Determination of antibiotic consumption index for animal originated foods produced in animal husbandry in Iran, 2010
© Aalipour et al.; licensee BioMed Central Ltd. 2014
Received: 24 February 2013
Accepted: 22 December 2013
Published: 27 January 2014
The public health concerns over the long-term exposure to antibiotics have risen in different parts of the world. The purpose of this study was to investigate the antibiotic consumption pattern in livestock and poultry and to estimate the quantity of antibiotic active ingredient (mg) consumed per unit weight (Kg) of red meat, milk and egg production in Iran in 2010. A cross-sectional study was designed in charmahal - bakhtiary province-Iran. A questioner has been developed by naming 110 types of antibiotics. Twenty two veterinary clinicians and three livestock pharmaceutical distributor companies were included in the survey to determine the antibiotic prescription and distribution pattern in the farms. Veterinary organization of Iran supplied the information of the total antibiotic consumption in different dosage forms. National and international data on the livestock and poultry production were obtained from the relevant official web sites. Tetracycline class of antibiotics was the most common types of antibacterial prescribed and sold to both livestock and poultry farms. Amino glycoside, penicillin and macrolide in the cattle farms and furofenocole in broiler farms were the second most used groups of antibiotics. The quantity of antibiotic active ingredients consumed per unit weight of animal-originated food products was counted as 107.4 mg/kg for both milk and red meat and 249.5 mg/kg for broiler meat and egg. Totally, it was estimated that 133 mg antibiotic substances was used per kg of milk, meat and egg produced in 2010. In comparison to available data for other countries, consumption of antibiotics in livestock and poultry in Iran is higher than developed countries with an exception of South Korea. The findings of the present study could be alarming for the legislative authorities in food security and safety. More clear evaluation should be carried out as well as implementation of national monitoring and inspective programs in order to reach an added safety regarding animal-originated foods.
KeywordsAntibiotic Animal farm Food Exposure Iran
Antibiotics are the most important group of anti-microbial drugs, widely prescribed for human, and animals. It is estimated that 100–200 thousand tons of antibiotic substances are annually produced in the world[1, 2]. According to World Health Organization (WHO), about half of the worldwide-produced antibiotics are consumed for non-human applications. Veterinary use of antibiotics was partially specified for prophylactic and growth promotion purposes. Uncontrolled use of antibiotics in animals leaves some residues in meat, milk and egg, which could be harmful to humans. In other words, development of antibiotic resistant bacteria and allergic reactions in humans is known as the consequences of long term ingestion of antibiotics. European Union (EU), Food and Agriculture Organization (FAO) and Food and Drug Administration (FDA) have established certain regulations to monitor the antibiotic residues in foods of animal origins. For instance, in Euro zone, In order to reduce the human exposure to antibiotic residues, the consumption of any antibiotic is prohibited for growth promotion purposes. However, the evaluation of the exposure to antibiotic residues has always been controversial particularly, in the geographical regions where do not follow the restrictive regulations on the use of veterinary antibiotics. In this regard, many attempts have been made to determine the antibiotic residues in animal-originated foods[7–9].
Exposure evaluation may also been performed using a deterministic approach where, in a certain society, the weight ratio of the total consumed antibiotics to the produced animal-originated foods is defined as an antibiotic consumption index[10, 11]. For instance, the antibiotic consumption index was previously reported to be 26 and 100 mg/Kg in animal products in Australia and the United State of America, respectively[10, 12].
However, no study has been conducted to demonstrate the exposure to antibiotics through food consumption. Moreover, there is no recorded report on the diversity of antibiotics consumption in livestock and poultry farms in Iran.
The objectives of this study were to characterize the antibiotic utilization pattern in Iran livestock and poultry farms. In addition, the antibiotic consumption index concerning animal-originated food produced in the year of 2010 was also investigated.
Materials and method
This survey was a cross-sectional descriptive study conducted in the Charmahal- Bakhtiary province in Iran. This province is considered as one of the major livestock production regions in Iran. The study was designed in three parts as following: Firstly, the prescription rate of antibiotics for livestock and broiler farms surveyed through a face-to-face interview by veterinary clinicians. Secondly, the distribution pattern of the sold antibiotics in the tested area was determined by some interviews with animal pharmaceutical distributors. Finally, the antibiotic consumption index was calculated by using the data obtained from official veterinary and agriculture authorities in Iran.
