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The first investigation on the use of antibiotics in pig and poultry production in the Red River Delta of Vietnam

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https://www.eduzhai.net Food and Public Health 2013, 3(5): 247-256 DOI: 10.5923/j.fph.20130305.03 First Survey on the Use of Antibiotics in Pig and Poultry Production in the Red River Delta Region of Vietnam Dang Pham Kim1,2,*, Claude Saegerman3, Caroline Douny2, Ton Vu Dinh4, Bo Ha Xuan5, Binh Dang Vu5, Ngan Pham Hong6, Marie-Louise Scippo2 1Central Laboratory, Faculty of Animal Science & Aquaculture, Hanoi University of Agriculture, Vietnam 2Department of Food Sciences, Laboratory of Food Analysis, Faculty of Veterinary M edicine, CART (Centre of Analytical Research and Technology), University of Liège, Belgium 3Department of infectious and parasitic diseases, Research unit of Epidemiology and risk analysis applied to veterinary sciences (UREAR), Faculty of Veterinary M edicine, University of Liège, Belgium 4Center for Interdisciplinary Research on Rural Development, Hanoi University of Agriculture, Vietnam 5Department of Animal genetics and breeding, Faculty of Animal Science & Aquaculture, Hanoi University of Agriculture, Vietnam 6Department of Veterinary Public Health, Faculty of Veterinary M edicine, Hanoi University of Agriculture, Vietnam Abstract In Vietnam where epidemics occur regularly in an imal production, the farmers consider antibiotics as one of the solutions to fight against livestock diseases, thus the risk of abuse, even illegal use of antibiotics in livestock is very high. However, this is a recent issue and has not yet been thoroughly investigated. A cross-sectional study on the use of antibiotics in pig and poultry production as well as the fa rmer’s knowledge on the danger of the antibiotic use in three diffe rent anima l production systems (farm household, semi-industrial and industrial) was conducted from July 2009 to March 2010 on 270 entities, in 3 representative localities of the Red River Delta (RRD). The results showed that a large volu me of antibiotics was used arbitrary in all animal production systems. Animals were not only treated for acute diseases, but also for disease prevention, and for growth promotion. At least 45 antibiotics of more than 10 classes were used. Fifteen antibiotics were used in pig and poultry feed. For d iseases treatment and prevention, antibiotics were used abusively and even illegally (e.g. chloramphenicol) by both farmers and veterinarians. The findings of this survey will permit developing new strategies for prudent use of antibiotics in livestock in Vietnam. These results will help not only to strengthen issues such as veterinary networks; antibiotics use guidance, residues monitoring systems and food safety, but also to improve awareness and ethics of producers and veterinary drug sellers. Keywords Antibiotics, Animal Production, Veterinary Drugs, Red River Delta, Vietnam 1. Introduction In Viet n am, a co un t ry wit h mo re th an 85 mil lio n inhabitants and a very high population density, especially in the Red River Delta (RRD), urb an izat ion and industrializa tion increase rapidly. The demands of foodstuff fro m animal origin for do mestic markets are more and more gro wing. The ann ual av erage co nsu mp t ion o f an imal p ro du cts p er Vietnamese capita in 2009 is 35 kg of carcass meat; 3 kg of milk and 80 eggs[1]. The development objective by 2020 is 56 kg of carcass meat , over 10 kg of milk and over 140 eggs [2]. As a cons equ en ce, t he increase o f int ens ive livestock husbandry models is an indispensable trend in the Vietnamese context. However, because of the low level of hygiene in livestock husbandry, the inadequacy of husbandry zo ne p lann ing and th e lack o f stat e man agement and * Corresponding author: pkdang2000@yahoo.com (Dang Pham Kim) Published online at http://journal.sapub.org/fph Copyright © 2013 Scientific & Academic Publishing. All Rights Reserved development strategies, it results in some new problems such as environmental pollution, as well as frequently occurring and uncontrolled epidemic diseases [2-4]. In 2003, during the avian influen za crisis, about 44 million poultry have either died because of the disease or have been slaughtered because of the crisis. The Po rcine Reproductive and Respiratory Syndro me (PRRS), and the Foot-and-Mouth disease have also been a constant threat causing regular outbreaks in recent