Chauhan et al.

Antimicrobial Resistance and Infection Control (2018) 7:60

https://doi.org/10.1186/s13756-018-0354-9

RESEARCH Open Access

The social biography of antibiotic use in

smallholder dairy farms in India
Abhimanyu Singh Chauhan1,2, Mathew Sunil George3,4, Pranab Chatterjee1,5, Johanna Lindahl6,7,8, Delia Grace6
and Manish Kakkar1*

Abstract
Background: Antimicrobial resistance (AMR) has been identified as one of the major threats to global health, food
security and development today. While there has been considerable attention about the use and misuse of
antibiotics amongst human populations in both research and policy environments, there is no definitive estimate of
the extent of misuse of antibiotics in the veterinary sector and its contribution to AMR in humans. In this study, we
explored the drivers ofirrational usage of verterinary antibiotics in the dairy farming sector in peri-urban India.
Methods and materials: The study was conducted in the peri-urban belts of Ludhiana, Guwahati and Bangalore. A
total of 54 interviews (formal and non-formal) were carried out across these three sites. Theme guides were developed
to explore different drivers of veterinary antimicrobial use. Data was audio recorded and transcribed. Analysis of the
coded data set was carried out using AtlasTi. Version 7. Themes emerged inductively from the set of codes.
Results: Findings were presented based on concept of ‘levels of analyses’. Emergent themes were categorised as
individual, health systems, and policy level drivers. Low level of knowledge related to antibiotics among farmers, active
informal service providers, direct marketing of drugs to the farmers and easily available antibiotics, dispensed without
appropriate prescriptions contributed to easy access to antibiotics, and were identified to be the possible drivers
contributing to the non-prescribed and self-administered use of antibiotics in the dairy farms.
Conclusions: Smallholding dairy farmers operated within very small margins of profits. The paucity of formal veterinary
services at the community level, coupled with easy availability of antibiotics and the need to ensure profits and
minimise losses, promoted non-prescribed antibiotic consumption. It is essential that these local drivers of irrational
antibiotic use are understood in order to develop interventions and policies that seek to reduce antibiotic misuse.
Keywords: Antimicrobial use, Antimicrobial resistance, Dairy farm, Dairy farmer, Veterinary, Qualitative, India

Background smallholder farms, which cover over 45% of agricultural

India is the global leader in the production of milk and land and account for over half of total production [2, 3].
dairy products, accounting for 18.5% of the global out- India has witnessed unprecedented growth in the
put, with an annual output of 146 million tons [1]. The urban population over the past decade [4]. Peri-urban
tremendous growth in the demand for milk and other fringes, developing in the shadows of India’s growing cities,
animal-source foods has been accompanied by a corre- play an increasingly important role in ensuring food secur-
sponding increase in small-scale ventures, characterised ity including dairy farms [5]. To maintain production
by farms that typically occupy less than one hectare, em- levels, these farms, which often function in jurisdictional
ploy within-family labour, and function with minimal in- grey zones, with minimal quality control, infrastructure,
put costs by adopting intensive, industry style rearing of support and oversight, practise which may result in adverse
livestock [2]. Over 80% of all cattle holdings in India are in public health impacts [6, 7]. One such practice, which may
have long-term adverse effects, is the non-therapeutic, ir-
rational use of antibiotics in farm animals [8, 9].
* Correspondence: [email protected]
1
Public Health Foundation of India, Plot 47, Sector 44, Gurgaon, Haryana
Antibiotics are arguably the single most important and
122002, India widely used medical intervention of our times. They
Full list of author information is available at the end of the article

© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 2 of 13

have been rampantly used not only in human medicine Sampling and data collection
but also in agricultural system(s), specifically in livestock Data collection at each of the field sites was carried out
production. Antibiotics are used therapeutically to treat in successive phases.. The dual strategies of purposive
sick animals, as well as prophylactically and metaphylacti- sampling and snowballing were employed to identify po-
cally to prevent infection and as growth promoters [10]. tential respondents with the help of the local partners in
Emergence of infectious agents which are resistant to each of the field sites. This enabled us to not only iden-
commonly used antimicrobial agents threatens the ad- tify those stakeholders whom knew to be relevant to this
vances made by modern medicine, and AMR organisms study, but also identify specific stakeholders at each site,
have rapidly become one of the primary public health who were involved, in some capacity, with smallholder
challenges the world over, but especially in developing and dairy farmers (eg: traders and veterinary field assistants in
low- and middle-income countries like India [11]. Guwahati, informal treatment providers in Ludhiana, and
Multiple studies in India, beginning with exploratory the Karnataka Milk Federation officials in Bangalore). At
studies in the 1980s, have consistently shown that a large each of the sites, we identified areas where most dairy
proportion of the tested milk samples contain antibiotic farms were clustered and fitted the project definition of a
residues [12–15]. A recent study undertaken in the orga- smallholding dairy farm (A farm with up-to 10 cattle, at-
nised as well as organised dairy farms has reported tetracyc- least one milking and contributing to a minimum of 25%
line, oxytetracycline, sulfadimidine and sulfamethoxazole of the total family income). From this list we then selected
above MRL in milk samples [16]. Similarly, antimicrobial farms that were spread across various locations, thus en-
residues was reported in 23.3% dairy farm in the settings suring representation of farms from across the various
similar to the current study [17]. However, there re- clusters (i.e., north, south, east and west). Using a phasic,
mains a dearth of evidence about the drivers and de- cyclical strategy for the fieldwork, data collection was
terminants of antibiotic use in dairy farms in India, stopped on reaching saturation point across the various
especially with respect to vulnerable areas like peri-urban key themes of inquiry.
areas [18]. This study was conducted to understand the The health related interviews were conducted by ASC
practices and drivers related to the veterinary use of anti- (male) and MSG (male). Both the interviewers were
biotics in peri-urban smallholder dairy farms in selected practicing public health researchers with over five years
sites of India. experience in qualitative data collection and held gradu-
ation in public health (MPH) at the time of field work.
Methods Face to face interviews with farmers were conducted at
Study setting their homes, whereas those with other stakeholders were
The study was conducted among smallholding dairy typically conducted at their places of employment (like,
farmers in peri-urban areas of Guwahati,east of India, veterinary hospital, pharmacy etc.). Local NGO facilitated
(26.1445° N, 91.7362° E); Ludhiana, north of India (30. the scheduling of interviews as per the time convenient to
9010° N, 75.8573° E); and Bangalore, south of India (12. farmers. An appointment was sought with the government
9716° N, 77.5946° E). Like any developing country, peri- functionaries in advance and almost all interviews were
urban areas of a typical city encompass a wide range of conducted in the office premises. Most interviews with
economic activities, including farming (dairy, poultry farmers and traders were conducted in the local language
etc.), husbandry and, small and medium scale industries, (Hindi, Punjabi and Kannada at Guwahati, Ludhiana and
land speculation, residential suburbanization and waste Bangalore site, respectively). However, government offi-
disposal [19]. Definition of Peri-urban is still context cials were comfortable in interacting in English. In order
specific and varies from city to city, it’s difficult to esti- to ensure that the mediator did not introduce bias and
mate the exact population. However, large proportion of followed the topic guide faithfully, mock interviews and
people from rural to urban migration settles in peri- training were carried out prior to the actual field visit. A
urban fringes of the cities [19]. The background review typical interview lasted between 45 min to 1 h. All inter-
of literature, the formative phase, and a formal consult- views were audio-recorded, transcribed, translated into
ation with experts enabled us to identify relevant stake- English, and crosschecked against the original recordings.
holders in each of the sites, whilst allowing us to refine
the topic guides that we used for data collection. The Data management and analysis
main phase of data collection was preceded by a forma- Data analyses was done using inductive approach and con-
tive phase that included scoping interviews with key tent analyses. The translated transcripts were then coded
informants at each site, as well as a pilot testing of using the software package AtlasTi 7.2®, utilizing a reflexive
instruments. Fieldwork was carried out between1st and inductive approach to allow codes and categories to
February 2015 to 30th September 2015 across all three emerge from within the data. The initial list of codes was
study sites. compared with newer codes, enabling refinement of the

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 3 of 13

coding framework, which was utilised to guide the coding farmers and sold to sweet shops and households, were
process. Coding was done by two coders and coding dis- interviewed in Guwahati. Officials of Karnataka Milk
agreements was sorted in consultation with senior re- Federation (KMF), a cooperative with a membership
searchers of the study (MK and DG). base of around 90% of the smallholder dairy farmers
In addition to the interview recordings, each researcher in periurban Bengaluru, were also interviewed. Those
maintained detailed field notes in field diaries. This en- who were approached, none of them refused to par-
abled capturing of details related to the key issues that ticipate in the study.
emerged in each location, concerns regarding the field- The results are presented as three core themes that
work, as well as any potential trends that emerged from emerged from insights of the different stakeholders: 1.
the participant responses. The field diary provided us with Self-treatment and peer learning; 2. Limited systems
adequate details to discuss during the daily review carried support, outreach and oversight; 3. Limited regulatory
out at the end of the day’s work and plan for subsequent framework to regulate use, market pressures and distri-
data collection. The field diaries also helped in identifying bution of veterinary antibiotics. Details of sub-themes
early patterns as well as assessing attainment of saturation and domains are listed in Table 2.
of responses. Themes could be further grouped into drivers operat-
At the end of each phase, data management and analysis ing at three levels of the system: individual, health sys-
of the previous site was completed, and summary results tems, and market or policy levels. The system, in this
prepared. This enabled further probing of specific areas. case, was defined as the smallholder dairy farm in peri-
This iterative process ensured that the data collected was urban settings and its associated veterinary antibiotic
grounded, rich in details, and saturation obtained prior to use practices. The concept of a “system” allowed us to
termination of data collection. study the linkages and interactions between the sub-
themes and core themes that operate at different levels.
Quality assurance For the purpose of this study, individual/community level
Interviews were conducted by trained investigators.They drivers were defined as practices at the level of farm
were monitored for completeness, correctness, and com- owners, labourers, family members, community, traders
prehensive transcription and translation of responses with and others players who can influence antimicrobial usage.
appropriate labelling of recordings. Thirty per cent of the Health systems drivers were defined as those associated
interviews from every site were randomly rechecked for with systems stakeholders like veterinary doctors, veterin-
transcription and translation. Due to inherent limitations ary field assistants, laboratory staff and others who could
of interpretation of qualitative data from different parts of possibly contribute to the dynamics of antimicrobial usage
the country, we undertook regular consultations with the in small holding dairy farms. Policy level drivers included
steering group (comprising of seven experts across the the drivers that were associated with the government, na-
fields of medical, veterinary and social sciences) about the tional as well as local, and policies affecting the use of an-
data and its interpretations. timicrobials in smallholding dairy farms.
It was ensured that interviews were conducted in place
where only interviewee and interviewer was present. The CORE THEME I - Self-treatment and peer learning:
study followed the COnsolidated criteria for REporting Individual and community level drivers for irrational
Qualitative research (COREQ) for reporting the findings usage of veterinary antibiotics
of this qualitative research study [20]. Self-treatment of animals by farmers and peer learning were
significant determinants of antibiotic usage, which emerged
Results as the core theme at the community/individual level. These
A total of 54 interviews (formal and non-formal) were core themes further comprised of limited knowledge, self-
conducted across the three sites (Table 1). These included treatment, and peer-learning as sub themes.
dairy farmers, veterinary officers, veterinary field assis-
tants, pharmacists, drug distributors and civic officials. Sub-theme I – Knowledge about veterinary antibiotics
Site-specific stakeholders were also identified through the Majority of the farmers across three sites were unaware of
snowballing process. Traders, who procured milk from the word ‘antibiotic’. No local name existed specifically for

