Some antibiotic resistant bacteria of public health hazard isolated from raw milk sold in some Assiut City markets بعض البکتريا ذات الخطورة علي الصحة العامة والمقاومة للمضادات الحيوية المعزولة من اللبن الخام المباع في بعض محلات مدينة أسيوط

Document Type : Original Article

Abstract

ABSTRACT
A total of 50 raw milk samples were collected in this study from some Assiut City markets,
Egypt, and examined for isolation of some human hazard pathogens. The percentages of the isolated
pathogens were 46, 76, 78, 4 and 24% for Staph. aureus, Enterococcus faecalis, E. coli, Citrobacter
freundii and Yersinia enterocolitica, respectively. In vitro Antibiogram was carried out on all isolates
against (8) different antimicrobial agents; moreover, all of these isolates showed multi-drug
resistance against tow or more of the tested antibiotics. The public heath hazards of the isolated
pathogens were also discussed.
الملخص العربي :
تم في هذه الدراسة تجميع عدد ٥٠ عينة من اللبن الخام المباع في بعض محلات مدينة أسيوط – مصر. وقد تم
فحص هذه العينات لعزل بعض البکتريا ذات الخطورة علي الصحة العامة وکانت نسب العزل هي ٧٦ ،٤٦،
٤ ٧٨، و ٢٤% لکل من المکور العنقودي الذهبي، المکور السبحي ألبرازي، الميکروب القولوني، ستروباکتر
فروندياي واليرسينيا انتيروکوليتيکا علي الترتب . وبفحص جميع العترات المعزولة لاختبار مقاومتها باستخدام ٨
أنواع من المضادات فقد أظهرت جميع العترات مقاومتها لمضادين أو أکثر من المضادات الحيوية. وقد تم مناقشة
الأهمية الصحية لهذه الميکروبات.

REFERENCES
A.P.H.A. (1985): Standard Methods for the
Examination of Dairy Products. 15th ed.,
American Public Health Association,
Washington, D.C., U.S.A.
Abdel-Hady, H.M. (1993): Studies on
Campylobacter jejuni and Yersinia
enterocolitica as food poisoning
organisms in milk and some dairy
products. Ph.D. Thesis, Fact. Vet. Med.,
Cairo Univ., Egypt.
Ahmad, N.; Rahman, U.; Ali, L.; Malik,
A.P. and Safeer, M. (2011):
Contamination of raw milk with
Escherichia coli sold in Peshawar
University campus and adjacent area.
KJMS., 3 (2): 72-75.
Akhila, S.; Priya, S.; Murugn, T. and
Thayumanavan, T. (2013): Molecular
diversity analysis of Yersinia
enterocolitica isolated from marine
marketed fish. Int. J. Current Microbiol.
App. Sci., 2 (9):204-214.
Ali, Asmahan, A. and Abdelgadir, Warda,
S. (2011): Incidence of Escherichia coli
in raw cow’s milk in Khartoum State.
British J. Dairy Sci., 2 (1): 23-26.
Al-Marjani, M.F. (2013): Van A in
vancomycin-resistant Enterococcus
faecalis isolated in Baghdad. African J.
Microbiol. Res., 7(2): 115-119.
Al-Tarazi, Y.; Al-Zamil, A.; Shaltout, F.
and Abdel-Samei, H. (2003): Sanitary
status of raw cow milk marketed in
northern Jordan. Assiut Vet. Med. J., 49
(96): 180-194.
Anonymous, (1975): E. coli enteritis. Lancet,
1131-1132.
Asperger, H. (1994): The significance of
pathogenic microorganisms in raw
milk . International Dairy Federation
(IDF). Document No. 292. Belgium.
Bali, O.S; Lajnef, R.; Felfoul, I.; Attia, H.
and Ayadi, A. (2013): Detection of
Escherichia coli in unpasteurized raw
Milk. International J. Agriculture Food
Sci., 3(2): 53-55.
Basha, O.A; Shaboury, F.A. and Fayed,
A.H. (2008): Some studies on the
occurrence of Yersinia microorganisms
in raw milk and some soft cheeses sold
in Alexandria Governorate. Assiut Vet.
Med. J., 54 (116): 133-143.
Benkerroum, N.; Bouhal, Y.; EI-Attar, Y.
and Marhaben, A. (2004): Occurrence
of Shiga toxin-producing E. coli
0157:H7 in selected diary and meat products marketed in the city of Rabat, 
Morocco. J. Food. Prot., 67: 1234-1237.
Bonfoh, B.; Wasem, A.; Traore, A.; Fane,
A.; Spillmann, H.; Simbe, C.;
Alfaroukh, I.; Nicolet, J.; Farah, Z.
and Zinsstag, J. (2003):
Microbiological quality of cow's milk
taken at different intervals from the
udder to the selling point in Bamako
(Mali). Food Control, 14: 495-500.
