by the Libyan Standards for Ice Cream. (2006) from 6% of samples..7x101 – 1. those numbers varied between 11 and 8.4x102 cfu/g.2x103 8. and 14%. coli was reported as 50% by Coskun (2005).. and Salmonella spp. Nafi ÇOKSÖYLER Table 1. Erol et al. Kivanc et al. ���������������������������� Baek ����������������������� et al. Several investigators reported higher TAMB counts in unpacked ice cream samples than that found in this study.54%. 1998. 4. Although coliform count in the unpacked samples of the current study ranged between <10 and 2. El-Sharef et al.5x106 cfu/g in similar studies (Coskun.16% of unpacked ice cream samples (14/48).4x102 <10 – 1. 2004.. E.0x102 cfu/g) from 22% of samples.0x107 cfu/g (Korel et al. 1994). and Korel et al. S. 2000). and Kivanc et al. (2006). 2005. Buket KUNDUHOĞLU. (2004): minimum of 2.09% by Digrak et al. (1994) isolated E.1x101 – b1.. L...4x103 cfu/g. >106 cfu/g (Yaman et al. 2006. 1994..2006).5x102 . 1998. 1998).. 97 . 2005).0x106 cfu/g..5x105 <10 – 1.4x103 <10 – 8. as 6%.7x101 – 6. maximum of 2. Patir et al. respectively. <10 to 7. The current results on the coliform count of patisserie samples were similar to the findings of Kanbakan.36–2 MPN/g). Warke et al. et al. (2000) isolated L.1x101 to 1. coli Yeast Mold a b Unpacked ice cream (n = 48) a Packed ice cream (n = 44) 2.8x102 to 5x108 cfu/g (���������������������������� El-Sharef ������������������ et al. aureus count in the range of <10 to 105 (Erol et al. aureus. coli (16 –3.4x103 <10 – 8. Microbiological loads of ice creams Microorganism Count (cfu/g) TAMB Coliform count E. (1998) isolated E. 2000). and Warke et al. 2006).9x102 <10 <10 <10 – 1.1% of samples. 2.0x108 3 6 cfu/g (Erol et al. monocytogenes from 100% of their samples. monocytogenes from 6.4x102 <10 – 1.5x102 to 3.0x106 <10 – 2. 1997. In our study.

The variation analysis on microbiological qualities of the packed and unpacked retail products showed a significant difference (p<0.22–6. <30 / <30 cfu/g. coli was more frequent in plain ice cream samples (50%) than in flavored ones (26.0x101–1. coli count of plain samples was significantly higher (p<0.05) in this study. In general. ���������������� (1998) <2.2. (2004) reported higher TAMB and coliform counts in plain and flavored ice cream samples than that found in this study.53x104 cfu/g. yeast counts between plain and flavored packed ice cream samples (p>0.4 x10 cfu/g. In the study of Korel et al.9x103 / 2. Coşkun (2005) determined the pH range of plain and strawberry ice creams as 6.5x102–9. respectively: 3. The E. The findings of this 98 3.5x102–9.4x10 cfu/g. Evrensel and Gunes (1998) 1. similar to the current study. and they reported not being able to isolate Salmonella spp. Kanbakan et al. Flavored ice cream samples from patisseries in the study of Ozcan and Kurdal (1997) had the following minimum and maximum TAMB and coliform counts. and coliform counts.52 and 3.2–6. Korel et al. coliform.5x106 cfu/g. coli isolation rate was higher in coliform-containing plain ice cream. similar to the results of Bostan and Akin (2002). 5.Comparison of the Microbiological Quality of Packed and Unpacked Ice Creams Sold in Bursa. the coliform count was higher. packed plain/flavored ice cream samples had the following minimum and maximum TAMB. (2000) 4.0x104 cfu/g. except the TAMB and S. <10 / <10 cfu/g.5x105 cfu/g.001). respectively. aureus counts.0x102–9. In this study. The reason for this occurrence is considered the lower pH of flavored ice cream.5x105 and 1. whereas flavored ones had a pH of 3. The minimum and maximum microorganism counts of plain and flavored ice cream samples are shown in Table 2. Although they determined that the TAMB count in flavored ice cream was higher than that in plain ice cream. respectively: 2. (2006) reported the range of coliform counts of plain and flavored ice creams from patisseries as 1. occurrence of E.05) than the flavored samples. (1994) 4.6x104–5. Researcher isolated E.1.9x103– 5. they stated that flavored packed samples had a higher microbial load.3x10 –7. Kivanc et al. Turkey Maximum yeast and mold counts in the unpacked ice cream samples tested in this study were 1.7x105 cfu/g. isolation was higher in flavored ones. Joshi et al. (2005).0 x 102–106 cfu/ 2 4 g. Patir et al. Their E.16.36. respectively. and Enterobacter spp. ������������� (2004) 3. microorganism counts were higher in the unpacked ice cream samples than in the industrially produced ice creams with reference to all microbiological criteria tested (Table 1).9x105 cfu/g. coli from 68% of plain and 47% of strawberry ice creams.08. Generally.0x10 –2. There was no significant difference in the TAMB.9x104 cfu/g and <1– 5. their TAMB count was higher than the values obtained in this study for both types of samples.2x103 cfu/g.9x106 cfu/g. respectively. Yeast-mold counts in similar studies were close to or higher than the current findings: Erol et al. ����������������� (2005) <10–3. yeast-mold. Korel et al. from one plain sample. They isolated Salmonella spp. Microbiological quality of plain and flavored ice cream samples . Although their specified TAMB count was closer to the findings of this study. (2005) stated that the average pH of plain ice cream was 6. 3 5 and Warke et al.2%).