Table 1 Details of the stakeholders interviewed

Study sites Dairy farmer Veterinary/ Ext. officer Veterinary field assistant Trader Pharmacist/Drug Distr. Civic official Or Union
Guwahati 7 5 3 3 3 3
Bangalore 4 6 2 N/A 2 3
Ludhiana 4 2 2 N/A 2 3

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 4 of 13

Table 2 Core themes and sub-themes emerged from the inductive data analyses
Sl. No. Domain Core themes Sub-themes
1 Community and Individual Self-treatment and peer learning Limited knowledge about antibiotics and their use
Self-treatment using veterinary antibiotics
Peer learning and self-treatment
2 Veterinary health system support Limited system support, outreach and oversight. Shortage of veterinary doctors
Laboratory support to diagnose diseases and make
informed prescription
Support from extension services
Shortage of pharmacists
3 Policy and market scenario Limited regulatory framework on usage, market Absence of regulation for veterinary antibiotics
pressures and distribution of veterinary antibiotics
Direct marketing of veterinary antibiotics to
consumer
Compulsion of milking - Market demand and
competition.

the term either. Most of the farmers could not differenti- medicines that the doctor prescribed last time.”
ate between antibiotics and non-antibiotic, allopathic (Dairy farmer, Guwahati).
medicines. However, the interviewed veterinarians re-
ported that many farmers administer antibiotics to the One of the reasons stated for self-treatment was the
farm cattle irrespective of the disease being infectious cost of getting a veterinarian to come to the farm, espe-
or not. Veterinarians also mentioned that choice of cially in Guwahati. While this was not an issue among
drug is based mostly on the ease of availability and the well-established farms, smallholding farmers found this
experience of the farmers with the drug while treating to be barrier.
similar symptoms on previous occasions, some of
which could be undertaken at the advise of a veterinar- “My biggest problem is if my animals fall sick. Getting
ian. Fin. a veterinarian to come to my farm is costly and I can’t
afford it. I give the animal what I can”. (Dairy farmer,
Sub-theme II - Self-treatment using veterinary antibiotics Guwahati).
Most information on how farmers prefer medicines that
give them ‘quick results’ came from pharmacists. Sick
animals are treated with broad-spectrum antibiotics on
Sub- theme III - Peer learning and self-treatment
the basis of prior experience. This experience could be
Many field veterinarians, as well as a few dairy farmers, re-
that of the concerned farmer or be obtained through by
ported that they follow the advice of the local elders, influ-
social peer learning networks (like elders or influential
ential persons, or village heads (‘Gaon budha’ (Guwahati)
farmers who had previously treated their cattle success-
and ‘sarpanch’ (Ludhiana)) for advice related to medica-
fully; more details in the next subsection). Intergenera-
tion. Most of these opinion leaders are commercial dairy
tional transfer of this information also played a significant
farmers with farms having more than 50 heads of cattle.
role. Additionally, nearly all the veterinarians reported that
They usually enjoy a good relationship with pharmaceut-
by the time a farmer brings his animal to a licensed veter-
ical representatives and drug distributors.
inarian, the farmer would have already tried out several
treatment strategies, none of which were successful in cur-
ing the affected animal. CORE THEME II - limited system support, outreach and
oversight
“We are trying this medicine for last three days but Limited systems support, outreach and oversight were sig-
not seeing much improvement; we will wait a bit and nificant reasons of antibiotic usage and emerged as the core
see, and if we do not see any improvements, we will theme at the veterinary health systems level. These core
try to call a doctor.” (Dairy farmer, Ludhiana). themes further could be split into the following factors: a
shortage of licensed veterinarians and a profusion of infor-
“If I know what the problem is then I try to manage mal prescribers; laboratory support to diagnose diseases
it. Sometimes it will be the same problem that and plan appropriate therapeutic strategies; inadequate
another cow had, so I will buy and give the same IEC (Information, Education and Communication) support

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 5 of 13

through extension services; and a shortage of veterinary disease screening programs specifically directed at cattle
pharmacists with a profusion of informal drug distributors. in smallholder dairy farms.

