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Antimicrobial Resistance: from Emerging Threat to Reality Eds: Rubina Lawrence, Anil K.

gulati, Gerard Abraham © 2009 Narosa Publishing House Pvt. Ltd.

Rural India perceives that use of antibiotics in farm animals must be influencing antibiotic resistance development in humans: Do the regulators think so?
A.J. Tamhankar1, S.S. Nerkar2, A.P. Patwardhan3 and C. Stalsby Lundborg4
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National Coordinator, Indian Initiative for management of Antibiotic Resistance (IIMAR) http://save-antibiotics.blogspot.com 2 Namdeo Umaji Agritech Pvt Ltd., Pune India 3 Conservation Action Trust, Teen hath naka, Thane, India 4 Division of International Health (IHCAR), Karolinska Institutet, Stockholm, Sweden. e-mail: ejetee@gmail.com

Most of the antibiotics produced globally are put to non-human use and a very large quantity of this is used to cure diseases of farm animals. This leads to the development of focal points of resistance in non-humans that can get transferred to humans, potentially a disastrous situation. WHO has repeatedly warned on this issue, but awareness and actions in this regard are still lacking in India amongst the highly placed stakeholders. What is the situation at the lower rung stakeholders in villages? We investigated on the knowledge and perception of farmers and drug providers in rural India about antibiotic use in animals and its importance in development of bacterial resistance to antibacterials in humans by conducting interviews in Maharashtra, Gujarat and Madhya Pradesh and analyzing interview transcripts using qualitative content analysis. All interviewees including farmers considered that antibiotics should be used only for curing diseases and not for growth promotion in animals. Most recognized that as some pathogens could be common between animals and humans and as same antibiotics are used in humans and animals, animal use might influence resistance development in humans. An urgent need was expressed by rural drug providers and farmers for campaigns on rational use of antibiotics. Thus, Stakeholders in rural India were aware about the antibiotic use related resistance development in bacteria and its transfer from animals to humans. Do the Indian laws and rules governing antibiotic use practices indicate that the regulators know this? And if so, are they acting on this?

Keywords: Public health, Zoonoses, Rural India; Antibiotic resistance, Dairy cattle; Poultry Half of the antibiotics produced globally are put to non-human use and a very large quantity of this is used for therapy, prophylaxis and growth-promotion in farm animals (WHO, 2002). Such large use can lead to the development and spread of resistance in bacteria infecting farm animals, which is transmissible further to those infecting humans (Simago and Rukure 1991, Kolawole and Shittu 1997, WHO 2001, Lu

et al. 2002, Angulo et al. 2004; Molbank 2004). Antibacterial resistance in pathogenic bacteria is a matter of global public health concern as it leads to increased deaths, prolonged treatments and economic losses (WHO 2001; Melander et al. 2002, Wilton et al. 2002; Coast and Smith 2003; WHO 2004; WHO 2007a). The issue has repeatedly been put on the global policy agenda calling for concerted actions emphasizing its implications (WHO 2001; WHO 2005; WHO 2007a; WHO 2007b), but apparently not much action is evident in India and /or proper implementation of regulations is lacking.

