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Determination of antimicrobial use in commercial poultry farms in Plateau and Oyo States, Nigeria

Determination of antimicrobial use in commercial poultry farms in Plateau and Oyo States, Nigeria Background Indiscriminate use of antimicrobials for the prevention and treatment of bacterial infection in animals is a common practice in Nigeria as in other developing countries. These antimicrobials are purchased over the counter without restrictions and often administered in form of medicated feedstuffs. In Nigeria, like most developing coun‑ tries, antimicrobial prescription data are not routinely collected or reported at the farm level, instead import data are used in reporting antimicrobial consumption. Farmers can be useful sources of data on the use of antimicrobial agents by class, animal species, production type and age. The objective of the study was to determine the knowledge, attitude and practices of poultry farmers on antimicrobial resistance and to generate data on antimicrobial use (AMU) in poultry farms in Plateau and Oyo states in accordance with the guidelines of the World Organization for Animal Health ( WOAH). Methods A questionnaire used by the Food and Agriculture Organization (FAO) of the United Nations in Ghana was adopted and modified to collect data on the knowledge, attitude and practices of farmers on AMR and AMU and to collect AMU data from selected poultry farms. A focus group discussion (FGD) was conducted in Plateau state with poultry farmers and representatives from the state veterinary services, using a checklist. The aim of the FGD was to have an idea on antimicrobial use among poultry farmers and to generate additional questions that might be added to the questionnaire. Stratified random sampling technique was used to select 50 farms from Plateau and Oyo states, using the list of registered poultry farms in the two states as sampling frame. Results Ninety eight percent (98%) of farmers gave antibiotics as prophylactic treatment to day old chicks. There were 47 different products used in the two states within the study period. We observed that five classes of antibiotics ( Tetracyclines, Penicillins, Aminoglycosides, Polypeptides and Fluoroquinolone) were used in the two states. A total of 351 kg of active ingredients from seven different classes, namely: tetracyclines, penicillins, aminoglycosides, polypep ‑ tide, fluoroquinolones, amphenicol and macrolides were recorded from the two states. Some products contained cocktail of antibiotics, having up to six different classes with very high concentration of active ingredients which are not in the list of registered antimicrobials reported to WOAH. Conclusion The concept used for this survey proved that the approach can be applied for AMU surveillance in the animal health sector. It also provided insight on farmers’ knowledge and practices with regards to the use of *Correspondence: Mwapu Dika Ndahi whitendahi@yahoo.com Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 2 of 9 antimicrobials which is missing in the national import data. The need for “stronger” antibiotics was identified as one of the drivers of antibiotic resistance. Keywords Antimicrobials, Antimicrobial resistance, Antimicrobial use, Active ingredients, Poultry and kobotool Background 2019, banned for use in livestock feed in many countries, Nigeria is a Federation of 36 States and the Federal Capi- including Nigeria [5]. tal Territory with a population of about 200 million These antimicrobials are purchased over the counter people and a livestock population of about 349 million without restrictions and in livestock management, the animals out of which 194 million are poultry [1]. use of antimicrobials for therapeutic and prophylactic Antimicrobial agents are used in livestock production purposes is common which is often administered in form to ensure good health and productivity of animals [2]. of medicated feedstuffs [6]. However, the inappropriate use of these drugs especially There is evidence of overreliance on and indiscriminate when the classes are the same as, or related to, the phar- use of antimicrobial drugs among broiler farmers across maceuticals used in the control of human infections [3] six stages of the value chain in Oyo state, Nigeria [7]. The in the livestock sector, or the use of substandard/sub- study also revealed that 80% of the farmers interviewed optimal dose may predispose to antimicrobial resistance utilized antimicrobial drugs as preventive or therapeutic (AMR). Antimicrobial resistance is an emerging One drugs without laboratory diagnoses and veterinary pre- Health issue that can be transmitted between animals, scriptions. Furthermore, most of the farmers indicated humans and the environment and is able to spread across non-compliance to withdrawal period. Non-therapeutic the globe. The global antimicrobial usage in food animals antimicrobial use, particularly for growth promotion or was estimated at 63,000 tons annually in 2015 and pro- prophylaxis, has generated significant concern due to jected to increase by almost 70% in 2030 [2]. However, increasing evidence of its contribution to AMR [8]. Nma- this may change due to the increased awareness of the Bida and Tajudeen [9] found out that 58.3% of herders in problem. North central Nigeria practiced self-prescription for their The surveillance of antimicrobial use in animals is livestock and 23.2% use antimicrobial agents as growth more complex than in humans due to the variation in promoters. Adesokan et  al. [3] reported an increase in use patterns by different animal species and production antibiotic consumption in animal health in Southwestern types (e.g., beef and dairy cattle). In order to monitor Nigeria between 2010 and 2012 and the study revealed antimicrobial use, the WOAH developed standards on tetracyclines, fluoroquinolones and betalactams/amino - “Monitoring of the quantities and usage patterns of anti- glycosides as the leading antimicrobials used in livestock microbial agents used in food producing animals” [4]. production. Nigeria has been submitting data on the amount of active Studies carried out in Nigeria in cattle, poultry, pig, ingredients of antimicrobial agents intended for use in goat, vegetables, human, bats, camel, sheep, and fish animal health using import data. The data on antimi - showed residues of antimicrobial agents in animals, as crobial agents for use in animals were obtained from the well as the presence of multiple drug resistant isolates [7, National Agency for Food and Drug Administration and 10]. Other studies showed the presence of multiple drug Control (NAFDAC). The amount of active ingredients in resistant bacteria in meat and ready to eat meat products each antimicrobial was calculated and converted into kil- in Nigeria [11]. It is a well-known fact that drug-resistant ograms as described in the WOAH guidance] for report- pathogens are currently responsible for about 700 000 ing antimicrobial agents (AMUse guidance – Additional deaths annually and this is likely to increase to 10 mil- file 1). lion by 2050 if left unchecked, which is expected to affect The amount of active ingredients of antimicrobial global economy [12]. agents were 207; 516; 331 and 339 thousand kilograms In Nigeria, like most developing countries, antimi- for the years 2014 to 2017 respectively, although the data crobial prescription data are not routinely collected or for 2014 was for 6  months only. The classes of antimi - reported from the farm level, instead import data is used crobial agents include Tetracyclines, Fluoroquinolones, in reporting antimicrobial use. Farmers can be useful Macrolides, Penicillin, Sulfonamides, Polypeptides, Ami- sources of data on consumption of antimicrobial agents noglycosides, Amphenicols, Glycopetides, Pleuromutilins by class, animal species, production type and age. In and Nitrofurantoin (Antimicrobial Use Report-Federal some countries, farmers are required to maintain records Department of Veterinary and Pest Control Services, of treatment, which can be a valuable source of data. In Nigeria). Due to its carcinogenic effect, Nitrofuran was in Nigeria, however, this is not the case. Therefore, it may Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 3 of 9 be necessary to carry out data collection on a subset or a Focus Group Discussion sample of farms. A focus group discussion (FGD) was conducted in Pla- teau state with officials of poultry farmers association Methodology and representatives from the state veterinary services, Study design, site and method using a checklist. The purpose of the focus group dis - The study was a cross sectional study aimed at establish - cussion (FGD) was to obtain additional information on ing a proof of concept for antimicrobial use data collec- antimicrobial use among poultry farmers to generate tion at farms level. additional questions that might be added to the question- The study was carried out in Plateau and Oyo states in naire. Questions in the checklist for the FGD included Nigeria. Plateau State is in the middle belt of Nigeria with poultry production type in the state, poultry manage- 17 Local Government Areas and a population of about ment system, common poultry diseases, access to veteri- 3.5 million people [13]. It has a near temperate climate nary services, access to antimicrobials and frequency of with an average temperature of between 13 and 22  °C. use, repeat treatments and what farmers do when birds Poultry population in Plateau State is estimated at 8 mil- do not recover from treatment with antimicrobials. The lion [1]. Poultry farming thrives very well in Plateau State responses of farmers and veterinary officials from the because of the relatively cool weather and poultry eggs FGD provided more insight on poultry production sys- tend to have longer shelf life (conversation with poultry tem and farmers practices, which were used to fine-tune farmers and marketers). Oyo State is in the South-west- the questionnaire. ern Nigeria with a population of about 6 million people [14]. The Climate is characterized by dry and wet seasons Use of Kobo tool for imputing questions with relatively high humidity and average temperatures The draft questionnaire was imputed into Kobo tool - between 25  °C and 35  °C, almost throughout the year. box (https:// www. kobot oolbox. org) and deployed onto The poultry population in Oyo State is estimated at 12 android phone for ease of administration. A link was cre- million [1]. ated to provide access to the questionnaire for farmers. The reasons for selecting these states are to have a rep - The idea was for farmers to be able to fill out the ques - resentation from the Northern and Southern parts of the tionnaire on their android phones. All questions related country and the fact that both states have relatively high to farmers’ knowledge, attitude and practice on AMR poultry population [1] as well as easy accessibility of data as well as questions to obtain quantity of antimicrobial from poultry farms. Furthermore, the two states have dif- agents used are  found in the following link (https:// ee. ferent weather conditions which makes it appropriate for human itari anres ponse. info/ single/ gOqBg WQO). comparison and finally, availability of contacts of the fed - eral and state officers and those of the poultry farmers. Pretest of questionnaire The aim of the study was to determine the level of anti - Twelve farmers were identified by the farmers associa - microbial resistance (AMR) awareness among poultry tion for the pretest. The questionnaire was administered farmers; develop an effective system for AMU surveil - physically to seven farmers, while five farmers were sent lance and to generate data on AMU in selected poultry the link to fill out the questionnaire. farms in Plateau and Oyo States, Nigeria. Information was only obtained from farmers to which The specific objectives of the study were to determine questionnaire was administered physically. The farm - the knowledge, attitude and practices of poultry farmers ers that got the link to the questionnaire made no with regards to antimicrobial use through a structured submission. questionnaire administration, to find out if farmers prac - The result of the pre-test was used to finalize the ticed biosecurity and vaccination as disease preventive questionnaire. measures through questionnaire administration; and to Convenience sampling method was used to select 50 identify the types and quantity of antimicrobial agents poultry farms from Plateau and Oyo states. prescribed/used in poultry through questionnaire admin- Stratified random sampling technique was used to istration and provision of evidence;A questionnaire used select 25 farms each from Plateau and Oyo states, using by the Food and Agriculture Organization (FAO) of the the list of registered poultry farms in the two states as United Nations [15] in Ghana was adopted and modified sampling frame. Therefore, a total of 50 farmers were to collect data on the knowledge, attitude and practices interviewed. of farmers with regards to antimicrobial use and to also collect AMU data from selected poultry farms. Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 4 of 9 Farmers’ interview using questionnaire with day-old-chicks, at the time of the study, 78% of the All farmers that were contacted gave their consent to farmers had laying hens above 23  weeks of age in both respond to the questionnaires. states. The predominant breed of poultry were Isa Brown Interviews were conducted for 50 poultry farmers dur- and Lohman Brown. All farmers kept age groups in sepa- ing a three month study period using Questionnaires rate pens and sold poultry manure to crop and vegetable on kobo collect tool on android phone and completed farmers. forms were uploaded (submitted) to the Kobo toolbox on the computer. Data collected include farmers knowl- Poultry disease information and use of antimicrobials edge, attitude and practices on antimicrobial resistance The administration of antibiotics as prophylactic treat - and use; use of biosecurity and vaccination as means of ment to day old chicks was exceeding common amongst reducing the impact of antimicrobial resistance and data all farmers (98%). All farmers reported issues with dis- on antimicrobial use in poultry.Survey data were down- eases on their farms and the most common diseases loaded from Kobo toolbox to Microsoft excel. Data col- reported were:: Newcastle Disease Chronic, Coccidiosis, lected during the pre-test were excluded from the final Fowl Typhoid, Escherichia Coli (E.coli) infection, Chronic analysis. Respiratory Disease, Egg Drop Syndrome, Fowl Pox, Data on antimicrobial agents used in poultry was for Gumboro, Marek’s disease, Infectious Coryza, Infectious a period of three months during the study period. The Bronchitis, Fowl Cholera and Avian Influenza (Fig. 1). amount of active ingredients in each antimicrobial agent Newcastle was the highest recurring disease in poul- was calculated and converted into kilograms as described try farms in the two states, followed by Coccidiosis, Fowl in the WOAH guideline for reporting antimicrobial typhoid and E. coli infection. Coccidiosis was higher in agents (Additional file  1).. All antimicrobial agents were Oyo state and this could be due to the fact that Oyo state grouped into the various classes. Antimicrobial agents has a warmer temperature and higher humidity than having more than one active ingredient were disaggre- Plateau state. Fowl typhoid and E. coli infection were gated into the respective classes and amount of active higher in Plateau state, although the reason for that was ingredients calculated. Microsoft excel was used in ana- not clear except for the fact that most farmers used well lyzing data. Results were presented in tables, percent- water in Plateau state as against deep borehole water in ages, graphs and charts. Oyo state. Farmers’ knowledge on antimicrobial resistance Results Seventy percent (70%) of farmers have heard about anti- Farmers’ demographic information and production system microbial resistance; 29% said they read about it; 59% In the two states, there were more males (80%) involved heard about it from private/government veterinarians; in poultry farming than females (20%) and the majority and 12% from a family member. Majority of the farmers (58%) of the farmers were above 50  years of age. There (92%) thought antimicrobial resistance would have great seemed to be a tendency that retired civil servants invest impact on them, their families/friends and their animals. their retirement benefits in poultry farming as a means of sustaining their families, and as a result, 68% of the farmers were into full time poultry farming. Only 4% were below the age of 40. All the farmers had some level of formal education; 58% had tertiary education, 30% had postgraduate education and 12% had secondary school certificate. It is mandatory for poultry farmers to be registered with the government in some states, includ- ing Plateau and Oyo. The study showed that 90% of the farmers were registered with the government and poultry farming is the main occupation of majority (78%) of the farmers in both states. The farms were on the average, between 6 to 8  years of production with most (44%) farms having three pens per farm with an average of 1000 birds per pen in the two states. Sixty percent (60%) of farmers had layers belong- ing to sector 3 poultry production system according to Fig. 1 Frequency of disease occurrence in the farms included in the FAO classification [16]. Although all the farmers started survey Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 5 of 9 All farmers agreed that it was important to get consul- The challenges associated with taking samples to the tation from a veterinarian before giving antibiotics to lab were described by the farmers as far distance to the poultry. lab (36%) and high cost of analysis (30%) (Table 1). Most farmers (70%) did not know about antimicrobial When farmers observed that the antibiotics they used residues, however, 74% read about withdrawal period regularly were no longer effective, 62% consulted ani - from the antibiotic containers/sachets, yet all farmers mal health professionals; 24% tried different antibiotics; interviewed sold eggs under current treatment with anti- while 14% increased the dosage of antibiotics. When biotics. Since there was no provision for compensation by birds were sick, most farmers separated sick birds from government, the farmers stated that the eggs were sold. healthy ones but the entire flock undergoes treatment. Most farmers thought that antibiotics were no longer Ninety-eight percent (98%) of farmers gave antibiot- effective because of the manufacturing company; reduced ics as prophylactic treatment to day old chicks. strength of the antibiotics and the fact that diseases were becoming untreatable (Fig.  2). Although farmers inter- Types of antimicrobials used and amount of active viewed in this survey have heard about AMR, this high- ingredients in kilograms lights the lowperception of AMR among farmers and the In Plateau state, a total of 39 different antibiotics prod - need for awareness creation and sensitization. ucts from six different classes were used for treating poultry during the three  month study period (Addi- Farmers’ attitude and practices towards antimicrobial use tional file  2). Within that period, 88% of the farmers All farmers in the two states bought and used antibi- interviewed used 311  kg of active ingredients of anti- otics to treat infections. Although most farmers (84%) biotics to treat poultry (Table  2). In Oyo state, a total consulted private or government veterinarians when of 24 different antibiotics products from six different the birds were sick, 16% bought antibiotics from the drug store without consulting veterinarians, reason being that they consider to have been in the poultry business long enough to know what antibiotics to give when the birds were sick. Farmers in Nigeria have been reported to treat animals with antimicrobials without prescription [9]. Seventy-four percent (74%) of farmers bought antibiotics from poultry drug stores, while the rest (26%) obtained theirs from private and government vets. Fifty eight percent (58%) of famers covered a dis- tance of 3 to 5 kms to buy antibiotics in the two states. Therefore, antimicrobial agents were readily accessible to farmers. Seventy-two percent (70%) of farmers took samples to the lab always; 14% took samples to the lab some- Fig. 3 Frequency of taking samples to the lab when birds were sick times, while 16% never took samples to the lab (Fig. 3). in farms included in the survey Fig. 2 Farmers responses on why antibiotics were no longer effective Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 6 of 9 Table 1 Farmers’ attitude to antimicrobial use Farmers’ attitude to antimicrobial use Agree (%) Disagree (%) Indifferent (%) Farmers observe withdrawal period before selling