Field veterinarians’ perspective Veterinarians reported

Sub-theme I: Shortage of veterinary doctors and active
that they do not depend on lab reports to treat any sick
informal prescribers
animals. Most treatment plans were based on case his-
All three levels of stakeholders in the three sitesreported
tory and symptomatic assessments. Lab support was
that there was an acute shortage of trained veterinarians.
only sought when the treatment administered to the ani-
Stakeholders, including veterinary doctors and state
mal did not give the desired results. Two reasons were
officials, also reported that veterinary field assistants and
stated by veterinarians for not seeking lab support: First,
informal prescribers attempt to fill the gap. This results
by the time a farmer reaches the veterinarian the farmer
in a cadre of untrained caregivers with a propensity to
has already spent time and money in trying out other al-
overprescribe, leading to irrational prescription and
ternatives and the veterinarian has to begin some treat-
usage of antibiotics. These informal prescribers are also
ment almost immediately to save the cattle. Secondly,
known as ‘private doctors’ among the dairy farmers.
even if labs do exist, most of them are not adequately
equipped; if they are equipped, it would be expensive
“How it is possible for a doctor to visit 30,000 cows? So
and unaffordable to access their services, and hence it
definitely, if you call me and someone else calls me at
was not considered to be practical to utilize them.
the same time and there is a distance of 10 KM
between the two houses, it is not possible for me to
“If the lab is in working condition we don’t have a
attend to both the cases simultaneously. I will definitely
microbiologist, if the microbiologist is there then there
have to send somebody to attend the other patient. So
is no proper equipment. So how do I make use of it? On
what I do is that I send the VFA and tell him to go and
paper it is all there but practically it is not possible. If I
check on the patient, and consult me over the phone.
need a lab report, then I ask them to go to the university
Mobiles are extensively used now, so it is possible. I do
or to some private labs to get a report.” (Veterinarian,
not go for visits nowadays, yet I have the information
Ludhiana).
that I need to know. I think non-availability [of enough
trained and licensed veterinarians] is one of the
“Look, we treat primarily from the case history of the sick
reasons, and because of that, slowly they (the VFAs)
animal and after some years of experience you know that
are emerging as the first point of care consultant; the
an animal which is in this condition, is suffering from this
other reason is that if they call the VFA then the fees
problem, and needs this treatment. Other than that not
will be much lower than that of a veterinarian, I think
much to do for us.” (Veterinarian, Guwahati).
that might also be one of the reasons” (Veterinary
doctor, Guwahati).
Sub theme III: Support from extension services in context to
“The private doctors, they keep visiting farms and are
veterinary use of antibiotics
very busy. In fact, they are occupied from early in the
morning to late evenings everyday. They are not really
Dairy farmers’ perspective It was striking that none of
doctors but that’s what they are known as. They treat a
the farmers across the three sites referred to benefitting
lot of animals in these farms” (Pharmacist, Ludhiana).
from any extension services. They perceived services to
be of poor quality. Also, according to them, these ser-
vices were conducted more out of the need to demon-
Sub theme II: Laboratory support to diagnose diseases strate activities to students, and were not particularly
and make informed prescription concerned with the welfare of a farmer or their animals.

Senior government officials’ perspective Across the “What services are you talking about? There is such a
three sites, senior officials in the animal husbandry de- big college here and they can’t even provide us with
partment pointed out that labs and diagnostic support proper semen.” (Dairy farmer, Guwahati).
services were functional and provided value addition to
the work of field veterinarians. However, when asked “No we do not get anything from the department or
specifically about testing and screening facility for vari- college.” (Dairy farmer, Ludhiana).
ous infections in cattle, very few veterinarians mentioned
regular testing done at the smallholder or commercial Many of those who attended demonstration sessions
dairy farms. None of the state level officials reported any and meetings happened to be owners of commercial dairy

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 6 of 13

farms. These were individuals who had no prior experi- pressures are significant determinants of antibiotic over
ence of dairying and had entered the sector recently. usage. These emerged as the core theme at the policy
level. These core themes could further be split into:
“The department does organise activities from time to absence of regulation for the prudent use of veterin-
time when they want to train their students. Other ary antibiotics, Direct-to-Consumer Marketing of Veter-
than that such activities are not focused on the small inary Antibiotics (DTCMVA) and compulsion to maintain
farmers and their farms.”(Dairy farmer, Guwahati). productivity to meet market demands in the face of stiff
economic competition.