Investigation of the prescription rate and the distribution pattern of different antibiotics
Two types of questionnaire were prepared in order to determine the prescription rate and distribution pattern of antibiotics, each contained 110 antibiotics in 10 major class including penicillins, tetracyclines, cephalosporins, macrolides, amino-glycosides, aminocyclitol, sulfonamides, nitrofourans, fluoroquinolones and fungicides, all are usable in veterinary practicing[17, 18]. The veterinary clinicians (n = 22) were asked to determine the prescription frequency of the given antibiotics in the questionnaire by scoring from one to five (zero = never, one = very low, two = low, three = moderate, four = high and five = very high). The distribution pattern of the sold antibiotics was determined using the information supplied by three main animal pharmaceutical distributer companies in the investigated area. They were asked to clearly determine the amount, type and the form of commercial antibiotics sold to livestock and poultry farms in 2010. Accredited veterinary references[17, 18] were used to determine the exact amounts of active ingredients, implemented in to the distributed commercial products. Volume percentage of each class of antibiotics being sold by interviewed companies was expressed as the consumption percentage.
Determination of antibiotic consumption index
Where E: The total amount of antibiotic active ingredient for each dosage form (kg), n: the number of each packaged antibiotic dosage form presented by the veterinary Organization of Iran C: the concentration of antibiotic active ingredient (%) for each type of antibiotic, included in each dosage form, V: the net weight or volume of the package (g or ml), N: the number of antibiotic types that were offered through the given dosage form and 10 3 is a conversion coefficient of g to kg.
Where E t is the total amount of antibiotic active ingredient consumed in Iran in 2010 (kg).
Information on the animal originated food production was obtained from the ministry of agriculture’s official website. Data on animal origin foods for other countries was derived from food and agriculture organization report.
Data analysis was performed using Microsoft Office Excel version 2003.
Selection of antibiotics based on their prescription rate by veterinary clinicians
Penicillin k, Na
The results of the questionnaires filled out by pharmaceutical distributor companies showed that 48 out of 110 questioned types of antibiotics have been frequently sold to the animal farms in 2010.
The total volume of antibiotics distributed in animal farms in Iran in 2010
Dosage form of antibiotic
aNumber of unite packaging
Mean weight of the packages (g)
Average concentration of the active ingredient (%)
Total active ingredient (kg)
Animal food production in Iran in 2010 ab
Fowl meat other than chicken
Livestock and poultry production data in different countries a
Using the official representative data, the overall production of meat, milk and egg in France, United state of America and Europe in 2007 was counted to be 2.2, 8.8 and 16.2 times more than that of Iran in 2010, respectively.
Total amount of utilized antibiotics and antibiotic consumption index in diferent countries
Weight of antibiotics utilized in the farms (Tons)
Antibiotic active ingredients consumed per one kg meat (mg/kg/year)
Antibiotic consumed per one kg of animal products (mg/kg/year)a
Studying the antibiotic consumption pattern in animals in the present work, revealed that tetracyclines had the highest rate of consumption in the investigated Iranian farms. Furthermore, oxytetracyclin was intensively prescribed for both livestock and poultry followed by gentamycin and tylosin in livestock and furofenocole and sulfodiazin in poultry.
Tetracyclines are broad-spectrum and the most commonly used antibiotics in many countries mainly for prophylactic and growth promotion purpose. It was reported that in Britain, tetracycline, sulfonamides and macrolids formed 90% of the total used livestock antibiotics by 61%, 19% and 9%, respectability, whilst the corresponding figure in South Korea was reported to be 45%, 15% and 4%, respectively. The findings of the present study on the antibiotic consumption index for some countries were in consistent with the previous reports[13, 15, 26]. It can be inferred that the lack of good husbandry practice (GHP) in livestock and poultry farms has led to a higher consumption of wide-spectrum antibiotic in Iran. As shown in Table 5, the antibiotic factor in Iran is lower than South Korea but more than other countries. Considering annual meat production, in Iran, antibiotic consumption factor is counted as 695 mg/kg, while in Australia, European and the USA it is reported to be 27,104 and 300 mg/kg, respectively. It means that antibiotic consumption factor in Iran is 25, 6.6 and 2.3 times more than that of Australia, Europe and the USA, respectively.