or eating animal products 74 16 10 Farmers stop giving antibiotics if symptoms improve 30 70 0 Farmers believe that if antibiotics are given too often, they might stop working 90 8 2 Farmers believe that giving animals that are not sick antibiotics will prevent them from 60 34 6 becoming sick in the future Farmers believe that giving animals antibiotics can help them grow bigger, faster, fatter 32 64 4 Others have 3 molecules in one e.g., Table 2 Amount of active ingredients of antibiotics used within three months in poultry farms included in the survey • Neo-furaseryl (neomycin 100  mg, oxytetracycline Antibiotics Amount of active Amount of active ingredients in kg ingredients in kg 50,000 mg, colistin sulphate 30,000,000 IU plus vita- (Plateau) (Oyo) mins); • Zogceryl (oxytetracycline 5,000  mg, colistin Tetracycline 290 15.4 2,500 mg, neomycin 200 mg); Penicillin 2 0.2 • Maxiceryl (colistin 225000  IU, oxytetracycline Aminoglycoside 4 7.4 5000 mg, neomycin 5000 mg); Polypeptide 12 0.1 • Keproceryl (oxytetracycline 50 mg, colistin sulphate Fluoroquinolone 2 3.8 225,000 IU and erythromycin 35 mg) and, Amphenicol 1 0 • N.C.O mix (florfenicol 150  mg, neomycin sulphate Macrolide 0 13.1 180 mg, colistin sulphate 1,200,000 IU). Total 311 40 The need for antibiotics with multiple molecules and high concentration of active ingredients to treat infec- classes were used for treating poultry during the three tions in poultry by the farmers interviewed  could be a month study period (Additional file  3). Most of the potential driver of antibiotic resistance. farmers interviewed in both states administered anti- Furazolidone (Oxazolidines) were being used by some biotics to poultry on a monthly basis, as prophylaxes; farmers in poultry in combination with other antibiotics just before the “monthly” vaccination against Newcas- even though it was banned for use in food producing ani- tle disease. All farmers interviewed in Oyo state used mals by the regulatory authorities in Nigeria. Ampheni- 40 kg of active ingredients of antibiotics to treat poultry col was found to be used by few farmers even though it within the three month study period (Table 2). is not in the national import data reported to the WOAH All antibiotics except the human preparation of gen- for the past four years. We also observed that some prod- tamycin were given in water to layers of all age groups ucts with very high concentration of active ingredients as treatment (55%) and prophylaxes (45%); 84% of the such as Neo-furaseryl , Floricol and Furamycin were not birds were actively laying during the period of the reported in the national import data, which is an indica- study. tor for importation through other means. Of concern was the fact that some products con- Some farmers used products containing a mixture of tained cocktail of antibiotics, having up to six different antibiotics and probiotics such as Biodox (Doxycycline classes with very high concentration of active ingredi- and Lactobacillus). Fifty-six percent (56%) of farmers ents e.g., interviewed used human preparation of injectable gen- tamycin (80  mg of 2  ml vials); and Septrin (Sulphur/ • Neo-furamycin (furazolidone 6000  mg, neomy- Trimethoprim) in water because the birds were not cin 200  mg, oxytetracycline 500  mg, streptomycin responding to treatment. Others used Zingiber offici - 200  mg, erythromycin 3500  mg, chloramphenicol nale (ginger) in water as prophylaxes. 2000 mg); Some farmers administered disinfectants in drink- • Embaceryl (tylosin base 3,800  mg, oxytetracycline ing water to poultry (e.g., Viru supa disinfectants , con- 4,000  mg, neomycin sulphate 1,200  mg, colistin sul- taining potassium peroxomonosulfate 59% and sodium phate 30,000,000 IU). dichloro-iso-synurate 10%; Corygiene ); and antiseptics Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 7 of 9 ® ® such as Fivevet (iodine preparation) and Aquaseptic ) Although a greater percentage of the farms were in drinking water. fenced, 64% of customers came into the farms to buy Farmers tend not to buy more antibiotics than they eggs, which is a risk factor for disease introduction. A need at a time, but in case antibiotics expire, 96% said risk assessment carried out by the Federal Department of they would throw them away. In case of mortalities, 56% Veterinary and Pest Control Services during the outbreak of farmers fed dogs with the carcasses. of Avian influenza in Nigeria in 2016, identified eggs We observed that five classes of antibiotics (Tetracy - and manure merchants as sources of transmission of the cline, Penicillin, Aminoglycoside, Polypeptide and Fluo- pathogen from infected to non-infected farms through roquinolone) were consistent in the two states. This is in used paper crates and used sacks. agreement with the national AMC data submitted to the Even though most farmers practiced good biosecurity, WOAH for the past six years [17]. However, amphenicol all the farms visited had disease problems. was only reported in Plateau state and likewise macrolide Ninety-six percent (96%) of farmers kept farm records was only reported in Oyo state. The reason for the vari - including sales/financial, mortality, vaccination and med - ation is not clear. Also, the amount of tetracycline was icine records. higher in Plateau state and this might be attrbuted to the The fact that 72% of farmers bought commercial feed type of products (products with very high concentration was advantageous in reducing the spread of disease- of active ingredients) used by poultry farmers. causing pathogens  that could occur through exchange of sacks at toll milling stations. Although 92% of farmers Information on vaccination and biosecurity admit that additives were added to the feed they used for All farmers interviewed began with day-old-chicks as poultry, none contained antibiotics. starter flock and 72% stated that the chicks were vacci - All farmers used well or borehole water for poultry and nated at day old against diseases such as Marek’s from drinkers were washed on a daily bases by most farmers. the hatcheries. All farmers vaccinated poultry against the following diseases: Newcastle disease, Gumboro disease, Discussion Coccidiosis, Fowl pox, Fowl typhoid, Marek’s disease, The use of structured questionnaire enabled us to col - Egg drop syndrome, Fowl cholera and Avian encephali- lect actual AMU data at the farm level. Seven classes of tis. Although there is a “No vaccination” policy on Avian antimicrobial agents (Tetracycline, Penicillin, Amino- Influenza in Nigeria, we found out during the course of glycoside, Macrolide, Fluoroquinolone, Amphenicol and the study that some farmers vaccinated against the dis- Polypeptide) were identified in the two states during ease. Following vaccination, some birds still came down the three month study period. Tetracyclines accounted with the same disease in some of the farms. Fifty-two for the highest antibiotics used in both states, followed percent (52%) of farmers agreed that using vaccines could by Polypeptides, Aminoglycosides and Fluoroquinolo- prevent the use of antibiotics, while 34% disagreed and nes  respectively. This finding is in concordance with 14% were indifferent. the annual AMC data reported to the WOAH by Nige- Fifty-eight percent (58%) of farms included in this sur- ria [Federal Department of Veterinary and Pest Control vey were fenced to regulate human and animal traffic as a Services (FDVPCS)]. Adesokan et  al. [3] also reported form of biosecurity. All the pens had wire mesh and the tetracyclines, fluoroquinolones, beta lactams and amino - floors made of concrete for ease of cleaning and disin - glycosides as the leading antimicrobials used in livestock fection. All the farms had foot dip at the entrance, and production in Nigeria. A total of 351 kg of active ingredi- most farmers (56%) changed the disinfectant water on a ents of antibiotics were used in poultry in the farms vis- daily bases, while others changed on a weekly (22%) or ited within the three month study period. monthly (22%) bases. Ninety-two percent (92%) of the The study revealed that farmers used cocktail of anti - farms had changing rooms and workers wore specific biotics, having up to six different classes with very high clothing and boots during work on the farm; 96% of the concentration of active ingredients. The study  also workers were almost always permanently assigned to revealed that farmers were using antibiotics banned by work in separate pens. None of the staff worked on other the regulatory authorities even though such products farms and only 20% had poultry at home. All farmers are not captured in the annual import data reported to cleaned and disinfected pens after selling each batch of the WOAH. These practices could aggravate the devel - poultry. opment and spread of resistance by microorganisms Most farms (96%) were neighbors with other poul- through selective pressure. try farms within 1  km radius and almost all farmers Farmers interviewed used antibiotics to treat infec- allowed their farms to rest for at least one month before tions, though not always based on laboratory test and restocking. prescription from veterinarians. The continuous overuse Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 8 of 9 of antimicrobial agents by poultry farmers in this study some insight on farmers’ practices with regards to the use could pose a public health threat, thereby exposing of antimicrobials which is missing in the national import humans to subclinical doses of antimicrobials through data. It can therefore be adopted to improve AMU sur- the food chain, especially since some antimicrobials are veillance in Nigeria. The concept is already being further potentially carcinogenic, allergenic mutagenic and tera- developed and expanded for national AMU data collec- togenic. Some farmers have resolved to using human tion in all the states of the federation, pending availability preparations of antibiotics especially injecting birds with of funds. gentamycin for treating infections that did not respond There is also clear evidence that the current surveil - to treatment. lance of AMU using the national import data is missing Most farmers interviewed were retirees, above the age some important data. Especially the fact that antimicro- of 50 who have used their retirement benefits to start bials such as Furazolidone is being used by some farm- up poultry farming as a main source of livelihood. Most ers in poultry in combination with other antibiotics even of the farms belonged