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Up to 70% of the Indian population is dependent on agriculture and agriculture related professions (O‘Brien 2005) like dairy, poultry farming, aquaculture, sheep growing etc., which exist both in organized and unorganized sector. Amongst these activities, unorganized cattle and poultry growing and semi-organized small-scale franchisee/contractual poultry farming is common and widely dispersed in rural parts of India. Studies in India show high levels of antibacterial resistance in bacterial samples from milk, cow stool, beef as well as poultry (Khan et al. 2002; Dutta et al. 2003; Saxena et al. 2005) and also humans (Verma et al. 2000; Jain et al. 2005, Raghunath 2008). In tropical climate the impact of such resistant organisms could be highly significant in spread of diseases and also of antibiotic resistance (Petersen et al. 2002), which could be a ´Hidden problem waiting to explode`. Importance of spread of resistant bacteria from farm animals to humans has been amply demonstrated in earlier studies (van Loo et al 2007, Walther et al 2008). In India as a large population lives in close contact with animals including poultry (Chugh 2008), the problem of zoonotic transmission can assume dangerous magnitude, particularly among the widely distributed subsistence level cattle and poultry farmers. In the absence of proper interventions, the animals from this sector may act as an uncontrolled repository of antibiotic resistant bacteria and/or antibiotic residues. To target this sector, generation of information on perceptions about antibiotic use and about antibacterial resistance amongst cattle and poultry farmers and their drug providers is highly relevant, as this would provide necessary information for the development of policies and proper. This paper attempts to do this by analyzing the contents of qualitative interviews conducted in rural India amongst cattle and poultry farmers, drug retailers and veterinarians. MATERIALS AND METHODS Study setting The study was conducted mainly in the state of Maharashtra in India, in two pockets separated by about 100 km. To include further wider variation in views, supplementary interviews were also conducted in two adjoining states-Gujarat and Madhya Pradesh. Substantial cattle and poultry growing exists in unorganized sector in the study area. The cattle farmers in the selected area have breeds like Jersey, Holstein-Friesian and their hybrids, which give higher milk yield than indigenous breeds. The farmers thus generate a level of income with which they generally can afford medical care including the use of antibiotics for their animals. In case of poultry, franchisee/contractual farms maintaining birds for both eggs and chicken purpose are common. Besides, typically most cattle farmers have small number of birds for home consumption and/or as home industry. The study area has two types of veterinary practitioners – diploma holders, who have a shorter training (2 years) in veterinary medicine and degree holders, who have a normal (4years) training leading to university degree. Most of the villages in which we took interviews, had a drug retailer also. Interview guide An interview guide with open-ended questions was developed which included questions on (i) Use of antibiotics, (ii) Commonality of antibiotic use and of pathogens amongst humans, cattle and poultry, (iii) Awareness about the phenomenon of resistance development, (iv) Potential importance of use of antibiotics in animals for resistance development among human pathogens, (v) Use of non-antibiotic prophylactic measures, (vi) Rational use of antibiotics and (vii) Interaction with clients (only for providers). After some pre-test interviews three slightly different interview-guides were prepared for the three types of interviewees i.e. cattle and poultry farmers, veterinary practitioners and drug retailers.

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Participants and data generation The individuals from the various stakeholder groups were selected purposively with various backgrounds so as to obtain a wide variation in views (Table 1). A higher number of cattle farmers were included as cattle farmers are more common. Most cattle farmers also had a few birds for home consumption. Interviews were conducted in the preferred language of the interviewee - in Marathi, Gujarati or Hindi. Before the interview, the purpose of the interview was explained to the interviewees and written consent was taken. The interviews were conducted in a place selected by the interviewee. Careful notes were taken during the interviews and expanded afterwards. Additional comments if any were also received in writing. No voice recordings were done, as it was not found acceptable to the interviewees. The interviews lasted 30-60 minutes. About 70 % of the initially approached persons agreed to be interviewed. Data analysis The interview-notes were translated into English and transcribed, whereafter the researchers verified that the contents of the English transcript conveyed the real meaning of the interviewee‘s statements. The English transcripts alongside the original notes were analyzed using qualitative content analysis. Emerging views regarding the areas in the interview guide were focussed (Graneheim and Lundman 2004; Hsieh and Shannon 2005). Two of the authors (AJT and CSL) independently read the transcripts and noted meaningful statements/quotes. These were discussed among the authors and the items were sorted into areas and sub-areas from the interview guide. RESULTS The results are presented as descriptions of issues emerging from the transcripts as related to the interview-guide areas. To bring authenticity to the presentation many quotations are included. Information added by the authors is marked in square brackets. Use of antibiotics Most farmers were aware that antibiotics are used when their animals suffer from disease and could mention at least one name from among the commonly used antibiotics (e.g. tetracycline, ampicillin, penicillin and gentamycin). The veterinarians and drug retailers reported tetracycline to be the most commonly prescribed antibiotic followed by ampicillin. One veterinarian felt that,

“There are too many antibiotics in the market now, if the numbers are reduced, the use will also get reduced”. (I-17=Interviewee17)
Most farmers were aware of the use of antibiotics as growth promoters, especially the poultry persons, but did not report such use by themselves and considered it improper.

