First survey on the use of antibiotics in pig and poultry production in the Red river delta region of Vietnam

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 Medicine, 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 Medicine, 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 Medicine, Hanoi University of Agriculture, Vietnam  
Abstract In Vietnam where epidemics occur regularly in an ima l production,the farme rs considerantibiotics as one ofthe  
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 farmer’s knowledge on the danger of the antibiotic use in three different anima l  
production systems (farm household, s emi-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 volume of antibiotics was  
used arbitrary in all anima l 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 diseases 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.  
Ke ywo rds Antibiotics, Animal Production, Veterinary Drugs, Red River Delta, Vietnam  
development strategies, it results in some new problems such  
as environmental pollution, as well as frequently occurring  
1. Introduction  
and uncontrolled epidemic diseases [2-4]. In 2003, during  
In Vietnam, a country with more than 85 million  
the avian influen za crisis, about 44 million poultry have  
inhabitants and a very high population density, especially in  
either died because of the disease or have been slaughtered  
the Red River Delta (RRD), urbanization andindustrializa  
because of the crisis. The Po rcine Reproductive and  
tion increase rapidly. The demands of foodstuff from animal  
Respiratory Syndrome (PRRS), and the Foot-and-Mouth  
origin for do mes tic markets are more and more growing. The  
disease have also been a constant threat causing regular  
annual average consumption of animal products per  
outbreaks in recent years[5]. In 2006, an epidemiological  
Vietnamese capita in 2009 is 35 kg of carcass meat; 3 kg of  
analysis about swine diseases in Northern Vietna m based on  
milk and 80 eggs[1]. The development objective by 2020 is  
4000 declarations highlighted a high incidence of porcine  
56 kg of carcass meat, over 10 kg of milk and over 140  
respiratory disease (50% of total reported cases). The  
eggs [2]. As a consequence, the increase of intensive  
proportion of digestive tract infections in piglets and  
livestock husbandry models is an indispensable trend in the  
Vietnamese context. However, because of the low level of  
hygiene in livestock husbandry,the inadequacy ofhusbandry  
zone planning and the lack of state management and  
reproductive disorders in newly raised e xo tic sows were 30%  
and 10% of total reported cases, respectively [6].  
Facing this situation, producers consider antibiotics, used  
for disease prevention and therapeutic purposes,as one ofthe  
solutions to fight diseases in livestock. In fact, antibiotics are  
the mos t common registered drugs (70% of all veterinary  
drugs) used in an ima ls in Vietnam[7]. However, the  
knowledge of famers is still very restricted while the state  
* Corresponding author:  
[email protected] (Dang Pham Kim)  
Copyright © 2013 Scientific & Academic Publishing. All Rights Reserved  
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, unmethodical manner, without any  
veterinary prescription and supervision, may lead to the  
presence of residues in anima l products 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 ima l 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 environment microbial ecosystem  
[14-16]. It could also contribute to the presence of antibiotic-  
resistant 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 anima l pathogens,  
creating a severe health risk by greatly limiting the  
antibiotics that can be used to treat infectious diseases[24].  
consumers. Therefore, this problem has been discussed on  
several occasions in meetings of the Vietna m National  
Ass embly[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  
information is availab le on antibiotic use.  
For the reasons above, as well as to contribute to a  
long-term strategy of the Vietnamese Government on food  
safety, the collection of detailed information about  
antibiotics used in animal production is necessary. The aim  
of this study was to provide information on the use of  
antibiotics in different pig and poultry production s ystems in  
the RRD of Vietna m. 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, s emi-  
industrial and industrial, in 3 representative localities of the  
RRD (Hai Duong, Thai Binh and Ha Noi) (Fig. 1)(Table 1).  