to sector 3 as categorized by the though it was banned for use in food producing animals FAO  [16]. Although all farms had some form of bios- by the regulatory authorities in Nigeria. Also, the fact ecurity measures in place, rationale behind the measures that Amphenicol was found to be used by few farmers on was not fully understood by farmers, for example, farm- the field even though it is not in the national import data ers allowed eggs and manure merchants into the farms. reported to the WOAH for the past four years. We also Hence, all farms visited were faced with disease problems observed that some products with very high concentra- in poultry such as Newcastle Disease, Coccidiosis, Fowl tion of active ingredients such as Neo-furaseryl , Floricol Typhoid, E. coli infection, among others. Newcastle dis- and Furamycin were not reported in the national import ease was the highest most recurring disease in the two data, which is an indicator for importation through other states. Coccidiosis was found to be higher in Oyo state. means. The use of human preparations of Septrin and Although most farmers interviewed have heard of anti- Gentamycin injection in poultry to treat resistant strains microbial resistance, there was a low-risk perception of is a clear indication of resistance to antibiotics used in antimicrobial resistance among them. The repeated use of poultry. Five classes of antibiotics (Tetracycline, Penicil- antimicrobials as prophylaxis instead of applying preven- lin, Aminoglycoside, Polypeptide and Fluoroquinolone) tive measures such as improved management practices were used in the two states, however, amphenicol was and biosecurity measures is an indication of low-risk per- only reported in Plateau state and likewise macrolide ception. Hence the need for continuous awareness crea- was only reported in Oyo state. This study is therefore tion and sensitization of farmers on the danger of AMR a pointer that the approach used could be applied to and trainings on the use of alternatives to antimicrobials gather useful information directly from the farms as well such as improved biosecurity practices, effective vacci - as generate and calculate the actual amount of antimi- nation and the use of pre and probiotics. The belief that crobial agents used in poultry using the WOAH guide- antibiotics were no longer effective because of reduced lines. The fact that AMU data was generated during the strength or because diseases were becoming untreatable survey indicated the possibility of using this approach for and not due to overuse of antibiotics or poor manage- national AMU surveillance. ment practices further buttressed this point. This study In order to generate the actual antimicrobial use data, revealed the possibility that a majority of eggs in the mar- there is need to collect data from the farms and clinics ket might contain some residues of antimicrobial agents levels especially since some antibiotics reported by farm- since eggs were sold during treatment. This would war - ers are not captured in the import data. There is also the rant further study and efforts to improve farmer practices need to increase awareness among poultry farmers on to minimize any risk to the food chain. the importance of biosecurity; disease preventive meas- Despite the fact that all farmers vaccinate birds against ures such as vaccination and promote the use of probi- preventable diseases and observe some level of bios- otics to enhance production. These would reduce disease ecurity measures, the fact that customers came into the introduction to farms and ultimately reduce the use of farms to buy eggs were identified as high-risk factors for antibiotics. Increased awareness creation and sensitiza- disease entry into farms and resultant increase in the use tion among private veterinarians and poultry drug sell- of antibiotics. ers on the danger of AMR and the need for prescriptions from laboratory test results before prescribing or selling Conclusion antibiotics to farmers will go a long way in mitigating The use of structured questionnaire for this survey AMR. proved that the approach can be applied for AMU sur- veillance in the animal health sector. It also provided Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 9 of 9 References Supplementary Information 1. Livestock population figures, FMARD, 2018, Animal husbandry Depart ‑ The online version contains supplementary material available at https:// doi. ment, Federal Ministry of Agriculture. org/ 10. 1186/ s13756‑ 023‑ 01235‑x. 2. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Laxminarayan R. Global trends in antimicrobial use in food animals. Proc Additional file 1. Annex to the Guidance for Completing the OIE tem‑ Natl Acad Sci. 2015;112(18):5649–54. plate for the collection of data on Antimicrobial Agents intended for use 3. Adesokan HK, Akanbi IO, Akanbi IM, Obaweda RA. Pattern of antimicro‑ in Animals. bial usage in livestock animals in southwestern Nigeria: The need for alternative plans. Onderstepoort J Vet Res. 2015;82(1):6. https:// doi. org/ Additional file 2. List of antibiotics used on farms (Plateau). 10. 4102/ ojvr. v82i1. 816. Additional file 3. List of antibiotics used on farms (Oyo state). 4. OIE. Terrestrial Animal Health Code. (2018). https:// www. oie. int/ en/ stand ard‑ setti ng/ terre strial‑ code/ access‑ online . 5. https:// www. nafdac. gov. ng/ veter inary‑ produ cts/ list‑ of‑ banned v‑eter Acknowledgements inary‑ drugs/. The authors appreciate the United Kingdom (UK) Government, through the 6. Antimicrobial use and Resistance in Nigeria – Situation Analysis and UK Department of Health and Social Services and the Fleming Fund Fellow‑ Recommendations, 2017. ship Project for funding this study. The authors are thankful to their beneficiary 7. Nurudeen OO, Ismail AA, Henriette van H, Olubunmi GF, Folorunso Institutions especially the management of the Federal Ministry of Agriculture OF. Antimicrobial drug administration and antimicrobial resistance of and Rural Development for the opportunity to be part of the Fellowship salmonella isolates originating from the broiler production value chain in program. Nigeria. Antibiotics 2019; 8, 75; https:// doi. org/ 10. 3390/ antib iotic s8020 Author contributions 8. Antimicrobial Use in Food‑Animal Production Problems, Solutions, Chal‑ MDN participated in the study design, modified the questionnaire used in the lenges. www. react group. org/ toolb ox (2017). study, participated in the focus group discussion, administered the question‑ 9. NmaBida AB, Tajudeen OI. Antimicrobial usage by pastoralists in food naire to farmers, collated the responses, analyzed the data and developed the animals in North central Nigeria: the associated cultural drivers for antimi‑ first draft of the manuscript. JKA participated in the study design, supervised crobial misuse and public health implications. Elsevier. 2011. https:// doi. the research, supported in the modification of questionnaire and reviewed org/ 10. 1016/j. onehlt. 2018. 11. 001. the manuscript. RH, BH and RMC provided guidance in the modification of 10. Omeiza GK, Ajayi IE, Okwoche OJ. Assessment of antimicrobial drug questionnaire and supervised the research. RMC also reviewed the manu‑ residues in beef in Abuja, the Federal Capital Territory. Nigeria Veterinaria script. IOF, OOA‑A, EE, VA and IA took part in the joint collaborative project. IOF Italiana. 2012;48(3):283–9. also participated in the focus group discussion. All authors read and approved 11. Ndahi MD, Kwaga JKP, Bello M, Kabir J, Umoh VJ, Yakubu SE, Nok AJ. the final manuscript. Prevalence and antimicrobial susceptibility of Listeria monocytogenes and Methicillin Resistant Staphylococcus aureus strains from raw meat and Funding meat products in Zaria Nigeria. Lett Appl Microbiol. 2013;58:262–9. This study was funded by the United Kingdom (UK) Government, through the 12. O’Neill J.. Review on Antimicrobial Resistance – Tackling a crises for the UK Department of Health and Social Services are the donors of the Fleming health and wealth of nations (2014). Fund Grants. The work was supervised by Jens Kirk Andersen of the Technical 13. https:// cityp opula tion. de/ en/ niger ia/ admin/ NGA03 2__ plate au/. University of Denmark (DTU). Retrieved on 15 September, 2020. 14. https:// cityp opula tion. de/ en/ niger ia/ admin/ NGA03 1__ oyo/. Retrieved Availability of data and materials on 15 September, 2020. A link to the questionnaire is given below: https:// ee. human itari anres ponse. 15. https:// ee. human itari anres ponse. info/ x/# FLRov 2EB info/ single/ gOqBg WQO 16. FAO (2004). Poultry production sectors. http:// www. fao. org/ docs/ eims/ uploa d// 224897/ facts heet_ produ ction secto rs_ en. pdf (Cited by Hanh, P.T. H., Burgos, S and Roland‑Holst, D. (2007). The Poultry Sector in Viet Nam: Declarations Prospects for Smallholder Producers in the Aftermath of the HPAI Crisis. Pro-Poor Livestock Policy Initiative A Living from Livestock Research Report, Ethical approval and consent to participants 1 – 14. Verbal informed consent was obtained from all participants before each 17. Antimicrobial Use Report‑Federal Department of Veterinary and Pest interview. Control Services, Nigeria. Competing interests The authors declare that they have no competing interests. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub‑ Author details lished maps and institutional affiliations. Department of Veterinary and Pest Control Services, Federal Ministry of Agri‑ culture and Rural Development, Area 11, Garki, Abuja, Nigeria. T echnical University of Denmark, Kongens Lyngby, Copenhagen, Denmark. Animal and Plant Health Agency, Weybridge, Woodham Lane, New Haw, Addlestone, Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : Surrey, UK. National Veterinary Research Institute, Vom, Plateau State, Nigeria. National Agency for Food and Drug Administration and Control, Lagos, Nige‑ fast, convenient online submission ria. Nigeria Centre for Disease Control Laboratory, Gaduwa, Abuja, Nigeria. thorough peer review by experienced researchers in your field 7 8 University of Ibadan, Ibadan, Nigeria. University College Hospital, Ibadan, rapid publication on acceptance Nigeria. support for research data, including large and complex data types Received: 29 August 2022 Accepted: 26 March 2023 • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance and Infection Control Springer Journals

Determination of antimicrobial use in commercial poultry farms in Plateau and Oyo States, Nigeria

