Food safety and sanitation practices survey in very small halal and non-halal beef slaughterhouses in the United States

Introduction

Halal foods are defined as free from pork/pork products and alcohol. In addition, halal meats are produced using a distinct method of animal slaughter, which has the most religious restrictions compared to the production of other halal foods (1). Halal is also meant to include high-quality food production practices regarding food safety and sanitation conditions (2). Food safety refers to the conditions and practices that prevent contamination of foods with illness-causing bacteria, viruses, parasites, or chemicals which are a significant public health concern worldwide (3). United States Department of Agriculture (USDA)/ Food Safety and Inspection Service (FSIS) is responsible for ensuring meat supply is safe, wholesome, and correctly labeled and packaged (4). FSIS inspects all raw meat, including imported products, and verifies compliance with the Humane Methods of Slaughter Act for livestock (4). Animals and carcasses handled during the slaughter process can significantly affect human health regarding the spread of diseases (5). Therefore, it is essential to effectively prevent contamination from the intestinal contents during the animal de-hiding and evisceration (6). Foodborne disease is a preventable public health issue in the United States and worldwide. An estimated 9 million foodborne illnesses are attributed to significant pathogens per year, of which 12% are attributed to meat products (7). Awkward food safety practices and inadequate education and training of food workers are common sources of foodborne diseases (8). FSIS conducts carcass by carcass inspection at all federally inspected slaughter facilities, including halal slaughterhouses, and verifies that establishments follow food safety regulations. In 1995, USDA-FSIS Food Labeling Division approved a labeling policy to allow using “Halal” on meat and meat products which they are certified halal by Islamic authority (Halal Certifying Bodies) (9 CFR 412.1 (c) (1)). FSIS inspects more than 6,635 federal licensed slaughterhouses and food establishments. These food establishments vary in size and type of manufacturing. According to the FSIS Meat, Poultry, and Egg Product Inspection Directory, the number of the halal slaughterhouses that have USDA registration in the United States is approximately 89, including 9 halal poultry slaughterhouses (9). In addition to the above number, many large slaughterhouses produce halal and non-halal meat and poultry, such as American Foods Group, Tyson Foods Inc, and pilgrim's pride corporation. In general, Research Triangle International (RTI International) conducted a food safety practices surveys in the federally inspected U.S. meat slaughterhouses in 2005 and 2015 to provide a nationwide assessment of the food safety practices (10).

However, no specific data is available on the level of food safety and sanitation practices at the halal slaughterhouses in the United States. Therefore, we aimed to conduct two web-based surveys. One survey is specific to very small halal beef slaughterhouses. The other one is specific for very small non-halal beef slaughterhouses. To determine the level of food safety and sanitation practices implemented in these slaughterhouses to prevent microbial contamination during the slaughtering procedure and allow comparisons between the two categories.

Materials and methods

Informed consent

The research protocol of this study was approved by the Clemson University Institutional Review Board (IRB). The IRB is a federally mandated body established under the Department of Health and Human Services (DHHS) regulations for the Protection of Human Subjects (45 CFR 46). Its purpose is to protect the rights and welfare of human subjects recruited to participate in research activities conducted under the auspices of Clemson University (CU).

Target population

No specific database (list) was available for halal slaughterhouses in the United States. We contacted FSIS- Freedom of Information Act (FSIS-FOIA) and halal certifying bodies about the names and addresses of the halal slaughterhouses in the U.S to construct a list of halal slaughterhouses. Additionally, we used an online search and general database of the USDA (Meat, Poultry, and Egg Product Inspection Directory) to look for Muslim names and the word "Halal" to avoid missing any halal slaughterhouse in our list. To summarize our search, we found 80 pure halal beef slaughterhouses in the United States, and it is used in our survey. Also, FSIS- FOIA provided us a list containing 590 very small beef slaughterhouses to use in the food safety and sanitation practices survey of non-halal slaughterhouses.

Survey instrument

The questionnaire was adapted from an instrument developed by RTI International and used to collect data about food safety and sanitation practices, microbiological testing, employee food safety training, and slaughter operation characteristics (11). We modified the instrument by eliminating some questions and specific questions for the halal beef slaughter operations survey. We designed the questionnaire as a web-based survey (SurveyMonkey) and paper-pencil self-administered survey instrument. Two versions of the survey were available, one for non-halal beef slaughter operations which includes food safety and sanitation practices questions and one for halal beef slaughter operations which includes food safety and sanitation practices questions and series of questions about halal slaughter procedures. Pretesting the instrument was performed before it was administrated to our study sample to establish the instrument's validity and reliability and identify any areas of confusion or unfamiliar terms.

