MATERIALS AND METHODS

Study area: The study was conducted in Tema Metropolis, Ghana from April-September, 2020. The Metropolis lies between latitude 5°38'32' North and longitudes 0°0'9' West and has a population of 29, 2773²⁷. The map of Ghana and Tema Metropolis (in yellow) where this study was conducted (Fig. 1).

Fig. 1:

Map of Ghana, Greater Accra Metropolis and Tema Metropolis (in yellow)

Ethics: The consent of the respondents was sought and only those willing to take part were interviewed. Furthermore, the respondents were assured of their confidentiality.

Data collection: A survey was conducted among butchers/meat sellers on their demographic characteristics, knowledge and perception of meat safety, antibiotic usage/resistance and antibiotic residues. The respondents were selected using a simple random design. A semi-structured questionnaire made up of both close and open-ended questions was used to obtain information from the respondents. Sample size determination was done according to Bartlett et al.²⁸. The population of butchers/meat sellers in Tema was 995 (personal communication with Tema Butchers/Meat sellers Association). Based on this population the sample size was computed to be 278 and the same were interviewed.

Data analysis: Data collected were subjected to analysis using Statistical Package for Social Sciences version 20, Armonk, NY. Chi-square (χ²) was used to determine the relationship among some of the data obtained at 5%.

RESULTS AND DISCUSSION

Demographic characteristics and information about butchers/meat sellers: The demographic characteristics of butchers/meat sellers can be found in Table 1. The majority of the butchers/meat sellers were males (75%) and between the ages of 21-40 years (46%). The majority were also single (69%), were Christians (42%) and had no formal education (51%). The majority of the respondents were both butchers and meat sellers (65%) and had more than 10 years of experience in butchering and selling meats as can be observed in Table 2. Mutton (27%), beef (25%), chicken (22%), chevon (15%) and pork (10%) were the meats mostly sold by the meat sellers. They sold these meats because of profit (44%) and based on consumers’ preferences (39%). The respondents were mainly involved in butchering/selling of meats business on a full-time basis (95%). COVID-19 harmed their business, especially in the areas of poor sales/low patronage (63%) and low supply of animals (28%).

This study revealed that the butchers/meat sellers were dominated by males, youth, single, Christians and people with non-formal education. Similar observations were made by Sulleyman et al.² in Accra and Adzitey et al.²⁹ in Tamale among meat sellers except for the percentage of Muslims involved in meat selling, which was higher in the study of Sulleyman et al.² and Adzitey et al.²⁹ compared to the current study. The majority were also both butchers and meat sellers and sold mutton, beef, chicken, chevon and pork based on consumers’ preference and for profit. The study also depicted that most of the butchers/meat sellers had more than ten years of experience in the butchering/selling of meat business and did that on a full-time basis. Adzitey et al.²⁹ also reported that the majority of meat sellers sold beef (62%), on a full-time basis (85%) and had more than 10 years of experience as meat sellers. COVID-19 harmed their business in that they made poor sales. Age (χ² = 674.467, df = 42, p = 0.000), education (χ² = 744.053, df = 42, p = 0.000) and years of experience in butchering/meat selling (χ² = 674.865, df = 42, p = 0.000) influenced the impact of COVID-19 on the butchering and meat selling business. COVID-19 was found to negatively impact the activities of cold chain operators and butchers in Ghana by Monten³⁰ and Adzitey et al.¹, respectively.

Knowledge and perception of butchers/meat sellers on microbiological meat safety: The butchers/meat sellers had heard about microbiological meat safety (71%) mostly from health officers (53%) and the media (38%) as can be seen in Table 3. The majority of the butchers/meat sellers knew that meat can be contaminated with bacteria/germs by poor handling and can cause foodborne diseases (62%), eating, drinking and smoking while selling meat increases the risk of its contamination (61%) and observance of meat hygiene by meat sellers/handlers reduces the risk of meat contamination (66%).

Fig. 2:

Bacteria that cause foodborne diseases-butchers/meat sellers response

According to the butchers/meat sellers, the best method for preserving meat is refrigeration (60%), followed by drying (23%). The reason is that these methods are appropriate (44%), cost-effective (40%) and safe (16%). The butchers/meat sellers had seen animals being slaughtered (63%) and did not like it (64%). Butchers/meat sellers preferred buying their meat from butcher shops (42%), open markets (35%) as well as supermarkets (15%) and considered the price (58%) as well as the neatness of the place (32%). Figure 2 shows that farmers knew some bacteria such as E. coli (48%), Bacillus spp. (48%), Campylobacter spp. (41%), Shigella spp. (41%), Listeria spp. (40%), Yersinia spp. (40%) and Salmonella spp. (39%) can cause foodborne diseases.

