PREVALENCE OF ENTERIC BACTERIA IN ICE-CREAM IN GIZA GOVERNORATE

Document Type : Research article

Authors

Dept. of Food Hygiene, Animal Health Research Institute, Dokki, Giza.

Abstract

 
A total of 50 samples of ice-cream were collected from different shops which have ice-cream machine at Giza governorate and subjected to bacteriological examination, the mean values of the Coliform (MPN/g) and Enterobacteriaceae count were 1.98x103± 0.5x103 and 1.5x10±0.34x 104,respectively, E. coli could be isolated and identified as EPEC 2% of O55: K59 (B5) and EIEC 2% of O124: K 72 (B17), While, Salmonella isolated from 2% of samples and identified as S.typhimurum, and the incidence of the Enterobacteriaceae members isolated from examined ice-cream were E. coli 4%, Klebsiella pneumoniae 6%, Klebsiella ozonae 16%, Enterobacter aerogenes 14%, Enterobacter agglomerans 4%, Citrobacter freundii 18%,  Proteus vulgaris 14% and Proteus mirabilis 22%. The public health importance of the isolated microorganisms were discussed, the sources of contamination of ice-cream and the measures which should be applied to minimize the bacterial load and safe guard the consumer are mentioned

Keywords


Dept. of Food Hygiene,

Animal Health Research Institute, Dokki, Giza.

 

Prevalence of Enteric bacteria in ice-cream in Giza governorate

(With 3 Tables)

 

By

Hala F. Hassan; Shireen M. Noseir

 and Hanaa M. Soultan

(Received at 15/3/2009)

 

تحديد مدى تواجد الميکروبات المعوية فى الايس کريم فى محافظة الجيزة

 

هاله فريد حسن ، شيرين محمود نصير ، هناء محمود سلطان

 

يعتبر الأيس کريم من منتجات الألبان الواسعة الانتشار، السهلة الهضم، ذات القيمة الغذائية العالية، وينتشر تداوله بين فئات کثيرة وأعمار مختلفة من المستهلکين، وهو مصدر للفيتامينات والأملاح المعدنية. وتحت ظروف الإنتاج المختلفة وکذلک التصنيع والتوزيع، قد يتعرض الايس کريم للتلوث الميکروبي بمختلف الأنواع الممرضة والتي تشکل خطورة     لا يستهان بها على صحة المستهلک، لذلک کانت هذه الدراسة لتحديد مدى تواجد الميکروبات المعوية فى الايس کريم فى محافظة الجيزة، وقد تم تجميع عدد 50 عينة من الايس کريم من المحلات التي بها ماکينة تصنيع الايس کريم ونقلت للمعمل وتم إجراء الفحوصات البکتريولوجية على العينات. وکان متوسط العد الکلي لبکتيريا المجموعة القولونية        1.98 x310 ± 0.5x 310 خلية بکتيرية /جم من العينة. وللبکتيريا المعوية کان1.5 x410 ± 0.34x 410 خلية بکتيرية /جم من العينة. وتم عزل ميکروب الايشريشيا کولاى من 4% من العينات وميکروب السالمونيلا من 2% من العينات وأيضا تم عزل الميکروبات المعوية بنسب وأنواع مختلفة. وقد تم اقتراح التوصيات المختلفة للحد من تلوث الايس کريم وزيادة جودة المنتج.

 

Summary

 

A total of 50 samples of ice-cream were collected from different shops which have ice-cream machine at Giza governorate and subjected to bacteriological examination, the mean values of the Coliform (MPN/g) and Enterobacteriaceae count were 1.98x103± 0.5x103 and 1.5x10±0.34x 104,respectively, E. coli could be isolated and identified as EPEC 2% of O55: K59 (B5) and EIEC 2% of O124: K 72 (B17), While, Salmonella isolated from 2% of samples and identified as S.typhimurum, and the incidence of the Enterobacteriaceae members isolated from examined ice-cream were E. coli 4%, Klebsiella pneumoniae 6%, Klebsiella ozonae 16%, Enterobacter aerogenes 14%, Enterobacter agglomerans 4%, Citrobacter freundii 18%,  Proteus vulgaris 14% and Proteus mirabilis 22%. The public health importance of the isolated microorganisms were discussed, the sources of contamination of ice-cream and the measures which should be applied to minimize the bacterial load and safe guard the consumer are mentioned.

