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Byline: Mamoona Chaudhrya, Haroon Rashidb, Manzoor Hussainc, Hamad Bin Rashidd and Mansur-ud-Din Ahmada

ABSTRACT: Total aerobic bacteria, Enterobacteriaceae, Coliforms, and Escherichia coli are used as indicators of poor microbiological quality. The present study was conducted to evaluate if chilled and processed skinless carcass contains less number of indicator microorganisms than with-skin carcass by conducting, total aerobic count (TAC) and Coliforms count. A total of 238, ready to cook carcass samples randomly collected were received from a commercial poultry processing plant near Lahore, Pakistan. The carcasses were comprised of two categories i.e. Skinless (n=119) and with-skin (n=119). Both categories were investigated to evaluate the microbial load over a period of twelve months.

The overall mean value of total aerobic count (4.01 log10 cfu/gm) when both categories were combined, was significantly larger than mean value of Coliforms count (2.92 log10 cfu/gm) at P less than 0.05. When each category was analyzed separately, statistically there was no significant difference in the counts of total aerobic bacteria between skinless carcasses (4.00 log10 cfu/gm) and with-skin carcasses (4.03 log10 cfu/gm). Likewise no difference in Coliforms count of skinless (2.90 log10 cfu/gm) and with-skin carcasses (2.95 log10 cfu/gm) was observed (P greater than 0.05). Consumer should not expect any difference in microbiological quality of skinless and with-skin chicken carcasses. The carcasses processed at a commercial processing plant are more hygienic than manually produced carcass or meat.

Key words: Coliforms count, Indicator microorganisms, Microbial quality, Skinless carcass, Total aerobic count.


In the recent years demand and consumption of poultry meat and its products has been increased due to advantages such as easy digestibility and availability. Pakistan poultry industry is also growing day by day and broiler meat production has considerably been increased upto 480 tones in 2006-07 as compared to 463 tones in the fiscal year 2005-2006 (Economic Survey., 2006-2007). Due to increased demand and production, the routine monitoring of quality of poultry meat is required for production of a safer product according to established standards for the consumption of public.

Processing of poultry carcass requires intensive microbiological quality control procedures as contamination of food with pathogens is a major public health concern worldwide (Mead et al. 1994). Most countries all over the world are trying hard to improve food quality to overcome foodborne illnesses and rising consumer concerns. In United State approximately 76 million food-borne illnesses are reported each year (Mead et al., 1999). The available epidemiological data about food-borne illness suggest that broiler meat consumption is still the primary cause and one of the main sources of food-borne infections in humans (Fitzgerald et al., 200).

Total aerobic bacteria, Enterobacteriaceae, Coliforms, and Escherichia coli are used as indicators of poor microbiological quality of carcass (Abu-Ruwaida et al., 1994; Capita et al., 2002; Nortje, et al., 1990; Stolle, 1988). During the slaughter and cleaning process most of these microorganisms are eliminated, but subsequent contamination is possible at any stage of the production process, from de-feathering, evisceration, and washing to storage by cooling or freezing (Kozacinski, et al., 2006; Mead, 2000). The Complete absence of these pathogens from broilers carcass is not possible but the risk of foodborne disease can be reduced substantially by minimizing their numbers by adopting different procedures e.g. separation of flocks, carcass decontamination and implementing a balanced and operational HACCP system (Goksoy et al., 2004; Unnevehr and Jensen, 1996).

Microorganisms from the environment, equipment and operator's hand can also contaminate meat. Further more, there are several reasons illustrating difficulties in control of contamination on broiler meat during processing. Some of them have been summarized by Mead (1989) e.g. the rapid rate of production keeps the birds in close proximity throughout processing, limitations in the design of processing equipment, including that used in scalding, defeathering, and evisceration, the difficulty of washing the abdominal cavity effectively after evisceration when the carcass remains whole, and retention of water by skin, which tends to entrap bacteria in the crevices and feather follicles (Lillard, 1989; McMeekin and Thomas, 1978; Notermans and Kampelmacher, 1974; Thomas et al., 1987).