Sample design

Managers of 160 very small beef slaughterhouses (halal and non-halal beef slaughterhouses) in the United States were asked to participate in this study. All halal slaughterhouses were included in our sample (n=80). We used a systematic sampling approach to select 80 non-halal beef slaughterhouses to represent the population (590 non-halal slaughterhouses). The purpose of using systematic sampling rather than random sampling was to ensure that the selected sample includes slaughterhouses with varying characteristics, such as geographic region (Northeast, Midwest, South, and West), type of species slaughtered, such as beef, lambs, goats, swine (pig), and poultry and density of halal beef slaughterhouses in the states. The reasoning behind this approach is that the distribution of halal slaughterhouses was not equal in each state of the United States. We selected non-halal beef slaughterhouses that match the same density of halal beef slaughterhouses in each state. Figure 1 describes the geographical distribution of the selected samples (slaughterhouses).

Figure 1: Geographical distribution of halal and non-halal selected samples (slaughterhouses).

Email script and consent form

A letter (email or physical mail) describing the project aims and a link to the web-based survey was mailed to all halal and non-halal beef slaughterhouses in our sampling frame. Consent was assumed when the respondent completed the survey. A total of three contacts were made (either email or physical mail) with each category (halal or non-halal operation).

Survey administration

The surveys were administered using similar procedures as described in (10). The surveys were implemented for a period from August 2018 through January 2019. According to the slaughterhouse contact information, one option (mail or web-online option) was offered to the plant manager to complete the survey. A reminder postcard or email script was sent to each participant to complete the survey. Telephone calls were made to non-respondents and re-mailed the survey to non-respondents to encourage participation. All follow-up contacts helped to maximize the response rates.

Data analysis

Web-online survey responses (multiple choice answers) were entered into a database as a completed respondent. Physical copy survey responses were verified before data analysis. The response rate was calculated using the following equation: Response rate = Respondents/ (Respondents + non-respondents). All analyses were performed using JMP^® 16.1 software (12). We conducted all statistical survey estimates by applying appropriate survey weights to the respondent record data. We computed proportions for questions in which respondents could select one or more responses from a list of responses. Respondents who did not answer a question were not included in calculating proportions. The Chi-square test was used to determine if there was a significant difference between the expected and the observed frequencies of the small halal and non-halal slaughterhouses, computed means for all quantitative data. Results were significant, with a P-value < 0.05.

Results

Slaughterhouse characteristics

Table 1 presents the summarized slaughterhouse characteristics of respondents in this study. Out of the 80 halal slaughterhouses included in this study, 56.25% (45 out of 80) participated (response rate), while 63.75% (51 out of 80) participated in non-halal slaughterhouse surveys.Respondents were from different states for halal and non-halal slaughterhouses (great diversity). All halal respondents (100%) slaughtered cattle, sheep, and goats. Most respondents of non-halal plants (88.2%) slaughtered both pigs and cattle, while 11.8% slaughtered pigs, cattle, sheep, goats, and deer.

Table 1: Characteristics of halal and non-halal slaughterhouses

Food safety and sanitation practices

The survey asked about various food safety and sanitation practices during slaughtering and processing. The survey also collected information on other practices that slaughterhouses may adopt to promote food safety (Table 2). USDA inspectors were presented in all halal and non-halal slaughter operations. Of the preharvest practices, 29% of halal slaughterhouses and 12% of non-halal slaughterhouses washed the cattle before slaughter. Clean-up times of unloading areas were 57.8% daily, 28.9% weekly, 13.3% twice per month in halal operations, while 45.1% daily, 33.3% weekly, 11.8% twice per month, and 9.8% when needed in non-halal operations.

Table 2: Food safety and sanitation practices used during the beef slaughter of halal and non-halal slaughterhouse

For practices used during slaughter, most of the slaughter operations used chemical detergents and/or hot water for cleaning and sanitizing food contact surfaces (slaughter tools). The frequency of hand sanitizer employees in the slaughter area was not different between halal and non-halal slaughter operations. Other food safety practices were performed to prevent microbial contamination which was 84.4% of halal operations were performed by cutting around the rectum to free it from the carcass, while 88.2% were performed the practice in non-halal operations. All food safety and sanitation practices were not statistically different between small halal and non-halal slaughter operations.

Food safety technologies and microbiological testing practices

The most common interventions (antibacterial treatments) used in halal slaughter operations were a combination of treatments (cold water + hot water (180 °F) + organic acid) (31.1%) (Table 3). The most common interventions used in non-halal slaughter operations were hot water (180 °F) only (33.5%). Slaughterhouses may conduct food safety training for new hires and current employees. The training may be formal training conducted by professional trainers. More than half of halal slaughter operations provide formal food safety courses. On the other hand, the most popular type of training in non-halal slaughter operations was informal, unscheduled on-the-job food safety training with 54.9% (Table 3).