 

Key words: Milk products, ice-cream, Enterobacteriaceae

 

Introduction

 

Milk and milk products are good sources of protein, minerals and vitamins for human especially for children and there is no need to state that ice-cream is the most palatable, nutritious and healthful inexpensive dairy product. Ice-cream is highly appreciable by all ages because it is considered a safe, enjoyable, energy giving and refreshing food because levels of water soluble vitamins and minerals are two to three times higher than those of full cream milk. Also, it is a valuable source of vitamin B, and contains twice vitamin A content as that of milk (Arbuckle, 1986 and Varnam and Sutherland, 1994).

The manufacture of ice-cream is a relatively complex operation, with a serious of steps which, in both compositional and microbiological terms, contribute to the overall quality of the ice-cream. It is not possible to give details here but several authors discuss this issue (Arbuckle, 1972 and Hyde and Rothwell, 1973). Ice-cream is often stored for few hours or even over night; so there is opportunity for bacterial growth and multiplication, rendering the product to be of public health hazard. Because ice-cream is consumed without any treatment that might reduce its microbial load, it is necessary to maintain a high level of microbial quality, for this purpose many countries have adopted mandatory manufacturing practices and standards to ensure an adequate and wholesome supply of such product.

This study was planned to evaluate the microbiological hygiene of the shops of ice-cream in Giza governorate through some indicator microorganisms as Coliform, E. coli and Salmonella as well as a trials for identification of some Enterobacteriacea organisms.

Materials and methods:

A total of 50 samples of ice-cream were collected from different shops which have ice-cream machine at Giza governorate.

Samples were transferred in an ice box without delay to the laboratory and subjected to the following examinations:

1-      Determination of Enterobacteriaceae: according to FDA 2002.

2-      Determination of Coliforms (MPN/g): according to FAO 1992.

3-      Isolation and identification of E.coli according to APHA 1992.

4-      Isolation and identification of Salmonellae APHA 1992.

5-      Identification of Enterobacteriaceae according to Elmer et al. 1997.                         

 

Results

 

Mean ±S.E

 

Max.

 

Min.

 

%

No

        50

         Organisms

1.5x104 ± 0.34x104

8x104

1.2x103

62

31

Enterobacteriaceae

(CFU/g)

1.98x103± 0.5x103

1.1x104

1.1x102

54

27

Coliform  

          (MPN/g)

Table 1: Statistical analysis of Enterobacteriaceae and Coliform (MPN/g) counts of examined ice-cream samples.

 

 

Table 2: Serodiagnosis of E. coli and Salmonella isolated from the examined ice- cream samples.

 

Type of strain

 

%

No.

    50

 

Organism

 

EPEC

2

1

E. coli  O55 : K59 (B5)             

EIEC

2

1

E. coli  O124: K72 (B17)

S.typhimurium

2

1

Salmonella 

 

Table 3: Incidence of Enterobacteriaceae members isolated from the examined ice-cream.

 

Enterobacteriaceae members

No./50

%

E. coli

2

4

Klebsiella pneumoniae

3

6

Klebsiella ozonae

8

16

Enterobacter aerogenes

7

14

 Enterobacter agglomerans

2

4

Citrobacter freundii

9

18

Proteus vulgaris

7

14

Proteus mirabilis

11

22

Salmonella

                 1

2

 

discussion

 

The results recorded in Table 1, showed that the Coliform (MPN/g) and Enterobacteriaceae counts varied from 1.1x 102 to 1.1x 104 and 1.2x 103 to 8x 104,  respectively with mean values 1.98x103± 0.5x103 and 1.5x104  ±0.34x 104,respectively. These results nearly agreed with those obtained by Mohamed and Al-Ashmawy (1980), Tammingo et al. (1980), Marin et al. (1985), Sharma and Joshi (1992), El-Prince and Hussein (2000) and Nawar (2001). While higher results were recorded by Hafez (1979), El-Essawy (1980) and Gad El-Rab (1983). However lower results were recorded by Delia et al. (1980) and El-Essawy and Riad (1990).