years[5]. In 2006, an epidemiological analysis about swine diseases in Northern Vietnam based on 4000 declarations highlighted a high incidence of porcine respiratory disease (50% o f total reported cases). The proportion of digestive tract infections in piglets and reproductive disorders in newly raised e xotic sows were 30% and 10% of total reported cases, respectively [6]. Facing this situation, producers consider antibiotics, used for d isease prevention and therapeutic purposes, as one of the solutions to fight diseases in livestock. In fact, antibiotics are the most common registered drugs (70% of all veterinary drugs) used in an imals in Vietnam[7]. However, the knowledge of famers is still very restricted while the state 248 Dang Pham Kim et al.: First Survey on the Use of Antibiotics in Pig and Poultry Production in the Red River Delta Region of Vietnam inspection and management haven’t met practical demands yet[8]. The use of antibiotics in animal production by farmers in a casual, un methodical manner, without any veterinary prescription and supervision, may lead to the presence of residues in animal p roducts and to antimicrobial resistance[9-11]. These residues cause a danger for public health[12], and bad influences on environment and animal therapeutic sciences. A high proportion of the antibiotics used in an imal production is excreted in urine or faeces and are found in manure[13]. When manure is applied on lands, these antibiotics can enter surface and/or groundwater and potentially alter the environ ment microbial ecosystem [14-16]. It could also contribute to the presence of antibioticresistant zoonotic agents and bacteria in the food chain [17-22]. The situation in Vietnam is amp lified by the integrated agriculture-aquaculture (IAA) farming system encouraged by the government, wh ich often involves an aquaculture system that is sustained through human and livestock waste. This creates an environment that greatly increases the ease through which antibiotic resistance genes can be spread[23]. These antibiotic resistance genes can be easily transferred to both human and animal pathogens, creating a severe health risk by g reatly limiting the antibiotics that can be used to treat infectious diseases[24]. In recent years, Vietnam had many alerts about veterinary drug residues in general and antibiotics in particular. These alerts have caused warnings to authorities and alarmed consumers. Therefore, this problem has been discussed on several occasions in meetings of the Vietnam Nat ional Assembly[25-27]. However, until now, there is no systematic monitoring neither is there any regulation and control strategy on antibiotic use in food animals, and litt le informat ion is availab le on antibiotic use. For the reasons above, as well as to contribute to a long-term strategy of the Vietnamese Govern ment on food safety, the collection of detailed information about antibiotics used in animal production is necessary. The aim of this study was to provide informat ion on the use of antibiotics in different pig and poultry production systems in the RRD of Vietnam. Th is info rmation can assist new strategies in the control of antibiotic use in pig and poultry production in Vietnam. 2. Experimental A cross-sectional study of antibiotic use in pig and poultry production as well as farmer’s knowledge about food safety related to the use of veterinary drugs in the region of the RRD was designed and conducted from Ju ly 2009 to March 2010, on 270 entit ies representing 3 different systems of livestock husbandry: farm household, semiindustrial and industrial, in 3 representative localities of the RRD (Hai Duong, Thai Binh and Ha Noi) (Fig. 1)(Table 1). Table 1. Estimation of the total number of pig and poultry production systems in the RRD System of animal production Animal species Industrial P ig Chicken Semi-industrial P ig Chicken Farm household (*) Pig, chicken Total (by localities) (*): only households who have both the pig and chicken Ha Noi 10 10 10 10 50 90 Provinces Hai Duong 10 10 10 10 50 90 Thai Binh 10 10 10 10 50 90 Total (by production system) 30 30 30 30 150 270 Figure 1. Map of Red River Delta region indicating the three representative localities where the samples were collected (Hai Duong, Thai Binh and Ha Noi) Food and Public Health 2013, 3(5): 247-256 249 2.1. Sampling Area The Red River Delta reg ion is a flat plain formed by the Red River and its distributaries join ing in the Thai Binh River in Northern