Several studies revealed that skin of processed broiler chicken harbors diverse microflora (Hinton and Cason, 2007), which include bacteria that normally inhibit the skin of the live, healthy chicken (Thomas and McMeekin, 1980) and pathogens which contaminate the skin during various processing operations (Berrang et al., 2001a; Cason et al., 2007). It has been suggested that the flesh of a live animal is essentially sterile but during processing, bacteria on the skin surface may contaminate the flesh (Avens and Miller, 1973).

In Pakistan, Skinless carcass or meat is preferred than with-skin carcass by the customers. One reason could be the cultural custom of consumption of skinless meat and other reason could be the fear of consumer about low hygienic quality of skinned carcass. The consumer of poultry meat in Fig-3: Distribution of Coliforms count in skinless and with skin carcasses Pakistan also prefers freshly slaughtered chicken purchased from a traditional manually slaughtering shop than a frozen processed carcass. The present study was conducted to compare the skinless and with-skin chilled carcass for the evaluation of microbiological quality by measuring the level of microbial load i.e. total aerobic bacteria and Coliforms and also to compare the quality of frozen and processed with manually processed carcass.

The main objective was to determine if chilled skinless whole carcass results in less bacterial contamination than that with-skin carcass and also industrially processed carcass contain less contamination level than manually processed chicken carcass.


2.1. Samples

Samples were collected during August 1999 to July 2000. A total of 238 chilled whole chicken carcasses comprising of two categories i.e. skinless (n=119) and with skin (n=119), packed in sterile polythene bags were randomly collected from a commercial processing plant near Lahore, Pakistan and were received at quality control laboratory of that plant at 4degC for evaluation of microbial load. At the time of processing the chilled samples were placed at room temperature until hard freeze was replaced by a softened pliable (but still cold) form.

2.2. Microbiological Analysis

The complete process of microbiological analysis was performed under a sterile condition in a laminar flow to avoid contamination from environment. The samples were subjected to microbiological analysis according to standard procedures (APHA, 1992). In brief, 25 grams of meat from different parts of each whole carcass e.g. legs, thighs, breast, wings was removed with the help of a sterile scalpel and minced manually. It was then thoroughly mixed in 225 ml of Buffered peptone water (BPW, CM 509, Oxoid Ltd, Basingstoke, Hampshire, UK) after vigorous shaking

Table-1: Bacterial Load Determined in 238 Whole Chicken Carcasses.

Sample (n = 238)###Mean Log10 of bacterial counts +- S.D


Whole Chicken###4.01+-0.73###2.23-6.08###2.92+-0.60###1.30-4.89

Carcass (with

and without


Carcass (with

and without


Mean log10 cfu/gm value of TAC count was significantly larger than mean log10 of Coliforms count (P less than 0.05).

Table-2: Bacterial Load Determined in Whole Chicken Carcasses of Different Categories i.e. Skinless and with-skin

###Mean Log10 bacterial counts +- S.D

Micro-Organisms###Skinless (n=119)###With-skin(n=119)

TAC###4.00a +-0.75###4.03 a+-0.72

Coliforms###2.90 a +-0.64###2.95 a +-0.56

Decimal dilutions were prepared from the same diluent and 0.1 ml aliquots of appropriate serial decimal dilutions were poured into a petri dish. Total aerobic count test (TAC) was carried out on Standard plate count agar (SPCA; CM 463, Oxoid Ltd.) by pour plate method (in duplicate) and plates were incubated for 48 hours at 37degC. The enumeration of Coliforms bacteria was carried out in violet red bile agar (VRBA; CM 107, Oxoid Ltd). The VRBA plates were incubated at 37degC for 48 hours. Plates with approximately 25-250 colonies were selected for counting of results. Total numbers of colonies were counted after 48 hours from each plate.