Table 3: Food safety technologies and microbiological testing practices used by halal and non-halal beef slaughter operations

* HACCP: Hazard Analysis Critical Control Point, SSOPs: Sanitation Standard Operating Procedures, GMP: Good Manufacturing Practice

All halal and non-halal slaughter operations conducted generic E. coli (100%). Nearly 70% of slaughter operations (halal and non-halal) conducted microbiological testing for E. coli O157:H7. All food safety technologies and microbiological testing practices used by halal and non-halal slaughter operations were not statistically different.

Discussion

USDA/FSIS conducts a carcass-by-carcass inspection at all federally inspected slaughter facilities, including halal slaughterhouses, and verifies that the slaughterhouse follows food safety regulations. Nearly all halal slaughterhouses were very small operations. However, all slaughter operations (very small, small, and large) followed the same food safety regulations during the slaughter. Therefore, we aimed to conduct this study to see any differences between halal and non-halal slaughter processes as an ethnic factor (halal for Muslim consumers) that may influence the slaughter process. There are differences between ritual slaughter (halal) and conventional slaughter methods in the United States. For example, most halal slaughter is not automated, and the daily slaughter rate is low. Furthermore, all slaughter steps are completed in a small slaughter hall, and the same worker is performed numerous tasks such as sticking, skinning, and evisceration on the same carcass (13).

This study showed no significant differences between halal and non-halal slaughter operations regarding food safety and sanitation practices, food safety technologies, and microbiological testing practices. This is due to several reasons: [1] both halal and non-halal slaughterhouses were the same size as slaughtering (both very small slaughterhouses). [2] both halal and non-halal operations were supervised by USDA/FSIS inspectors, resulting in strictly implemented food safety regulations. [3] the ethnic factor (the method of halal slaughter) had no effect on the slaughtering operations, which means there was no dereliction in applying food safety regulations in halal slaughterhouses.

 Very small slaughterhouses are flexible in using various food safety practices before and during slaughter. There were no significant differences in the pre-harvest practices between halal and non-halal slaughter operations, such as de-hide carcass methods, brisket saw cleaned, sanitized frequency and other practices performed to prevent bacterial contamination. The techniques and practices used were almost the same in both operations. However, large-sized slaughterhouses use more food safety technologies than small or very small slaughterhouses that tend to rely more on unautomated equipment (14). Larger slaughterhouses have higher speeds in the slaughter lines because they rely more on automated equipment to accommodate higher production rates (10).

On the other hand, producing safe meat is the primary purpose of using different food safety programs such as HACCP, SSOPs, GMPs, and other topics relevant to food safety systems and microbiological testing practices. All food safety technologies and microbiological testing practices used by halal and non-halal slaughter operations were not statistically different. In this study, all very small slaughterhouses (halal and non-halal) had at least a HACCP plan documented in their plants. Written programs are required to allow slaughterhouses to design their practices and approaches to suit the needs of their operations and meet standard regulations (15,16). Various practices are applied during the slaughter process. For example, antimicrobial interventions (organic acid, hot water, and cold water) are used before carcasses enter the chilling room to reduce the bacterial load on beef carcasses. Approval of antimicrobial interventions may be affected by FSIS approvals of intervention methods over time (17,18).

Following USDA/FSIS, slaughterhouses must perform a generic E. coli test for beef carcasses. However, slaughterhouses may voluntarily conduct other tests for carcasses, equipment, and food contact surfaces such as Listeria spp., Salmonella spp., and Staphylococcus (19,20). Control measures for E. coli O157:H7 and Salmonella include implementing the HACCP program in beef slaughterhouses and processing plants, proper handling during transport, proper cooking, and handling by consumers (21).

Conclusion

Halal meat produced in very small halal slaughterhouses did not differ from those produced in non-halal slaughterhouses (very small operations) regarding food safety and sanitation practices application. Both halal and non-halal slaughterhouses (very small size) have demonstrated that they follow all food safety regulations required by the USDA/FSIS for meat production and processing. Results of the study provide an overview of the current status of food safety practices in the very small slaughterhouses (halal and non-halal) and can help focus on some areas for future research and awareness efforts to assist meat plants in improving their food safety practices.

Acknowledgment

We would like to thank all the slaughterhouses that participated in this study. We appreciate their efforts.

Conflict of interest

The author of this manuscript stated there is no conflict of interest regarding the writing process or data analysis.