Vietnam. It is an agricu lturally rich area and densely populated (1225 persons/km2, 4.8 t imes higher than the average population density of Vietnam). It includes the capital, Hanoi, and 10 others surrounding provinces (Fig. 1). The pig and poultry production of this region are the most developed of Vietnam (about 50% o f the whole country production) with 7.0 million pigs, 66.5 million poultry in 2008[28]. Three representative provinces were selected not only for their production capacity but also representative of their geographic location and population density: Hanoi (3344 km2), Hai Duong (1661 km2) and Thai Binh (1542 km2). The population density of Hanoi, Hai Duong and Thai Binh are 1943; 1030 and 1155 persons/km2, respectively. The population of pig and poultry is the largest in Hanoi (1.2 106 pigs and 15.7 106 poultry), followed by Hai Duong (0.6 106 pigs and 6.9 106 poultry) and Thai Binh (1.0 106 pig and 7.9 106 poultry)[28]. 2.2. Sampling Method In each province, on the basis of the list provided by the local agricu ltural office (for industrial and semi-industrial systems), as well as fro m the lists provided by local veterinarians, 50 farm households who have both pig and poultry, 20 semi-industrial farms (10 for pig and 10 for poultry) and 20 industrial farms (10 for pig and 10 for poultry) were selected by random samp ling for the survey. Official local agricultural criteria were used to classify the different farming systems. Farm household systemdisplays a small number of animals, primarily fo r ho me consumption or local markets or ceremonial use. Livestock is raised in the garden, near the house of the farmer, and are fed with available vegetables, product and by-products of agriculture, or leftovers of the family kitchen (there is no supplementary feeding). Semi-industrial systems are farms with at least 50 pigs or 10 sows for the pig and 200 animals for the poultry. 2.3. Informati on Collection Questionnaires, contents of which were co mpiled after test survey and adjustment, were used for direct interviews of owners, technical collaborators or veterinary doctors of the farm. The information of veterinary drugs, antibiotic components and active elements which weren’t noted in the farm were t racked down and collected through labels on remedy packs or jars left around animal housing or at local veterinary med icine pharmacy. In order to ensure the objectivity of full remedy use information exploitat ion, all householders’ names and addresses were kept in security through encoding addresses just at the survey time. In this survey, antibiotics are considered to be used abusively when they are used unscientifica lly and incorrectly (under/overdosing, no exact diagnosis or result of a susceptibility testing …). 2.4. Statistical Analysis All data and information were registered and checked using Microsoft Excel 2003. The data were analysed statistically and co mpared, in 2x2 and 2x3 contingency tables, using the chi-square test and the Fisher's Exact Test, when the chi-square test was not relevant, using the SAS® Software 9.0. A Fisher exact test was performed using the data of number of p roduction system using antibiotics for disease prevention, therapy or growth promotion (Tab le 2a), in order to assess if there is a significant difference with p<0.05) in the use of antibiotics between the three production systems (household farms, semi-industrial and industrial production systems), as well as to assess if there is a significant difference in the use of antibiotics (total of the three production systems) between the different production stages (piglets, fattening pigs and sows for the pig production) and production systems (breeding poultry, broilers and laying hens for the poultry production) (Tab le 2b). Table 2a. Ant ibiot ics use as growt h promoter, for disease prevent ion and therapy purpose in three different pig or poultry product ion syst ems (in % of product ion systems using ant ibiot ics) Pe rcentage of production system using antibiotic Livestock P iglet s Fattening pigs Sows* Breeding chicken Broilers Laying Hens Growth promoter Farm household (n=150) 38.7a 31.3 a 16.2 a Semi- in dust rial (n=30) 43.3b 40.0b 20.0b Industrial (n=30) 63.3c 66.7c 43.3c 11.3a 33.3b 53.3b 8.7 a 26.7 b 43.3b 0.0a 0.0a 0.0a Disease pre vention Farm household (n=150) 13.3I 4.7 I 7.6I Semi - in dust rial (n=30) 10.0 I, II 13.3 I,II 3.3 I Industrial (n=30) 30.0II 26.7II 16.7I 20.0 I 53.3II 53.3II 11.3I 2.7I 6.7 I 6.7I,II 30.0II 13.3II