Exposure evaluation of a food contaminant is usually carried out by measuring the residues in food samples. When antibiotic residue in animal originated food comes in to consideration as a potential human hazard, it needs to perform a study in a very large size. In addition, elaborated laboratory techniques are required. Alternatively, estimation of per capita exposure to antibiotics using a representative national data is applicable. However, in Iran, official reports do not cover the antibiotics utilized in the animal husbandry. Therefore, in the presented study, such information was provided via correspondence from the veterinary organization. Determination of the type and the quantity of antibiotic consumption at the farm level is not mainly feasible due to farmers’ economic problems. Antibiotic consumption factor is considered as a general index for risk assessment of exposure to antibiotic residues. Based on the results of a study, 100 mg antibiotic substances is consumed in animal husbandry per unite weight (kg) of produced meat in Europe. Such data was reported to be 26 mg in Australia[10, 12].
In line with the results of present study, recent experimental studies in this country, carried out on the antibiotic residues in the food animals highlighted a high violation rate among the tested samples; in a couple of studies 14 to 24% of the raw milk samples were detected to be positive in terms of antibiotic residues[13, 14]. In addition, a market survey showed that up to 17.6% of the chickens specimens (liver, kidney and mussel) were contaminated with chloramphencol residues. In another study, 60 percent of the chiken meat samples were shown to have tetracyclin residue of which 10 percent exeeded the regulated limit (100 μg/kg). Also, conatamination of raw as well as processed bovin milk samples with the high levels of tertacyclin residues were observed in a few studies[16, 28, 29].
Based on the information presented in Table 2. in 2010, over 1806 tons of antibiotic active substances were consumed in livestock and poultry farms in Iran of which 66.4% was used in cattle farms. Considering the annual production of meat, milk and egg, the antibiotic consumption index was 133 mg/kg; Note that if meat annual production comes in to consideration, the antibiotic index will increase to 695 mg/kg.
It has been reported that annually thousands ton of antibiotics were used in the world. The United States of America with the annual consumption of 11148 tons is the highest consumer of livestock antibiotic worldwide. According to an official report, 78% of a total of 15890 ton antibiotic substances used in US was specified for non- therapeutic agricultural purpose. However, because of the higher animal production rate, the antibiotic consumption index seems to be less than that of Iran.
Previous studies have shown that a direct relation exists between the long-term antibiotic consumption in a society and the prevalence of antibiotic resistant bacteria[6, 11]. According to the results of the present study, for instance, antibiotic consumption factor in South Korea was counted as the highest (728.6 mg/kg) among the investigated countries. This may be associated with the high prevalence of antibiotic resistant strains, isolated from livestock in Korea. In addition, a high level of antibiotic consumption factor in Iran, reported in this study, might explain the development of antibiotic resistance among microbial strains isolated from animal-originated foods in several reports in Iran. In a study carried out in a western part of Iran, Escherichia coli and Streptococcus strains involved in mastitis infection were positive for antibiotic resistance; 52-84% of E. coli isolates and 13-20% of Streptococcus strains were found to be resistant to penicillin, oxy-tetracycline, streptomycin, erythromycin and colistin. Moreover, there is also substantial evidence on the existence of antibiotic resistant bacteria from human origin in Iran[34, 35]. This could be partly due to the long-term intake of antibiotic residues via animal products. Such issues may become more complicated in future if the national supervision and inspection are not implicated. Factors such as improvement of monitoring system on the distribution and consumption of livestock specified antibiotics in the community, implementation of Good Husbandry Practices (GHP) in the farms, progress in farmers educational programs can be helpful in this regards.
Focusing on the farms located in a specific geographical area could be regarded as a limitation in this study and it is necessary to perform a more comprehensive study in future. The heterogeneous nature of previous research works on the exposure assessment of antibiotics through foods in Iran makes it difficult to reach to a precise conclusion in the current situation of public exposure to antibiotics in Iran.
The present study shows that in Iran, antibiotic consumption in veterinary is noticeable and the consumption index is more than the developed countries. The qualitative pattern of antibiotic consumption in both cattle and poultry farms almost resembled that of other countries in which bacteriostatic antibiotics such as tetracycline has the highest share. However, their consumption found to be good among other countries. It seemed that the risk assessment of exposure to this class of antibiotics is an urgent need in Iran.