In recent years, Vietna m had many alerts about veterinary  
drug residues in general and antibiotics in particular. These  
alerts have caused warnings to authorities and alarmed  
Ta b l e 1. Est imat ion of the tot al number of pig and poultry production sy st em s inthe RRD  
Provinces  
Hai Duong  
Total ( by production  
Syst em of animal production  
Industrial  
Animal species  
Ha Noi  
10  
10  
10  
10  
Thai Binh  
system)  
30  
30  
30  
30  
150  
270  
Pig  
Chicken  
Pig  
Chicken  
Pig, chicken  
10  
10  
10  
10  
50  
90  
10  
10  
10  
10  
50  
90  
Semi-industrial  
Farm household (* )  
Total ( by localit ies)  
(*): only households who have both the pig and chicken  
50  
90  
Fi gure 1. Map of Red River Delt a region indicatingthe three represent at ive localit ies where the samples were collect ed (Hai Duong, Thai Binh and Ha  
Noi)  
Food and Public Health 2013, 3(5): 247-256  
249  
2.1. Sampling Area  
pigs or 10 sows for the pig and 200 anima ls for the poultry.  
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 Vietna m. It is an agricu lturally rich area  
and densely populated (1225 persons/km2, 4.8 t imes higher  
than the average population density of Vietna m) . 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% of the whole country  
production) with 7.0 million pigs, 66.5 million poultry in  
2008[28].  
2.3. Information Collection  
Questionnaires, contents ofwhich were compiled 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 tracked down and collected through labels on  
re medy packs or jars left around anima l housing or at local  
veterinary med icine pharmacy. In order to ensure the  
objectivity of full re medy use information exploitation, all  
householders’ names and addresses were kept in security  
through encoding addresses just at the survey time .  
Three representative provinces were selected not only for  
their production capacity but also representative of their  
geographic location and population density: Hanoi (3344  
2
km ), Hai Duong (1661 km2) and Thai Binh (1542 km2). The  
In this survey, antibiotics are considered to be used  
abusively when they are used unscientifically and incorrectly  
(under/overdosing, no exact diagnosis or result of a  
susceptibility testing …).  
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].  
2.4. Statistical Analysis  
All data and information were registered and checked  
using Microsoft Excel 2003. The data were analysed  
statistically and compared, 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 production 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 ofantibiotics 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).  
2.2. Sampling Me th od  
In each province, on the basis of the list provided by the  
local agricultural office (for industrial and semi-industrial  
systems), as well as from the lists provided by local  
veterinarians, 50 farm households who have both pig and  
poultry, 20 s e mi-industrial farms (10 for pig and 10 for  
poultry) and 20 industrial fa rms (10 for pig and 10 for  
poultry) were selected by random s amp ling for the survey.  
Official local agricultural criteria were used to classify the  
different farming systems.Farm household systemdisplays a  
s mall number of animals, primarily for 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  
Ta b l e 2a. Antibiotics use as gr o wt h promoter, for disease prevention and therapy purpose in three different pig or poultry production sy st em s (in % of  
production systems using antibiotics)  
Percentage of production system using antibiotic  
Growth promoter  
Disease prevention  
Th e ra py  
Livestock  
Farm  
Semi-  
Farm  
household  
(n=150)  
Semi -  
industrial  
(n=30)  
Farm  
Semi-  
household industrial  
Industrial  
(n=30)  
Industrial  
(n=30)  
Industrial  
(n=30)  
household  
(n=150)  
industrial  
(n=30)  
(n=150)  
(n=30)  