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Abstract

Background Indiscriminate use of antimicrobials for the prevention and treatment of bacterial infection in animals is a common practice in Nigeria as in other developing countries. These antimicrobials are purchased over the counter without restrictions and often administered in form of medicated feedstuffs. In Nigeria, like most developing coun‑ tries, antimicrobial prescription data are not routinely collected or reported at the farm level, instead import data are used in reporting antimicrobial consumption. Farmers can be useful sources of data on the use of antimicrobial agents by class, animal species, production type and age. The objective of the study was to determine the knowledge, attitude and practices of poultry farmers on antimicrobial resistance and to generate data on antimicrobial use (AMU) in poultry farms in Plateau and Oyo states in accordance with the guidelines of the World Organization for Animal Health ( WOAH). Methods A questionnaire used by the Food and Agriculture Organization (FAO) of the United Nations in Ghana was adopted and modified to collect data on the knowledge, attitude and practices of farmers on AMR and AMU and to collect AMU data from selected poultry farms. A focus group discussion (FGD) was conducted in Plateau state with poultry farmers and representatives from the state veterinary services, using a checklist. The aim of the FGD was to have an idea on antimicrobial use among poultry farmers and to generate additional questions that might be added to the questionnaire. Stratified random sampling technique was used to select 50 farms from Plateau and Oyo states, using the list of registered poultry farms in the two states as sampling frame. Results Ninety eight percent (98%) of farmers gave antibiotics as prophylactic treatment to day old chicks. There were 47 different products used in the two states within the study period. We observed that five classes of antibiotics ( Tetracyclines, Penicillins, Aminoglycosides, Polypeptides and Fluoroquinolone) were used in the two states. A total of 351 kg of active ingredients from seven different classes, namely: tetracyclines, penicillins, aminoglycosides, polypep ‑ tide, fluoroquinolones, amphenicol and macrolides were recorded from the two states. Some products contained cocktail of antibiotics, having up to six different classes with very high concentration of active ingredients which are not in the list of registered antimicrobials reported to WOAH. Conclusion The concept used for this survey proved that the approach can be applied for AMU surveillance in the animal health sector. It also provided insight on farmers’ knowledge and practices with regards to the use of *Correspondence: Mwapu Dika Ndahi whitendahi@yahoo.com Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 2 of 9 antimicrobials which is missing in the national import data. The need for “stronger” antibiotics was identified as one of the drivers of antibiotic resistance. Keywords Antimicrobials, Antimicrobial resistance, Antimicrobial use, Active ingredients, Poultry and kobotool Background 2019, banned for use in livestock feed in many countries, Nigeria is a Federation of 36 States and the Federal Capi- including Nigeria [5]. tal Territory with a population of about 200 million These antimicrobials are purchased over the counter people and a livestock population of about 349 million without restrictions and in livestock management, the animals out of which 194 million are poultry [1]. use of antimicrobials for therapeutic and prophylactic Antimicrobial agents are used in livestock production purposes is common which is often administered in form to ensure good health and productivity of animals [2]. of medicated feedstuffs [6]. However, the inappropriate use of these drugs especially There is evidence of overreliance on and indiscriminate when the classes are the same as, or related to, the phar- use of antimicrobial drugs among broiler farmers across maceuticals used in the control of human infections [3] six stages of the value chain in Oyo state, Nigeria [7]. The in the livestock sector, or the use of substandard/sub- study also revealed that 80% of the farmers interviewed optimal dose may predispose to antimicrobial resistance utilized antimicrobial drugs as preventive or therapeutic (AMR). Antimicrobial resistance is an emerging One drugs without laboratory diagnoses and veterinary pre- Health issue that can be transmitted between animals, scriptions. Furthermore, most of the farmers indicated humans and the environment and is able to spread across non-compliance to withdrawal period. Non-therapeutic the globe. The global antimicrobial usage in food animals antimicrobial use, particularly for growth promotion or was estimated at 63,000 tons annually in 2015 and pro- prophylaxis, has generated significant concern due to jected to increase by almost 70% in 2030 [2]. However, increasing evidence of its contribution to AMR [8]. Nma- this may change due to the increased awareness of the Bida and Tajudeen [9] found out that 58.3% of herders in problem. North central Nigeria practiced self-prescription for their The surveillance of antimicrobial use in animals is livestock and 23.2% use antimicrobial agents as growth more complex than in humans due to the variation in promoters. Adesokan et  al. [3] reported an increase in use patterns by different animal species and production antibiotic consumption in animal health in Southwestern types (e.g., beef and dairy cattle). In order to monitor Nigeria between 2010 and 2012 and the study revealed antimicrobial use, the WOAH developed standards on tetracyclines, fluoroquinolones and betalactams/amino - “Monitoring of the quantities and usage patterns of anti- glycosides as the leading antimicrobials used in livestock microbial agents used in food producing animals” [4]. production. Nigeria has been submitting data on the amount of active Studies carried out in Nigeria in cattle, poultry, pig, ingredients of antimicrobial agents intended for use in goat, vegetables, human, bats, camel, sheep, and fish animal health using import data. The data on antimi - showed residues of antimicrobial agents in animals, as crobial agents for use in animals were obtained from the well as the presence of multiple drug resistant isolates [7, National Agency for Food and Drug Administration and 10]. Other studies showed the presence of multiple drug Control (NAFDAC). The amount of active ingredients in resistant bacteria in meat and ready to eat meat products each antimicrobial was calculated and converted into kil- in Nigeria [11]. It is a well-known fact that drug-resistant ograms as described in the WOAH guidance] for report- pathogens are currently responsible for about 700 000 ing antimicrobial agents (AMUse guidance – Additional deaths annually and this is likely to increase to 10 mil- file 1). lion by 2050 if left unchecked, which is expected to affect The amount of active ingredients of antimicrobial global economy [12]. agents were 207; 516; 331 and 339 thousand kilograms In Nigeria, like most developing countries, antimi- for the years 2014 to 2017 respectively, although the data crobial prescription data are not routinely collected or for 2014 was for 6  months only. The classes of antimi - reported from the farm level, instead import data is used crobial agents include Tetracyclines, Fluoroquinolones, in reporting antimicrobial use. Farmers can be useful Macrolides, Penicillin, Sulfonamides, Polypeptides, Ami- sources of data on consumption of antimicrobial agents noglycosides, Amphenicols, Glycopetides, Pleuromutilins by class, animal species, production type and age. In and Nitrofurantoin (Antimicrobial Use Report-Federal some countries, farmers are required to maintain records Department of Veterinary and Pest Control Services, of treatment, which can be a valuable source of data. In Nigeria). Due to its carcinogenic effect, Nitrofuran was in Nigeria, however, this is not the case. Therefore, it may Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 3 of 9 be necessary to carry out data collection on a subset or a Focus Group Discussion sample of farms. A focus group discussion (FGD) was conducted in Pla- teau state with officials of poultry farmers association Methodology and representatives from the state veterinary services, Study design, site and method using a checklist. The purpose of the focus group dis - The study was a cross sectional study aimed at establish - cussion (FGD) was to obtain additional information on ing a proof of concept for antimicrobial use data collec- antimicrobial use among poultry farmers to generate tion at farms level. additional questions that might be added to the question- The study was carried out in Plateau and Oyo states in naire. Questions in the checklist for the FGD included Nigeria. Plateau State is in the middle belt of Nigeria with poultry production type in the state, poultry manage- 17 Local Government Areas and a population of about ment system, common poultry diseases, access to veteri- 3.5 million people [13]. It has a near temperate climate nary services, access to antimicrobials and frequency of with an average temperature of between 13 and 22  °C. use, repeat treatments and what farmers do when birds Poultry population in Plateau State is estimated at 8 mil- do not recover from treatment with antimicrobials. The lion [1]. Poultry farming thrives very well in Plateau State responses of farmers and veterinary officials from the because of the relatively cool weather and poultry eggs FGD provided more insight on poultry production sys- tend to have longer shelf life (conversation with poultry tem and farmers practices, which were used to fine-tune farmers and marketers). Oyo State is in the South-west- the questionnaire. ern Nigeria with a population of about 6 million people [14]. The Climate is characterized by dry and wet seasons Use of Kobo tool for imputing questions with relatively high humidity and average temperatures The draft questionnaire was imputed into Kobo tool - between 25  °C and 35  °C, almost throughout the year. box (https:// www. kobot oolbox. org) and deployed onto The poultry population in Oyo State is estimated at 12 android phone for ease of administration. A link was cre- million [1]. ated to provide access to the questionnaire for farmers. The reasons for selecting these states are to have a rep - The idea was for farmers to be able to fill out the ques - resentation from