Extension department officials’ opinion Extension de- Sub theme I: Absence of regulation for the prudent use of
partments are functional and claimed to offer relevant veterinary antibiotics
services to local dairy farmers on a regular basis. These Nearly all veterinary doctors and senior state level offi-
services include sessions on the updated management cials expressed the need to deploy potent regulations to
practices in dairy farming, inputs on fodder manage- deal with the situation of antibiotic growth promoters
ment, disease management, breeding techniques, shed and non-therapeutic use of antibiotics. Many of the
design, to name a few. Most services were offered com- senior officials also reported the absence of evidence-
pletely free of charge so that local dairy farmers belong- based guidelines related to the prudent use of veterinary
ing to the lower socioeconomic strata could reap the antibiotics; even when they were present, they were
benefits. However, when asked about the specific activ- constrained by the complete absence of a strategy to
ities related to the use of antibiotics and their role in operationalize the recommendations and monitor their
maintaining the health of animals, the interviewed stake- implementation.
holders (state-level officials and veterinarians) failed to
mention any particular programs. Sub theme II: Direct to consumer Marketing of Veterinary
Antibiotics (DTCMVA)
“Regular meetings are organized by the department
and we have sessions taken by experts to give them “While visiting a village in Guwahati to capture the
[dairy farmers] the latest know-how on various issues insights from small holder dairy farmers related to
on how to manage a dairy farm.” (Senior extension veterinary use of antibiotics, we observed a Medical
department official, Ludhiana). Representative (MR) from a renowned pharmaceutical
company visiting the most learned and influential
Many veterinarians reported that farmers often chose (village leader) dairy farmer in the village. He was
to not attend these sessions. According to them, this is carrying boxes with a range of medicines - concentrates,
due to the farmers’ belief and reliance on traditional calcium supplements as well as veterinary antibiotics.
knowledge, which is often handed down generations. In When asked about the content and why he has been
contrast, relatively new commercial dairy farmers, were keeping these items at the leader’s house, we were
more open to learning and behaviour modification in re- informed by the dairy farmers that this was the ‘drug
lation to dairy farming practices. depot’ of the village. All farmers could access and
purchase these medicines as and when required.
Sub-theme IV: Shortage of pharmacists and presence of Pharmacies are too far away and a significant cost is
informal drug distributors incurred when visiting them. Older members of the
Some veterinary officers and state level officials reported village informed that the depot holder received financial
the scarcity of trained pharmacists in the peri-urban incentives from the MR as well as a supply of medicines
areas; this was especially notable in Guwahati. According at a discounted rate. As the depot holder is
to them, most of the drugs were distributed by drug dis- comparatively more qualified and influential, dairy
tributors. Even if a pharmacist is present, prescription- farmers often consult him for the medicines and
based purchase is minimal in all the studied settings. treatment. We discussed and validated these responses
They forwarded this as one of the reasons for the ir- with local veterinarian and state level officials.”
rational use of veterinary antibiotics. [Excerpt from field diary, 13th March 2015, Guwahati,
Description of DTCMVA phenomena].
CORE THEME III: Limited regulatory framework on usage
and distribution of veterinary antibiotics, and market During field observations in Guwahati, we observed
pressure: Policy and market level drivers that the antibiotics are directly marketed in the village.
Limited legislative frameworks to regulate the use and The most influential or community leader or commer-
distribution of veterinary antibiotics, and mitigate market cial dairy farmer acts as mediator between MR and

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 7 of 13

smallholder dairy farmers. The relationship is mutually Behavioural model of drivers and determinants of
beneficial as the farmer gets the drugs at a discounted non-prescribed use of antibiotics in smallholder
rate and without having to travel to a distant pharmacy; periurban dairy farms
in return, this helps the pharmaceutical representatives We developed a conceptual framework explaining the
to meet their sales targets. For the village elders or opin- interplay of factors leading to non-prescribed usage of vet-
ion leaders, this offers a position of relative power, which erinary antibiotics using The theory of planned behaviour
further consolidates their status in the community. Some (Fig. 1) [21]. We mapped these factors to address the rea-
smallholder farmers also reported that the depot holder soned action for non-prescribed or self-administered use
was often offered medicines at a discounted rate by the of veterinary antibiotics in the peri-urban smallholder
pharmaceutical representative. dairy farms. This was determined by: [1] attitude towards
irrational use of antibiotics, [2] subjective belief about the
Sub theme III: Compulsion of milking - market demand and irrational use of antibiotics at the community level, and
economic compulsion [3] the perceived control exerted over the act of irrational
Nearly all the stakeholders reported that the business of antibiotic use in livestock. Subjective belief is the per-
smallholding dairy farms operates at razor thin profit ceived social pressure to perform or not to perform the
margins and to keep their livelihood intact the farmers behaviour and perceived control is an individual’s beliefs
need to maintain productivity in their animals on a daily about the presence of factors that may facilitate or hinder
basis. A majority of the farmers were unaware about the performance of the behaviour. We classified the drivers
concept of withdrawal period following antimicrobial operational at the community, the system, and the market
chemotherapy. However, even those who were aware of and policy levels. These drivers, in combination, resulted
the importance of the withholding period reported that in the practice of self-administered use of antibiotics in
it was impractical due to high economic implications to livestock. The conceptual model, shown in Fig. 1, indicates
their business. Additionally, famers also reported that a closely knit, inter-related, web of factors with recursive
they faced competition from milk cooperatives and pri- and reversible relationships. It is essential to disrupt this
vate companies. This resulted in dwindling demands for chain at the critical linkages to make a meaningful reduc-
non-packaged milk in the urban areas. As a result with- tion in the irrational and non-prescribed consumption of
holding milking and not supplying milk even for a day veterinary antibiotics in the peri-urban smallholder dairy
or two could result in an irreversible loss of customers farms of India.
which would have a significant adverse impact on their
business. In absence of a formal system of incentives or Discussion
disincentives, it was virtually impossible to practise the This qualitative study adds to the growing body of evi-
withholding. Health system level stakeholders also rein- dence related to the issue of antimicrobial consumption.
forced these concerns. According to them, withholding The study explicitly dealt with the non-prescribed and
should be incentivised to prevent milk tainted with anti- self-administered veterinary antibiotic usage in the small-
microbial residues from entering into the food chain. holder dairy farms in peri-urban areas. Through in-depth-
interviews across various stakeholders, this paper attempts
“Who will pay for the milk I throw out?. Each cow gives to elucidate the complexities of antimicrobial usage in the
an average of 10 litres of milk everyday. I have four smallholder dairy farming sector in peri-urban India. Each
milking cows, and if one is on treatment and milking is core theme was further explained under sub themes.
withheld, it translates into a loss of INR 300 minimum.
We need to continuously feed the animal, irrespective of Antibiotic use practices in small holder dairy farms
whether we are selling the milk or not. From where will I In dairy farming, practices, knowledge and beliefs handed
get money for this?” (Dairy farmer, Guwahati) down from one generation to the next [22, 23]. Experi-
enced dairy farmers have traditionally managed animal
“We need to take appropriate measures. How can health issues using ethnoveterinary practices rooted in the
we expect a poor farmer to discard the milk? The use of indigenous medicinal herbs, utilising the Indian
Government should identify certain incentives so Systems of Medicine [24, 25]. The current generation has
that these farmers comply with the policy.” retained the self-reliance to manage livestock diseases on
(Senior official, Guwahati) their own, and supplemented the traditional knowledge
with their understanding of modern medicine. This self-
“Monetary loss for a day is just one way of looking at it. reliance, in combination with market pressures and
What about the customers we lose? Who is going to economic compulsions, has resulted in the widespread
explain to them the reason behind why we are not practice of self-administration of antibiotics in livestock
providing the milk to them?” (Dairy farmer, Bangalore) for therapeutic, prophylactic and metaphylactic purposes,