Bulajić, S. and Mjačević, Z. (2004):
Enterococci in cheese–phenotypization
and antibiotic resistance. Acta
agriculturae slovenica, 84(1): 25 : 30.
Chao, G.; Zhou, X.; Jiao, X.; Qian, X. and
Xu, L. (2007): Prevalence and
antimicrobial resistance of food borne
pathogens isolated from food products
in China. Foodborne Pathogens Disease,
4: 277-284.
Daka, D.; Silassie, S. and Yihdego, D.
(2012): Antibiotic-resistance
Staphylococcus aureus isolated from
cow’s milk in the Hawassa area, South
Ethiopia. Annals Clinical Microbiology
Antimicrobials, 11(26): 1-6.
Dharmilk, P.G. and Gomashe, A.V. (2011):
Isolation, characterization and antibiotic
susceptibility profile of Staphylococcus
aureus from raw milk samples in
Nagpur district, India. J. Appl. Nat. Sci.,
3 (2): 319-322.
Ekici, K.; Bozkurt, H. and Isleyici, O.
(2004): Isolation of some pathogens
from raw milk of different milch
animals. Pakistan J. Nutrition, 3 (3):
161-162.
El-Kholy, A.M. (1990): Incidence of Yersinia
enterocolitica in farm bulk milk. Assiut
Vet. Med. J., (54 (116): 133-141.
El-Leboudy, Ahlam, A. (1989): Potential
food poisoning organisms in some dairy
products at the consumer level. Ph.D.
Thesis, Fac. Vet. Med., Alexandria
Univ., Egypt.
Farzana, K.; Shah, S. and Jabeen, J. (2004):
Antibiotic resistance pattern against
various isolates of Staphylococcus
aureus from raw milk samples. J. Res.
Sci., 15 (2): 145-151.
Finegold, S.M. and Martin, W.J. (1982):
Bailey and Scott Diagnostic
Microbiology. 6th Ed., C.V. Mosby Co.,
St. Louis, Toronto, London.
Gajan, E.B.; Shirmohammadi, A.;
Aghazadeh, M.; Alizadeh, M.;
Deljavan, A. and Ahmadpour, F.
(2013): Antibiotic resistance in
Enterococcus faecalis isolated from
hospitalized patients. J Dental Res.
Dental Clin .Dental Prospect, 7(2):102-
104.
Gwida, Mayada, M. and EL-Gohary,
Fatma, A. (2013): Zoonotic bacterial
pathogens isolated from raw milk with
special reference to Escherichia coli
and Staphylococcus aureus in Dakahlia
Governorate, Egypt. 2: 705
doi:10.4172/scientificreports.705.
Hahn, G. (1996): Pathogenic bacteria of raw
milk situation and significance.
Proceedings bacteriological quality of
raw milk, IDF, Brussels (Belgium), 13-
15 March, pp: 67-83.
Hassan, S.A and Elmalt, Laila, M. (2008):
Informally raw milk and Kareish cheese
investigation on the occurrence of
toxigenic Escherichia coli in Qena City,
Egypt with emphasis on molecular
characterization. Assiut Univ. Bull.
Environ. Res., 11 (2): 35-42.
Hugot, J.P.; Alberti, C.; Berrebi, D. ;
Bingen, E. and Cezard, J.P. (2003):
Crohn’s disease: the cold chain
hypothesis. Lancet, 362: 2012-2015.
Hussien, M.F.; Amin, Manal, M.; Sadek,
O.A. and Koriem, A.M. (2013):
Occurrence and virulence of Yersinia
enterocolitica in raw and pasteurized
milk. Assiut Vet. Med. J., 59 (137): 51-
56.
Huys, G., D’Haene, K., Collard, J. C., and
Swings, J. (2004): Prevalence and
molecular characterization of
tetracycline resistance in Enterococcus
isolates from food. Applied
Environmental Microbiology, 70: 1555–
1562.
Javaid, S.B.; Gadahi, J.A.; Khaskeli, M.;
Bhutto, M.B.; Kumbher, S. and Panhwar, A.H. (2009): Physical and 
chemical quality of market milk sold at
Tandojam, Pakistan. Pakistan
Veterinary Journal, 29(1): 27-31.
Johnston, D. W.; Bruce J. and Hill, J.
(1983): Incidence of antibiotic-resistant
Escherichia coli in milk produced in the
west of Scotland. J. Appl. Bact., 54(1):
77-83.
Khudor, M.H.; Abbas, B.A. and Idbeis, H.I.
(2012): Detection of enterotoxin genes
of Staphylococcus aureus isolates from
raw milk. Basrah J.Vet. Res., 11
(1):254-264.
