AN ASSESSMENT OF THE MICROBIOLOGICAL RISKS INVOLVED WITH QUAIL EGG QENA CITY, UPPER EGYPT.

AN ASSESSMENT OF THE MICROBIOLOGICAL RISKS INVOLVED WITH QUAIL EGG QENA CITY, UPPER EGYPT.

LAILA M. EL MALT

Department of Food Hygiene, Faculty of Veterinary Medicine, South Valley University, Qena Upper Egypt.

Email: lailael.malt@ymail.com

INTRODUCTION

Today, eggs remain a stable food within the human diet, consumed by people throughout the world. They are consumed worldwide in various dishes and considered very nutritious and a cheap source of protein. Though eggs are considered as complete food for growth and sustenance, studies indicated that microorganisms often contaminate eggs (MAFF, 2000 and Osei-Somuah et al., 2003).

Quail is the smallest avian species farmed for meat and egg production (Panda and Singh, 1990) and their eggs are used in the same manner as those of chicken. Quail eggs taste like chicken eggs but they provide a good alternative for some people who are allergic to chicken eggs (Shanaway, 1994). In addition, because of their small size and attractive appearance, quail eggs are used whole or sliced in salad and casseroles or served boiled or whole with a sauce (Martin et al., 1999).

Freshly laid eggs are generally devoid of organisms. However, following exposure to environmental conditions (for example, soil, dust and dirty nesting materials), eggs become contaminated with different types of microorganisms (Ellen et al., 2000 and Smith et al., 2000). Furthermore, these microorganisms may contaminate the egg contents either by penetration or withdrawal through pores of the shells (Harry, 1963 and Schoeni et al., 1995), and also through the transovarian route (Bruce and Drysdale, 1994). Some other factors such as environmental temperature and humidity influence the bacterial penetration and thus, enhance the infection and spoilage (Theron et al., 2003).

Food-borne diseases caused by microorganisms are a large and growing public health problem. Contamination of eggs and egg products with microorganisms can affect egg quality, which may lead to spoilage and pathogen transmission. This may induce cases of food-borne infection or intoxication to consumers, which constitute public health hazards. Several pathogenic microorganisms have been isolated from the surface of quail egg shells and contents. Among them, Listeria monocytogenes, Yersinia enterocolitica, Escherichia coli O157:H7, Salmonella and Campylobacterwere detected (Adesiyun et al., 2005).

Likewise, aflatoxins contaminate a vast array of foods and agriculture commodities, and produced by certain species of fungi. Such mycotoxins pose profound challenges to food safety widespread in many countries, especially in tropic and subtropical regions where temperature and humidity conditions are optimum for growth of moulds and production of toxins. The possible transmission of such toxic residues to edible eggs results in potential hazards to human health (Martins et al., 1998). Aflatoxin are known to be human carcinogens based on sufficient evidence of carcinogenicity in humans (Yaling et al., 2008).

Because of the continuous consumer demands worldwide for eggs, periodical assessment is required to offer safe and good quality eggs for consummation. The present investigation, was, therefore, planned to assess shell and interior quality of consumed eggs at retail levels in Qena city (Upper Egypt). Microbiological quality and presence of food pathogens   were investigated.

MATERIALS and METHODS

- Samples collection:

One hundred and fifty quail eggs (30) group (each group consists of 5 eggs) were collected from Qena (Upper Egypt) farms and were tested microbiologically. Preparation of egg shell samples:

• • Rinse solution method was carried out as reported by Perales and Audicana (1989).
• • Preparation of egg content samples:

 The eggs were prepared for evacuation of their contents according to Speck (1976).

• • Experimental techniques:

Ten fold serial dilutions up to 10^-6 were aseptically prepared from the rinse solution of egg shells, as well as, the homogeneous egg contents samples. Then subjected to the following examinations:

1- Aerobic plate count (A.P.H.A., 1992).

2- Enterococci count using KF Streptococcal agar (Deible and Hartman, 1976).

3- Total coliforms, faecal coliforms and E. coli using three tubes Most Probable Number (MPN) technique was employed (FAO, 1992). MPN was streaked on to Eosin Methylene Blue (EMB, OXOID, England). Typical isolates of E.coli were confirmed based on their IMVIC pattern according to Koneman et al. (2005).

4- Enumeration and isolation of viable yeast and mold using Sabourauds dextrose agar (Mislivec et al., 1992). The isolated fungi were identified according to different guidelines adopted by Raper and Fennell (1965); Pitt and Hocking (1997) and Klich (2002).

5- Isolation and identification of Staph. aureus.

• • Enrichment procedure, loopful of the incubated broth was streaked into plates of selective media˝ Baired Parker agar˝ (Finegold and Martin, 1982).
• • The identification was carried out using Gram staining, production of coagulase ,catalase and fermentation of mannitol (Bennett and Lancette, 1995).

6- Isolation and identification of Listeria species.

• Enrichment procedure: 1ml of each rinse solution, as well as, from homogenous egg contents was placed aseptically in the Listeria enrichment broth.

• Plating using Palcam medium (Curtis et al., 1989).