Authors would like to acknowledge Dr. Habibi, the manager of veterinary organization of Iran. In addition, managers of Aban, Yass Teb and MehrGoster Zagrous companies, and Dr. Soltani are deeply appreciated for their collaborations. In addition, the authors would like to thank the Food Security Research Center in the Isfahan University of Medical Science for financial support.
- Kümmerer K: Significance of antibiotics in the environment. J Antimicrob Chemother 2003, 52(1):5–7. 10.1093/jac/dkg293View ArticleGoogle Scholar
- Wise R: Antimicrobial resistance: priorities for action. J Antimicrob Chemother 2002, 49: 585–586. 10.1093/jac/49.4.585View ArticleGoogle Scholar
- World Health Organization (WHO): Use of antimicrobials outside human medicine and resultant antimicrobial resistance in humans. Geneva: World Health Organization; 2002.Google Scholar
- Nisha AR: Antibiotic residues - a global health hazard. Vet World 2012, 1: 375–377.Google Scholar
- Botsoglou NA, Fletuvris DJ: Drug residue in food: pharmacology, food safety, and analysis. Chapter 3 edition. New York: Basel: Marcel Dekker, Inc; 2001:112.Google Scholar
- Aarestrup FM, Wegener HC, Collignon P: Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti Infect Ther 2008, 6(5):733–750. 10.1586/14787220.127.116.113View ArticleGoogle Scholar
- Khaskheli M, Malik RS, Arain MA, Soomro AH, Arain HH: Detection of ß-lactam antibiotic residues in market milk. Pak J Nutr 2008, 7(5):682–685. 10.3923/pjn.2008.682.685View ArticleGoogle Scholar
- Oliveria RP, Jonas AR, Reyes FGR: Streptomycin and dehydrostreptomycin residues in bovine milk from the Brazillian retail market. Food Addit Contam 2010, B(3):156–162.View ArticleGoogle Scholar
- Maia PS, Ernani C, Rath S, Reyes FG: Residue content of oxytetracycline applied on tomatoes grown in open field and greenhouse. Food Control 2009, 20: 11–16. 10.1016/j.foodcont.2008.01.007View ArticleGoogle Scholar
- Sahoo KC, Tamhankar AJ, Johansson E, Lundborg CS: Antibiotic use, resistance development and environmental factors: a qualitative study among healthcare professionals in Orissa, India. BMC Public Health 2010, 10: 629. 10.1186/1471-2458-10-629View ArticleGoogle Scholar
- Aarestrup FM: Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol Toxicol 2005, 96(4):271–281. 10.1111/j.1742-7843.2005.pto960401.xView ArticleGoogle Scholar
- Kools SAE, Moltmann JF, Knacker T: Estimating the use of veterinary medicines in the European union. Regul Toxicol Pharmacol 2008, 50(1):59–65. 10.1016/j.yrtph.2007.06.003View ArticleGoogle Scholar
- Movassagh MH: Detection of antibiotics residues in cow raw milk in Bostanabad Region, Iran. Res Opin Anim Vet Sci 2012, 2(1):1–3.Google Scholar
- Movassagh MH: Study of antibiotics residues in Cow Raw milk by Copan milk test in parsabad region, Ardabil province, Iran. Annals Biol Res 2011, 2(4):355–359.Google Scholar
- Tajik H, Malekinejad H, Razavi-Rouhani SM, Pajouhi MR, Mahmoudi R, Haghnazari A: Chloramphenicol residues in chicken liver, kidney and muscle: a comparison among the antibacterial residues monitoring methods of four plate test, ELISA and HPLC. Food Chem Toxicol 2010, 48(8–9):2464–2468.View ArticleGoogle Scholar
- Aalipour F, Mirlohi M, Jalali M: Prevalence of contamination with antibiotic residues in commercial milk as affected by the season and different thermal processing. Int J Env Health Eng 2013, 2(1):41. 10.4103/2277-9183.122429View ArticleGoogle Scholar
- Najafzadeh VH: Antibiotics and antimicrobial drugs: (basic concepts and veterinary clinical indications. chapter 4 edition. Iran, Ahvaz: Tarava publication; 2007:51–59.Google Scholar
- Ghamarian AR: Compendium of data sheets for veterinary products. Iran, Tehran: Ghamarian publication; 2008.Google Scholar