2.3. Statistical Analysis

All bacterial counts (Total aerobic count and Coliforms count) were expressed as log10 colony forming units (cfu) before statistical manipulation. Results recovered from samples with and without skin were compared by One Way of Analysis of Variance (ANOVA) for each type of test (total aerobic count and Coliforms count) to determine difference in group means at P value [?] 0.05. All statistical analyses were conducted using R(c) Software (version 2.7.0 2008 Edition)1.


The mean log10 cfu/gm values for TAC and Coliforms count for whole chicken carcasses (both skinless and with-skin) are presented in Table-1, and mean log10 values for different categories of carcasses i.e. skinless and with-skin carcasses are given in Table-2.

In whole chicken carcass (both categories included), the total aerobic count ranged from 2.23 to 6.08 log10 cfu/gm and for Coliforms count it was between 1.30 to 4.89 log10 cfu/gm (Fig-1). The mean log10 value for TAC (4.01+-0.73) were significantly larger (P less than 0.05) than the mean log10 value of Coliforms count (2.92+-0.60).

Total aerobic count in skinless carcasses ranged from 2.23-6.00 log10 cfu/gm. It was a little higher in with-skin carcasses ranging from 2.43-6.08 log10 cfu/gm (Fig-2) but statistically there was no difference in the mean value of log10 of skinless (4.0+-0.75) and mean log10 value of with-skin (4.03+-0.72) carcasses (P= 0.74). Coliforms count in skinless carcass was a little bit higher ranging from 1.90-4.90 log10 cfu/gm as compared to with-skin in which it ranged from 1.30-4.70 log10 cfu/gm (Fig-3). Statistically the mean log10 values of Coliforms count were also not significantly different for skinless (2.90+-0.64) and with-skin (2.95+-0.56) carcasses (P= 0.34)

1R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL


The TAC and Coliforms count (table-1) were lower than many other studies. For example, Sofos (1994) has reported a microbial count ranging from 2.18 to 5.18 log10 cfu/gm for mesophilic aerobics and 1.82 to 5.82 log10 cfu/gm for Coliforms in refrigerated chicken carcasses. Capita, et al. (2002) also reported contamination level of 5.19 log10 cfu/gm for TAC in chicken carcasses in Spain, This value is also higher than one reported in present study. The level of Coliforms count reported by them was 2.73 log10 cfu/gm, this level is slightly lower than one reported in the current study i.e. 2.92 log10 cfu/gm.

In contrast to our results, Lillard (1989) found mean aerobic bacteria count in refrigerated poultry carcass as 3.71 log10 cfu/gm which is lower than our findings. The reason of this lower level could be that he processed the sample very shortly after slaughtering.

Abu-Ruwaida et al. (1994) detected the levels of TAC and Coliforms counts in refrigerated neck skin in Chicken Carcasses from slaughterhouses in Kuwait as 6.5 to 6.6 log10 cfu/gm and 4.1 to 4.9 log10 cfu/gm respectively. Izat et al. (1989) studied the aerobic count in chicken skin obtained from slaughterhouses before refrigeration in Arkansas and found a mean load of 5.55 log10 cfu/gm for TAC and 3.08 log10 cfu/gm for Coliforms count. Mead et al. (1993) found that the maximum final mean TVC on skin samples of chicken carcasses obtained after packaging from 4 broiler slaughter houses was 5.3 log10 cfu/gm. Coliforms count was 3.8 log10 cfu/gm in VRBD. The above results are higher than the ones described in the current study for with-skin carcasses i.e. 4.03 log10 cfu/gm (TAC) and 2.95log10 cfu/gm (Coliforms).

When comparing our results with the above studies, it was obvious that the carcasses produced at the local processing plant in current study have less no. of indicator bacteria than reported by many authors, It is concluded that the quality of meat or carcass produced at a local processing plant is satisfactory and hygienic.

