Awareness of human health risks associated with the use of antibiotics among livestock keepers and factors that contribute to selection of antibiotic resistance bacteria within livestock in Tanzania

A A S Katakweba, M M A Mtambo*, J E Olsen** and A P Muhairwa*

Pest Management Centre, Sokoine University of Agriculture, P.O. Box 3010, Morogoro, Tanzania.
katakweba@suanet.ac.tz   or   selemani.abdul@yahoo.com
* Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, P.O. Box 3021, Morogoro, Tanzania
** Department of Veterinary Disease Biology, Copenhagen University, Stigboejlen 4, DK-1870 Frederiksberg C. Denmark

Abstract

Awareness of human health threats due to the use of antimicrobials in livestock and the factors that can contribute to selection of resistant bacteria were assessed among 160 randomly chosen Tanzanian small-scale livestock keepers.  Thirty percent of the respondents were not aware of the concept of antibiotic resistance, 52% were not aware of which types of diseases can be treated with antibiotics, 22% did not know the principle of withdrawal period after treatment of animals with antibiotics and 40% did not know if antibiotics used in livestock pose risk to human health. Side effects of antibiotics to human beings stated by the respondents included drug resistance, allergy, poisoning, skin rashes, cancer and resistance to treatment. The most commonly used antibiotics were oxytetracyline (62.9 %), sulphadimidine (23.2 %), penicillin-streptomycin (13.4 %) and gentamycin (0.5 %). Points of selling antibiotics and their prescriptions were found to be agriculture and veterinary implements shops, veterinarians, livestock markets and exhibition areas. Only 54 % of respondents obtained their antibiotics through prescription by veterinarians. Livestock management systems, antibiotics handling and types of antibiotics used in the study areas were identified as potential risk factors to the development of antimicrobials resistance. This study has revealed gross lack of awareness on health threats associated with antibiotics resistance among the farming communities posing serious public health threats in Tanzania

Key words: antibiotic prescriptions, antibiotic sources, education, management systems

Introduction

Domestic animals are found everywhere in poor communities across the developing world, and high rates are even found in the most densely populated, lower-income urban areas, where farm animals are in close contact with people. The poor livestock keepers often stock a mix of different species, trading off specialization for better protection against risks (Randolph et al 2007). Regardless of the important role on the economy and social life, livestock expose the animal keepers, the environment and consumers to agents of zoonotic infections and food-borne diseases.

Infectious zoonotic agents, as well as non-zoonotic diseases that are affecting livestock, are commonly treated with antibiotics (WHO 2007). All antibiotics used in veterinary medicine are the same or closely related to antibiotics used in human medicine, or they may induce cross-resistance (Ungemach et al 2006). The veterinary use of antibiotics, including the use growth promoters in livestock, is therefore thought to be a risk factor for the emergence of antibiotic resistance in human pathogens (Lathers 2002), and the use of antibiotics in livestock is considered as one of the reasons for increased occurrence of antibiotic resistant strains of bacteria in both animals and human beings (Callie et al 2012).

Antibiotic resistant bacteria can be transferred from animals to humans and vice versa, and food-borne transmission through food of animal origin is a recognized risk.  For example, a study conducted in the Washington DC found 20 % of the sampled meat was contaminated with Salmonella spp and 84 % of those bacteria were resistant to antibiotics used in human medicine and animal agriculture (Swartz 2002). Workers in the livestock industry may pick up resistant bacteria by handling animals, feed, and manure, and they can then transfer the bacteria to family and community members (Van den Bogaard et al 2002). Manure that contains resistant bacteria creates an immense pool of resistance genes available for transfer to bacteria that cause human and animal diseases. Farm wastes are spread on agricultural fields as fertilizers, and waste run-off can enter rivers, lakes, and ground water (Osterberg and Wallinga 2004). 