Coliforms group is considered as an indicator of poor sanitation and handling of the ice-cream during preparation (Finstein, 1973 and Banwart, 1981).

However, it seems to be the experience in many countries that ice-cream produced on small scale often has a poor bacteriological quality than the output of the large scale factory (Hamann and Weber, 1978), for often ,these small factories have no system of quality control at all.

Table 2, showed that E. coli could be isolated and identified as EPEC 2% of O55: K59 (B5) andEIEC 2% of O124: K 72 (B17), While Salmonella isolated from 2% of samples and identified as S.typhimurum.

Nearly the same results were recorded by Sharma and Joshi (1992) and El-Prince and Hussein (2000) as they could isolate Salmonella species from ice-cream samples, while Hafez (1979), Delia et al. (1980 )  and Tammingo et al. (1980) failed to detect Salmonella.

Table 3, showed the incidence of the Enterobacteriaceae members isolated from examined ice-cream as E. coli 4%, Klebsiella pneumoniae 6%, Klebsiella ozonae 16%, Enterobacter aerogenes 14%, Enterobacter agglomerans 4%, Citrobacter freundii 18%, Proteus vulgaris 14%, Proteus mirabilis 22% and Salmonella 2%. These results agreed with that recorded by El-Essawy and Riad (1990), El-Prince and Hussein (2000), Nawar (2001) and Ahmed (2004).

Many opportunities exist for contamination of ice-cream from the hands of workers and other equipments. Coliforms group is considered as an indicator of both questionable and acceptable, it may indicate fecal contamination from either human or animal sources, and also its presence indicates poor sanitation and handling (Banwart, 1981).

Because the reservoir of E. coli is the intestinal tract of man and animals, the presence of such organism in other environments like food and water is used as an indicator of contamination from the natural reservoirs (Doyle and Padhye, 1989), so its presence in the ice-cream indicates a general lack of cleanness during transportation, handling and processing of ice-cream. The public health importance of E. coli has been emphasized by many authors; these enteropathogenic serotypes have been implicated in case of gastroenteritis, epidemic diarrhea in infants, sporadic summer diarrhea in children as well as in case of food poisoning (kornacki and Marth, 1982).

Among the requirements for any food to be of good sanitary quality it must be free from hazardous microorganisms, or those present should be at a safe low level therefore, nearly all countries now adopt standards for composition and bacterial content, so that the public may be assured of a safe healthful product.

The following measures should be adopted to ensure safety and high quality ice-cream.

1- High quality ingredients, properly balanced, of low microbial content and governed by standards specifications should be used.

2- Handling and distribution should be done under strict hygienic measures.  

3- Standards must be applied to all aspects of production, processing and distribution. These standards must be adequate to provide an acceptable product, without imposing unrealistic requirements.

4- Application of good manufacturing practices in milk manufacturing units and should be regarded by the regulatory authorities as basic or compulsory requirements.  

In order to obtain the best bacterial standard which is required, the utmost attention must be given to the cleaning and sanitation of all the plant and equipment used, to the personal hygiene of the entire operator, and to the general cleanliness of the factory.

                                      

References

 

Ahmed, M.M. (2004): Microbiological studies on raw milk and some dairy products. M.V.Sc. Thesis, Faculty of Veterinary Medicine Minufiya University.

APHA (1992): American Public Health Association: Standard Methods for Examination of Dairy Products, Washington, D.C., USA.  

Arbuckle, W.S. (1972): Ice-cream. AVI, Westport, Connecticut.

Arbuckle, W.S. (1986): Ice-cream.4th Ed.  P.313. Publ. by Van Nostrand Reinhold Company, New York.

Banwart, G.J. (1981): Basic food microbiology 2nd ed. AVI Publishing co., Westport, Connecticut, USA.