Piglets  
Fatteningpigs  
Sows*  
38.7a  
31.3 a  
16.2 a  
43.3b  
40.0b  
20.0b  
63.3c  
66.7c  
43.3c  
13.3I  
4.7 I  
7.6I  
10.0 I, II  
13.3 I,II  
3.3 I  
30.0II  
26.7II  
16.7I  
54.7α  
54.7α  
14.3α  
43.3α  
43.3α  
10.0α  
66.7α  
66.7α  
30.0α  
Breeding  
chicken  
Broilers  
Laying Hens  
11.3a  
33.3b  
53.3b  
20.0 I  
53.3II  
53.3II  
10.7α  
30.0β  
23.3αβ  
8.7 a  
0.0a  
26.7 b  
0.0a  
43.3b  
0.0a  
11.3I  
2.7I  
6.7 I  
30.0II  
13.3II  
4.0α  
0.7α  
23.3β  
16.7β  
23.3β  
13.3β  
6.7I,II  
*: Only 105 household farm s were having breeding sows from the 150 household farm s investigated  
a, b, c : the % of production systems using antibiotics for growth stimulation without the same letter in the same row di ffer significantly (P < 0·05)  
I, II : the % of production systems using antibiotics for disease prevention without the same roman number in the same row di ffe r significantly (P < 0·05)  
α, β : the % of production systems using antibiotics for therapy without the same symbol in the same row di ffe r 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  
Ta b l e 2b. Antibiotics use as growth promoter, for disease prevention and therapy purpose in three different types of pig and poultry products (in % of  
production sy stem s using antibiotics)  
Percentage of production systems using antibiotics  
Livestock  
Growt h promoter  
(n= 210)  
42.9a  
Disease prevention  
Therapy  
(n= 210)  
54.8a  
(n= 210)  
15.2a  
9.0a  
Piglets  
Fattening pigs  
37.6a  
54.8a  
*
Sows  
21.8c  
8.5a  
16.4b  
Breeding chicken  
Broilers  
Laying hens  
20.5α  
29.5α  
13.3β  
4.8γ  
15.2α  
16.2α  
9.5αβ  
0.0β  
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 di ffer significantly (P < 0·05)  
α, β, γ: the % of production systems using antibiotics for chicken production without the same letter in the same column di ffe r significantly (P < 0·05)  
Table 3. Antibiotic use in pig andpoultry production in Red River Delta expressed in number of entities having used the antibiotic at least once  
Use frequency (expressedin number ofentities)  
Grou p  
Antibiotic  
Growt h promoter (n=210)  
Disease prevention (n=210)  
Therapy (n= 210)  
Chicken  
Pig  
-
-
-
-
-
-
6
-
-
Chicken  
Pig  
-
3
-
3
5
3
7
2
1
-
Chicken  
Pig  
1
78  
13  
4
33  
17  
19  
18  
1
Bycomycin  
Gentamicin  
-
-
-
-
-
-
-
-
-
5
5
-
5
2
3
8
31  
-
-
5
12  
1
2
-
3
9
13  
-
Kanamycin  
Neomycin  
Aminoglycosides  
Spectinomycin  
Streptomycin  
Amoxicillin(i)  
Ampicillin  
Cefotaxime  
Cefalexin  
Beta-lactams  
-
-
-
-
1
-
-
1
Cepharadin  
-
-
Penicillin  
-
-
2
1
1
14  
Danofloxacin  
Enrofloxacin(f)  
Flumequine  
Norfloxacin  
Maduramycin  
Monensin(r) (p)  
Salinomycin(r) (p)  
Erythromycin  
Josamycin  
-
-
-
-
3
6
38  
-
-
-
-
-
-
14  
-
6
-
-
-
1
1
-
10  
-
17  
-
-
-
-
-
-
5
-
5
-
-
-
-
-
2
62  
2
16  
-
-
-
-
-
Fluoroquinolons  
-
Ionophores  
Macrolides  
5
13  
-
-
-
Kitasamycin  
Spiramycin(r)  
Tiamulin(i)  
-
-
-
-
-
-
-
-
-
-
-
-
29  
-
-
5
4
-
4
6
9
-
-
-
1
7
-
-
-
-
-
-
-
-
72  
-
1
1
-
3
20  
78  
-
-
5
2
15  
2
-
1
23  
2
4
2
9
1
11  
13  
11  
-
2
-
1
1
-
8
-
5
1
2
-
1
-
1
1
1
11  
5
-
-
-
5
2
1
20  
3
-
3
12  
1
6
5
8
1
5
8
7
-
12  
94  
6
17  
21  
1
1
2
-
2
Tylosin  
Chloramphenicol(f)  
Florfenicol  
Fenicols  
Thiamphenicol  
Sulfachlorpyrazin  
Sulfadimidin  
Sulfamethoxazole  
Sulfaquinoxaline  
Sulfaguanidine  
Chlortetracycline  
Doxycyline  
Sulfonamides  
1
12  
31  
4
-
24  
-
56  
-
Tetracyclines  
Others  
Oxyt et racycline  
Tet racycline(i)  
Bambermycin  
Lincomycin  
BMD(*)  
9
-
12  
-
-
1
-
22  
-
-
Colistin(i)  
44  
-
6
Diclazuril(i)  
Toltrazuril  
-
2
Diaverindine  
Trimethoprim  
Number of different antibiotics used  
-
-
9
-
-
11  
9
16  
31  
-
4
25  
4
16  
29  
-
6
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 disease prevention is lower in farm  
households than in industrial systems (Table 2a).  