The presence of bacteria on skinless as well as skin on carcasses remained an interesting issue for researcher. Conflicting results have been published by various authors regarding level of bacteria beneath the skin of poultry carcass. The study by Avens and Miller, (1973) supported the idea that the meat beneath the skin has lower contamination level, but Stern et al. (1995) reported that a carcass skinned after bleed still had 7.5 log10 cfu/gm of aerobic bacteria per rinse and according to them de-skinning did not guarantee freedom from bacteria.

In the current study the level of bacterial counts in skinless and with-skin carcasses were compared to investigate the hypothesis that with-skin carcass contains more number of bacteria than skinless carcass. The result showed that there is no significant difference in the microbial load of skinless and with-skin carcass (P greater than 0.05) as shown in Table-2. Berrang et al., (2001b) also investigated the bacterial population on broiler parts purchased from retail outlets in New York and found that broiler parts are not microbiologically different because of presence or absence of skin. In another study, Berrang et al.,(2002) reported that TAC were lower in skinless carcasses (5.8 log10 cfu/sample) but the Coliforms counts were not different (4.4 log10 cfu/sample) for skinless and (4.9 log10 cfu/sample) for with-skin carcasses.

The results of another study by Koszaciski et al.,(2006) disagree with the above studies as they reported that no. of aerobic mesophilic bacteria was higher in chicken breast (skinless) averaging 4.72 log10 cfu/gm as compared to chicken breast (with-skin) i.e. 3.67 log10.

In Pakistan, the demand and consumption of traditionally slaughtered fresh whole carcasses or meat is more than industrially processed chilled whole carcass or meat. A comparison of results was made with those who published result of traditional slaughtered fresh poultry meat. Amara et al. (1994) reported a high level of TAC (6.56 to 7.15 log10 cfu/gm) in fresh carcasses from traditional slaughtering shop in Morocco. This is higher than the results of this study i.e. 4.01 log10 cfu/gm for TAC from processed chilled whole carcasses. Cohen et al. (2007) also reported the highest bacterial counts (6.6 log10 cfu/gm for aerobic plate count and 3.8 log10 cfu/gm for fecal Coliforms) in poultry meat product. Samples were collected from the traditional slaughtering process during the host season. These high levels of microbial contamination reflect the poor hygienic quality of poultry meat in freshly slaughtered poultry on traditional shops.

Fliss et al. (1991) found a mean contamination level of TAC and Coliforms were 6.01 log10 cfu/gm and 3.95 log10 cfu/gm respectively in 30 poultry carcasses bought in from Tunisian markets. According to them, this higher count was also due to unhygienic traditional slaughtering methods, which was manual. These all studies showed a higher microbial count on manually slaughtered chicken as compared to processed and frozen carcasses from current study, which resulted in lower mean value of TAC (4.01 log10 cfu/gm) and Coliforms count (2.92 log10 cfu/gm).

The current study concluded that the level of bacterial population on skinless and with-skin carcass was not significantly different (P greater than 0.05) thus consumer should not expect any difference in the microbiological quality of skinless carcass than with-skin carcass. The level of microbial contamination was much lower in the chilled and processed carcass as compared to traditionally slaughtered meat. It indicates that meat or carcass processed and packed at a processing plant with operational HACCP system is more hygienic than traditional manual slaughtering shops. The level of TAC and Coliforms count were also lower than many studies which showed that the working efficiency of a local processing plant in Pakistan to be satisfactory.


The authors express their sincere thanks to Mr. Kohei Maketa for assistance in statistical analysis.


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Author:Chaudhrya, Mamoona; Rashidb, Haroon; Hussainc, Manzoor; Rashidd, Hamad Bin; Ahmada, Mansur-ud-Din
Publication:Science International
Article Type:Report
Geographic Code:9PAKI
Date:Dec 31, 2011

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