Farm household (n=150) 54.7α 54.7α 14.3α 10.7α 4.0α 0.7α The rapy Semiin dust rial (n=30) 43.3α 43.3α 10.0α 30.0β 23.3β 16.7β Industrial (n=30) 66.7α 66.7α 30.0α 23.3αβ 23.3β 13.3β *: Only 105 household farms were having breeding sows from the 150 household farms investigated a, b, c : the % of production systems using antibiotics for growth stimulation without the same letter in the same row differ signi ficantly (P < 0·05) I, II : the % of production systems using antibiotics for disease prevention without the same roman number in the same row differ significantly (P < 0·05) α, β : the % of production systems using antibiotics for therapy without the same symbol in the same row differ significantly (P < 0·05) 250 Dang Pham Kim et al.: First Survey on the Use of Antibiotics in Pig and Poultry Production in the Red River Delta Region of Vietnam Table 2b. Ant ibiot ics use as growth promot er, for disease prevent ion and therapy purpose in t hree different types of pig and poult ry product s (in % of production systems using antibiotics) Livestock Piglets Fattening pigs Sows* Breeding chicken Broilers Laying hens Pe rcentage of production systems using antibiotics Growth promoter Disease prevention Therapy (n= 210) 42.9a 37.6a 21.8c 20.5α 16.2α 0.0β (n= 210) 15.2a 9.0a 8.5a 29.5α 13.3β 4.8γ (n= 210) 54.8a 54.8a 16.4b 15.2α 9.5αβ 4.8β * Except for sows: n = 165 a, b, c: the % of production systems using antibiotics for pig production without the same letter in the same column differ signifi cantly (P < 0·05) α, β, γ: the % of production systems using antibiotics for chick en production without the same letter in the same column differ significantly (P < 0·05) Table 3. Antibiotic use in pig and poultry production in Red River Delta expressed in number of entities having used the antibiotic at least once Grou p Anti bio ti c Use frequency (expresse din number of entities) Growth promoter (n=210) Disease prevention (n=210) Therapy (n= 210) Chicken P ig Chicken P ig Chicken P ig Bycomycin - - 5 - 5 1 Gentamicin - - 5 3 12 78 Aminoglycosides Kanamycin Neomycin - - - - 1 13 - - 5 3 2 4 Sp ect ino my cin - - 2 5 - 33 St reptomy cin - - 3 3 3 17 Amoxicillin(i) - 6 8 7 9 19 Ampicillin - - 31 2 13 18 Bet a-lactams Cefotaxime Cefalexin - - - 1 - 1 - - - - 1 - Cepharadin - - - - - 1 P en icillin - - 2 1 1 14 Danofloxacin - - - - - 2 Fluoroquinolons Enrofloxacin(f) - - 14 10 5 62 Flumequine - - - - - 2 Ionophores Macrolides Norfloxacin - - 6 17 5 16 Maduramycin 3 - - Monensin(r) (p) 6 5 - - - - - - - Salinomycin(r) (p) 38 13 - - - - Eryt hromy cin - - 1 - - - Josamycin - - 1 - - - Kitasamycin Spiramycin(r) Tiamulin(i) - - - 1 - - - - 5 1 2 5 - 1 2 - 1 12 Fenicols Tylosin - Chloramphenicol(f) - Florfenicol - 7 15 8 20 94 - 2 - 3 6 - - 5 - 17 Thiamphenicol - Sulfachlorpyrazin - Sulfadimidin - - 1 1 3 21 - 23 2 12 1 - 2 - 1 1 Sulfonamides Sulfamethoxazole - - 4 1 6 2 Sulfaquinoxaline - - 2 - 5 - Sulfaguanidine - - 9 1 8 2 Ch lort et racy clin e 29 72 1 1 1 1 Tet racyclines Doxycyline Oxyt et racy clin e - - 11 1 5 12 1 13 11 8 31 Tet racycline(i) 5 1 11 5 7 4 Bambermycin 4 - - - - - Lincomycin - 3 2 9 1 24 Others BMD(*) Colistin(i) Diclazuril(i) 4 20 - - - - 6 78 44 12 22 56 9 - - - - - Toltrazuril - - 6 - - 2 Diaverindine - - 9 - 4 - Trimethoprim - - 16 4 16 6 Number of different antibiotics used 9 11 31 25 29 33 (*): Bacitracin Methylene-Disalicylate -: not used (f): illegal use and (r): restricted use in veterinary medicine (MARD 2009d). (p): illegal use as growth promoter for pig and (i) : illegal use as growth promoter for both chicken and pig (MARD 2006, 2009b,c) Food and Public Health 2013, 3(5): 247-256 251 3. Results and Discussion the use of antibiotics for d isease prevention is lower in farm households than in industrial systems (Table 2a ). 3.1. Identification of Anti biotics Used in Pig and Poultry When the antibiotics are used for therapy, a significant Production in the RRD difference (p<0.05) between farm household and industrial At least 45 antibiotics representing more than 10 classes were used in pig and poultry production in the provinces studied, not only for treatment of diseases, but also for disease prevention and to promote growth. For disease prevention purpose, 31 and 25 d ifferent antibiotics were found to be used in poultry and pig production, respectively, wh ile the nu mber of different antibiotics used for curative purpose in pig and poultry were 33 and 29 respectively (Table 3). These data show that in pig