International Journal of Food Properties

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Antimicrobial drug residues in poultry products

and implications on public health: A review

Muhammad Danish Mund, Umair Hassan Khan, Uruj Tahir, Bahar-E- Mustafa
& Asad Fayyaz

To cite this article: Muhammad Danish Mund, Umair Hassan Khan, Uruj Tahir, Bahar-E-
Mustafa & Asad Fayyaz (2017) Antimicrobial drug residues in poultry products and implications
on public health: A review, International Journal of Food Properties, 20:7, 1433-1446, DOI:
10.1080/10942912.2016.1212874

To link to this article: https://doi.org/10.1080/10942912.2016.1212874

Published online: 17 Nov 2016.

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INTERNATIONAL JOURNAL OF FOOD PROPERTIES
2017, VOL. 20, NO. 7, 1433–1446
http://dx.doi.org/10.1080/10942912.2016.1212874

Antimicrobial drug residues in poultry products and implications

on public health: A review
Muhammad Danish Munda, Umair Hassan Khanb, Uruj Tahir c
, Bahar-E- Mustafab,
and Asad Fayyazd
a
Department of Poultry Sciences, University of Agriculture Faisalabad, Sub-Campus Toba Tek, Singh, Pakistan;
b
Department of Microbiology, University of Agriculture Faisalabad, Sub-Campus Toba Tek, Singh, Pakistan;
c
Department of Environmental Sciences, Fatima Jinnah Women University, Rawalpindi, Pakistan; dDepartment of
Physiology, University of Agriculture Faisalabad, Pakistan

ABSTRACT ARTICLE HISTORY

Poultry meat and eggs are important foods for fulfilling the dietary needs of the Received 20 January 2016
ever-growing human population. Efficient poultry production, however, neces- Accepted 11 July 2016
sitates use of pharmaceutical products, such as antibiotics, as prophylactic and
KEYWORDS
curatives to ensure rapid growth and health. Nevertheless, inappropriate and Poultry industry; Drug
non-judicious use of these drugs results in an accumulation of toxic and harmful residues; Human health;
residues in meat and eggs of treated birds which affect consumer health by Allergic reactions;
triggering allergic reactions and transmitting antibiotic-resistant microbial infec- Immuno-pathological
tions. Therefore, regulatory authorities must take rigorous steps to curtail inap- effects; Microflora
propriate use of numerous drugs for animal use in order to provide safe animal modifications
origin food to humans.

Introduction
Over the past few decades poultry has gone through tremendous growth; however, with the increase
in production, the use of certain drugs and feed additives has become crucial in order to prevent
diseases, their treatment, and growth promotion.[1–4] However, one of the drawbacks of excessive use
of antimicrobial drugs is that they get accumulated in the tissues and organs of treated animals as
residues and eventually become part of the food pyramid,[1–3,6] hence excessive usage has been
recognized as illegal and prohibited by the food regulatory and health authorities.[1,3–5] This article
elucidates the use of various antimicrobial agents in the poultry industry, their distribution and
accumulation in various body parts and tissues and their subsequent effects on human health.

Medicinal drugs and antimicrobial agents used in poultry industry

Modern approaches applied for efficient chicken production have resulted in wide-spread disease
havocs across the world. For instance, intensive rearing conditions with high stock densities in
poultry houses have provided ideal conditions for manifestation and transmission of parasitic and
viral diseases. In addition to that, due to poor condition management, the disease incidences are not
only becoming more frequent, pronounced, and unmanageable, but also difficult to control in the
long run.[8] The most prevalent diseases are typhoid, mycotoxicosis, E. coli infections, coccidiosis,
Salmonellosis, enteritis, ascites, Newcastle disease, Marek’s disease, hydropericardium syndrome, and
Gumboro disease.[8–10] These diseases are not only influencing poultry growth and production, but
are also contributing considerably to the economic losses due to a high mortality among the

CONTACT Uruj Tahir [email protected] Department of Environmental Sciences, Fatima Jinnah Women
University, The Mall Road, near Kachehri Chowk, Rawalpindi 46000, Pakistan.
© 2017 Taylor & Francis Group, LLC
1434 M. D. MUND ET AL.

flocks.[10,11] Additionally, high disease loads call for heavy uses of veterinary medicines, antiparasitic,
or antibiotic drugs in order to prevent and treat microbial infestation.[10,12]