―Such `aushadh` (antibiotic) [for growth promotion], could remain in chicken meat ate by humans, why should it be given in feed to `nirogi` [healthy] animal, it is unnecessary. `aushadh` [medicine/antibiotic] should be given as disease cure not otherwise‖. (I-12)
However it was also mentioned that

―if the veterinarian advises such use [for growth promotion], it is proper use‖. (I-8) 3

Tamhankar et al. Use of Antibiotics in Farm Animals Table 1. Information on interviewed farmers, veterinarians and drug- retailers
S. No. Type of Interviewee Education If farmer, type of animals If Vet., treated animals Land holding Remarks

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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

Farmer Farmer Farmer Farmer Farmer Farmer Farmer Farmer Farmer Farmer Poultry farm Supervisor Poultry farmer Poultry farmer Veterinarian Veterinarian Veterinarian Veterinarian Veterinarian Veterinarian

B. Com. 7 years H.S.C. 10 years H.S.C. B.A. 6 years B.Sc. B.A. H.S.C. Dip. A. H. & D.M. M.A. H.S.C. Dip. A.H.& D.M. Dip. A.H.& D.M. B. V. Sc. & A. H. B. V. Sc. & A. H. B. V. Sc. M. V. Sc., Ph.D.

3 cows, 5 chickens, 3 goats 5 cows, 4 chickens 4 cows, 5 chickens 4 cows 5 cows, 10 chickens 4 cows 4 cows, 2 buffalos, 4 chickens 3 cows 6 cows 3 cows ~ 12,000 birds ~ 2500 birds, 3 cows ~ 2500 birds Cattle, goats Cattle, goats Cattle Cattle, goats, poultry Cattle, goats, dogs Cattle, goats

4 acres 8 acres 15 acres 6 acres 10 acres 17 acres 5 acres 8 acres 15 acres 5 acres NIL 9 acres 4 acres NIL NIL NIL NIL NIL NIL

Former village head

Franchisee poultry farm (Egg purpose) Contractual poultry farmer (Meat Purpose) Contractual poultry farmer (Meat Purpose) Dispensary Dispensary Dispensary Dispensary Dispensary Private consultant, Former Dean-Faculty of Vet. Science, Agricultural University Shop providing both human and veterinary drugs Shop providing both human and veterinary drugs Shop providing both human and veterinary drugs

20 21 22

Medical store Professional Medical store Professional Medical store Professional

Dip. Pharm. Dip. Pharm. Dip. Pharm.

NIL NIL NIL

NIL NIL NIL

Note- # Years=No. of years in school; H.S.C.=12 year schooling; B.A.=Bachelor of Arts; M.A.=Master of Arts; B. Com.=Bachelor of commerce; B.Sc.=Bachelor of science; Dip.Pharm.=Diploma in Pharmacy; Dip.A.H.& D.M.=Diploma in Animal Husbandry & Dairy Management; B.V.Sc.& A.H.=Bachelor of Veterinary Science & Animal Husbandry; M.V.Sc.=Master of Veterinary Science. (Diploma/Degree vet. =2/4 years after H.S.C.

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―`Aushad` could be used for prevention of disease, if it helps animal remain `nirogi´ ‖. (I-11)
Though not the diploma holders, the degree holders said they never prescribed growth promoters. Instead they prescribed calcium, iron, phosphorous, B complex, liver tonic and Aurvedic (Indian medicine system) supplements. The retailers did not offer any specific views on growth promoters. Use of antibiotics in animals and resistance development among pathogens infecting humans All the interviewees recognized that the same antibiotics were used in both humans and animals, but in different doses.