The study revealed that most butchers/meat sellers had heard about meat safety and heard about it from health officers, the media and schools. More so, most of the butchers/meat sellers had some knowledge of how meat is contaminated by bacteria, risks associated with certain practices of handling meat and means of reduction of meat contamination. Refrigeration was identified as the best method of preserving meat because it is safe, appropriate and cost-effective. Most of the butchers/meat sellers had seen animals being slaughtered but did not like it. In addition, most of them preferred buying meat from the open market and butcher’s shop because of the price and neatness of the place and meat. Age (χ² = 664.318, df = 18, p = 0.000), education (χ² = 744.053, df = 10, p = 0.000) and years of experience in butchering/meat selling (χ² = 681.802, df = 18, p = 0.000) by the butchers/meat sellers influenced their hearing of meat safety. The majority of the butchers/meat sellers interviewed did not know that Listeria spp., E. coli, Shigella spp., Salmonella spp., Yersinia spp., Bacillus spp. and Campylobacter spp., can cause foodborne diseases. Foodborne pathogens are one of the important sources responsible for morbidity and mortality worldwide. Education and training of butchers/meat sellers are necessary to create awareness and to help reduce the risk of transfer of these pathogens from animals to their carcasses during slaughtering and meat selling.

Adzitey et al.³⁰ found that education had a significant association with the hearing of meat safety among butchers. Adesokan and Raji³¹ reported that educational level had a significant association with knowledge, attitude and practice of meat safety among meat handlers. The finding of refrigeration as the best method of meat preservation in this study is also consistent with the findings of Adzitey et al.³² on the handling and storage of leftover meat by butchers in the Tamale Metropolis and Bolgatanga Municipality of Ghana.

Knowledge and perception of butchers/meat sellers on antibiotic resistance: The knowledge and perception of butchers/meat sellers on antibiotic usage are shown in Table 4. The butchers/meat sellers had heard about antibiotic resistance (52%) from health officers (76%) and had ever taken or used antibiotics (48%) to treat infections (51%) and injury (41%). The antibiotics ever used by butchers/meat sellers are presented in Fig. 3a. They were amoxicillin/clavulanic acid (66%), ciprofloxacin (50%), teicoplanin (47%), chloramphenicol (46%), tetracycline (43%), ceftriaxone (42%), gentamicin (37%), azithromycin (37%) and sulphamethoxazole/trimethoprim (36%). Those who had never used antibiotics stated that no one has ever prescribed antibiotics to them (50%), do not know antibiotics (40%) and have never been sick (9%). The butchers/meat sellers also knew that antibiotics have effects on humans (68%). Such effects include nausea and allergies (36%) as well as body reaction and pains (34%). Most of the butchers/meat sellers agreed (59%, slightly to strongly agree) that animals on antibiotics are sometimes slaughtered for sale. Generally, 67% of the butchers/meat sellers disagreed (slightly to strongly disagree) that locally produced meats on the Ghanaian market sometimes contain antibiotic-resistant bacteria (Fig. 3b), while 59% of them disagreed (slightly to strongly disagree) that imported meats on the Ghanaian market sometimes contain antibiotic-resistant bacteria (Fig. 3c).

This study showed that most of the butchers/meat sellers had heard about antibiotic resistance mostly from health officers. Close to half of the butchers/meat sellers interviewed had ever used antibiotics such as chloramphenicol, ceftriaxone, tetracycline, teicoplanin and gentamicin, ciprofloxacin, amoxicillin/clavulanic acid, azithromycin and sulphamethoxazole/trimethoprim to treat infections, injuries, sore throat and body pains.

Fig. 3(a-c):

Knowledge and perception of butchers/meat sellers on (a) antibiotic usage and antibiotic resistant bacteria in (b) local and (c) imported meats

Knowledge and perception of butchers/meat sellers on antibiotic residues: The knowledge and perception of butchers/meat sellers on antibiotic residues are presented in Table 5. Most of the butchers/meat sellers had heard about antibiotic residues (51%). They heard of antibiotic residues from health officers (60%), teachers (13%), their colleagues (12%) and the media (11%).