- Ministry Agriculture Jahad (MAJ): Food consumption capital. Tehran-Iran: Ministry Agricalture Jahad; 2010. http://dla.agri-jahad.ir/portal/File/ShowFile.aspx?ID=b6197830–8391–42c8–9d61–4c32b911e281Google Scholar
- Food and Agriculture Organization (FAO): The state food and agriculture in world. Rome: Food and Agriculture Organization; 2009. http://www.fao.org/docrep/012/i0680e/i0680e00.htmGoogle Scholar
- Moulin G, Cavalie P, Pellanne I, Chevance A, Laval A, Millemann Y, Colin P, Chauvin C: A comparison of antimicrobial usage in human and veterinary medicine in France from 1999 to 2005. J Antimicrob Chemother 2008, 62(3):617–625. 10.1093/jac/dkn213View ArticleGoogle Scholar
- Beechinor JG: Report on consumption of veterinary antimicrobial drugs in Ireland in 2009. Ir Med J 2011, 104(4):1–3.Google Scholar
- Sarmah AK, Meyer MT, Boxall A: A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 2006, 65(5):725–759. 10.1016/j.chemosphere.2006.03.026View ArticleGoogle Scholar
- Kim KR, Owens G, Kwon SI, So KH, Lee DB, Ok YS: Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water Air Soil Pollut 2011, 214(1–4):163–174.View ArticleGoogle Scholar
- Ungemach FR, Müller-Bahrdt D, Abraham G: Guidelines for prudent use of antimicrobials and their implications on antibiotic usage in veterinary medicine. Int J Med Microbiol 2006, 296: 33–38.View ArticleGoogle Scholar
- Mohamadi SA, Nikpooyan H, Moshiri R: Aflatoxin M1 contamination and antibiotic residue in milk in Khorasan province, Iran. FoodChem Toxicol 2010, 48(8–9):2130–2132.View ArticleGoogle Scholar
- Ehsani EA: Measurement of tetracycline residue in consumed broiler meats in Ahvaz City by HPLC. Research 2010, 2(2):119–130.Google Scholar
- Hosseini M-J, Bakhtiarian A, Khavar RK, Pirali-Hamedani M, Ghazi-Khansari M, Amini M: Monitoring of oxytetracycline in bovine milk by high-performance liquid chromatography with UV-detector. Toxicol Lett 2006, 164(Supplement(0)):S279.View ArticleGoogle Scholar
- Aalipour F MSc thesis. In Risk Assessment of Tetracycline residues in the marketed pasteurized and sterilized milk in Iran. : Isfahan University of Medical Science, School of Nutrition and Food Science, Departmet of Food Technology; 2013.Google Scholar
- Shea KM: Antibiotic resistance: what is the impact of agricultural uses of antibiotics on children’s health. Pediatrics 2003, 112(1):253–258.Google Scholar
- Sung Y, Lee JK, Lee KH, Lee KT, Kang CI: The clinical epidemiology and outcomes of bacteremic biliary tract infections caused by antimicrobial-resistant pathogens. Am J Gastroenterol 2012, 107(3):473–483. 10.1038/ajg.2011.387View ArticleGoogle Scholar
- Taremi M, Mehdi SDM, Gachkar L, MoezArdalan S, Zolfagharian K, Reza ZM: Prevalence and antimicrobial resistance of campylobacter isolated from retail raw chicken and beef meat Tehran, Iran. Int J Food Microbiol 2006, 108(3):401–403.Google Scholar
- Ebrahimi A, Kheirabadi KH, Nikookhah F: Antimicrobial susceptibility of environmental bovine mastitis pathogens in west central Iran. Pak J Biol Sci 2007, 1(10(17)):3014–3016.Google Scholar
- Firoozeh F, Shahcheraghi F, Salehi TZ, Karimi V, Aslani MM: Antimicrobial resistance profile and presence of class I integrongs among salmonella enterica serovars isolated from human clinical specimens in Tehran, Iran. Iran J Microbiol 2011, 3(3):112–117.Google Scholar
- Ghorashi Z, Ghorashi S, Soltani-Ahari H, Nezami N: Demographic features and antibiotic resistance among children hospitalized for urinary tract infection in northwest Iran. Infect Drug Resist 2011, 4: 171–176.Google Scholar
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