―Man is also animal, antibiotics used in all animals must be same‖ (I-08)
Most farmers and drug retailers thought that some pathogens might be common between animals and humans and few cited examples of dysentery and diarrhea. While the diploma holders could not mention any, the degree-holder veterinarians gave the names of various common bacteria as Salmonella, Clostridium, Staphylococcus, Streptococcus, Pseudomonas, E.coli, Shigella, tuberculosis. All interviewees were aware of the concept of resistance. A representative summing up from among the responses of the farmers was,

“If you are using same `aushadh` continuously then slowly, slowly it may become ineffective.” (I-12)
Almost all farmers believed that antibiotic resistance developed in pathogens in animals could influence resistance development in pathogens infecting humans. Most thought that this would happen through ingestion of farm products. One comment, repeated in various words was

“Yes, it may be happening, as many a times, humans are not getting cured easily by antibiotics, antibiotic use in animals might be responsible.” (I-08)
In general the farmers felt that something is wrong if the cows do not recover quickly from disease even after using antibiotics. However, for resistance one cattle farmer said that “When such a small quantity of medicine is taken where is the question of development of

resistance in such a huge animal body and such a small amount is given” (I-10)
Regarding the issue, ‗whether it matters for transfer of resistance if the same antibiotics are given to humans and animals‘, One cattle farmer said,

“How or why should it matter? Whatever happens in humans will happen to animals, similar body and diseases, same antibiotics and resistance.” (I-03)
Some farmers considered that if antibiotics were used even for prophylaxis or for growth promotion, development of resistance could take place. Among the veterinarians, the diploma holders could not say anything about use of antibiotics as growth promoters and its role in development of resistance, while

the degree holders varied in opinion from ―Definitely yes‖ to ―No comments‖ to ―A possibility can not be ruled out‖. All the veterinarians considered that resistance could be transferred from animals to humans.

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“Research is needed to carefully study and confirm the transfer of resistance from animals to humans. It is also important to analyze antibiotic contamination in animal products before use by humans”. (I-16) The veterinary educationist among the veterinarians felt that, “Use of tetracycline on farms is pushing the evolution of resistant genes. Once the resistant genes make their way into drinking water they will go to guts of peoples, animals and wildlife and will pass genes cycle continuously in the environment and transfer resistance to human beings”. (I-19) The retailers were aware of the concept of resistance to antibiotics, but their views varied. One line of thinking was that as the same antibiotics are used in animals as in humans resistance may develop, while on the other hand antibiotic consumption was considered less in animals which was expected to give less resistance. Several farmers made the analogy between resistance development in bacteria to antibiotics with the development of resistance to pesticides among crop infecting pests, which is a well-known issue to Indian farmers. Rationality in antibiotic use and prevention of disease and resistance All but one farmer said that they always listened to veterinarian‘s advice regarding antibiotic use and most veterinarians agreed. One however added that “Only under outbreak conditions the advice is totally followed, otherwise at times the farmer’s response is lukewarm”. (I-14) The prescribers were asked whether they explained to the client‘s the adverse effects of over or under use of antibiotics. Among diploma holders one comment was “Under use does not result in any adverse effect”. (I-15) The degree holders said that they explained to the farmers that overuse may lead to resistance or complications in other systems of animals and opined that the possibility of resistance development due to inappropriate use of antibiotics couldn‘t be ruled out. The cattle farmers saw vaccination as a major prevention for infection resulting in reduced need for the use of antibiotics. A franchisee poultry farmer said that the company provides them with healthy chickens, thus diseases are uncommon. Also, between two broods, the shade is kept empty for two months, further minimizing spread of disease and vaccination is done whenever required. The poultry farmers were not sure whether the feed formula supplied by the company contained antibiotics or not. Regarding non-pharmacological prevention, all veterinarians reported often giving such advice. They advised vitamin supplements for improving immunity in cattle and also segregation of sick animals, killing of birds and antiseptic sprays. “It is important to develop vaccines to avoid antibiotic use.” (I-17) All veterinarians informed that clients generally agreed and followed the advice on primary nonantibiotic preventive measures but reported that, `when an animal is sick, farmers insisted on fast recovery by use of antibiotics as production was at stake (for cattle) and it appeared they also felt it justified.‘ 6

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The farmers considered that a campaign on proper use of antibiotics was needed for veterinarians as they give the medical advice, however, the veterinarians thought that a campaign is needed for farmers as they insist on quick relief for their animals and so they have to prescribe antibiotics. The veterinarians also said that a general campaign was needed for all concerned regarding proper use of antibiotics. A retailer summed up the typical situation of antibiotic use in the animal sector as, “There is incorrect use of antibiotics in the animal sector but incorrect use is a bigger problem in human than in veterinary medicine, so a general campaign is needed.” (I-21)