Antibiotic abuse is prevalent in most developing countries; however, the extent to which it contributes to antibiotic resistance has not been quantified. According to Komolafe (2003) and Carlos (2010) treatment and handling of infectious diseases in most developing countries is left in the hands of undertrained physicians, drug sellers, livestock keepers, owners of implement shops and untrained personnel.  However, there is no published work on the awareness of livestock keepers in developing countries about antibiotic resistance as a problem and their role in controlling this problem. The aim of this study was to find out how livestock keepers in Tanzania generally obtain antibiotics, what determines the choice of antibiotic, if they were aware of any potential health risks due to the use of antibiotics in their animals, and more generally to identify risk practices that could contribute to development of antimicrobial resistance.

Materials and methods

Study area and livestock composition

The study was carried out in both Kinondoni (urban and peri urban) and Morogoro (urban, peri urban and rural) districts in Dar-es-Salaam and Morogoro regions respectively. The study was conducted between July 2010 and January 2011. The sampling frame was district, wards, and finally a household with livestock. Random sampling was used to pick the districts and wards with large numbers of dairy and beef cattle, layers and broiler chickens, pigs and indigenous scavenging chickens. This type of sampling was very useful because livestock keepers were rearing livestock commercially, used a lot of antibiotics and all targeted livestock species were found in the study areas. In each district four wards were selected, hence, a total of 8 wards were surveyed in both districts. Within a ward, the list of livestock keepers was used as a sampling frame from which respondents were randomly picked using a Table of random numbers. The heads of the households (father and mother) were the main respondents; however, other members of the household attended the interview in the absence of heads of households. Where the livestock project belonged to a group of people the group leader was interviewed on behalf of others. 

Data collection

Data collection followed the approach described by Gonsalves et al (2005). Briefly, the work included individual interviews using semi-structured questionnaire and participant observation. Individual interviews of selected livestock keepers were conducted using questionnaires targeting household heads. Both closed and open-ended questions were included in the questionnaires. The information sought included household bio data characteristics (age, education, family position and employment), livestock (types of livestock, experience on livestock keeping, purpose of keeping livestock, duration of keeping livestock), herd size, types of antibiotics commonly used and stored, sources of antibiotics, involvement in antibiotic prescription, knowledge on the effects of using animal products treated with antibiotics to humans. 

Data analysis

Data derived from questionnaires were recorded into the spreadsheets for statistical analysis. The data were analyzed using EPI INFO statistical software Release 3.5 (June 2008) and descriptive statistics such as: means, standard deviations, frequencies and percentages were generated.

Results

Respondents demographic information

Demographic information on the 160 respondents regarding sex, age, family role, education and occupation is summarized in Fig 1. The majority of the livestock keepers (84%) with ordinary and primary school education levels were mainly dependent on the income from livestock, while post secondary school (degree and diploma) commonly had other occupations..

Figure 1. Demographic information of respondents in the study area ("Y" axis is percentage)

Respondents in the study area mentioned the types of livestock they were keeping. The majority of the livestock keepers were rearing chickens. Other species included pigs, dairy cattle, beef cattle, goats and rabbits. Some of the respondents had more than one species of animals in the same area with different management systems (Table 1).

Management of animals in the studied area was divided into four systems namely indoor, free range, grazing and both grazing and indoor. Different types of livestock were associated with different management systems. Beef cattle had free range, grazing and indoor, dairy cattle had grazing, indoor and both indoor and grazing, Broiler, layers and also pigs had indoor systems. Indigenous chicken had free range. Both family and hired labor were used in the study area. The hired labor was sometimes shared (8.9 % of cases) by neighbors.

Use of antibiotics and antibiotics stored in the farms during the study

The most used and commonly reported antibiotics were tetracycline, sulphadimidines and penicillin-streptomycin (Table 2). The same drugs were found in the stores of individual livestock keepers. The information obtained from respondents and antibiotics found in stores confirmed that antibiotics were used in the study area for treating livestock.

Knowledge on antibiotic resistance and rules for use of antibiotics in animals

Thirty percent (48) of respondents had never heard of antibiotic resistance in humans and animals (Table 3). Other respondents had heard the information from different sources including seminars and workshops (10), brochures and books (13), exhibitions (19) radio and TVs (26), Veterinarians (35) and livestock field officers (9). Thirty six of respondents (22.5%) had not heard of withdrawal periods after use of antibiotics and did not observe such a period.