• Identification and species differentiation were carried out (Warburton et al., 2003) including Gram staining,Catalase teste, Carbohydrate fermentation, B-haemolysis on blood  agar and CAMP test.

7- Isolation and identification of Salmonella.

• • Pre-enrichment
• • Selective- enrichment according to Rappaport et al. (1956).
• • Selective plating using Xylose Lysine Desoxycholate agar (XLD; Oxoid).
• • Identification of isolates.
• • Morphological examination (A.P.H.A., 1992) motility test (Baron et al., 1994).
• • Biochemical identification by hydrolysis of Christensen urea agar (Koneman et al., 1992), triple sugar iron (TSI) agar reaction (Baron et al., 1994), Gelatin liquefaction test (Quinn et al., 1994) Indole test, Methyle red test, Voges Prskauer test, citrate utilization test (Koneman et al., 1992) and sugar fermentation reaction (A.P.H.A., 1992).
• • Serological identification according to Kauffmann (1974).

RESULTS

Table 1: Statistical analytical results of various microorganisms recovered from the examined quail egg shells / ml.

*Colonies could not be detect on the plates.

Table 2: Statistical analytical results of various microorganisms recovered from the examined quail egg Contents / ml.

Table 3: Frequency distribution of the positive shells and contents of quail eggs samples based on their total Coliform, Fecal coliform and E. coli counts.

Table 4: Incidence of Staph. aureus and Sal. spp. isolated from quail eggs samples.

    CNS = Coagulase Negative Staphylococci

Table 5: Incidence of Listeria species isolated from quail eggs samples.

Table 6: Incidence of fungi recovered from the examined quail eggs.

DISCUSSION

Although eggs are valuable and even indispensable food, they may play an important role in transmitting different diseases. Human infection due to consumption of infected eggs has been reported in numerous countries all over the world (Ko and Chang, 1995).

Results presented in Table 1 declared that the average counts of aerobic plate, enterococci, total coliforms,  faecal coliforms, E. coli and yeast and mold / ml of the rinsing solution of the examined quail eggs shell samples were 1 x10⁴, 7 x10², 5x10², 1x 10, .784 x10 and 9 x10³ml  ,respectively.

The average aerobic plate counts were counts 1 x10⁴ and 7 x10³ for shell and content of quail eggs were less than the accepted 10 x10⁵ cfu / ml as recommended by the International Commission on the Microbiological Specification for Food (ICMSF, 1998).

The most important index of microbiological quality is aerobic plate counts,  coliforms, yeast and mold counts and detection of specific pathogens and their toxins is recorded by A.P.H.A.(1992) as the microbial quality reflected the care with which quail eggs were handled and stored.

In addition from the data recorded in Table 2, it is evident that the average values of the aforementioned fresh homogenous contents were lower than that of examined quail eggs shells. This finding substantiates what has been postulated by Labaque et al. (2003); Jones et al. (2004) and Bahobail et al. (2012). Moreover, Humphrey (1994) reported that the final microbial load of egg contents depends on temperature and length of storage.

The results given in (Tables 1-2) pointed out that the average values of enterococci 7x10² and 1x10³ for shells and contents, respectively, of quail eggs nearly agree with El- Prince et al. (2003). Moreover, fecal coliform failed to detect in contents, these results agree to a certain extant with those obtained by Saleim and El- Prince (2000) in chicken eggs and El- Prince et al. (2003) in quail eggs. Also the results pointed out that E. coli was the most prevalent bacteria recovered from the egg shell in a percentage of 7% and an average. 784 x10 however E. coli could not be detected in egg contents. In contrast, the contamination of egg shell and content with E. coli was previously investigated by Abdel -Hady and Emara (1997); Chang (2000); Moustafa et al. (2001) and Sabreen (2001) also could isolate E.coli in an incidence of 5% from examined infertile quail eggs while El–Prince et al. (2003) found E.coli in egg shell in a percentage of 6% from quail eggs and Bahobail et al. (2012) found 3 (7%) of (n=45 pooled samples) had E. coli in their shells but not in the egg content in chicken eggs It has been stated that avian pathogenic E.coli causes airsacculitis, polyserositis, septicemia and other avian species. Avian pathogenic E.coli are found in the intestinal microflora of healthy birds and most of the disease associated with them are secondary to environmental and host predisposing factors (Dho-Moulin and Fairbrother, 1999). They also added that prevention and control of these infections include control humidity and ventilation.

The results in Table 3, revealed that the highest frequency distribution of positive samples of total coliform in shells quail eggs were 55% lied in the range of 10³- < 10⁴ cfu/ ml while in contents were 83% lied in the range of 10²->10³cfu/ml. The rest of the positive samples of total coliforms in shells were distributed as 36 and 9% lied between 10¹-> 10² and 10² > 10³cfu /ml. Otherwise the highest frequency distribution of positive samples of fecal coliforms and E. coli in shells were 100% lied in the range of          10¹->10² cfu/ml.

A health issue associated with quail eggs is their contamination by pathogenic bacteria in this study (Table 4), Staph. aureus was recovered from 12 (40%) and 5(17%) of the total examined shells and contents of quail eggs, respectively. As well the Staph. aureus scored higher percentage of contamination than that recorded by Korashy et al. (2008) and Abdel-Hameed and El–Malt (2009).