DISCUSSION
There is an important bi-directional link between agriculture including farm animals and health, and failing to think systematically about this link may undermine the efforts to address diseases of public health importance (Hawkes and Ruel 2006; Hawkes, Ruel and Babu, 2007). India is one of the largest producers of milk and poultry, where `production is by masses and not by mass-production` and because of this feature, it offers an unusual opportunity to study such perceptions in this sector. Even the less educated farmers in this study were generally aware of the names of common antibiotics. This may be due to the commonality of antibiotics in the human and veterinary medicine. Another contributory factor could be the availability of both animal and human medicines from the same shop/pharmacy. Poultry farmers mentioned antibiotic use as prophylaxis but denied their use as growth promoters. The farmers and the diploma holders felt that there must be commonality of pathogens between humans and animals but they could not mention the name of any organism. This is understandable as diploma holders only practice empirical therapy, and refer complicated cases to degree holders. Importantly, most farmers and prescribers were aware about the possibility of development of resistance to antibiotics, and many also thought that resistance could be transferred from bacteria infecting animals to bacteria infecting humans. All appreciated the importance of non-antibiotic preventive measures. In general, the need for an intervention to educate all concerned was felt by all interviewees. Non pharmacological preventive measures, especially keeping of good hygiene is acknowledged as highly important in human medicine as well as in veterinary medicine (WHO 2001). Because of the scare of `bird-flu`, poultry farmers are cautious about maintaining good hygiene and observing health of birds. As for cattle, we observed that they are mostly kept in shades that allow free circulation of air and the shades are usually washed regularly. An interesting observation in this study was that initially farmers claimed that their animals were mostly healthy and do not fall ill, so the need of any medicine does not arise, but after a little discussion further on, all acknowledged intermittent use of antibiotics. An important non-finding was that despite common use of `non-prescribed antibiotics‘ amongst humans in India (Kamat and Nichter 1998), this was not mentioned as a major problem in the non-human sector by any of our interviewees. Estimates from USA in 2001, indicate a yearly non-therapeutic use of antibiotics of 12,00070,000 tons in animal husbandry (cited in Okeke et al. 2005), which has an impact on development of resistance and antibiotic residues may also be found in food products (Muriuke et al. 2001; Dipeolu and Alonge 2002 Dutta et al. 2003). Growth promoter`s impact on 7

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resistance development has been acknowledged by many countries. They were banned in Sweden in 1986; the European Union banned all antimicrobial animal growth promoters, which are also used in human medicine in 1997. Denmark followed in 1999, which resulted in reduction of >60% of antimicrobial use in livestock without significant negative impact on animal health, food safety or economic aspects (WHO 2002). In our study, interviewees generally denied or did not agree with such use. If this is true, this is the appropriate time to develop and implement policies regarding avoiding the use of antibiotics as growth promoters in India. Farmers term antibiotics as ‗aushadh‘ (literally meaning medicine) that cures diseases. They don‘t know whether it is used against bacteria or virus, a perception also commonly observed in human use. Farmers use `aushadh or dawa` (medicine) as a very broad term. They refer to even insecticides as `aushadh or dawa` (probably because it improves crop health), indicating that in any campaign on rational use of antibiotics, the concepts `medicines` and `antibiotics` are difficult to use in information material without explaining their meaning. There appeared a surprisingly high awareness of the concept of resistance among the Indian farmers. In India, farmers have suffered heavy losses due to resistance towards insecticides by the pests of the cash generating crop cotton and so there is a great awareness amongst farmers that organisms can develop resistance to the control agents used against them. Therefore, when promoting rational use of antibiotics, an appropriate intervention could be to bring to their notice the parallel between the insecticide resistance and the antibiotic resistance problem and how it will be economically beneficial to the cattle and poultry farmers, if the use of the relatively cheap first line antibiotics gets extended for a longer period of time by rationally using antibiotics. Interventions like small group discussion have been effective in other contexts (Santoso et al. 1996). This may be possible in Maharashtra, where this study was mainly conducted, as the state has a well-organized animal husbandry department at the government level (Department of animal husbandry, Maharashtra state, 2008) and also a network of cooperatives and private companies in the dairy and poultry sector. Despite the WHO acknowledging non-human use of antibiotics as an important area, particularly in the animal/agricultural sector (WHO 2001; WHO 2002), little attention has been paid to the antibiotic use by farmers. Farmers such as in our study in India individually possess comparatively few animals. However, such farmers exist in very large numbers in the poor and middle-income countries. Collectively, their animals may be consuming very large quantities of antibiotics and may thus constitute a significant component of the non-human use. This antibiotic use has potential to create resistant bacteria in the animals, which after excretion from the animals or through animal products can spread in the environment. Such resistant bacteria may also transfer genetic material to other bacteria, which may ultimately adversely affect the possibility to treat diseases in humans (Angulo et al. 2004; Molbak 2004). Therefore, we cannot ignore the importance of antibiotic use in this sector, from a public health perspective (WHO 2001; Molbak 2004; Okeke et al. 2005, Chugh 2008). It is interesting to note that views both on antibiotic use and resistance revealed in our study were relatively similar to the study conducted in South Carolina in US (Friedman et al 2007). For obtaining appropriate and prudent antibiotic use a number of countries have evolved national programmes (Carbon et al 2002) for Surveillance of antibiotic use and resistance rates, optimizing antibiotic use with treatment guidelines, education of professionals and the public, 8