Most of the butchers/meat sellers did not know that: (1) antibiotic residues can occur in humans (49%), (2) antibiotic residues can occur in bacteria/germs (49%), (3) antibiotic residues are molecules that remain in meat from animals that have been treated with antibiotics (51%), (4) antibiotic residues in meat can be reduced by observing withdrawal periods (57%), (5) antibiotic residues can be transferred from meat to humans via consumption (60%) and (6) animal farmers play a significant role in antibiotic-resistant residues in meat (46%). The butchers/meat sellers have heard of the following antibiotic residues: Amoxicillin (62% butchers/meat sellers), chlortetracycline (52% butchers/meat sellers), ciprofloxacin (52% butchers/meat sellers), danofloxacin (47% butchers/meat sellers), doxycycline (44% butchers/meat sellers), norfloxacin (55% butchers/meat sellers), oxytetracycline (41% butchers/meat sellers), sulfadiazine (38% butchers/meat butchers/meat sellers), tylosin (47% butchers/meat sellers), chloramphenicol (39% butchers/meat sellers) and metronidazole (38% butchers/meat sellers) in Fig. 4a. In addition, 53% of the butchers/meat sellers disagreed (slightly to strongly disagree) that locally produced meats on the Ghanaian market sometimes contain antibiotic residues (Fig. 4b), while 55% of them agreed (slightly to strongly agree) that imported meats on the Ghanaian market sometimes contain antibiotic residues (Fig. 4c).

This study revealed that most the butchers/meat sellers had heard about antibiotic residues such as Amoxicillin, chlortetracycline, ciprofloxacin, danofloxacin, doxycycline, norfloxacin, oxytetracycline, sulfadiazine, tylosin, chloramphenicol and metronidazole mostly from health officers. However, most of them did not know that antibiotic residues can occur in humans, bacteria and meats from faulty usage of antibiotics and consumption of meats.

Fig. 4(a-c):

Knowledge and perception of butchers/meat sellers on (a) antibiotic residues and their presence in (b) local and (c) imported meats

The majority of them also did not know that withdrawal periods can reduce the occurrence of antibiotic residues in meats and that farmers play a key role in the deposition of antibiotic residues in meats. Most of the farmers disagreed that locally produced meat contained antibiotic residues but not imported meats. Age (χ² = 673.186, df = 24, p = 0.000), education (χ² = 722.220, df = 24, p = 0.000) and years of experience in butchering/meat sellers (χ² = 696.855, df = 24, p = 0.000) of the butchers/meat sellers influenced their knowledge in antibiotic residues. Antibiotic residues occur in meats when farmers treat animals with antibiotics and withdrawal periods for these antibiotics are not observed before slaughtering. Poultry farmers mentioned that one of the effects of using antibiotics is the occurrence of drug residues in animal products³⁵. Butchers can contribute to reducing this incidence by asking for the health status and treatment history of animals before purchase and slaughter.

CONCLUSION

The majority of the butchers/meat sellers were males, young and had no formal education. Butchering and meat (beef, chevon, chicken, mutton, pork) selling was mainly done on a full-time basis and COVID-19 harmed their business. Most butchers/meat sellers had heard about microbiological meat safety, antibiotic resistance and antibiotic residues. Most of the butchers/meat sellers disagreed that locally produced and imported meats on the Ghanaian market sometimes contain antibiotic-resistant bacteria. Most of the butchers/meat sellers disagreed that locally produced meats on the Ghanaian market sometimes contain antibiotic residues but agreed on the same for locally produced meats. Education of butchers/meat sellers on antibiotic usage and its consequences is warranted as it will contribute to reducing the spread of antibiotic resistance.

SIGNIFICANCE STATEMENT

Antibiotic resistance and residues hurt human health, such as leading to prolong or fail treatment regimes, allergies, mutation of cells and sometimes death. Key to the acquisition of antibiotic resistance and residues is the use of antibiotics in animal farming, faulty slaughtering/processing and selling of meat under unhygienic conditions. Therefore, hygienic slaughtering and selling could contribute to reducing the menace of antibiotic resistance and residues. Knowledge and perception of butchers/meat sellers in microbiological meat safety, antibiotic usage/resistance and antibiotic residues will help stakeholders to know areas where education is needed since butchers/meat sellers can play significant roles in reducing the menace of multi-resistant germs and deposition of antibiotic residues that pose threat to human life.

ACKNOWLEDGMENTS

The authors are grateful to the butchers/meat sellers who willingly took part in this survey. The authors also acknowledge the staff of Tema Food and Drugs Authority for their assistance with data collection.