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Microbial Quality and Antimicrobial Resistance of Staphylococcus aureus and Escherichia coli Isolated from Traditional Ice Cream in Hamadan City, West of Iran

1 Student Research Center, Hamadan University of Medical Sciences, Hamadan, Iran
2 Nutrition Health Research Center, Hamadan University of Medical Sciences, Hamadan, Iran
3 Food and Drug Laboratory, Hamadan University of Medical Science, Hamadan, Iran
4 Department of Food Science and Engineering, University College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
*Corresponding author: Ali Heshmati, Nutrition Health Research Center, Hamadan University of Medical Sciences, Hamadan, Iran. Tel: +98-8138381821, Fax: +98-38381822, E-mail: a.heshmati@umsha.acir.
Avicenna Journal of Clinical Microbiology and Infection. 4(1): e39781 , DOI: 10.17795/ajcmi.39781
Article Type: Research Article; Received: Jun 7, 2016; Revised: Aug 26, 2016; Accepted: Oct 3, 2016; epub: Oct 16, 2016; collection: Feb 2017


Background: Foodborne diseases are one of the most major public health concerns in the world. Ice cream flavors, especially the traditional ones, have a high potential for the transmission of the pathogenic bacteria.

Objectives: The aim of the current study is to investigate the microbiological status and antibiotic resistance of Escherichia coli and Staphylococcus aureus isolated from traditional ice cream.

Methods: A total of 114 traditional ice creams were randomly collected from retail stores in Hamadan, Iran. Samples were investigated for the total bacteria count (TBC) and contamination with the coliform, Enterobacteriaceae and Salmonella as well as the prevalence and antibiotic resistance of Staphylococcus aureus and Escherichia coli.

Results: The count of Enterobacteriaceae (89.47%), mold and yeast (50%), coliform (40.35%) and TBC (28.07%) of samples was higher than Iran’s standard. Salmonella was not found in all samples. The prevalence of Staphylococcus aureus and Escherichia coli was confirmed in 50% and 37.72% of samples, respectively. Collected Escherichia coli had the highest antibiotic resistance to ampicillin 67.44%, nalidixic acid 39.53% and co-amoxyclav 37.21%. Staphylococcus aureus showed a higher antibiotic resistance to penicillin (82.46% of isolates) and oxacillin (38% of isolates).

Conclusions: The results showed high contamination levels of traditional ice cream with spoilage and pathogenic microorganisms as well as considerable resistance of isolated Staphylococcus aureus and Escherichia coli to common antibiotics. Therefore, good hygienic practice during processing and personal hygiene should be considered to improve the quality of ice cream. In addition, it is necessary that the regulatory authorities carry out more control on the production centers of traditional ice cream.

Keywords: Staphylococcus aureus; Escherichia coli; Foodborne Disease; Ice Cream; Drug Resistance

1. Background

Foodborne disease is a major cause of morbidity and mortality all over the world. Thirty-one pathogens are known to cause foodborne disease and have an adverse impact on humans (1). Escherichia coli and Staphylococcus aureus are dangerous pathogens that were found in contaminated food substances. E. coli caused haemorrhagic colitis (HC), bloody diarrhea and haemolytic-uremic syndrome (HUS) (2). The presence of Staphylococcus aureus in food causes poisonous symptoms such as nausea, abdominal cramps, diarrhea and vomiting (3, 4).

Milk is a nutritious food and an excellent culture medium for microbial growth; therefore, it is one of the most important sources of foodborne illness. Many dfferent pathogenic bacterias are found in milk, such as E. coli, S. aureus, Salmonella, Listeria monocytogenes, Shigella, Campylobacter jejuni and Bacillus cereus (5, 6).

Traditional foods are considered all over the world. These foods have specific characteristics, which differ from other similar products of the same category due to the utilization of traditional ingredients (raw materials of primary products), traditional composition or traditional type of production and/or processing method (7). There is much concern about microbial contamination of traditional foods. Traditional ice creams are one of the most favorite consumed foods in warm seasons in Iran. Its production process is different from industrial ice cream. Ice cream has high nutritional value and neutral pH; thus, it is a suitable environment for microbial growth. In addition, several raw materials are used for ice cream production; some of which is contaminated and can create any health hazard (8). The utilization of unpasteurized milk for traditional ice cream production is one of the main microbial contaminants (9). Furthermore, suitable thermal processing was not applied during manufacturing of these products to preserve its desirable taste. Therefore, this product is an important source of transmission of pathogenic bacteria. Since most of the ice cream is consumed by children and is popular amongst adults, the study of the microbial status of this product is very useful (10). On the other hand, the worldwide use of antibiotics in livestock could increase the emergence of resistance bacteria strains in the food chain (6). The information of antibiotic susceptibility pattern of bacteria helps treat the infectious disease (11). Transmission of resistant microorganisms through milk, specifically ice cream, can cause several problems for the consumers.