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Does India have any or all of these? Are they sufficient and is the compliance checked? In both human and veterinary, generally, there is little control on the use of antibiotics, which is compounded by over-the-counter availability of the same. There is no initiative for regulation or enforcement of infection control in both human and non-human situations resulting in transmission and acquisition of antibiotic resistance across the board. There is no Central Monitoring Agency at the national level, probably except for M.tuberculosis and Leishmania donovani.. and in animal sector for situations like bird flue etc. The threat of international ramifications in case of bird flu and has forced the regulators to take some action. There is no proper control/ban over the use of growth promoters for animals as in Europe (WHO,2002). There is no control /ban for using the same antibiotics for humans and non-humans. The result of all these is that the poorer communities are squeezed between rampant resistance and inadequate resources. At world level (World Health Organization 2002) strategic plans have been prepared, to educate public and professional towards rational use of antimicrobials, to Coordinate surveillance of antibiotic resistance and antibiotic use in human and animal health sectors, to regulate antibiotic registration for use in both sectors, to promote and evaluate medical and veterinary guidelines, to restrict antibiotic use as growth promoters in animals. In India, at public level, a movement has been launched – the ‗Indian Initiative for management of Antibiotic Resistance (IIMAR)‘ (http://save-antibiotics.blogspot.com) to create awareness on this issue. India needs to initiate efforts at both government and non-government level to tackle the problem of antimicrobial resistance seriously; otherwise we may have a disaster in waiting.

ACKNOWLEDGEMENT This study was conducted within the project ‗Non-human use of antibiotics‘, for which Government of India granted permission to AJT. Sida/SAREC, Sweden and Swedish Research Council through Asia-Link funded the project. Amol P. Patawardhan provided preliminary inputs during the planning of this project. REFERENCES Angulo FJ, Nargund VN, Chiller TC. 2004. Evidence of an association between use of antimicrobial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance. Journal of Veterinary Medicine, series B 51: 374-9. Coast J and Smith R. 2003. Antimicrobial resistance: cost and containment. Expert Review Anti-infective Therapy 1: 241-51. Department of animal husbandry, Maharashtra State. http://mahavet.mah.nic.in/setup.htm (accessed July 28, 2008). Dipeolu M, Alonge D. 2002. Residues of streptomycin antibiotic in meat sold for human consumption in some states of Nigeria. Archivos de Zootecnia 51: 477-80.

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This paper may be cited as -

A.J. Tamhankar, S.S. Nerkar, A.P. Patwardhan and C. Stalsby Lundborg (2009) Rural India perceives that use of antibiotics in farm animals must be influencing antibiotic resistance development in humans: Do the regulators think so? In ‗Antimicrobial Resistance: from Emerging Threat to Reality‘ (Eds: Rubina Lawrence, Anil K. gulati, Gerard Abraham) Narosa Publishing House Pvt. Ltd.; New Delhi.

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