production, antibiotics fro m aminoglycosides, tetracyclines, fenicols, beta-lactams and fluoroquinolones groups are the most commonly used for mostly disease treatment, and to a lesser extent for d isease prevention. In poultry, antibiotics fro m sulfonamides, beta-lactams, tetracyclines, aminoglycosides and ionophores, as well as colistin are commonly used mostly for disease prevention and to a lesser extent for therapy. For both prophylactic and therapeutic purposes, most producers use antibiotics to prevent infection diseases not according to the prophylactic or therapeutic dosage, length of treatment and withdrawal t ime indicated on the product label, but most of them use a higher dosage and don’t respect the recommendations of the drug producer. In the 45 antibiotics identified in this survey, colistin, chlortetracycline and o xytetracycline are the most commonly used. Chlortetracycline was overall used for growth pro moter purpose, o xytetracycline for disease prevention and therapy, while colistin was used for all three purposes. In particu lar, colistin was indicated for p revention and therapy of gastrointestinal disorders in piglets and poultry caused by gram negative bacteria (in particular E. coli and Salmonella spp). production systems is observed only for poultry production (breeding poultry, broilers or laying hens), but not for pig production (Table 2a). In a general manner, antib iotics are less used in farm households, and equally used in both semi-industrial and industrial production systems, except for growth pro motion purpose in pig production, where the industrial systems are the largest antibiotic users (up to 66.7 % for fattening pigs), and for d isease prevention purpose in bro ilers, where farm households and semi-industrial production systems use less antibiotics than industrial systems (11.3% and 6.7% against 30.0% respectively) (Table 2a). In pig production, the use of antibiotics is not significantly different between the three kinds of age groups (piglets, fattening pigs and sows), when the antibiotics are used for disease prevention. On the contrary, the use is significantly different (p<0.05), when the antibiotics are used for therapy or for gro wth pro motion (Table 2b). For growth pro motion and therapy, antibiotics are less used in sows than in piglets, and are equally used for pig lets and fattening pigs (Table 2b). In poultry production, the use of antib iotics is significantly different (p<0.05) between the three production systems (breeding poultry, b roilers and laying hens), for all considered purposes (disease prevention, therapy or growth promotion) (Table 2b). Growth pro moters are equally used in breeding poultry and broilers and not used in laying hens. Antibiotics are mo re used in breeding poultry for disease prevention, equally used for therapy of breeding poultry and broilers, and less used for therapy of laying hens (Table 2b). If we consider the overall use of antibiotics for the 3 purposes, in the 3 production systems, the number of farms 3.2. Anti bi otic Use in Different S ystems of Li vestock It appeared that the use of antibiotics as growth promoters which do not use antibiotics are the following: 2 out of 150 farm households, 13 out 30 semi-industrial pig farms, 2 out of 30 se mi-industrial poultry farms, 1 out of 30 industrial pig in pig production was significantly diffe rent (p<0.05) in the farms and 6 out of 30 semi-industrial poultry fa rms. three production systems, displaying the following order: Besides the non-compliance with dosage, length of industrial production system > semi-industrial production treatment and withdrawal time, the nu mber of different system > farm household. In breeding poultrys and broilers antibiotics used in each production system appeared to be production, growth promoters are significantly less used in high. The data in the Table 4 show that up to six categories of farm households (11.3% and 8.7% respectively) than in different antibiotics can be used in a production system for semi-industrial and industrial production systems (up to 53.3% therapy of pig and poultry. The rate of breeders who used of the farm for breeding poultrys), for which there is no fro m 1 to 2 antibiotics is high for all kinds of livestock and significant difference (Table 2a). production systems. Except for breed ing poultry raised in The use of antibiotics for disease prevention is semi-industrial systems, the rate of farmers using from 3 to 6 significantly d ifferent with p<0.01 fo r p iglets and with antibiotics is higher than those using 1 or 2 antibiotics p<0.05 in farm households than in semi-industrial or (16.7% co mpared with 13.3%). Fo r fattening pigs, the rate of industrial production systems for fattening pigs, breeding farmers using fro m 3 to 6 antib iotics in the three production poultry, broilers and laying hens, but not in sows (Table 2a). systems (farm household, semi-industrial and industrial) is In piglets, fattening pigs, breeding poultry and laying hens, rather high (20%; 6.7% and 26.7% respectively). 