Delia, S.; Mauro, A. and Dania, D. (1980): Application of Ministerial Ordinance of 11 October 1978 on ice-cream in the city of Messina. Italiana Discienza dell' Almentaziane, 9, 6,437. Dairy Science Abst., 43, 10(1981).

Doyle, M.P. and Padhye, V.V. (1989): Escherichia coli – in Doyle, M.P.(ed.) Food borne bacterial pathogens. Marcel Dekker, NewYork, NY.P: 235.   

El-Essawy, H.A. (1980): Public health importance of Enterobacteriaceae and Enterococci in some dairy products. Thesis, PhD. Faculty of Veterinary Medicine, Cairo University.

El-Essawy, H.A and Riad, A.A.M. (1990): Incidence of Coliform organisms in cream and ice-cream with special reference to enteropathogenic strains of E.Coli. Assiute Veterinary Medical Journal, Vol. 24, No.47.

Elmer, W.; Stephen, D.; William, M.; Paul, C. and Washington, C. (1997): Color Atlas and Textbook of Diagnostic Microbiology 5th. Ed. Lippincott, Philadelphia, New York.

El-Prince, E. and Hussein, A.A. (2000): Occurrence of Enterobacteriaceae in ice-cream with special reference to Salmonella species. Assiute Veterinary Medical Journal, Vol. 45, No.89.

FAO (1992): Manual of food quality control. Part 4 microbiological analysis, United Nation, Roma, Italy.

FDA (2002): U.S. Food and Drug Administration Bacteriological Analytical Manual. Center for Food Safety and Applied Nutrition, Ch., 4.

Finstein, M.S. (1973): Sanitary bacteriology in CRC. Hand book of microbiology . Vol.1. CRC Press, Gleve land, Ohio.

Gad El-Rab, H.M. (1983): Enterobacteriaceae in milk and milk products. M.V.Sc. Thesis, Faculty of Veterinary Medicine Assiute University.

Hamann, R. and Weber, H. (1978): Archiv Fur Lebensmitte- Hygiene, 29(1) 5.

Hyde, K.A. and Rothwell, J. (1973): Ice-cream. Churchill Livingastone , Edinburgh.

Hafez, R.S. (1979): Microbiological studies on market ice-cream in Cairo and its suburbs.  Thesis, PhD.  Faculty of Veterinary Medicine, Cairo University.

Kornacki, J.L. and Marth, E.H. (1982): Food- borne illness caused by  E. Coli A review. Journal of Food Protection, 45; 1051.

Marin, V.; Zitelli,A and Campre, G.D. (1985): Hygienic and microbiological incidence of ice-cream from small scale producers in the Venice province, Industries Alimentari, 24 (255): 270-274. Dairy Science Abstract, 48: 551(1986).

Mohamed, S.M. and Al-Ashmawy, A.M. (1980): Bacteriological quality of ice-cream in Cairo. Egypt. Veterinary Medical Journal, Vol. 28, No.59.

Nawar, D.M.M. (2001): Hygienic quality of some street vender dairy products. M.V.Sc.Thesis, Faculty of Veterinary Medicine Alex. University.

Sharma, D.K. and Joshi, D.V. (1992): Bacteriological quality of milk and milk products with special reference to Salmonella and its Public health significance. Journal of Food Science Technology Mysore, 29(2): 105-107.

Tammingo, S.K.; Beumet, R.R. and Amplanacher, E.H. (1980): Bacteriological examination of ice-cream in Netherland: comparative studies on method. Journal of Applied Bacteriology, 45 (2): 239.

Varnam, A.H. and Sutherland, J.P. (1994): Milk and Milk products technology, Chemistry and Microbiology. 1st Ed., Chapman and hall Publ., London.