2. Objectives

Currently, there is little information regarding microbial contamination of traditional ice cream and antibiotic resistance patterns of pathogenic bacteria isolated from this product in the west of Iran and therefore the present communication was done for this purpose.

3. Methods

3.1. Sample Collection

A total of 114 ice cream samples (38 fruit-flavored, 38 plain and 38 pistachio) were randomly collected from retail stores in Hamadan city during April 2015 to March 2016. All samples were stored at - 18°C. Analyses were carried out within 24 hours after sampling.

3.2. Chemicals and Media

Gioliti-Cantoni Broth, Baird-Parker agar (BPA), nutrient agar, Lauryl sulphate broth and EC broth media were purchased from Merck Co. (Darmstadt, Germany). Mueller Hinton agar, YGC, VRBD and VRBG media were obtained from HiMedia Co. (Mumbai, India). All of the following antibiotic disks testing were obtained from Padtan Teb Co. (Karaj, Iran): all other chemicals were purchased from Merck.

3.3. Microbiological Analyses
3.3.1. Preparation of Serial Dilution

For obtaining 0.1 dilutions, 5g of molted ice cream were aseptically transferred into a 95 mL ringer solution and homogenated by vertex. Subsequent decimal dilutions were prepared using the same diluents.

3.3.2. Total Bacteria Count (TBC)

1 mL of diluted ice cream was poured into to a sterile Petri dish containing medium of plate count agar and incubated at 30°C for 24 h. At the end of the incubation, microbial colonies were enumerated (12) and all culturing examinations were carried out in duplicates.

3.3.3. Enterobacteriaceae

1 ml of each dilution was added to 15 ml of violet red bile glucose agar (VRBG) and incubated for 48 hours at 45 - 47°C. The characteristic colonies, violet red, were counted and confirmed by oxidase and fermentation tests (13).

3.3.4. Coliform

Coliform enumeration was performed on VRBL medium after incubation at 37°C for 24 hours (14).

3.3.5. Escherichia coli

The Lauryl Sulphate Broth and incubation at 37°C for 48 hours were used for the detection of E. coli. If gas was observed in the tubes, the solution was inoculated to EC broth and incubated at 44.5°C for 24 - 48 hours. E. coli was detected in tubes containing gas by free-indole peptone water, Kovac’s reagent as well as incubation at 44°C for 24 hours (15).

3.3.6. Salmonella

To detect salmonella in ice cream samples, 25g of samples were cultured in 225 mL of peptone water broth at 37°C. After, 1.0 mL of this solution was transferred into 10 mL of tetrathionate broth and incubated at 37 ºC. Then, about 5 - 10 μL of obtained solution was transferred into xylose desoxycholate (XLD), incubated at previous conditions and then diagnostic media was used for biochemical test (16).

3.3.7. Staphylococcus aureus

The Gioliti-Cantoni agar medium and pour-plate method were used for the detection of S. aureus. Black colonies with a positive coagulase were confirmed and considered as S. aureus (17).

3.3.8. Molds and Yeast

1 mL of diluted ice cream was transferred into the YGC medium and was then incubated at aerobic conditions at 25 ± 1°C for 3 - 5 days and then the colonies were enumerated (18).