. (2005). According to our results.7x103 <10 – 1. Buket KUNDUHOĞLU.7x101 – 6.2. ice creams must not contain Salmonella spp.1x101 – 5.5x102 2. A similar result was observed by Korel et al. Nafi ÇOKSÖYLER study showed similarity concerning yeast. Minimum and maximum numbers of microorganisms in ice cream samples.0x101 – 1.64%. coli Yeast Mold a Minimum and maximum numbers of microorganisms in unpacked ice cream samples collected from patisseries.1x101 – 1.9x103 <10 <10 – 8. a statistically significant difference (p<0. b All the industrially produced packed samples tested in this study complied with the TFC (2001) standards.05) was only detected between the mold and E. is <10 cfu/g.5x103 6. Table 2. However.4x102 <10 <10 – 4. which exceeded the TFC limits. and S.4x101 Coliform E.5x105 <10 – 1. The ratio of samples produced by C. aureus count.55%.0x106 2. All the samples tested conform to the TFC criteria for Salmonella spp. Minimum and maximum numbers of microorganisms in industrially produced. and 31. 54. Microorganism Count (cfu/g) TAMB Plain ice cream (n = 18) 2.81%. L. aureus. respectively. were 13.Gülben ERMAN ÇAĞLAYANLAR.4x103 <10 – 10 <10 – 35 <10 <10 – 1.4x102 – 7. D and E. Ice cream samples that did not comply with the TFC (2001) norms (n = 22) were plain with 82 % and flavored with 18 %.0x101 a b Flavored ice cream (n = 74) 8.05) between the samples collected from two factories (producers A and B). the microbiological load of plain ice cream was lower than that of flavored ones. monocytogenes (in 25 g) and the acceptable limit of S. According to TFC (2001). prepared by the patisseries.8x101 <10 <10 – 2. grouped according to ice cream types.2x103 <10 – 1. coli counts. There was no significant difference in the microbiological qualities (p>0. and L. packed ice cream samples. Evaluation based on producers .8x101 <10 – 1. mold. Minimum and maximum microorganism counts of samples from two different factories and three different patisseries are provided in Table 3. Especially. 50% of samples from patisserie D did not 99 3. Minimum and maximum microorganism counts in incompliant patisserie samples and the permissible limits laid down by the TFC are shown in Table 4.2. and coliform counts. according to the same standards. monocytogenes.9x102 <10 – 2.

.0x103 1.1x101 – 2.1 63. Kivanc et al.0x101 <10 – 2.1 50. Digrak and Özcelik. This situation is replicated in the current study. Table 3. There was no significant difference among the three patisseries with reference to E.3x104 <10 – 5.0x106 <10 – 2.4 a TFC* 1.2x103 n 2 13 14 5 8 % 9. and coliform counts in the samples from producer D were higher than those in the samples from the other two patisseries (p<0.8x101 <10 – 1.0x106 2.2x103 *A (n = 22) a7.7 36. 2006).9x102 1.3x102 – 1. C.05).8x101 <10 – 9.5x102 <10 – 3.4x105 5. coli <10 <10 <10 – 8. coli Yeast Mold Table 4.. 1991. TAMB. Digrak et al. Patir et al.0x105 95 9 - - 2. The mold count in samples of producer E was higher than that in samples of producer C.4x101 Yeast <10 – 1.4x103 8.4x102 1. no significant difference could be detected between the samples from producers C and E for other microorganism counts. Evrensel and Gunes. 1997. Kanbakan and Çon. Ozcan and Kurdal. Minimum 2.0x101 – b5. Turkey comply with the standards concerning 3–5 microbiological criteria. a Minimum number of microorganisms b Maximum number of microorganisms Microorganism Count (cfu/g) TAMB Coliform E.7x101 <10 – 1.0x101 1.6x103 <10 – 1.4x102 – 1. and E represent patisseries. 1998. Erol et al. however.6x102 9 1.2x102 *A and B represent factories.5x102 1..9x102 <10 – 1.mold. 2006.5x101 <10 – 1.Comparison of the Microbiological Quality of Packed and Unpacked Ice Creams Sold in Bursa. 1999.6 22. Many studies on the microbiological quality of ice cream produced under unstandardized conditions by small-scale manufacturers have shown remarkable abundance of samples incompliant with standards in Turkey (Coskun.0x102 b * Permissible limits of the Turkish Food Codex (20) a Limits for plain ice cream b Limits for flavored ice cream 100 . 2000.. Producer Microorganism count (cfu/g) TAMB Coliform E.. 1994. 1997. Yaman et al.05). coli counts (p>0.4x101 <10 – 2.9x102 <10 – 3.5x102 <10 B (n = 22) 2.3x101 <10 – 5.4x103 E (n = 20) 1.3x103 D (n = 14) 4. yeast. 2005. Sezgin et al.7x101 – 6. Unpacked ice cream samples that did not comply with TFC specifications.4x102 <10 – 5.4x104 Mold <10 – 1. D.5x105 1. 1998.0x101 C (n = 14) 8..0x105 4.2x103 Maximum 1. Microbiological quality of ice cream samples according to producer.

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