 

 

 

 

 

 


                       

 

 
Ahmed, M.M. (2004): Microbiological studies on raw milk and some dairy products. M.V.Sc. Thesis, Faculty of Veterinary Medicine Minufiya University.
APHA (1992): American Public Health Association: Standard Methods for Examination of Dairy Products, Washington, D.C., USA.  
Arbuckle, W.S. (1972): Ice-cream. AVI, Westport, Connecticut.
Arbuckle, W.S. (1986): Ice-cream.4th Ed.  P.313. Publ. by Van Nostrand Reinhold Company, New York.
Banwart, G.J. (1981): Basic food microbiology 2nd ed. AVI Publishing co., Westport, Connecticut, USA.
Delia, S.; Mauro, A. and Dania, D. (1980): Application of Ministerial Ordinance of 11 October 1978 on ice-cream in the city of Messina. Italiana Discienza dell' Almentaziane, 9, 6,437. Dairy Science Abst., 43, 10(1981).
Doyle, M.P. and Padhye, V.V. (1989): Escherichia coli – in Doyle, M.P.(ed.) Food borne bacterial pathogens. Marcel Dekker, NewYork, NY.P: 235.   
El-Essawy, H.A. (1980): Public health importance of Enterobacteriaceae and Enterococci in some dairy products. Thesis, PhD. Faculty of Veterinary Medicine, Cairo University.
El-Essawy, H.A and Riad, A.A.M. (1990): Incidence of Coliform organisms in cream and ice-cream with special reference to enteropathogenic strains of E.Coli. Assiute Veterinary Medical Journal, Vol. 24, No.47.
Elmer, W.; Stephen, D.; William, M.; Paul, C. and Washington, C. (1997): Color Atlas and Textbook of Diagnostic Microbiology 5th. Ed. Lippincott, Philadelphia, New York.
El-Prince, E. and Hussein, A.A. (2000): Occurrence of Enterobacteriaceae in ice-cream with special reference to Salmonella species. Assiute Veterinary Medical Journal, Vol. 45, No.89.
FAO (1992): Manual of food quality control. Part 4 microbiological analysis, United Nation, Roma, Italy.
FDA (2002): U.S. Food and Drug Administration Bacteriological Analytical Manual. Center for Food Safety and Applied Nutrition, Ch., 4.
Finstein, M.S. (1973): Sanitary bacteriology in CRC. Hand book of microbiology . Vol.1. CRC Press, Gleve land, Ohio.
Gad El-Rab, H.M. (1983): Enterobacteriaceae in milk and milk products. M.V.Sc. Thesis, Faculty of Veterinary Medicine Assiute University.
Hamann, R. and Weber, H. (1978): Archiv Fur Lebensmitte- Hygiene, 29(1) 5.
Hyde, K.A. and Rothwell, J. (1973): Ice-cream. Churchill Livingastone , Edinburgh.
Hafez, R.S. (1979): Microbiological studies on market ice-cream in Cairo and its suburbs.  Thesis, PhD.  Faculty of Veterinary Medicine, Cairo University.
Kornacki, J.L. and Marth, E.H. (1982): Food- borne illness caused by  E. Coli A review. Journal of Food Protection, 45; 1051.
Marin, V.; Zitelli,A and Campre, G.D. (1985): Hygienic and microbiological incidence of ice-cream from small scale producers in the Venice province, Industries Alimentari, 24 (255): 270-274. Dairy Science Abstract, 48: 551(1986).
Mohamed, S.M. and Al-Ashmawy, A.M. (1980): Bacteriological quality of ice-cream in Cairo. Egypt. Veterinary Medical Journal, Vol. 28, No.59.
Nawar, D.M.M. (2001): Hygienic quality of some street vender dairy products. M.V.Sc.Thesis, Faculty of Veterinary Medicine Alex. University.
Sharma, D.K. and Joshi, D.V. (1992): Bacteriological quality of milk and milk products with special reference to Salmonella and its Public health significance. Journal of Food Science Technology Mysore, 29(2): 105-107.
Tammingo, S.K.; Beumet, R.R. and Amplanacher, E.H. (1980): Bacteriological examination of ice-cream in Netherland: comparative studies on method. Journal of Applied Bacteriology, 45 (2): 239.
Varnam, A.H. and Sutherland, J.P. (1994): Milk and Milk products technology, Chemistry and Microbiology. 1st Ed., Chapman and hall Publ., London.