252 Dang Pham Kim et al.: First Survey on the Use of Antibiotics in Pig and Poultry Production in the Red River Delta Region of Vietnam Table 4. Number of ant ibiot ics used in each product ion system (in % of production syst ems) Livestock P iglet s Fattening pigs Sows Breeding chicken Broilers Laying hens Number of antibiotic used No use 1 to 2 3 to 6 No use 1 to 2 3 to 6 No use 1 to 2 3 to 6 No use 1 to 2 3 to 6 No use 1 to 2 3 to 6 No use 1 to 2 3 to 6 Pe rcentage of production systems using antibiotics Farm household (n=150) Semi-industrial (n=30) Industrial (n=30) 45.3 56.7 33.3 46.0 36.7 43.3 8.7 6.7 23.4 45.3 56.7 33.3 34.7 36.7 40.0 20.0 6.7 26.7 85.7 90.0 70.0 12.4 10.0 23.3 1.9 0 6.7 89.3 70.0 76.7 7.3 13.3 16.7 3.3 16.7 6.7 96.0 76.7 76.7 2.7 16.7 13.3 1.3 6.7 10.0 99.3 83.3 86.7 0.7 3.3 10.0 0 13.4 3.3 3.3. Veterinary Acti vities and Issues Linked to Food S afety in the Use of Anti bi otics Table 5. Veterinary activities and issues linkedto food safety concerning the antibiotics use, in three different pig and poultry production systems in the Red River Delta Pe rcentage of production system (%) Criteria of assessment Farm household Semi-industrial Industrial Tot al (n=150) (n=60) (n=60) (∑n=270) Vet erin ary act iv it ies Use of v et erinary drugs in compliance with sanitary legislat ion Vet erin ary act iv it ies Owner Local veterinarian Both of them Experience Basis of choosing drugs Drug seller After sending samples Vet erin arian Others (friends, market ing, books and newspapers...) Percentage of production systems respectingthe withdrawal time, in which: Motivation of respect is: Required by purchasers Protecting consumers Others (economic, weight gain) Percentage of production systems in which : Technical staff safety Medias (T V, Radio ...) information Friends and colleagues sources are : Drug sellers Others (indication on product labels) Changing remedies What is done Selling quickly with ill Slaughtering & consuming in family livestock with Destroying bad prognosis Feeding other animals Others 59.3a 39.3a 1.3a 7.3a 33.3a 0a 39.3a 20a 41.3a 8.1a 37.1a 54.8a 72.7a 2.8a 85.3a 0.9a 5.5a 5.5a 21.3a 44.7a 8.0a 16.0a 4.0a 6.0a 95.0b 5.0b 0a 13.3a 38.3a 6.7b 5.0b 36.7b 58.3b 8.6a 37.1a 54.3a 86.7a 1.9a 61.5ab 1.9a 0a 35b 31.7a 18.3b 10.0a 26.7a 6.7a 6.7a 100.0b 76.3 0b 23.0 0a 0.7 40.0a 15.9 36.7a 35.2 13.3b 4.4 0b 23.0 10.0a 21.5 73.3b 52.2 4.5a 7.1 56.8a 43.3 38.6a 49.6 81.7a 77.8 0a 1.9 73.5b 76.7 2.0a 1.4 2.0a 3.3 22.4b 16.7 20.0a 23.3 40.0a 37.8 6.7a 8.1 18.3a 18.9 11.7a 6.3 3.3a 5.6 a, b, c : Percentage of production system without the same letter in the same row differ signi ficantly (P < 0·05) Few animal raising householders are trained on veterinary practices; however, they are themselves in charge of most veterinary activ ities such as vaccination, animal prophylactic and t reat ment . Especially fo r th e indust rial and semi-indu strial production systems, veterinary activit ies and therapy are main ly assumed by the owners (95% of them for semi-industrial farms and 100% for industrial farms), wh ile, for farm households, about 60% of them undertake Food and Public Health 2013, 3(5): 247-256 253 themselves the therapy of their anima ls and nearly 40% need the assistance of animal health workers, veterinary technicians or para-veterinarians (Table 5). The antibiotics were mainly chosen on the basis of the experience of the farmer, or advice fro m representatives of pharmaceutical co mpanies or local drug sellers[according to symptoms told by farmers) (15.9% and 35.2% respectively). Very few samples of ill animals are sent to laboratories for diagnosis or susceptibility testing before therapy. This shows that the use of antibiotic by farmers without any veterinary prescription and supervision is very frequent in this region. This can be explained by the fact that in practice, the leading role and the actions of local veterinarians are limited. In each