Antibiotics for therapeutic and prophylactic purposes

Antibiotics are naturally occurring, semi-synthetic, or synthetic compounds with antimicrobial activity
and are most widely used drugs in the poultry industry. They are administered parenterally or intrave-
nously, topically, and orally.[13,14] Antibiotic drugs are typically used to serve three purposes in poultry,
(1) therapeutic use where animals (either individually or in small groups) are administered with high
doses of antibiotics for relatively shorter periods, (2) prophylactic use that involves exposure of animals
with moderate doses of antimicrobials for longer time durations, and (3) growth promotion where
antibiotics in subtherapeutic doses, for example, 10 or 100 times less than therapeutic doses are given for
a very long duration or throughout the entire lifespan of the animals.[12,15] The antibiotics are known to
inhibit (1) DNA replication, (2) Ribo-nucleic acid (RNA) and protein synthesis, (3) cell division,
differentiation and development, (4) target folic acid metabolism, or (5) disrupt cell membrane and
cell wall synthesis of microorganisms responsible for dissemination of infections.[16,17]
In developing countries, the use of antibiotics is quite common. The most commonly used
antibiotics are: tetracycline,[19] gentamicin,[20] neomycin, tylosine, erythromycin,[21] virginiamycin,
ceftiofur, and bacitracin which are usually helpful in the reduction and prevention of respiratory
diseases and necrotic enteritis infections; flouroquinolones and/or quinolone compounds are used
for treating gastroenteritis, skin, or soft tissue infections;[23,24] sulfonamide compounds are adminis-
tered as preventive and chemotherapeutic agents against coccidiosis, fowl typhoid, coryza, and
pullorun disease;[24,26] while, piperazine, oxytetracycline, amoxicillin, amprolium, ciprofloxacillin,
and sulfa drugs are used to treat coccidiosis.[27]
Likewise, many anticoccidial drugs (narasin, salinomycin, sulphonamides, clopidol, amprolium,
nicarbazin, etc.) and vaccines (derived from non-attenuated or attenuated oocysts of coccidia strains)
are widely utilized as antidotes in poultry feed to prevent and treat coccidiosis.[10,39] Coccidiosis, a
parasitic disease caused by several Eimeria species, is known to inhibit the growth and progression of the
poultry industry. The disease manifests itself in intestinal epithelial tissues and inflicts birds with diarrhea
(feces with blood), reduction in weight gain, decreased production of eggs, and feed conversion rates,
thereby causing higher morbidities and mortalities.[8,11,40] Some of these drugs are employed in combi-
nations for effective poultry production such as, narasin and nicarbazin.[10] However, extensive admin-
istration of coccidiostats in hens reared for egg-laying purposes without any knowledge of withdrawal
periods, results in deposition of residues within edible tissues and products from animals (such as eggs)
in different concentrations and negatively influence human health.[8,41] The majority of antibiotics are
administered either through feed or in drinking water.[13] Some of the antimicrobial agents used in
poultry along with their derivatives, mode of actions and their withdrawal period is given in Tables 1
and 2.

Antibiotics for growth promotion

The use of antimicrobial agents for growth promotion purposes in farm animals was prescribed in the
mid-1950s. Since then tetracycline, chloramphenicol, and procaine penicillin (subtherapeutic doses)
supplemented feeds were extensively employed in the poultry industry to promote growth and egg
production.[12,42] Virginiamycin, avoparcin, tylosin, and numerous ionophores have also been reported
to be used as growth promoters.[12,15,17] In addition to antibiotics, due to role of hormones in better
growth and improvement in feed efficiencies, food producing animals are also administered with natural
and synthetic hormones in developing countries. For instance, applications of oestradiol (female sex
hormone) in castration of young birds, either subcutaneously or as feed additives, in the past has been
reported by some authors.[44] As a matter of fact, the mechanisms by which antibiotics promote growth
are not yet defined; however, studies have indicated that antibiotics may stimulate growth by their
 INTERNATIONAL JOURNAL OF FOOD PROPERTIES 1435

Table 1. Commonly applied antibiotics in poultry industry.