the Northern and Southern parts of the tionnaire on their android phones. All questions related country and the fact that both states have relatively high to farmers’ knowledge, attitude and practice on AMR poultry population [1] as well as easy accessibility of data as well as questions to obtain quantity of antimicrobial from poultry farms. Furthermore, the two states have dif- agents used are  found in the following link (https:// ee. ferent weather conditions which makes it appropriate for human itari anres ponse. info/ single/ gOqBg WQO). comparison and finally, availability of contacts of the fed - eral and state officers and those of the poultry farmers. Pretest of questionnaire The aim of the study was to determine the level of anti - Twelve farmers were identified by the farmers associa - microbial resistance (AMR) awareness among poultry tion for the pretest. The questionnaire was administered farmers; develop an effective system for AMU surveil - physically to seven farmers, while five farmers were sent lance and to generate data on AMU in selected poultry the link to fill out the questionnaire. farms in Plateau and Oyo States, Nigeria. Information was only obtained from farmers to which The specific objectives of the study were to determine questionnaire was administered physically. The farm - the knowledge, attitude and practices of poultry farmers ers that got the link to the questionnaire made no with regards to antimicrobial use through a structured submission. questionnaire administration, to find out if farmers prac - The result of the pre-test was used to finalize the ticed biosecurity and vaccination as disease preventive questionnaire. measures through questionnaire administration; and to Convenience sampling method was used to select 50 identify the types and quantity of antimicrobial agents poultry farms from Plateau and Oyo states. prescribed/used in poultry through questionnaire admin- Stratified random sampling technique was used to istration and provision of evidence;A questionnaire used select 25 farms each from Plateau and Oyo states, using by the Food and Agriculture Organization (FAO) of the the list of registered poultry farms in the two states as United Nations [15] in Ghana was adopted and modified sampling frame. Therefore, a total of 50 farmers were to collect data on the knowledge, attitude and practices interviewed. of farmers with regards to antimicrobial use and to also collect AMU data from selected poultry farms. Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 4 of 9 Farmers’ interview using questionnaire with day-old-chicks, at the time of the study, 78% of the All farmers that were contacted gave their consent to farmers had laying hens above 23  weeks of age in both respond to the questionnaires. states. The predominant breed of poultry were Isa Brown Interviews were conducted for 50 poultry farmers dur- and Lohman Brown. All farmers kept age groups in sepa- ing a three month study period using Questionnaires rate pens and sold poultry manure to crop and vegetable on kobo collect tool on android phone and completed farmers. forms were uploaded (submitted) to the Kobo toolbox on the computer. Data collected include farmers knowl- Poultry disease information and use of antimicrobials edge, attitude and practices on antimicrobial resistance The administration of antibiotics as prophylactic treat - and use; use of biosecurity and vaccination as means of ment to day old chicks was exceeding common amongst reducing the impact of antimicrobial resistance and data all farmers (98%). All farmers reported issues with dis- on antimicrobial use in poultry.Survey data were down- eases on their farms and the most common diseases loaded from Kobo toolbox to Microsoft excel. Data col- reported were:: Newcastle Disease Chronic, Coccidiosis, lected during the pre-test were excluded from the final Fowl Typhoid, Escherichia Coli (E.coli) infection, Chronic analysis. Respiratory Disease, Egg Drop Syndrome, Fowl Pox, Data on antimicrobial agents used in poultry was for Gumboro, Marek’s disease, Infectious Coryza, Infectious a period of three months during the study period. The Bronchitis, Fowl Cholera and Avian Influenza (Fig. 1). amount of active ingredients in each antimicrobial agent Newcastle was the highest recurring disease in poul- was calculated and converted into kilograms as described try farms in the two states, followed by Coccidiosis, Fowl in the WOAH guideline for reporting antimicrobial typhoid and E. coli infection. Coccidiosis was higher in agents (Additional file  1).. All antimicrobial agents were Oyo state and this could be due to the fact that Oyo state grouped into the various classes. Antimicrobial agents has a warmer temperature and higher humidity than having more than one active ingredient were disaggre- Plateau state. Fowl typhoid and E. coli infection were gated into the respective classes and amount of active higher in Plateau state, although the reason for that was ingredients calculated. Microsoft excel was used in ana- not clear except for the fact that most farmers used well lyzing data. Results were presented in tables, percent- water in Plateau state as against deep borehole water in ages, graphs and charts. Oyo state. Farmers’ knowledge on antimicrobial resistance Results Seventy percent (70%) of farmers have heard about anti- Farmers’ demographic information and production system microbial resistance; 29% said they read about it; 59% In the two states, there were more males (80%) involved heard about it from private/government veterinarians; in poultry farming than females (20%) and the majority and 12% from a family member. Majority of the farmers (58%) of the farmers were above 50  years of age. There (92%) thought antimicrobial resistance would have great seemed to be a tendency that retired civil servants invest impact on them, their families/friends and their animals. their retirement benefits in poultry farming as a means of sustaining their families, and as a result, 68% of the farmers were into full time poultry farming. Only 4% were below the age of 40. All the farmers had some level of formal education; 58% had tertiary education, 30% had postgraduate education and 12% had secondary school certificate. It is mandatory for poultry farmers to be registered with the government in some states, includ- ing Plateau and Oyo. The study showed that 90% of the farmers were registered with the government and poultry farming is the main occupation of majority (78%) of the farmers in both states. The farms were on the average, between 6 to 8  years of production with most (44%) farms having three pens per farm with an average of 1000 birds per pen in the two states. Sixty percent (60%) of farmers had layers belong- ing to sector 3 poultry production system according to Fig. 1 Frequency of disease occurrence in the farms included in the FAO classification [16]. Although all the farmers started survey Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 5 of 9 All farmers agreed that it was important to get consul- The challenges associated with taking samples to the tation from a veterinarian before giving antibiotics to lab were described by the farmers as far distance to the poultry. lab (36%) and high cost of analysis (30%) (Table 1). Most farmers (70%) did not know about antimicrobial When farmers observed that the antibiotics they used residues, however, 74% read about withdrawal period regularly were no longer effective, 62% consulted ani - from the antibiotic containers/sachets, yet all farmers mal health professionals; 24% tried different antibiotics; interviewed sold eggs under current treatment with anti- while 14% increased the dosage of antibiotics. When biotics. Since there was no provision for compensation by birds were sick, most farmers separated sick birds from government, the farmers stated that the eggs were sold. healthy ones but the entire flock undergoes treatment. Most farmers thought that antibiotics were no longer Ninety-eight percent (98%) of farmers gave antibiot- effective because of the manufacturing company; reduced ics as prophylactic treatment to day old chicks. strength of the antibiotics and the fact that diseases were becoming untreatable (Fig.  2). Although farmers inter- Types of antimicrobials used and amount of active viewed in this survey have heard about AMR, this high- ingredients in kilograms lights the lowperception of AMR among farmers and the In Plateau state, a total of 39 different antibiotics prod - need for awareness creation and sensitization. ucts from six different classes were used for treating poultry during the three  month study period (Addi- Farmers’ attitude and practices towards antimicrobial use tional file  2). Within that period, 88% of the farmers All farmers in the two states bought and used antibi- interviewed used 311  kg of active ingredients of anti- otics to treat infections. Although most farmers (84%) biotics to treat poultry (Table  2). In Oyo state, a total consulted private or government veterinarians when of 24 different antibiotics products from six different the birds were sick, 16% bought antibiotics from the drug store without consulting veterinarians, reason being that they consider to have been in the poultry business long enough to know what antibiotics to give when the birds were sick. Farmers in Nigeria have been reported to treat animals with antimicrobials without prescription [9]. Seventy-four percent (74%) of farmers bought antibiotics from poultry drug stores, while the rest (26%) obtained theirs from private and government vets. Fifty eight percent (58%) of famers covered a dis- tance of 3 to 5 kms to buy antibiotics in the two states. Therefore, antimicrobial agents were readily accessible to farmers. Seventy-two percent (70%) of farmers took samples to the lab always; 14% took samples to the lab some- Fig. 3 Frequency of taking samples to the lab when birds were sick times, while 16% never took samples to the lab (Fig. 3). in farms included in the survey Fig. 2 Farmers responses on why antibiotics were no longer effective Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 6 of 9 Table 1 Farmers’ attitude to antimicrobial use Farmers’ attitude to antimicrobial use Agree (%) Disagree (%) Indifferent (%) Farmers observe withdrawal period before selling or eating animal products 74 16 10 Farmers stop giving antibiotics if symptoms improve 30 70 0 Farmers believe that if antibiotics are given too often, they might stop working 90 8 2 Farmers believe