3.1. Identification of Antibiotics Us ed in Pig and Poultry  
Produc tion in the RRD  
When the antibiotics are used for therapy, a significant  
difference (p<0.05) between farm household and industrial  
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 s emi-industrial and  
industrial production systems, except for growth promotion  
purpose in pig production, where the industrial s ystems are  
the largest antibiotic users (up to 66.7 % for fattening pigs),  
and for disease prevention purpose in bro ilers, where farm  
households and s emi-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 growth promotion (Table 2b).  
For growth promotion 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 ofantib iotics is significantly  
different (p<0.05) between the three production systems  
(breeding poultry, broilers and laying hens), for all  
considered purposes (disease prevention, therapy or growth  
promotion) (Table 2b).  
Growth promoters 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  
which do not use antibiotics are the following: 2 out of 150  
farm households, 13 out 30 s e mi-industrial pig farms , 2 out  
of 30 semi-industrial poultry farms , 1 out of 30 industrial pig  
farms and 6 out of 30 semi-industrial poultry fa rms .  
Besides the non-compliance with dosage, length of  
treatment and withdrawal time, the number of different  
antibiotics used in each production system appeared to be  
high.The data in the Table 4 showthat up to sixcategories of  
different antibiotics can be used in a production system for  
therapy of pig and poultry. The rate of breeders who used  
from 1 to 2 antibiotics is high for all kinds of livestock and  
production systems. Except for breeding poultry raised in  
s emi-industrial systems, the rate of farmers using from 3 to 6  
antibiotics is higher than those using 1 or 2 antibiotics  
(16.7% compared with 13.3%). For fattening pigs, the rate of  
farmers using from 3 to 6 antib iotics in the three production  
systems (farm household, s emi-industrial and industrial) is  
rather high (20%; 6.7% and 26.7% respectively).  
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 als o for  
disease prevention and to promote growth.  
For disease prevention purpose, 31 and 25 different  
antibiotics were found to be used in poultry and pig  
production, respectively, wh ile the number 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 from aminoglycosides, tetracyclines,  
fenicols, beta-lactams and fluoroquinolones groups are the  
mos t commonly used for mos tly disease treatment, and to a  
lesser extent for disease prevention. In poultry, antibiotics  
from  
sulfonamides,  
beta-lactams,  
tetracyclines,  
aminoglycosides and ionophores, as well as colistin are  
commonly used mos tly for disease prevention and to a lesser  
e xten t for therapy.  
For both prophylactic and therapeutic purposes, mos t  
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 mos t 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 oxytetracycline are the mos t  
commonly used. Chlortetracycline was overall used for  
growth promoter purpose, oxytetracycline for disease  
prevention and therapy, while colistin was used for all three  
purposes. In particular, colistin was indicated for prevention  
and therapy of gastrointestinal disorders in piglets and  
poultry caused by gram negative bacteria (in particular E.  
coli and Salmonella spp).  
3.2.Antibiotic Use in Different Systems of Li vestock  
It appeared that the use of antibiotics as growth promoters  
in pig production was significantly different (p<0.05) in the  
three production systems, displaying the following order:  
industrial production system > s e mi-industrial production  
system > farm household. In breeding poultrys and broilers  
production, growth promoters are significantly less used in  
farm households (11.3% and 8.7% respectively) than in  
s emi-industrial and industrial production systems (up to 53.3%  
of the farm for breeding poultrys), for which there is no  
significant difference (Table 2a).  