3.3.9. Antibiotic Susceptibility Testing

The antimicrobial susceptibility tests for S. aureus and E. coli were performed by the Kirby-Bauer disc diffusion method as recommended by the clinical and laboratory standards institute on Mueller Hinton agar plates (19). For this purpose, the microbial suspension with the turbidity equivalant to the McFarland Standard of 0.5 was prepared and cultured on the Mueller Hinton agar plates. After preparation and incubation of the plates, the diameter of the growth inhibition zones around each of the antibiotic disks were measured and the susceptibility was categorized as either susceptible, intermediate and resistant. The disk diffusion method was repeated 5-times with one antibiotic for the investigation of accuracy of antibiogram disks. Disk diffusion used for the antimicrobial susceptibility tests included Erythromycin (15 µg), Rifampin (5 µg), Clindamycin (2 µg), Tetracycline (30 µg), Co-amoxiclav (25 µg), Tylosin (15 µg), Nalidixic acid (30 µg), Methicillin (5 µg), Ampicillin (10 µg), Streptomycin (10 µg), Neomycin (30 µg), Chloramphenicol (30 µg), Ciprofloxacin (5 µg), Trimethoprim (5 µg), Penicillin (10 µg), Vancomycin (30 µg), Gentamicin (10 µg), Oxacilli (1 µg) and Ceftazidime (30 µg).

3.4. Statistical Analysis

All experiments were performed in triplicates. The data analysis was carried out by the SPSS statistical software (version 16.0, SPSS Inc., Chicago, USA). Differences in the prevalence of microorganism amongst various ice creams were analyzed using a chi-square test. Differences were considered significant at values of P < 0.05.

4. Results

The microbial results of ice cream samples are shown in Table 1. No significant differences in the contamination and prevalence rates of spoilage and pathogenic are observed amongst various ice creams. 28.95% of plain, 28.95% of pistachio and 26.32% of fruit-flavored ice creams had exceeded the TBC than Iran standard levels (5 × 104 CFU g-1). All the analyzed ice cream samples showed heavy contamination (in average, 89.47%) of Enterobacteriaceae. Overall, coliform count in 40.35% of samples was higher than legal limit (10 CFU g-1); samples of plain ice cream had the highest contamination. 39.47 - 57.89% of analyzed samples were contaminated with S. aureus and the highest positive samples were found in fruit-flavored ice cream. Between 31.58 and 42.11% of ice cream samples were contaminated with E. coli. Salmonella was not found in all samples. In general, the highest mold contamination (57.89% of samples) was found in pistachio ice cream. Isolated S. aureus showed a significant resistant to antibiotics and the highest resistance was found for penicillin, oxacillin, erythromycin and clindamycin, respectively (Table 2). Overall, 38 of 47 S. aureus isolates (80.85%) were resistant to two or more antimicrobial agent. Although, antibiotic resistance of E. coli to gentamicin and chloramphenicol was very low, it showed the highest resistant to ampicillin, nalidixic acid and co-amoxyclav, respectively (Table 3). Multiresistance, resistance to three or more antibiotics, was found in 16 of 43 (37.21%) isolated E. coli.

Table 1.
Microbial Quality of Traditional Ice Cream Consumed in Hamadan, Irana

Table 2.
Results of the Antibiotic Sensitivity of Staphylococcus aureus Isolated from Traditional Ice Cream Samples (114 Samples) Consumed in Hamadan, Iran

Table 3.
Results of the Antibiotic Sensitivity of E. coli Isolated from Traditional Ice Cream Samples (114 Samples) Consumed in Hamadan, Iran

5. Discussion

Traditional ice cream is one of the most abundant and popular dairy products that is consumed in warm seasons by vulnerable groups, especially children, therefore; its microbial contamination is very important. This study has shown the high microbial contamination levels of traditional ice creams in Hamadan, Iran.

Several studies have been done in relation to antibiotic resistance patterns in traditional ice cream, raw milk and other dairy products all around the world (6, 20-24). According to the results, 28.7% of all traditional ice cream samples had TBC than recommended criteria according of Iran standard (5 × 104 CFU g-1). In other surveys, more TBC (51 to 78.8%) than the current study has been reported (25-27).

The Enterobacteriaceae and coliform count in food has been considered as an index of food hygiene. The prevalence of Enterobacteriaceae in the present study (89.48%) was higher than the results of other studies (17.2 to 82.9%) (26-28). The coliform count in 55% of the samples was above the approved limit (10 CFU g-1) while 30% - 46% of ice cream samples examined by Abou and Khair (2014) and Ambily et al. (2012) had a higher coliform count than the legal limit (25, 29). Although, contamination level of 100% was also found in a study conducted in India (30). High levels of traditional ice cream contamination of coliforms might be due to the utilization of unpasteurized milk, contaminated water, post-treatment contamination or contaminated utensils used for ice cream storage, distribution, poor sanitation practices during preparation and production and the lack of personal hygiene (21).