Antibiotics Derivatives Mechanism References
Βeta-Lactams Amoxicillin (aminopinicillin), penicillin, Bactericidal (prevents bacterial cell synthesis, [22,28]
cephalosporin, ampicillin, monobactam, disrupts cell wall integrity, inhibit
carbapenem transpeptidase)
Tetramisole Levamisole Effective against lungworms and [29,30]
gastrointestinal nematodes, mimics thymic
hormone thymopoietin which affects many
components of immune system
Quinolones/ Oxolinic acid, nalidixic acid, flumequine, Arrest bacterial cell growth via inhibiting DNA [23,24,31]
Fluoroquinolones enrofloxacin, norfloxacin, ciprofloxacin gyrases involved in DNA replication,
recombination and repairing
Tetracyclines Chlortetracycline, tigecycline, minocycline, Bacteriostatic and bactericidal, inhibit protein [19,32]
oxytetracycline, chelocardine synthesis
Sulfonamides Sulfacetamide, sulfamethoxypyridiazine, Act as competitive antagonists in microbial [26,32]
sulfamethoxydiazine, sulfamethoxazole, cells, block formation of folic acid
sulfadimidine, suflamethoxine, sulfadiazine,
sulfafurazole,
Aminocyclitol Spectinomycin, apramycin Bacteriostatic and bacteriocidal, irreversible [32,33]
inhibition of protein synthesis
Amphenicols Chloramphenicol, thiamphenicol, florfenicol Inhibit protein synthesis [1,32]
Coccidiostats Salinomycin, diclazuril, robenidine, Disrupt ion gradients across parasite cell [10,34]
naduramicin, lasalocid, toltrazuril, membrane, inhibit parasite mitochondrial
halfoginone, nicarbazin, narasin, monensin, respiration, folic acid pathway, competitive
clopidol, ionophores, amprolium inhibition of thiamine uptake
Macrolide Erythromycin, tylosin, spiramycin Act on 50S ribosomal subunit and inhibit [1,32]
protein synthesis
Nitrofurans Furazolidone, furaltadone, nitrofurantoin, Bacteriostatic or bacteriocidal (at high doses) [1,35]
nitrofurazone
Aminoglycosides Neomycin, canamycin, gentamycin, Irreversible inhibition of protein synthesis [32,36]
netilmycin

Table 2. Recommended withdrawal periods for some of the antimicrobial substances used in poultry industry.
Feed withdrawal
Antimicrobial substances period (days) Legislating authority References
Levamisole 7 Australia [30]
Nicarbazin Narasin 5 European Commission [37]
Ciprofloxacin 15–19 European Health Law and National [38]
Office of Animal Health, UK
Lasalocid Salinomycin Narasin Maduramicin 5 Finnish National Feed Control [2]
Semduramicin Programme
Monensin 3 Finnish National Feed Control [2]
Programme
Oxytetracycline Sulphadimidine 5 Saudi Arabia [21]
Ampicillin 6 Saudi Arabia [21]

antimicrobial activities against pathogens and harmful bacteria. It has been speculated that antimicrobial
agents may protect nutrients against bacterial destruction by reducing growth of intestinal bacteria,
facilitate improved nutrient absorption by thinning of intestinal barriers, minimizing toxins production
by intestinal bacteria, and lowering subclinical (intestinal) disease incidences.[43]
For years, the use of antibiotics and/or antimicrobials was seen as hallmark and allowed to be
used without any restrictions, regulations, and supervision in various commercial poultry enter-
prises. However, the negative effects of these growth promotants remained undetected until acquisi-
tion of resistance against antimicrobials. The concerns about therapeutic and growth promotion
deployments of antimicrobials aroused mainly due to emergence of increased number of resistant
bacteria.[12,43] The extensive use of antibiotics and growth hormones, however, has been banned in
developed countries, but the situation is quiet contrary in developing or underdeveloped countries
1436 M. D. MUND ET AL.

Table 3. Permitted MRLs for various anticoccidial drugs in poultry products.