commune, there is a livestock committee of 1 to 2 responsible animal health workers (usually para-vets). Most of veterinarians are only concerned by comme rcia l act ivities (distributor of feed, or veterinary d rugs) or in the marketing network of feed or drug co mpanies. The results of this survey reveal that overuse and illegal use of antibiotics in pig and poultry production in the region of the RRD is worrisome. At least 45 antib iotics of mo re than 10 different classes were shown to be used: - fourteen antimicrobial g rowth pro moters used as pig or poultry feed additives, - thirty four antibiotics used for disease prevention (31 antibiotics in poultry production and 25 antibiotics in pig production), - thirty six used for disease treatment (in which 29 antibiotics in poultry production and 33 antibiotics in p ig production). Antimicrobia l feed additives have been used worldwide in animal production for many decades because of their favourable economic e ffects in livestock. However, there has been an increasing public concern about the possible links between their use and the transfer of antibiotic resistant organisms and resistance genes to humans[29]. Through studying bacterial strains isolated fro m eggs in Greece, Papadopoulou et al[30] concluded that antibiotic-resistant strains might be transmitted to human by the consumption of eggs containing multiresistant bacteria. In addition, the results of an other study on antibiotic resistance of co mmon foodborne pathogens isolated fro m major meat products[31] indicated that meat can be a source of resistant strains, which could potentially be spread to the commun ity through the food chain. Many scientists agree on the fact that the use of antibiotics in animal production for g rowth pro motion, prophylaxis and treat ment can lead either to the selection of resistant bacteria, wh ich can be transmitted through the food chain[32, 33], or to the horizontal t ransfer of resistance genes to human pathogenic or co mmensal microflo ra[34]. So, the use of antibiotics, both in human and animals should be avoided, as far as possible[35]. Due to the emergence of cross-resistance to antibiotics that are used in human med icine and also in animal infections, the European Co mmission decided to totally ban antimicrobial growth promoters since the 1st January 2006[36]. In contrast, antimicrobial growth pro moters continue to be authorized in the USA under the FDA regulation and controlled on a case-by-case basis[37]. Meanwh ile, in Vietnam, th is is still permitted[38-41]. Nine and 11 different antibiotics are used for gro wth pro motion in poultry and pig production, respectively (Table 2), fro m which 3 (colistin, diclazuril and tetracycline) and 6 (amo xycillin, t iamulin, monensin, salinomycin, colistin and tetracycline) antimicrobials, respectively, are not allowed by the Vietnamese legislation [38-41]. This result confirm that, in spite of their absence on the list of permitted antibiotics for growth promotion, some antibiotics are popularly used yet, especially colistin and chlortetracycline in pig feed, found in 78 and 72 pig farms respectively. This use may be related to diarrhea and oedema in pig lets, one of the most co mmon diseases in Vietnam[42, 43]. One study in Hai Duong[44] shows that diarrhea in p ig is very high (48%) and that this occurs in any season of the year. The state of antibiotic use in animal production is worrisome in developing countries, where the antibiotic use is not tightly controlled and where few detailed information is availab le on these problems[9]. The results of this study are co mpletely consistent with the above statement of the WHO. Antibiotics fro m the groups of aminoglycosides, tetracyclines, fenicols, beta-lactams and fluoroquinolones are the most commonly used for disease prevention and treatment, mainly for therapy in pig p roduction, while antibiotics fro m the groups of sulfonamides, beta-lactams, tetracyclines, aminoglycosides, ionophores, as well as colistin, are co mmon ly used for poultry d isease prevention and therapy, but mainly for disease prevention. The results of this study confirm that antibiotics listed here, and considered as critically important for hu mans by WHO, are still commonly used in animal production. Allowed antibiotics were used but also banned substances, such as chloramphenicol and enroflo xacin, by both famers and veterinarians. In other countries, such as for examp le Australia, the pig industry is based on drugs of low importance to human health (e.g. tetracyclines, penicillins (including amo xicillin and ampicillin) and sulfonamides). Only t wo drugs of h igh importance for hu mans (ceftiofur and virgin iamycin) can be used legally in p ig production[45]. Moreover, tetracyclines, sulfonamides and tylosin were shown to be commonly used these last years in pig production not only in China, Russia and Southeast Asia, but also in the European Union[46] and in the Un ited States[47]. A recent study carried out by Kools et al.