Additionally, Staph. aureus was detected in 17% of the content examined quail eggs. From Table 4, the low incidence of Staph. aureus in the egg contents may be due to the presence of lysozyme in the inner shell membrane which act as an effective agent against Gram positive organisms. Regarding CNS, they were isolated from 5 shell surfaces, (17 %) and 2 egg contents (7%) samples contamination.

In this study, L. gray was detected in examined eggs with low ratio 2 samples (7%) of 150 quail eggs (n=30 samples) in their shells but not in the contents (Table 5). El-Malt, and Abdel-Hameed (2009) examined table eggs obtained L. gray high ratio 13.33 % in egg shells and 11.71 in egg contents. The presence of Listeria species other than L.monocytogenes as indicators of the presence that organisms have been proposed Johnson et al. (1990). The presence of other Listeria species could be attributed to unsanitary measures during handling and transportation of eggs. Similar prevalence was found by Nitcheva et al. (1990) who isolated L. monocytogenes from the egg shells (1of 71 samples) but not from egg contents. In contrast, L. monocytogens was isolated with high frequency from samples of eggs collected at processing plants Leassor and Forgeding (1989) from the outer surface of the egg shells Likewise, Farber    et al. (1992). Sayed et al. (2009) found that egg shells were contaminated with 7% of Listeria spp. while no contamination was found in egg contents. On the other hand, Moore and Maddan (1993) recorded that 72% of raw blended egg samples were positive for Listeria spp. which 37.8% were identified as L. monocytogenes.

Failure to isolate Salmonella spp. from quail eggs in the current study may due to strict control measures applied against these bacteria. Similarly, Salmonella was absent in all samples analyzed by Favier et al. (2000) and Anon (2004). Other studies reported variable and very low incidence of Salmonella in eggs. Begum et al. (2010) only isolated three Salmonella strains out of 1100 domestic eggs. Also, Musgrove    et al. (2005) identified one out of 105 Enterobacteriaceae isolates, recovered from 84 shell surfaces, as Salmonella. Poppe et al. (1998); De Reu et al. (2006) and de Boer and Witt (2000) reported that 0.07 to 0.4% (egg shell and egg content), 0.18% and 0.03% of table eggs, respectively were Salmonella-positive. This variability in Salmonella occurrence may be due to sample size, timing of sampling, sites of the eggs that were tested, techniques used, and investigations of eggs lay by artificially or naturally infected hens (Humphrey, 1994).

The fungal load found averaged 9x10³ cfu /ml in eggs shells while averaged 6x10³/ ml in the contents (Tables 1- 2). However, lower fungal count was reported in table eggs Ahmed et al. (2002); Suba et al. (2005) and Salem et al. (2009) which was reported to be > 5 log ₁₀ cfu/ ml. Other studies indicated lower count of 1 log₁₀ cfu /ml in egg samples Ahmed et al. (1987) and El-Essawy et al. (1989). Jones et al. (2004) found an average fungal concentration of 1.5 log cfu/ ml egg shell in the day of egg collections while averaged o.1 log cfu/ml in the content, while Bahoball et al. (2012), the fungal load found averaged 1.3 log₁₀ cfu/ml.

It is apparent from results outlined in Table 6, that 16 (53%) and 8 (27%) fungi species belong to 6 genera were presented in samples of shells and contents, respectively. Pencillium was the most prevalent genus constituting 6(20%) it was represented by 4 species, P.crysogenum and P. funiculosum 1(3.3%), P. paxilli and P. cyclopium 2 (6.7%) in egg shells. However in egg contents, Pencillium was represented by 2 species P.cryscogenum and P. cyclopium 2 (6.7%). The genus Cladosporium ranked second in percentage of isolation constituting (16.7% and 6.7%) in shells and contents samples, respectively. Furthermore, Fusarium spp, Mucor heimalis, Trichoderma viride, and Trichothecium roseum were infrequently recovered from examined shell and content samples.

It is worth to mention that some of fungi species such as Fusarium moniliforme and Trichothecium rosarium are mycotoxin – producing molds which posses potential hazards to food safety and human health Martins et al., (1998). Likewise, Sanchez et al. (1980) studied the environmental fungus genera were encountered most frequently, furthermore different types of molds were isolated by several investigators as El-Essawy et al. (1989); Obi and Igbokwe (2007); Salam et al. (2009) and Bahobail et al. (2012). These molds including Penicillum, cladosporium, Aspergillus, Alternaria alternaria, Mucor, Rhizopus genera from examined avian eggs.

CONCLUSION

From the above achieved results, it is noted that quail eggs need more care during handling, also, they were liable to contamination by some pathogenic microorganisms. If such eggs are consumed raw or semi-raw may be responsible for sporadic or epidemic diseases. Moreover, some species of fungi encountered are known to be mycotoxin producers which threaten human health. Therefore, to safeguard human from being infected, the hygienic measures adapted in the farm during handling and storage are necessary to obtain good quality eggs and fit for human consumption. 

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