that giving animals that are not sick antibiotics will prevent them from 60 34 6 becoming sick in the future Farmers believe that giving animals antibiotics can help them grow bigger, faster, fatter 32 64 4 Others have 3 molecules in one e.g., Table 2 Amount of active ingredients of antibiotics used within three months in poultry farms included in the survey • Neo-furaseryl (neomycin 100  mg, oxytetracycline Antibiotics Amount of active Amount of active ingredients in kg ingredients in kg 50,000 mg, colistin sulphate 30,000,000 IU plus vita- (Plateau) (Oyo) mins); • Zogceryl (oxytetracycline 5,000  mg, colistin Tetracycline 290 15.4 2,500 mg, neomycin 200 mg); Penicillin 2 0.2 • Maxiceryl (colistin 225000  IU, oxytetracycline Aminoglycoside 4 7.4 5000 mg, neomycin 5000 mg); Polypeptide 12 0.1 • Keproceryl (oxytetracycline 50 mg, colistin sulphate Fluoroquinolone 2 3.8 225,000 IU and erythromycin 35 mg) and, Amphenicol 1 0 • N.C.O mix (florfenicol 150  mg, neomycin sulphate Macrolide 0 13.1 180 mg, colistin sulphate 1,200,000 IU). Total 311 40 The need for antibiotics with multiple molecules and high concentration of active ingredients to treat infec- classes were used for treating poultry during the three tions in poultry by the farmers interviewed  could be a month study period (Additional file  3). Most of the potential driver of antibiotic resistance. farmers interviewed in both states administered anti- Furazolidone (Oxazolidines) were being used by some biotics to poultry on a monthly basis, as prophylaxes; farmers in poultry in combination with other antibiotics just before the “monthly” vaccination against Newcas- even though it was banned for use in food producing ani- tle disease. All farmers interviewed in Oyo state used mals by the regulatory authorities in Nigeria. Ampheni- 40 kg of active ingredients of antibiotics to treat poultry col was found to be used by few farmers even though it within the three month study period (Table 2). is not in the national import data reported to the WOAH All antibiotics except the human preparation of gen- for the past four years. We also observed that some prod- tamycin were given in water to layers of all age groups ucts with very high concentration of active ingredients as treatment (55%) and prophylaxes (45%); 84% of the such as Neo-furaseryl , Floricol and Furamycin were not birds were actively laying during the period of the reported in the national import data, which is an indica- study. tor for importation through other means. Of concern was the fact that some products con- Some farmers used products containing a mixture of tained cocktail of antibiotics, having up to six different antibiotics and probiotics such as Biodox (Doxycycline classes with very high concentration of active ingredi- and Lactobacillus). Fifty-six percent (56%) of farmers ents e.g., interviewed used human preparation of injectable gen- tamycin (80  mg of 2  ml vials); and Septrin (Sulphur/ • Neo-furamycin (furazolidone 6000  mg, neomy- Trimethoprim) in water because the birds were not cin 200  mg, oxytetracycline 500  mg, streptomycin responding to treatment. Others used Zingiber offici - 200  mg, erythromycin 3500  mg, chloramphenicol nale (ginger) in water as prophylaxes. 2000 mg); Some farmers administered disinfectants in drink- • Embaceryl (tylosin base 3,800  mg, oxytetracycline ing water to poultry (e.g., Viru supa disinfectants , con- 4,000  mg, neomycin sulphate 1,200  mg, colistin sul- taining potassium peroxomonosulfate 59% and sodium phate 30,000,000 IU). dichloro-iso-synurate 10%; Corygiene ); and antiseptics Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 7 of 9 ® ® such as Fivevet (iodine preparation) and Aquaseptic ) Although a greater percentage of the farms were in drinking water. fenced, 64% of customers came into the farms to buy Farmers tend not to buy more antibiotics than they eggs, which is a risk factor for disease introduction. A need at a time, but in case antibiotics expire, 96% said risk assessment carried out by the Federal Department of they would throw them away. In case of mortalities, 56% Veterinary and Pest Control Services during the outbreak of farmers fed dogs with the carcasses. of Avian influenza in Nigeria in 2016, identified eggs We observed that five classes of antibiotics (Tetracy - and manure merchants as sources of transmission of the cline, Penicillin, Aminoglycoside, Polypeptide and Fluo- pathogen from infected to non-infected farms through roquinolone) were consistent in the two states. This is in used paper crates and used sacks. agreement with the national AMC data submitted to the Even though most farmers practiced good biosecurity, WOAH for the past six years [17]. However, amphenicol all the farms visited had disease problems. was only reported in Plateau state and likewise macrolide Ninety-six percent (96%) of farmers kept farm records was only reported in Oyo state. The reason for the vari - including sales/financial, mortality, vaccination and med - ation is not clear. Also, the amount of tetracycline was icine records. higher in Plateau state and this might be attrbuted to the The fact that 72% of farmers bought commercial feed type of products (products with very high concentration was advantageous in reducing the spread of disease- of active ingredients) used by poultry farmers. causing pathogens  that could occur through exchange of sacks at toll milling stations. Although 92% of farmers Information on vaccination and biosecurity admit that additives were added to the feed they used for All farmers interviewed began with day-old-chicks as poultry, none contained antibiotics. starter flock and 72% stated that the chicks were vacci - All farmers used well or borehole water for poultry and nated at day old against diseases such as Marek’s from drinkers were washed on a daily bases by most farmers. the hatcheries. All farmers vaccinated poultry against the following diseases: Newcastle disease, Gumboro disease, Discussion Coccidiosis, Fowl pox, Fowl typhoid, Marek’s disease, The use of structured questionnaire enabled us to col - Egg drop syndrome, Fowl cholera and Avian encephali- lect actual AMU data at the farm level. Seven classes of tis. Although there is a “No vaccination” policy on Avian antimicrobial agents (Tetracycline, Penicillin, Amino- Influenza in Nigeria, we found out during the course of glycoside, Macrolide, Fluoroquinolone, Amphenicol and the study that some farmers vaccinated against the dis- Polypeptide) were identified in the two states during ease. Following vaccination, some birds still came down the three month study period. Tetracyclines accounted with the same disease in some of the farms. Fifty-two for the highest antibiotics used in both states, followed percent (52%) of farmers agreed that using vaccines could by Polypeptides, Aminoglycosides and Fluoroquinolo- prevent the use of antibiotics, while 34% disagreed and nes  respectively. This finding is in concordance with 14% were indifferent. the annual AMC data reported to the WOAH by Nige- Fifty-eight percent (58%) of farms included in this sur- ria [Federal Department of Veterinary and Pest Control vey were fenced to regulate human and animal traffic as a Services (FDVPCS)]. Adesokan et  al. [3] also reported form of biosecurity. All the pens had wire mesh and the tetracyclines, fluoroquinolones, beta lactams and amino - floors made of concrete for ease of cleaning and disin - glycosides as the leading antimicrobials used in livestock fection. All the farms had foot dip at the entrance, and production in Nigeria. A total of 351 kg of active ingredi- most farmers (56%) changed the disinfectant water on a ents of antibiotics were used in poultry in the farms vis- daily bases, while others changed on a weekly (22%) or ited within the three month study period. monthly (22%) bases. Ninety-two percent (92%) of the The study revealed that farmers used cocktail of anti - farms had changing rooms and workers wore specific biotics, having up to six different classes with very high clothing and boots during work on the farm; 96% of the concentration of active ingredients. The study  also workers were almost always permanently assigned to revealed that farmers were using antibiotics banned by work in separate pens. None of the staff worked on other the regulatory authorities even though such products farms and only 20% had poultry at home. All farmers are not captured in the annual import data reported to cleaned and disinfected pens after selling each batch of the WOAH. These practices could aggravate the devel - poultry. opment and spread of resistance by microorganisms Most farms (96%) were neighbors with other poul- through selective pressure. try farms within 1  km radius and almost all farmers Farmers interviewed used antibiotics to treat infec- allowed their farms to rest for at least one month before tions, though not always based on laboratory test and restocking. prescription from veterinarians. The continuous overuse Ndahi et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 8 of 9 of antimicrobial agents by poultry farmers in this study some insight on farmers’ practices with regards to the use could pose a public health threat, thereby exposing of antimicrobials which is missing in the national import humans to subclinical doses of antimicrobials through data. It can therefore be adopted to improve AMU sur- the food chain, especially since some antimicrobials are veillance in Nigeria. The concept is already being further potentially carcinogenic, allergenic mutagenic and tera- developed and expanded for national AMU data collec- togenic. Some farmers have resolved to using human tion in all the states of the federation, pending availability preparations of antibiotics especially injecting birds with of funds. gentamycin for treating infections that did not respond There is also clear evidence that the current surveil - to treatment. lance of AMU using the national import data is missing Most farmers interviewed were retirees, above the age some important data. Especially the fact that antimicro- of 50 who have used their retirement benefits to start bials such as Furazolidone is being used by some farm- up poultry farming as a main source of livelihood. Most ers in poultry in combination with other antibiotics even of the farms belonged to sector 3 as categorized by the though it was banned for use in food producing animals FAO  [16]. Although all farms had some form of bios- by the regulatory authorities in Nigeria. Also, the