The use of antibiotics for disease prevention is  
significantly different with p<0.01 for p iglets and with  
p<0.05 in farm households than in s emi-industrial or  
industrial production systems for fattening pigs, breeding  
poultry, broilers and laying hens, but not in sows (Table 2a).  
In piglets, fattening pigs, breeding poultry and laying hens,  
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  
Ta b l e 4. Number of antibiotics used in each production sy stem (in % of production systems)  
Percentage of production systems using antibiotics  
Number of antibiotic  
Livestock  
Piglets  
Farm household  
(n=150)  
45.3  
Semi-industrial  
(n=30)  
56.7  
used  
Industrial (n=30)  
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  
33.3  
43.3  
23.4  
33.3  
40.0  
26.7  
70.0  
23.3  
6.7  
46.0  
36.7  
8.7  
6.7  
45.3  
56.7  
Fatteningpigs  
Sows  
34.7  
36.7  
20.0  
6.7  
85.7  
90.0  
12.4  
10.0  
1.9  
89.3  
7.3  
3.3  
96.0  
2.7  
1.3  
99.3  
0.7  
0
0
70.0  
13.3  
16.7  
76.7  
16.7  
6.7  
76.7  
16.7  
6.7  
Breeding chicken  
Broilers  
76.7  
13.3  
10.0  
86.7  
10.0  
3.3  
83.3  
3.3  
Layinghens  
13.4  
3.3. Veterinary Ac ti vities and Issues Linked to FoodS afety in the Use of Antibiotics  
Ta b l e 5. Vet erinary act ivit ies and issues linkedtofood safety concerning the antibiotics use, inthree different pigand poultry production sy stem s in the Red  
River Delta  
Percentage of production system (%)  
Criteria of assessment  
Owner  
Farm household Semi-industrial Industrial  
Total  
(∑n=270)  
(n=150)  
(n=60)  
(n=60)  
59.3a  
39.3a  
1.3a  
95.0b  
5.0b  
0a  
100.0b  
0b  
76.3  
23.0  
0.7  
15.9  
35.2  
4.4  
Veterinary  
Local vet erinarian  
Both of them  
act ivit ies  
0a  
Experience  
7.3a  
13.3a  
38.3a  
6.7b  
5.0b  
40.0a  
36.7a  
13.3b  
0b  
Veterinary  
act ivit ies  
Drug seller  
After sending samples  
Vet erinarian  
Others (friends, market ing, books and  
newspapers...)  
33.3a  
0a  
Basis of  
choosing  
drugs  
39.3a  
23.0  
20a  
36.7b  
10.0a  
21.5  
P ercent age of production sy st em s respect ingthe withdrawal  
t ime, in which:  
41.3a  
58.3b  
73.3b  
52.2  
Required by purchasers  
8.1a  
37.1a  
54.8a  
72.7a  
2.8a  
8.6a  
37.1a  
54.3a  
86.7a  
1.9a  
4.5a  
56.8a  
38.6a  
81.7a  
0a  
7.1  
43.3  
49.6  
77.8  
1.9  
76.7  
1.4  
3.3  
16.7  
23.3  
37.8  
8.1  
18.9  
6.3  
Mot ivat ion of  
Prot ect ing consumers  
respect is:  
Others (economic, weight gain)  
P ercent age of production sy stem s in which :  
Technical st aff  
Use of  
vet erinary  
drugs in  
compliance  
wit h sanit ary  
legislation  
safety  
information  
sources are :  
Medias (T V, Radio ...)  