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 8 of 13

Behavioural belief Subjective belief Perceived control

Limited
Self-treatment Advice from untrained peer group
Community Level knowledge related Presence of depot
using veterinary [Peer learning and self-medication]
Drivers to antibiotics
antibiotics system
among dairy

Lack of correct Limited extension

Informal prescribers
System Level advice [Shortage of services Direct access to drug
or non-availability
Drivers veterinary doctors [IEC related to distributors
of veterinary doctors
and pharmacist] antibiotics]

Market and Policy Absence of regulatory

Direct marketing of veterinary
Drivers framework for veterinary
antibiotics to consumer
antibiotics

Non-prescribed self-drug administration

Irrational Usage of Veterinary Antibiotics

Fig. 1 Behavioural model of drivers and determinants of non-prescribed use of antibiotics in small holder periurban dairy farms. Based on theory
of planned behaviour, a diagrammatic representation of different individual, health system and policy level drivers affecting antimicrobial usage in
small holder dairy farms

thus augmenting the risk of emergence of AMR (Fig. 2).

Along with easy over-the-counter access to antibiotics,
often without any prescriptions, or with invalid prescrip-
tions, or with prescriptions from unlicensed practitioners,
there is a fertile socioeconomic backdrop encouraging ir-
rational use of antibiotics in livestock held by peri-urban
smallholder farmers. Irrational use of antibiotics is further Traditional
fuelled by veterinarians who are more influenced by social practice of
self
expectations than by scientific reasoning, as has been the Peer treatment
case with human antibiotics prescribing practices [26]. learning

Direct
Drivers of antibiotic usage in Peri-urban smallholder dairy availability
of
farms antibiotics
The following key drivers directly influence the irrational
usage of veterinary antibiotics: (a) direct marketing of
veterinary antibiotics to consumer; (b) enabling of infor-
mal prescribers and caregivers to fill the gap created by
inadequate coverage of veterinary services; (c) failure to
regulate informal antibiotic supply chains in the commu-
nity through drug depots and unfettered access to drug Attitude for self-administration of veterinary antibiotics
distributors; and (d) low literacy levels and poor aware- Fig. 2 Attitude for self-administration of veterinary antibiotics.
Diagrammatic presentation of Individual level drivers affecting
ness of antibiotics and the role they play in animal and
antimicrobial usage in small holder dairy farms
human health.

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 9 of 13

a. Direct Marketing of Veterinary Antibiotics to consumer b. Lack of qualified veterinarians and the role of informal
Although direct marketing and selling drugs without pre- caregivers
scriptions is illegal in India, there are several loopholes in Use of veterinary antimicrobials without veterinarian
the existing regulatory provisions which have failed to consultation was reported in past with 87% and 38%
keep up with the changing technological and socioeco- among urban and rural farmers, respectively [32]. How-
nomic milieu [27]. Direct-to-Consumer Pharmaceutical ever, study did not report the drivers responsible for this.
Advertising (DTCPA) is a heavily debated issue which re- In the current study, a universal finding was the scarcity
mains strongly regulated and closely monitored in devel- of trained veterinarians to cater for the animal health
oped countries [28]. In the present study, some interesting needs. There was significant convergence of all stake-
facets with elements of DTCPA emerged as drivers of holders on this matter. This is in concurrence with pre-
antibiotic use in livestock. Several veterinarians, pharma- vious reviews on the veterinary capacity in the nation,
cists, and dairy farmers reported being approached by rep- which clearly demonstrated India’s constrained veterin-
resentatives of pharmaceutical companies advertising their ary service delivery and the need to meet the scarcity
products, some of which were veterinary antibiotics. through a systematic assessment of the human re-
Additionally, several respondents reported receiving free sources, both in terms of the number as well as the
samples of the products. It is likely that bypassing the for- competence of the workforce, followed by the establish-
mal drug value chain (Fig. 3) by using informal channels ment of new veterinary colleges and other institutions to
of drug distribution, geared towards building a user base, bridge the human resources gap [33–35].
further resulted in an irrational drug distribution (Fig. 4), In addition to the perceived shortage of veterinarians,
increased the profit margins for the individual representa- in the present study, informal interactions also revealed
tives who are usually required to meet time-bound that the veterinarians are more interested in private vet-
sales targets [29, 30]. A previous study reported that the erinary practice, which is oriented towards treating pet an-
pharmaceutical companies do not impose the same influ- imals (Mostly, dogs, cats, rabbits and birds.), in contrast to
ence in veterinary practice as in human [31]. However, the government sector facilities which had a stronger
the evidences from the current study strongly suggests focus on livestock. This is likely to be a factor promoting
pharmaceutical companies as potential influencer behind the informal or unauthorized (para-vet/veterinary field as-
non-prescribed use. sistants etc.) prescriber network, which endeavours to