Prescription of antibiotics and sources of antibiotics for use in livestock

Livestock keepers in the study area received services of prescription of antibiotics to treat their livestock from different sources (Table 4). The majority used veterinary services, others obtained the services from the implement/agricultural shops that were involved in selling livestock antibiotics. Field officers within the study area also provided clinical veterinary services. Other livestock farmers used their own knowledge without consulting other experts. Few livestock keepers depended on their neighbors for the same service and the rest from drug sellers in the markets.

As can be seen from Table 4, most of livestock keepers purchased their antibiotics from agriculture and veterinary implement shops and Veterinarians, but also livestock field officers, neighbors, livestock markets; mobile vet drug shops and exhibition areas.  

Actions taken by livestock keepers when antibiotics failed

The respondents were asked how they reacted to failure of antibiotic treatment. The responses that were given included change of medications without consulting anybody (25 %). They also used wood ash, kerosene and herbs (12.6 %) (Aloe vera and neem tree (Azadirachta indica)) to treat their animals. Others consulted farm and veterinary implement shops (7.6 %), field officers (14.3 %), veterinarians (35.1 %), pharmacists (3.6 %) and neighbors (1.8 %).

Awareness about possible impact on human health from the use of antibiotics in livestock

When livestock keepers in the study area were asked if they knew any possible effects on human health from the use of antibiotics in animals, forty percent (64) of respondents said they new nothing regarding any effect, while sixty percent (96) said that there were possible effects when animal products from animals treated with antibiotics were consumed (Figure 2). The most commonly mentioned effects were deaths to humans, body swelling, diarrhea, drug residues in animal products, itching, poison to humans, resistance of bacteria to drugs, skin lashes, stomach problems, body swelling, cancer and flue.

Figure 2. Health effects on human after eating animal products from livestock treated with antibiotics – as mentioned by respondents.

Discussion

Livestock keepers in the study area used antibiotics to treat their livestock when they felt sick, and in addition, those who were keeping layers and broilers also used antibiotics for prophylaxis. Forty percent of livestock keepers were not aware of possible human health threats caused by the use of antibiotics in livestock, few had heard what antibiotic resistance meant, and few observed a withdraw periods after using the antibiotics. Together, these results show that a selective pressure for antibiotic resistant bacteria was present, but that the majority of livestock keepers were not aware of the health threats that can emanate from their use of antimicrobials, nor that their livestock management systems and handling of antibiotics is the most important risk factors for the development of antimicrobials resistance in livestock in Tanzania.

The results confirm previous reporting from a rural district in China on lack of knowledge on prudent use of antibiotics and antibiotic resistance in developing countries (Chenggang et al 2011). This could be due to low level of education of the respondents as majority of them had primary and secondary school education. A socio-demographic analysis conducted by SPECIAL EUROBAROMETER 338 in 2010 within European countries (European Commission 2010) reveals that women seem to be better informed than men on this topic and age also plays a role and as regards to knowledge of antibiotics. Respondents who have gone on to higher education are also more likely to have a better knowledge of the effects of antibiotics. Another factor could be the lack of formal livestock keeper education and good advisory services in most developing countries. In the developed countries, formal education and good communication measures through advisory services have been used by health professionals to communicate this issue of antibiotic resistant to lay people that are lacking biomedical knowledge (Chenggang et al 2011).

The most important factors that may contribute to antibiotic resistance problems in developing countries, such as Tanzania, have been proposed to include 1) lack of access to appropriate antimicrobial therapy, 2) lack of regulation in use of antibiotics for human and animal, 3) lack of surveillance of antibiotic use and resistance levels, 4) lack of updated antibiotic use and treatment guidelines, and 5) lack of continuing medical education on antibiotic use for prescribers (Mtenga et al 2011). Based on the current study, lack of basic knowledge on the concept of antibiotic resistance among livestock keepers should be added to that list.