Koneman, E.W.; Allen, S.D.; Janda, W.M.;
Schreckenberger, P.C. and Winn,
W.C. (1992): Color Atlas and Textbook
of Diagnostic Microbiology. 4th Ed., R.
Winters, (ed.) Lippincott Company,
Philadelphia.
Kročko, M.; Čanigová, M.; ová, V. and
Artimová, A. (2011): Antibiotic
resistance of Enterococcus species
isolated from raw foods of animal origin
in South West Part of Slovakia. Czech
J. Food Sci., 29 (6): 654–659.
Larsen, J.H. (1980): Yersinia enterocolitica
infection and rheumatic diseases. Scand.
J. Rheumatol., 5: 207-215.
Levy, S.B. (1998): Antimicrobial resistance:
bacteria on the defence. British Med. J.,
317 (7159): 612–613.
Lopez-Diaz, T.M.; Santos, J.A.; Gonzales,
C.J.; Moreno, B. and Garcia, M.L.
(1995): Bacteriological quality of
traditional Spanish blue cheese.
Milchwissenschaft, 50: 503–505.
Mahami, T.; Odonkor, S.; Yaro, M. and
Adu-Gyamfi, A. (2011): Prevalence of
antibiotic resistant bacteria in milk sold
in Accra. Int. Res. J. Microbiol.
2(4):126-132.
Mannu, L.; Paba, E.; Daga, R.; Comunian,
R.; Zanetti, S.; Dupre, I.; Sechi, L.
(2003): Comparison of the incidence of
virulence determinants and antibiotic
resistance between Enterococcus
faecium strains of dairy, animal and
clinical origin. Int. J. Food Microbiol.,
88: 291-304.
Marth, E.H. and Steele, J.L. (2001): Applied
Dairy Microbiology. 2nd ed., Marcel
Dekker, Inc., New York.
McEwen, S.E. and Fedorka–Cray, P.J.
(2002): Antimicrobial use and
resistance in animals. Clinical
Infectious Diseases, 34: 93–10.
Meshref, A.M.S. (2013): Bacteriological
quality and safety of raw cow’s milk
and fresh cream. Slov. Vet. Res., 50 (1):
21-30.
Mohamed, Nahid, N. and El-Zubeir,
Ibtisam, E. (2007): Assessment of
microbial loads and antibiotic residues
in milk supply in Khartoum State,
Sudan. International J. Dairy Science, 2
(10): 33-41.
Mugampoza, D.; Muyanja, C.; Ogwok, P.;
Serunjogi, M.L. and Nasinyama,
G.W. (2011): Occurrence of Listeria
monocytogenes in bulked raw milk and
traditionally fermented dairy products in
Uganda. African J. Food Agriculture
Nutrition Development, 11 (2): 4610-
4622.
NCCLS (2001): Development of in vitro
susceptibility testing criteria and quality
control parameters, 2nd ed. NCCLS
document M23-A2. NCCLS, Wayne,
PA.
Nováková, I.; Kačániová, M.; Arpášová, H.;
Haščík, P.; Kunová, S. and Čuboň, J.
(2010): Antibiotic resistance of
enterococci and coliform bacteria in
dairy products from commercial farms.
Animal Sci. Biotech., 43 (1): 307-309.
Olawale, A.K.; Akintobi, A.O. and
Famurewa, O. (2010): Prevalence of
antibiotic resistant Enterococci in fast
food outlets in Osun State Nigeria. New
York Sci. J.3 (1): 70-75.
Oli, A.K.; Rajeshwari, H.; Nagaveni, S. And
Kelmani, C.R. (2012): Antimicrobial
susceptibility pattern of Enterococcus
species isolated from clinical samples in
South India. J. Recent Advances
Applied Sci., 27: 6-10.
Oliveira, Lílian, P.; Barros, Ludmilla, S.;
Silva, V.C. and Cirqueira, Marina, C.
(2011): Study of Staphylococcus aureus
in raw and pasteurized milk consumed
in the Reconcavo area of the State of
Bahia, Brazil. J Food Process Technol.,
2 (6): 1-6.
http://dx.doi.org/10.4172/2157-
7110.1000128.
Pourhassan, M. and Taravat, N. (2011): The
spatial distribution of bacteria
pathogens in raw milk consumption on
Malayer City, Iran. Shiraz E-Medical J.,
12 (1): 1-9. Available at
http://semj.sums.ac.ir/vol12/jan2011/88
047.htm.
Pugazhenthi, T.; Elango, A.; Kumar, C.;
Dhanalakshmi, B. and
Bharathidhasan, A. (2013): Antibiotic
sensitivity pattern of Yersinia
enterocolitica isolated from milk and
dairy products. Tamilnadu J. Vet.
Animal Sci., 9 (2): 14 -145.