The occurrence of Salmonella contamination in ice cream is likely due to the use of egg in ice cream formulation. This substance is vehicle for transmission of this organism. Salmonella was not found in all samples that it is in agreement with studies in Iran and other countries (25, 27, 28, 31), although the contamination levels of 3.7 to 33% have been reported in some studies (21, 29, 30).

In our study, 50% of ice cream samples had higher mold contamination than the permitted standard levels, although Salehian et al. (2013) reported that 24% of samples showed a higher mold count than the acceptable limit (28).

The prevalence of S. aureus in our study was 50%. The contamination level of 2.8% - 41.8% with S. aureus was also reported in similar studies that were lower than our results (21, 25, 27-29). The presence of S. aureus in ice cream can be due to poor hygiene practices of handlers. This microorganism, is naturally found on the hands, nasal cavity and skin of humans (32, 33), therefore droplets containing microbe might be produced during coughing, talking and sneezing, which could settle on ice cream (31). Ice cream and other dairy products are good sources for S. aureus growth and can contribute to its outbreaks (4). S. aureus is a main cause of mastitis in cows. One of the utilization reasons of antibiotics in cows is for treatment of this disease, which might result in antibiotic resistance (22). Our recent reports had indicated that although S. aureus had not had any resistance to ciprofloxacin and gentamicin, it showed the highest resistance to penicillin and oxacillin. The previous research surveys that have been conducted on the antibiotic resistance pattern of S. aureus isolated from milk, dairy products, ice cream and mastitis. The highest resistance was observed in penicillin, oxacillin, ampicillin, cefuroxime, tetracycline and amoxicillin and the results of penicillin and oxacillin were not in agreement with the present study (6, 20, 21, 34, 35).

The results of the current study showed that 30.56% of assessed samples were contaminated with E. coli. Salehian et al. (2013), Hasanzad et al. (2013), Abou and Khair (2014) and Jadhav and Raut (2014), have reported the contamination levels of E. coli in ice cream to be between 40 to 52%, which is higher than present study (25, 28, 30) although lower contamination levels, 6 to 21.4%, have been found by some researchers (7, 13, 27). E. coli is considered as an indicator of faecal contamination of foods and emergence of some pathogen strains and causes severe concerns (23, 36). The use of antibiotics in livestock for treatment of infections led to emergence of antibiotic resistance bacterial strains, which is a serious concern not only in animals but also in human health (30). These strains could be transmitted to humans through animal-derived foods such as milk and dairy products and can threaten their health. Antibiotic resistance of pathogenic bacteria is one of the important hygiene problems of today’s world that results in reduced effectiveness of antibiotics. Therefore, it is necessary to have information regarding antibiotic resistance patterns of bacteria in order to select an appropriate antibiotic for treatment of microbial infections (11). The highest antibiotic resistance of E. coli was observed to ampicillin, whilst all isolates were susceptible to ciprofloxacin. In other studies, isolated E. coli from milk and dairy products showed the most resistance to ampicillin (6, 21). In some studies, E. coli isolated from raw milk and unpasteurized cheese showed the highest resistance to penicillin and clindamycin, this finding was different than our results (14). These antibiotics weren’t use in present research. Investigation of antibiotic resistance in this study revealed that isolated S. aureus had the highest sensitivity to gentamicin and ciprofloxacin and E. coli showed the most sensitive to ciprofloxacin. Thus, the use of these antibiotics for treatment of disease caused by mentioned bacteria could be effective.

In general, the results obtained in this study showed a high contamination level of traditional ice cream with pathogen and spoilage microorganisms. The presence of S. aureus and E. coli in traditional ice cream and their resistance to two or more antibiotics might be a potential risk for disease in the consumer, especially vulnerable groups such as children. Therefore, the implement of good hygiene practices (GHP) is a necessity for improving ice cream safety. Worker and staff education especially in relation to food safety as well as handling washing and machine and utensil cleaning could be effective in improvement of the situation. The quality of raw material used in the final product, their storage under suitable and hygienic conditions and heat treatment during processing could prevent growth and multiplication of pathogenic microorganisms in ice cream.


The authors are sincerely grateful to Hamadan University of medical sciences and health services for financial supports (Project No. 9408124401).