WHO (2001) has defined prudent (or optimal) use of antibiotics in food animal production as the cost-effective use of antimicrobials which maximizes clinical therapeutic effect, minimizes drug-related toxicity and minimizes the development of antimicrobial resistance. In order to have proper use of antibiotics, prescription, delivery and record keeping of antibiotics used in livestock should be under the care of the prescribing veterinarian, and all therapeutic antibiotics should be supplied by, or with a prescription from a veterinary surgeon. The present findings show that only half of the livestock keepers in the study area obtained antibiotics for animal treatments with veterinary prescription. The remaining antibiotics were supplied in the shops without any prescription and were dispensed by untrained personnel in the shops. Furthermore livestock keepers without consulting veterinarians changed the antibiotics once they thought that the former ones used were not effective; over and above they also used indigenous herbs.

Komolafe (2003) and Carlos (2010) found that antibiotic abuse is one or perhaps the most important cause of the high prevalence of resistance among bacteria. This includes the use of wrong antibiotics, wrong doses, or the use of antibiotics for diseases that cannot be treated with antibiotics. Findings by Karimuribo et al (2005) stressed that this may be a particularly relevant problem in the least developed countries, since animal health services have been sub optimal with an increased tendency for animal owners to stock drugs in their houses and engaging unskilled people such as farmers themselves and animal attendants to treat the animals.  In another study Mmbando (2004) found a high degree of drugs abuse by livestock keepers through failure in observing the recommended therapeutic doses, use of wrong routes of administration, arbitrary drug combinations and non observance of withdraw periods, all known causes of developing and promoting spread of resistance to antibiotics (Iruka and Ojo 2010). This study supports these observation, and it has shown that there is a need for better information to uneducated livestock keepers on how, when and why to use antibiotics. Further, regulation on antibiotic use and prescription needs to be improved. Recommendations for policymakers should stress those antimicrobial agents should not be used in agriculture in the absence of disease. Use of antimicrobials for economic purposes such as growth promotion or feed efficiency should be discouraged. Antimicrobials should be administered to animals only when prescribed by a veterinarian and improved surveillance and national regulation is needed in both human medicine and food animal production to ensure that antibiotics are used prudently.

Although the extent of antibiotic use in animals in developing countries is unknown, one study from Kenya reported that tetracyclines, sulfonamides, and aminoglycosides were the most commonly used antimicrobials for veterinary purposes. Over 90 percent of the antibiotics used were for therapeutic purposes. This study has shown that tetracyclines,  sulphadimidines and penicillin-streptomycin were the most commonly used antibiotics in the study area. The same drugs were found in the stores of individual livestock keepers for the first time in Tanzania confirming the validity of the responses given by the livestock keepers. Frequent use of same antibiotics for long time has been shown elsewhere to cause selective pressure to bacteria resistant to those specific antibiotics (Lathers 2002; Serrano 2005; Carlos 2010).

Conclusions

• Misuse of antibiotics in livestock in a developing country such as Tanzania is high, and the current study shows that this may in part simply be due to lack of knowledge.

• Many of the livestock keepers were not aware of the concept of antimicrobial resistance and did not know that use of antibiotics can have effects on health of their animals and their own health.

• Many factors were identified, which could contribute to development of antibiotic resistance in the study area, not least that antibiotics are prescribed, sold and used by unskilled personnel.

Acknowledgements

This study was supported by DANIDA through the project Transforming Smallholder Livestock Farms into Profitable Enterprises (Livestock Enterprises) with grant number 66-08-LIFE. The authors wish to thank the District Livestock Officers in Morogoro and Kinondoni districts and the Ward Extension Officers in the study areas for the assistance they provided during the field work. We acknowledge the livestock keepers who voluntarily participated in this study and provided relevant information regarding them and their animals on the whole issue of antibiotics.

References

Callie H T, Amy P, Robert E J, Partha P R and Katharine F K 2012  Excretion of Antibiotic Resistance Genes by Dairy Calves Fed Milk Replacers with Varying Doses of Antibiotics, Journal of Front Microbiology 3:139.   
 