[48] showed that tetracyclines, beta-lactams, and sulfonamides are the most used groups in animal production in EU. In 2005, tetracyclines were the most prescribed antibiotics among the 1,320 tons used for animal production in France[49]. In comparison, about 12,650 tons of antimicrobials were used in 2007 in the USA in veterinary medicine[50], 40% of which were tetracyclines and about 13% of the total a mount of antimicrobials was used as growth promoters. Livestock breeders have very low awareness of the reasonableness and safety of antibiotic use as well as of food safety. According to regulations and guidelines of the use of veterinary drugs, antibiotics should only be emp loyed to treat bacterial infections, respecting the dose, the length of 254 Dang Pham Kim et al.: First Survey on the Use of Antibiotics in Pig and Poultry Production in the Red River Delta Region of Vietnam treatment and the withdrawal t ime provided by the manufacturer or indicated by the veterinarian. However, referring to the Vietnamese veterinary ordinance promu lgated in 2004[51], the vio lations on the veterinary activities of livestock breeders are very widespread. Their use of antibiotics is very unmethodical and unscientific, mainly based on their experiences or on advices from veterinary drug sellers. The results of this study show that, although the appropriate withdrawal period is mentioned on the label of the antibiotic used, in practice, only about 52% of the farmers surveyed were respecting the withdrawal t ime, fro m which 60%, 40% and 27% were fro m farm household, semi-industrial and industrial system, respectively (Table 5). Furthermore, animals in d isease and therapy can be sold quickly in o rder to save funds (this is the case in 40% of the farms investigated) or slaughtered and used for food, or feed for other animals. This creates both difficult ies for prophylaxis of ep idemic diseases and unsafety for consumers. In particu lar, these practices lead to a high risk of undesirable residues in animal products[10]. Th is is one of the reasons why traces of residues of veterinary drugs in general, and antibiotics in particu lar, have been found in animal products and also in the environment[52]. One study about the emergence of fluoroquinolone resistance in the native Campylobater coli population of pigs[53] indicates that a single course of enroflo xacin treat ment contributes directly to the emergence and persistence of quinolone resistant C. coli. To collect information on the consumption of veterinary drugs in general, and of antibiotics in particular, is not easy in developing countries. In this context, the background of animal production in Vietnam is low, scale is small and scattered, the organization system and management qualification of the animal production and veterinary sector display a lot of inadequacies which do not meet the real development requirements. The quality o f food, safety and hygiene is an urgent requirement for consumers. Differences in animal production systems between developed and developing countries lead to the need for different approaches to control antibiotics. 4. Conclusions and ethics of producers and veterinary drug sellers as well as training of para-veterinarians and farmers, public awareness and strength of surveillance systems in slaughterhouses. In conclusion, antibiotics have been used largely and even illegally (e.g. ch loramphenicol) in both poultry and pig production for disease prevention and treatment. ACKNOWLEDGMENTS This study was financially supported by BTC (Belg ian Technical Cooperation), the Be lgian Un iversity Co mmission toward Develop ment (CUD) and HUA. Thanks to all local veterinarians, Ir. Dong Bu i Quang - Researcher of Center for Interdisciplinary Research on Rural Develop ment, Ngai Pham Thi and Tuyen Tran Thi - Veterinary students of HUA for their co-operation to this study. REFERENCES [1] Tuyen, D.K., (2010). 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