Friends andcolleagues  
Drug sellers  
85.3a  
0.9a  
61.5ab  
1.9a  
73.5b  
2.0a  
5.5a  
0a  
2.0a  
Others (indicat ion on product labels)  
Changing remedies  
Selling quickly  
Slaughtering & consuming in family  
Destroying  
5.5a  
35b  
22.4b  
20.0a  
40.0a  
6.7a  
21.3a  
44.7a  
8.0a  
31.7a  
18.3b  
10.0a  
26.7a  
6.7a  
What is do ne  
wit h ill  
livestock with  
bad prognosis  
16.0a  
4.0a  
18.3a  
11.7a  
3.3a  
Feedingother animals  
Others  
6.0a  
6.7a  
5.6  
a, b, c : Percentage of production system without the same letter in the same row di ffer significantly (P < 0·05)  
Few animal raising householders are trained on veterinary strial production systems, veterinary activit ies and therapy  
practices; however, they are themselves in charge of mos t are main ly assumed by the owners (95% of them for  
veterinary activ ities such as vaccination,anima l prophylactic s emi-industrial farms and 100% for industrial farms), wh ile,  
and treatment. Especially for the industrial and s emi-indu 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 permitted[38-41]. Nine and 11 different antibiotics are used  
the assistance of animal health workers, veterinary for growth promotion in poultry and pig production,  
technicians or para-veterinarians (Table 5).  
respectively (Table 2), from which 3 (colistin, diclazuril and  
The antibiotics were mainly chosen on the basis of the tetracycline) and 6 (amo xycillin, t iamulin, monensin,  
experience of the farmer, or advice from representatives of salinomycin, colistin and tetracycline) antimicrobials,  
pharmaceutical companies or local drug sellers[according to respectively, are not allowed by the Vietnamese legislation  
symptoms told by farmers) (15.9% and 35.2% respectively). [38-41]. This result confirmthat, in spite of their absence on  
Very few s a mples of ill animals are sent to laboratories for the list of permitted antibiotics for growth promotion, s ome  
diagnosis orsusceptibility testing before therapy. This shows antibiotics are popularly used yet, especially colistin and  
that the use of antibiotic by farmers without any veterinary chlortetracycline in pig feed, found in 78 and 72 pig farms  
prescription and supervision is very frequent in this region. respectively. This use may be related to diarrhea and oedema  
This can be explained by the fact that in practice, the leading in pig lets, one of the mos t co mmon diseases in Vietnam[42,  
role and the actions of local veterinarians are limited. In each 43]. One study in Hai Duong[44] shows that diarrhea in p ig  
commune, there is a livestock committee of 1 to 2 is very high (48%) and that this occurs in any season of the  
responsible anima l health workers (usually para-vets). Most year.  
of veterinarians are only concerned by comme rcia l act ivities  
(distributor of feed, or veterinary drugs) or in the marketing worrisome in developing countries, where the antibiotic use  
network of feed or drug companies.  
is not tightly controlled and where few detailed information  
The state of antibiotic use in anima l production is  
The results of this survey reveal that overuse and illegal is availab le on these problems[9]. The results of this study  
use of antibiotics in pig and poultry production in the region are completely consistent with the above statement of the  
ofthe RRD is worrisome. At least 45 antib iotics of mo re than WHO. Antibiotics from the groups of aminoglycosides,  
10 different classes were shown to be used: - fourteen tetracyclines, fenicols, beta-lactams and fluoroquinolones  
antimicrobial growth promoters used as pig or poultry feed are the mos t commonly used for disease prevention and  
additives, - thirty four antibiotics used for disease prevention treatment, mainly for therapy in pig production, while  
(31 antibiotics in poultry production and 25 antibiotics in pig antibiotics from the groups of sulfonamides, beta-lactams,  
production), - thirty six used for disease treatment (in which tetracyclines, aminoglycosides, ionophores, as well as  
29 antibiotics in poultry production and 33 antibiotics in p ig colistin, are commonly used for poultry disease prevention  
production).  
and therapy,but mainly for disease prevention.The results of  
Antimicrobial feed additives have been used worldwide in this study confirm that antibiotics listed here, and considered  
animal production for many decades because of their as critically important for humans by WHO, are still  
favourable economic effects in livestock. However, there has commonly used in anima l production. Allowed antibiotics  
been an increasing public concern about the possible links were used but also banned substances, such as  
between their use and the transfer of antibiotic resistant chloramphenicol and enrofloxacin, by both famers and  
organisms and resistance genes to humans[29]. Through veterinarians. In other countries, such as for exa mp le  
studying bacterial strains isolated from eggs in Greece, Australia, the pig industry is based on drugs of low  
Papadopoulou et al[30] concluded that antibiotic-resistant importance to human health (e.g. tetracyclines, penicillins  
strains might be transmitted to human by the consumption of (including amo xicillin and ampicillin) and sulfonamides).  