Authors’ Contribution: Study concept and design: Ali Heshmati and Sabah Ghadimi; acquisition of data: Sabah Ghadimi and Mehdi Azizi Shafa; Analysis and interpretation of data: Ali Heshmati and Sabah Ghadimi; drafting of the manuscript: Sabah Ghadimi and Ali Heshmati; critical revision of the manuscript for important intellectual content: Ali Heshmati and Majid Nooshkam; statistical analysis: Ali Heshmati; administrative, technical, and material support: Ali Heshmati; study supervision: Ali Heshmati.
Funding/Support: This article was financially supported by the Vice-Chancellor for research and technology of Hamadan University of Medical Sciences.


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Table 1.

Microbial Quality of Traditional Ice Cream Consumed in Hamadan, Irana

Type of Ice Cream N Total Bacteria Count (CFU g-1) Enterobacteriaceae (CFU g-1) Coliform (CFU g-1) E. coli (CFU g-1) Salmonella (CFU g-1) S. aureus (CFU g-1) Mold and Yeast (CFU g-1)
ND-5 × 104 > 5 × 104 ND - 10 > 10 ND - 10 > 10 Positive Negative Positive Negative coagulase-positive coagulase-negative ND - 102 > 10
Plain 38 27 (71.05) 11 (28.95) 7 (18.42) 31 (81.58) 25 (65.79) 13 (34.21) 12 (31.58) 26 (68.42) 0 38 (100) 15 (39.47) 23 (60.53) 22 (57.89) 16 (42.11)
Pistachio 38 27 (71.05) 11 (28.95) 2 (5.26) 36 (94.74) 20 (52.63) 18 (47.37) 16 (42.11) 22 (57.89) 0 38 (100) 20 (52.63) 18 (47.37) 16 (42.11) 22 (57.89)
Fruit-flavored 38 28 (73.68) 10 (26.32) 3 (7.89) 35 (92.11) 23 (60.53) 15 (39.47) 15 (39.47) 23 (60.53) 0 38 (100) 22 (57.89) 16 (42.11) 19 (50) 19 (50)
Total 114 82 (71.93) 32 (28.07) 12 (10.53) 102 (89.47) 68 (59.65) 46 (40.35) 43 (37.72) 71 (62.28) 0 114 (100) 57 (50) 57 (50) 57 (50) 57 (50)
P value 0.957 0.141 0.5 0.615 - 0.255 0.388
Abbreviations: N: Number of Analyzed Samples; ND: Not Detected.
a Value ithin parenthesis indicates contaminated sample percentages

Table 2.

Results of the Antibiotic Sensitivity of Staphylococcus aureus Isolated from Traditional Ice Cream Samples (114 Samples) Consumed in Hamadan, Iran

Type of Antibiotic Resistant Intermediate Sensitive
N Percent N Percent N Percent
Penicillin 47 82.46 0 0 10 17.54
Oxacillin 38 66.67 0 0 19 33.33
Erythromycin 26 45.61 14 24.57 17 29.82
Clindamycin 24 42.11 10 17.54 23 40.35
Rifampin 12 21.05 6 10.53 39 68.42
Tetracycline 10 17.54 4 7.02 43 75.44
Trimethoprim.s 7 12.28 0 0.00 50 87.72
Chloramphenicol 1 1.76 7 12.28 49 85.96
Gentamicin 0 0 0 0 57 100
Ciprofloxacin 0 0 4 7.02 53 92.98

Table 3.

Results of the Antibiotic Sensitivity of E. coli Isolated from Traditional Ice Cream Samples (114 Samples) Consumed in Hamadan, Iran

Type of Antibiotic Resistance Intermediate Sensitive
N Percent N Percent N Percent
Ampicillin 29 67.44 2 4.65 12 27.91
Nalidixic acid 17 39.53 8 18.61 18 41.86
Co-Amoxyclav 16 37.21 3 6.98 24 55.81
Trimethoprim.s 14 32.56 6 13.95 23 53.49
Streptomycin 14 32.56 12 27.91 17 39.53
Ceftazidime 12 27.91 4 9.3 27 62.79
Chloramphenicol 4 9.3 2 4.65 37 86.05
Gentamicin 4 9.3 0 0 39 90.7
Ciprofloxacin 0 0 0 0 43 100