Drug manufacturer

Drug distributor

Veterinary pharmacist

Veterinary
Veterinarian Dairy farmer
consultation

Dairy farm
Fig. 3 A typical formal drug distribution channel. Flow chart represents a formal and rational drug delivery system

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 10 of 13

Drug manufacturer

Drug distributor

Marketing
Demand Veterinary pharmacy Medical of drugs Dairy farmer
representative including
antibiotics

Dairy farmer

Dairy
farm

Fig. 4 Informal channels of introduction of veterinary antibiotic in dairy farms

reach the underserved population. Similar finding was re- informal supply chain through which the dairy farmers
ported in an earlier study conducted among veterinary may access antibiotics and other veterinary drugs. The
doctors in south eastern part of India [31]. Study reported dairy farmers preferred this informal supply chain as
that veterinary doctors perceives that prior prescription by well, since it provides direct access to medications per-
unqualified prescribers was influencing antimicrobial pre- ceived to be effective, without the accompanying costs,
scriptions for animals. Recent study in northern India re- both in terms of money and time, of consulting a veter-
ported low level of knowledge among para-vet about inarian. Similar findings were reported in a study from
antibiotic resistance and its public health impact [36]. The Peru where farmers preferred prescription as well as pur-
use of antibiotics not prescribed by a veterinarian, or the chase of drug from other channels such as direct purchase
use of antibiotics from non-accredited sources was fre- from pharmacies and feed-store vendors [42]. Conse-
quently reported in different parts of the world [37]. How- quently, the farmers often contacted the pharmaceutical
ever, no single study has explained the interplay of representatives directly when they needed to explore op-
different drivers at different levels potentially responsible tions for treating their animals.
for the non-prescribed usage of veterinary antimicrobials. Another phenomenon which raised concerns is the
The shortage of trained and licensed pharmacists was depot system. An elderly or experienced farmer, who often
also identified to be an issue by some state-level stake- happened to be the opinion leader in the community, was
holders. The pharmacist has a vital role to play in limit- approached by the pharmaceutical representatives, and
ing access to antibiotics and providing proper guidance provided sample medications to distribute to neighbour-
to care-seeking farmers. It is essential to incorporate ing farmers. The possibility remained that such informal
them within the ambit of community-based antibiotic routes, in addition to encouraging irrational use, could
stewardship efforts to reduce the unintended conse- also promote multi-drug use or use of supra-therapeutic
quences of overuse and abuse of veterinary antibiotics doses, as the elderly farmers would want to ensure clinical
[38–40]. The absence of adequately trained pharmacists success and consolidate their position in the social hier-
could contribute to the nexus between non-licensed dis- archy. A further consequence of the unregulated access to
tributors and representatives of pharmaceutical compan- the supply chain of veterinary antibiotics is the repeated
ies. According to a report based on a survey conducted use of the same drug for different clinical conditions even
in the WHO European Member States, adequately if the underlying pathophysiology is different and warrants
trained pharmacists can act as gatekeepers to rational a different therapeutic approach.
drug usage interventions and are uniquely positioned
to influence prudent antibiotic consumption [41]. The d. Poor literacy, low level of education and low level of
shortage of such a vital component of the healthcare awareness
delivery system, is, therefore, of special concern. Access to information has been cited to be an important
factor in promoting equity in healthcare [43, 44]. Building
c. Easy access through informal antibiotic supply chains awareness about antibiotics has been identified as one of
The depot system, direct accessibility of community the key strategic objectives espoused by the World Health
opinion leaders to pharmaceutical representatives, and Organization (WHO) in its global action plan to contain
easy access to over-the-counter antibiotics represents an AMR [45]. In the present study, an additional layer of