eggs containing multiresistant bacteria. In addition, the Only two drugs ofh igh importance for humans (ceftiofur and  
results of an other study on antibiotic resistance of co mmon virgin iamycin) can be used legally in p ig production[45].  
foodborne pathogens isolated from major meat products[31] Moreover, tetracyclines, sulfonamides and tylosin were  
indicated that meat can be a source of resistant strains, which shown to be commonly used these last years in pig  
could potentially be spread to the community through the production not only in China, Russia and Southeast Asia, but  
food chain. Many scientists agree on the fact that the use of also in the European Union[46] and in the Un ited States[47].  
antibiotics in anima l production for growth promotion, A recent study carried out by Kools et al.[48] showed that  
prophylaxis and treatment can lead either to the selection of tetracyclines, beta-lactams, and sulfonamides are the mos t  
resistant bacteria, wh ich can be transmitted through the food used groups in anima l production in EU. In 2005,  
chain[32, 33], orto the horizontaltransfer of resistance genes tetracyclines were the mos t prescribed antibiotics among the  
to human pathogenic or commensal microflora[34]. So, the 1,320 tons used for anima l production in France[49]. In  
use of antibiotics, both in human and anima ls should be comparison, about 12,650 tons of antimicrobials were used  
avoided, as far as possible[35]. Due to the emergence of in 2007 in the USA in veterinary medicine[50], 40% of  
cross-resistance to antibiotics that are used in human which were tetracyclines and about 13% of the total amount  
med icine and also in animal infections, the European of antimicrobials was used as growth promoters.  
Co mmission decided to totally ban antimicrobial growth  
Livestock breeders have very low awareness of the  
promoters since the 1st January 2006[36]. In contrast, reasonableness and safety of antibiotic use as well as of food  
antimicrobial growth promoters continue to be authorized in safety. According to regulations and guidelines of the use of  
the USA under the FDA regulation and controlled on a veterinary drugs, antibiotics should only be employed to  
case-by-case basis[37]. Meanwh ile, in Vietna m, th is is still 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 and ethics of producers and veterinary drug sellers as well as  
manufacturer or indicated by the veterinarian. However, training of para-veterinarians and farmers, public awareness  
referring to the Vietnamese veterinary ordinance and strength of surveillance systems in slaughterhouses.  
promulgated in 2004[51], the vio lations on the veterinary  
In conclusion, antibiotics have been used largely and even  
activities of livestock breeders are very widespread. Their illegally (e.g. chloramphenicol) in both poultry and pig  
use of antibiotics is very unmethodical and unscientific, production for disease prevention and treatment.  
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  
ACKNOWLEDGMENTS  
This study was financially supported by BTC (Belg ian  
the antibiotic used, in practice, only about 52% of the  
Technical Cooperation), the Belgian Un iversity Co mmission  
farmers surveyed were respecting the withdrawal t ime, from  
toward Development (CUD) and HUA. Thanks to all local  
which 60%, 40% and 27% were from farm household,  
veterinarians, Ir. Dong Bu i Quang - Researcher of Center for  
s emi-industrial and industrial system, respectively (Table 5).  
Interdisciplinary Research on Rural Development, Ngai  
Furthermore, anima ls in disease and therapy can be sold  
Pham Thi and Tuyen Tran Thi - Veterinary students of HUA  
quickly in order to save funds (this is the case in 40% of the  
for their co-operation to this study.  
farms investigated) or slaughtered and used for food, or feed  
for other animals. This creates both difficult ies for  
prophylaxis ofep idemic diseases and unsafety for consumers.  
In particular, these practices lead to a high risk of undesirable  
residues in anima l products[10]. Th is is one of the reasons  
why traces of residues of veterinary drugs in general, and  
antibiotics in particular, have been found in anima l products  
and also in the environment[52]. One study about the  
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