Carlos F 2010 Global Perspectives of Antibiotic Resistance. In: Anı´bal de J. Sosa Denis K. Byarugaba Carlos F. Ama´ bile-Cuevas Po-Ren Hsueh Samuel Kariuki Iruka N. Okeke(Editors). Antimicrobial resistance in developing countries. US Springer Science and Business Media pp 3 - 14
 

Chenggang J, Adrian E, Lijie F and Xiaoyun L 2011 Framing a global health risk from the bottom-up: User perceptions and practices around antibiotics in four villages in China  13  (5) 433-449
 

European Commission 2010 E C. SPECIAL EUROBAROMETER 338 2010 “Antimicrobial Resistance” TNS Opinion & Social Avenue Herrmann Debroux, 40 1160 Brussels Belgium http://ec.europa.eu/health/antimicrobial_resistance/docs/ebs_338_en.pdf
 

Gonsalves J, Becker T, Braun A, Campilan D, De Chavez H, Fajber E, Kapiriri M, Rivaca- Caminade J and Vernooy R  (eds) 2005  Participatory Research and Development for Sustainable Agriculture and Natural Resources. Pp: 1 - 276 http://www.idrc.ca/openebooks/181-7/

Iruka N O and Ojo K K 2010 Antimicrobial resistance and use in Africa. In: Anı´bal de J. Sosa l Denis K. Byarugaba l Carlos F. Ama´ bile-Cuevas l Po-Ren Hsueh l Samuel Kariuki l Iruka N. Okeke (Editors). Antimicrobial resistance in developing countries, US Springer Science and Business Media, pp 301-314.

Karimuribo E D, Mdegela R H, Kusiluka L J M and Kambarage D M 2005 Assessment of drug usage and antimicrobial residues in milk on small holder farms in Morogoro, Tanzania, Bulletin Animal Health and Production 53: 234 – 241

Komolafe O O 2003 Antibiotic resistance in bacteria- an emerging public health problem, Malawi Medical Journal 15(2) 63 – 67.

Lathers C M 2002 Antibiotic use Selects for Resistance in Pathogenic Bacteria and in the Endogenous Flora of Exposed Animals and Humans, Journal of Clininical Pharmacology 42(6) 587-600

Mmbando T L 2004 Investigation of OTC used and abuse, Determination of its residues in meat comsumed in Dodoma and Morogoro Municipalities. MSc Thesis, Sokoine University of Agriculture, Morogoro, Tanzania. pp 19 -27

Mtenga A, Emanuel M, Mabula J and Peter R 2011 Consumer and Practitioner Education: Status of Antibiotic Resistance Alliance for the Prudent us of Antibiotics (APUA 136 Harrison Avenue, Boston. http://www.tufts.edu/med/apua/intl_chapters/tanzania.shtml

Osterberg D and Wallinga D 2004 Addressing externalities from swine production to reduce public health and environmental impacts, American Journal of Public Health 94(10) 1703–1708.

RandolphT F, Schelling E, Grace D, Nicholson C F, Leroy J L ,Cole D C, Dentment M W, Omore A,  Zinsstag J and  Ruel M 2007 Invited review (2012): Role of livestock in human nutrition and health for poverty reduction in developing countries, Journal of Animal Science 85 (11): 2788-2800. http://www.journalofanimalscience.org/content/85/11/2788.full

Serrano P H 2005 Responsible use of antibiotics in aquaculture, FAO fisheries technical paper. Rome, Italy: Food and Agriculture Organization of the United Nations.

Swartz M 2002 Human diseases caused by food-borne pathogens of animal origin, Clinical Infectious Diseases 34:111-122

Ungemach F R, Müller-Bahrdt D and Abraham G  2006 Guidelines for prudent use of antimicrobials and their implications on antibiotic usage in veterinary medicine, International Journal of Medical Microbiology 296 Suppl 41:33-38.

Van den Bogaard A E, Willems R, London N, Top J and Stobberingh E E 2002 Antibiotic resistance of faecal enterococci in poultry, poultry farmers and poultry slaughterers. Journal of Antimicrobial Chemotherapy 49:497-505 http://jac.oxfordjournals.org/content/49/3/497.full.pdf

World Health Organization 2001 WHO Global Health Strategy for Containment of Antimicrobial Resistance, accesed from. http://www.who.int/drugresistance/WHO_Global_Strategy_English.pdf

World Health Organization 2007 WHO The world health report 2007 - A safer future: global public health security in the 21st century : http://www.who.int/whr/2007/en/index.html

Received 5 August 2012; Accepted 22 September 2012; Published 1 October 2012

Go to top