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 11 of 13

complexity was added to irrational antibiotic use by peri- misuse was further stimulated by the sense of control that
urban smallholder dairy farmers because of the relatively most traditional dairy farmers felt they had on the farming
low levels of literacy and awareness, which has been previ- process (unpublished findings, “Stakeholder mapping and
ously reported by studies conducted in similar settings analysis in peri-urban dairy farms of India”, Manish
[46, 47]. This implies that the farmers might be unable to Kakkar). A typical finding was the creation of a depot
interpret complex medical information even if they have system. This was seen to be a recursive issue, since the
access to it. This assertion receives endorsement from the presence of a depot system encouraged farmers to self-
veterinarian input that farmers are often unable to com- administer antibiotics, and the depots were sustained by
prehend why a drug is inappropriate for a given clinical the continued interest of farmers in having quick access to
scenario, even when symptoms mimic a previous episode medications, by-passing the somewhat onerous conven-
where the same drug was prescribed. tional animal healthcare system. This also created a per-
The veterinarians also admitted that there is a definite verse peer-support group, which functioned to propagate
“pull” from farmers who insist on antibiotics for illnesses the misinformation about antibiotics and their utility, fur-
where they may not be recommended; they preferred a ther ensuring their entrenchment in the community [51].
shorter course of more expensive or newer antibiotics National Livestock Mission (NLM) could be a platform to
over a recommended, longer regimen. Similar findings engage the dairy farm owners to raise awareness related to
were reported in a previous study from New Zealand, prudent use of veterinary antimicrobials [52]. The mission
where 22% of the veterinary doctors admitted that their has national presence and is supported by the central gov-
prescribing decision was influenced by non-clinical rea- ernment. The current objective of the sub-mission in con-
sons such as farmers’ preferences [48]. Similarly, veteri- text to IEC involves increased awareness among all
narians reported ‘external pressures’, such as pressure stakeholders involved in the animal husbandry sector re-
from clients, legislation and public perception, strongly garding scientific methods of rearing, susceptibility to dis-
influence their antimicrobial prescribing behaviour [49]. ease, vaccination, breed improvement, animal nutrition,
Limited or no evidence is available to compare the find- schemes implemented by various agencies and support for
ings in this context from India. Farmers interacted more Livestock Extension at various levels. An evidence-based
often with pharmaceutical representatives or informal intervention package related to knowledge on antibiotics,
practitioners, who are likely to be more amenable to giv- need for using prescribed antibiotics, adherence to pre-
ing in to such demands. This could potentially lead to a scribed therapy and observing withholding period can be
vicarious pressure on veterinarians to prescribe per the incorporated in the revised NLM IEC strategies [52].
farmers’ wishes to retain their patients. Longer duration In addition to the centrally run schemes and missions,
of therapy could result in adverse economic implications there are schemes under the state governments which
for the farmers, hence, when such a course is recom- aim to attract smallholders into the supply cycle to pro-
mended at government hospitals or licensed veterinar- vide increased returns for their produce, thus stimulat-
ians, they risk losing their credibility with the farmers ing production and encouraging the uptake of improved
unless the farmers are adequately informed and coun- technologies. Inclusion of rational use of veterinary anti-
selled. These perverse financial forces could distort pre- biotics as an objective under the awareness programme
scription practices even in the formal clinical systems, might result in changing the risk practices of dairy farmers
resulting in inappropriate use or overuse of antibiotics. with respect to veterinary antimicrobial consumption [53].
Though there is limited evidence related to the market Similarly, other programmes like the National Programme
pressures on smallholder dairy farmers contributing to for Bovine Breeding and Dairy Development (NPBBD),
compulsion to milking and overlooking the issue of which was initiated in February 2014, could be used
withholding, the current study indicates that in the ab- as a platform to raise awareness related to veterinary
sence of quality-based incentives, farmers have no motiv- antimicrobial use among smallholder dairy farmers, as
ation to withhold milking cattle undergoing antimicrobial well as strengthening the laboratory screening facility
chemotherapy. Nearly all farmers reported a very small of residues in [54].
profit margin and the compulsion of milking to ensure
solvency. There is a small, but growing body of published Limitations of the study
evidence, advocating for incentives to ensure milk quality. A very small number of state-level civic officials were in-
These incentives should be deployed in addition to IEC volved in this study. Notwithstanding this, the limited
activities focussing on the improvement of mammary number provided rich and meaningful data as the re-
health, milk hygiene and safety was envisaged [50]. spondents who participated had decades of experience
The lack of outreach activities, targeting the information in animal husbandry and veterinary medicine. IDI with
needs of the community further deepened the crisis of dairy farmers were performed in the local languages
misinformation in the farmers. This pattern of antibiotic and then translated into English. Despite the rigorous

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Chauhan et al. Antimicrobial Resistance and Infection Control (2018) 7:60 Page 12 of 13

verification process, some subtle nuances might have specific regulatory permissions from their colleges required for the conduct
been missed during the verbatim transcribing. of the study in their site.

Competing interests
Conclusion The authors declare that they have no competing interests.
The current study identifies several factors which come
together to determine the use of antibiotics in the small-
holding dairy farms located in peri-urban fringes of Indian Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
cities. The qualitative nature of the enquiry provides us published maps and institutional affiliations.
with unique insights which are difficult to identify using
the traditional quantitative surveillance approaches. In this Author details
1
Public Health Foundation of India, Plot 47, Sector 44, Gurgaon, Haryana
study we explore the social biography of antibiotics, as 122002, India. 2Department of Public Health Sciences, Faculty of Medicine,
they find their way through formal and informal routes, University of Liège - Hospital District, Hippocrates Avenue 13 - Building
into the peri-urban smallholder dairy farms, often in 234000, Liège, Belgium. 3Indian Institute of Public Health, Gurgaon, Haryana
122002, India. 4Centre for Research and Action in Public Health (CeRAPH),
the form of irrational, non-therapeutic, sub- or supra- University of Canberra, Building 22, Floor B, University Drive, Bruce ACT 2617,
therapeutic usage. Australia. 5Indian Council of Medical Research, Division of Epidemiology,
The study concludes that in the presence of weak vet- National Institute of Cholera and Enteric Diseases, Kolkata 700010, India.
6
International Livestock Research Institute, Nairobi 30709-00100, Kenya.
erinary care infrastructures with limited outreach activ- 7
Zoonosis Science Laboratory, Uppsala University, Po Box 582, Uppsala
ities, severe human resource limitations, poor legislative SE-751 23, Sweden. 8Department of Clinical Sciences, Swedish University of
and regulatory oversight, and limited knowledge and Agricultural Sciences, PO Box 7054, Uppsala SE-750 07, Sweden.
awareness of the role of antibiotics in consumers, it would Received: 4 January 2018 Accepted: 24 April 2018
be difficult to combat the issue of emergent antibiotic re-
sistance. Interventions such as community awareness pro-
grammes related to veterinary antibiotics, establishing an References
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