Quinn, P.J.; Garter, M.E.; Markey, B.A.
and Carter, G.R. (2004): Clinical
Veterinary Microbiology. Published by
Wolfe Publishing, an imprint of Mosby
Elsevier Limited.
Roberts, D.; Hoopa, W. and Greenwood, M.
(1995): Practical Food Microbiology.
2nd ed., Public Health Laboratory
Service, London.
Schiemann, D.A. (1979): Synthesis of a
selective agar medium for Yersinia
enterocolitica. Canadian J.
Microbiology, 25: 1298-1304.
Singh, V.; Kaushal, S.; Tyagi, A. and
Sharma, P. (2011): Screening of
bacteria responsible for the spoilage of
milk. J. Chem. Pharm. Res., 3(4):348-
350.
Skočková, A.; Cupáková, S.; Karpíšková,
R. and Janštová, B. (2012): Detection
of tetracycline resistance genes in
Escherichia coli from raw cow’s milk.
J. Microbiology Biotechnology Food
Sciences, 1 (February Special issue):
777-784.
Soomro, A.H.; Arain, M.A.; Khaskheli, M.
and Bhutto, B. (2002): Isolation of
Escherichia coli from raw milk and
milk Products in relation to public
health sold under market conditions at
Tandojam. Pakistan J. Nutrition, 1(3):
151-152.
Subha, B.; Ramakrishnan, D. and Suganthi,
V. (2009): Antimicrobial resistance
pattern of selected Yersinia
enterocolitica isolates from raw cow
milk and pork samples of Namakkal
District, Tamilnadu, South India. Global
J. Environ. Resea., (3): 169-177.
Thabet, Salwa, S. (2003): Occurrence of
Escherichia coli in milk and some milk
products in Assiut City. M.V.Sci.
Thesis, Fac. Vet. Med., Assiut Univ.,
Egypt.
Thaker, H. C.; Brahmbhatt, M. N. and
Nayak, J. B.. (2013): Isolation and
identification of Staphylococcus aureus
from milk and milk products and their
drug resistance patterns in Anand,
Gujarat. Vet. World, 6 (1):10-13.
Thaker, H.C.; Brahmbhatt, M.N. and
Nayak, J.B. (2012): Study on
occurrence and antibiogram pattern of
Escherichia coli from raw milk samples
in Anand, Gujarat, India. Vet. World,
5(9):556-559.
Thompson, T.L. and Marth, E.H. (1986):
Changes in Parmesan cheese during
ripening: Microflora – coliforms,
enterococci, anaerobs, propionibacteria
and staphylococci. Milchwissenschaft,
41: 201–204.
Tolle, A. (1980): The Microflora of the
Udder, P4 In Factors Influencing The
Bacteriological Quality of Raw Milk.
International Dairy Federation Bulletin,
Document 120.
Tsakalidou, E.; Manolopoulou, E.;
Tsilibari, V.; Georgalaki, M. and
Kalantzopoulos, G. (1993): Esterolytic
activities of Enterococcus durans and E.
faecium strains isolated from Greek
cheese. Netherlands Milk Dairy J., 47:
145–150.
Vahedi, M.; Nasrolahei, M.; Sharif, M. and
Mirabi, A. (2013): Bacteriological
study of raw and unexpired pasteurized
cow’s milk collected at the dairy farms
and super markets in Sari City in 2011.
J. Prev. Med. Hyg., 54: 120-123.
Vidon, J.M. and Delmas, C.L. (1981):
Incidence of Yersinia enterocolitica in
raw milk in Eastern France. App.
Environ. Microbiology, 41(2): 355-359.
Virpari, P.K.; Nayak, J.B.; Brahmbhatt,
M.N. and Thaker, H.C. (2013): Study
on isolation, molecular detection of
virulence gene and antibiotic sensitivity
pattern of Escherichia coli isolated from
milk and milk products. Vet. World
6(8): 541-545.
Vyletělova, M.; Hanuš, O.; Karpiškova, R.
and Šťastkova, Z. (2011): Occurrence
and antimicrobial sensitivity in
staphylococci isolated from goat, sheep
and cow’s milk. Acta univ. Agric.
Silvic Mendel Brun 59 (3): 209214
WHO (2007): The world health report – A
safer future: global public health
security in the 21st century.
Yagoub, Sanaa, O.; Awadalla, Nazik, E.
and El Zubeir, Ibtisam, E.M. (2005):
Incidence of some potential pathogens
in raw milk in Khartoum North (Sudan)
and their susceptibility to antimicrobial
agents. J. Animal Veterinary Advances,
4 (3): 341-344.
Yameen, M.; Iram, S.; Mannan, A.; Khan,
S. and Akhtar, N. (2013): Nasal and
perirectal colonization of vancomycin
sensitive and resistant enterococci in
patients of paediatrics ICU (PICU) of
tertiary health care facilities. BMC
Infectious Diseases 13: 156165