fact ecurity measures in place, rationale behind the measures that Amphenicol was found to be used by few farmers on was not fully understood by farmers, for example, farm- the field even though it is not in the national import data ers allowed eggs and manure merchants into the farms. reported to the WOAH for the past four years. We also Hence, all farms visited were faced with disease problems observed that some products with very high concentra- in poultry such as Newcastle Disease, Coccidiosis, Fowl tion of active ingredients such as Neo-furaseryl , Floricol Typhoid, E. coli infection, among others. Newcastle dis- and Furamycin were not reported in the national import ease was the highest most recurring disease in the two data, which is an indicator for importation through other states. Coccidiosis was found to be higher in Oyo state. means. The use of human preparations of Septrin and Although most farmers interviewed have heard of anti- Gentamycin injection in poultry to treat resistant strains microbial resistance, there was a low-risk perception of is a clear indication of resistance to antibiotics used in antimicrobial resistance among them. The repeated use of poultry. Five classes of antibiotics (Tetracycline, Penicil- antimicrobials as prophylaxis instead of applying preven- lin, Aminoglycoside, Polypeptide and Fluoroquinolone) tive measures such as improved management practices were used in the two states, however, amphenicol was and biosecurity measures is an indication of low-risk per- only reported in Plateau state and likewise macrolide ception. Hence the need for continuous awareness crea- was only reported in Oyo state. This study is therefore tion and sensitization of farmers on the danger of AMR a pointer that the approach used could be applied to and trainings on the use of alternatives to antimicrobials gather useful information directly from the farms as well such as improved biosecurity practices, effective vacci - as generate and calculate the actual amount of antimi- nation and the use of pre and probiotics. The belief that crobial agents used in poultry using the WOAH guide- antibiotics were no longer effective because of reduced lines. The fact that AMU data was generated during the strength or because diseases were becoming untreatable survey indicated the possibility of using this approach for and not due to overuse of antibiotics or poor manage- national AMU surveillance. ment practices further buttressed this point. This study In order to generate the actual antimicrobial use data, revealed the possibility that a majority of eggs in the mar- there is need to collect data from the farms and clinics ket might contain some residues of antimicrobial agents levels especially since some antibiotics reported by farm- since eggs were sold during treatment. This would war - ers are not captured in the import data. There is also the rant further study and efforts to improve farmer practices need to increase awareness among poultry farmers on to minimize any risk to the food chain. the importance of biosecurity; disease preventive meas- Despite the fact that all farmers vaccinate birds against ures such as vaccination and promote the use of probi- preventable diseases and observe some level of bios- otics to enhance production. These would reduce disease ecurity measures, the fact that customers came into the introduction to farms and ultimately reduce the use of farms to buy eggs were identified as high-risk factors for antibiotics. Increased awareness creation and sensitiza- disease entry into farms and resultant increase in the use tion among private veterinarians and poultry drug sell- of antibiotics. ers on the danger of AMR and the need for prescriptions from laboratory test results before prescribing or selling Conclusion antibiotics to farmers will go a long way in mitigating The use of structured questionnaire for this survey AMR. proved that the approach can be applied for AMU sur- veillance in the animal health sector. It also provided Ndahi  et al. Antimicrobial Resistance & Infection Control (2023) 12:30 Page 9 of 9 References Supplementary Information 1. Livestock population figures, FMARD, 2018, Animal husbandry Depart ‑ The online version contains supplementary material available at https:// doi. ment, Federal Ministry of Agriculture. org/ 10. 1186/ s13756‑ 023‑ 01235‑x. 2. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Laxminarayan R. Global trends in antimicrobial use in food animals. Proc Additional file 1. Annex to the Guidance for Completing the OIE tem‑ Natl Acad Sci. 2015;112(18):5649–54. plate for the collection of data on Antimicrobial Agents intended for use 3. Adesokan HK, Akanbi IO, Akanbi IM, Obaweda RA. Pattern of antimicro‑ in Animals. bial usage in livestock animals in southwestern Nigeria: The need for alternative plans. Onderstepoort J Vet Res. 2015;82(1):6. https:// doi. org/ Additional file 2. List of antibiotics used on farms (Plateau). 10. 4102/ ojvr. v82i1. 816. Additional file 3. List of antibiotics used on farms (Oyo state). 4. OIE. Terrestrial Animal Health Code. (2018). https:// www. oie. int/ en/ stand ard‑ setti ng/ terre strial‑ code/ access‑ online . 5. https:// www. nafdac. gov. ng/ veter inary‑ produ cts/ list‑ of‑ banned v‑eter Acknowledgements inary‑ drugs/. The authors appreciate the United Kingdom (UK) Government, through the 6. Antimicrobial use and Resistance in Nigeria – Situation Analysis and UK Department of Health and Social Services and the Fleming Fund Fellow‑ Recommendations, 2017. ship Project for funding this study. The authors are thankful to their beneficiary 7. Nurudeen OO, Ismail AA, Henriette van H, Olubunmi GF, Folorunso Institutions especially the management of the Federal Ministry of Agriculture OF. Antimicrobial drug administration and antimicrobial resistance of and Rural Development for the opportunity to be part of the Fellowship salmonella isolates originating from the broiler production value chain in program. Nigeria. Antibiotics 2019; 8, 75; https:// doi. org/ 10. 3390/ antib iotic s8020 Author contributions 8. Antimicrobial Use in Food‑Animal Production Problems, Solutions, Chal‑ MDN participated in the study design, modified the questionnaire used in the lenges. www. react group. org/ toolb ox (2017). study, participated in the focus group discussion, administered the question‑ 9. NmaBida AB, Tajudeen OI. Antimicrobial usage by pastoralists in food naire to farmers, collated the responses, analyzed the data and developed the animals in North central Nigeria: the associated cultural drivers for antimi‑ first draft of the manuscript. JKA participated in the study design, supervised crobial misuse and public health implications. Elsevier. 2011. https:// doi. the research, supported in the modification of questionnaire and reviewed org/ 10. 1016/j. onehlt. 2018. 11. 001. the manuscript. RH, BH and RMC provided guidance in the modification of 10. Omeiza GK, Ajayi IE, Okwoche OJ. Assessment of antimicrobial drug questionnaire and supervised the research. RMC also reviewed the manu‑ residues in beef in Abuja, the Federal Capital Territory. Nigeria Veterinaria script. IOF, OOA‑A, EE, VA and IA took part in the joint collaborative project. IOF Italiana. 2012;48(3):283–9. also participated in the focus group discussion. All authors read and approved 11. Ndahi MD, Kwaga JKP, Bello M, Kabir J, Umoh VJ, Yakubu SE, Nok AJ. the final manuscript. Prevalence and antimicrobial susceptibility of Listeria monocytogenes and Methicillin Resistant Staphylococcus aureus strains from raw meat and Funding meat products in Zaria Nigeria. Lett Appl Microbiol. 2013;58:262–9. This study was funded by the United Kingdom (UK) Government, through the 12. O’Neill J.. Review on Antimicrobial Resistance – Tackling a crises for the UK Department of Health and Social Services are the donors of the Fleming health and wealth of nations (2014). Fund Grants. The work was supervised by Jens Kirk Andersen of the Technical 13. https:// cityp opula tion. de/ en/ niger ia/ admin/ NGA03 2__ plate au/. University of Denmark (DTU). Retrieved on 15 September, 2020. 14. https:// cityp opula tion. de/ en/ niger ia/ admin/ NGA03 1__ oyo/. Retrieved Availability of data and materials on 15 September, 2020. A link to the questionnaire is given below: https:// ee. human itari anres ponse. 15. https:// ee. human itari anres ponse. info/ x/# FLRov 2EB info/ single/ gOqBg WQO 16. FAO (2004). Poultry production sectors. http:// www. fao. org/ docs/ eims/ uploa d// 224897/ facts heet_ produ ction secto rs_ en. pdf (Cited by Hanh, P.T. H., Burgos, S and Roland‑Holst, D. (2007). The Poultry Sector in Viet Nam: Declarations Prospects for Smallholder Producers in the Aftermath of the HPAI Crisis. Pro-Poor Livestock Policy Initiative A Living from Livestock Research Report, Ethical approval and consent to participants 1 – 14. Verbal informed consent was obtained from all participants before each 17. Antimicrobial Use Report‑Federal Department of Veterinary and Pest interview. Control Services, Nigeria. Competing interests The authors declare that they have no competing interests. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub‑ Author details lished maps and institutional affiliations. Department of Veterinary and Pest Control Services, Federal Ministry of Agri‑ culture and Rural Development, Area 11, Garki, Abuja, Nigeria. T echnical University of Denmark, Kongens Lyngby, Copenhagen, Denmark. Animal and Plant Health Agency, Weybridge, Woodham Lane, New Haw, Addlestone, Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : Surrey, UK. National Veterinary Research Institute, Vom, Plateau State, Nigeria. National Agency for Food and Drug Administration and Control, Lagos, Nige‑ fast, convenient online submission ria. Nigeria Centre for Disease Control Laboratory, Gaduwa, Abuja, Nigeria. thorough peer review by experienced researchers in your field 7 8 University of Ibadan, Ibadan, Nigeria. University College Hospital, Ibadan, rapid publication on acceptance Nigeria. support for research data, including large and complex data types Received: 29 August 2022 Accepted: 26 March 2023 • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

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Antimicrobial Resistance and Infection Control – Springer Journals

Published: Apr 10, 2023

Keywords: Antimicrobials; Antimicrobial resistance; Antimicrobial use; Active ingredients; Poultry and kobotool

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