MRL
Antimicriobial agents Derivatives (µg Kg−1) Poultry item Legislating authority References
Anticoccidials Monensin 2 Eggs European union [34,46]
Narasin 2 Eggs
Nicarbazin 100 Eggs
Diclazuril 2 Eggs
Semduramicin 2 Eggs
Maduramicin 2 Eggs
Robenidine 25 Eggs
Decoquinate 20 Eggs
Halofuginone 6 Eggs
Toltrazuril 600 Liver
400 Kidney
100 Muscle
200 Skin, fat
Lasalocids 150 Eggs
100 Liver, skin, fat
50 Kidney
20 Muscle

due to inadequate safety standards and regulations or in some cases these standards or regulations
do not even exist.[13]
Despite prohibition, many broiler chickens and layers (egg-laying hens) are administered with
overdoses or inappropriate doses of antibiotic drugs for therapeutic, prophylactic, as well as non-
therapeutic purposes throughout their entire lifespan.[2,42] If these drugs are not absorbed, or if
they are metabolized by the animal, it would be harmless to products, not being problematic.
Unfortunately, that is not what always happens. Hence, unsafe drug residues tend to accumulate
in various concentrations in the edible parts of treated animals.[3] These residues are primarily
comprised of parent and derivative compounds (or both) including metabolites, conjugates, and
remnants bound with macromolecules.[21,45] Ingestion of tissues and organs (meat, offals, eggs,
etc.) containing drug remnants above safe maximum residual levels (MRLs), given in Tables 3
and 4, is associated with numerous health hazards and vulnerabilities (1) directly as initiation of
hypersensitive or allergic reactions, cutaneous eruptions, dermatitis, alteration of intestinal
microflora etc., (2) indirectly as carcinogens, teratogens, development of antibiotic resistances
among microbial strains, and (3) often leads to drug toxicity.[1,3,7,21,50,51]

Presence and distribution of drug residues in poultry products

Since traditional backyard and intensive poultry farming is a common practice in many devel-
oping countries, and farmers have easy access to veterinary drugs and the use of medicines, the
use in indiscriminate and inappropriate higher doses of antimicrobial drugs is common, which
eventually accumulates harmful residues in edible tissues of the poultry.[1,42,52,53] The other cases
where poultry can have harmful residues in their meat and egg products are (1) unintentional or
accidentally cross-contaminated feed in feed mills, (2) recirculation through litter, and (3)
administration of feed ingredients or water contaminated with metals, pesticides, or toxic
chemicals, etc.[13,42] All these residues produce potential threats of direct toxicity in humans
and alteration of micro-flora with possible development of resistant strains due to low and
continuous exposure to antibiotics, thus causing failure of antibiotic therapies.[51]

Drug residues in egg matrix

Since eggs are consumed by almost every individual, the deposition of drug residues in various egg
components is of considerable concern. Upon administration, antibiotics get absorbed into the
Table 4. Permitted MRLs for various drugs in poultry products.
MRL (µg
Antimicriobial agents Derivatives Kg−1) Poultry item Legislating authorities References
Sulfonamides — 100 Tissues, eggs Council Regulation (EEC), Codex Alimentarius, FAO/WHO and Code of Federal [25]
Regulations
Sulfadiazine 100 Eggs Codex Alimentarius Commission [47]
Chloramphenicol 0 Liver, European Union (EU) [48]
muscles
Beta-Lactams Benzylpenicillin (penicillin 50 Kidney, liver FAO/WHO [49]
G)
Quinolones/ Ciprofloxacin + 200 Liver [36]
flouroquinolones enrofloxacin 100 Muscles European Union
300 Kidneys
Flumequine 50 Skin, fat [31]
Aminoglycosides Neomycin 500 Muscles, liver European Union, Health Canada Veterinary Drugs Directorate, Australia [36]
5000 Kidney European Union
10000 Health Canada Veterinary Drugs Directorate, Australia
Gentamicin 100–400 Eggs USA [45]
100 Holland
200 Germany
100–200 France
Tetracyclines Chlortetracycline 100 Muscles/ European Union, Australia [36,48]
200 meat Health Canada Veterinary Drugs Directorate
2000 United States Food and Drug Administration (USFDA)
300 Liver European Union
600 Health Canada Veterinary Drugs Directorate
6000 United States Food and Drug Administration
100 Kidney European Union
1200 Health Canada Veterinary Drugs Directorate
Oxytetracycline 100 Muscles/ European Union, Australia
200 meat Health Canada Veterinary Drugs Directorate
2000 United States Food and Drug Administration
100–300 Liver European Union
6000 United States Food and Drug Administration
600 Health Canada Veterinary Drugs Directorate
1200 Kidney Health Canada Veterinary Drugs Directorate
Doxycycline 300 Liver European Union
INTERNATIONAL JOURNAL OF FOOD PROPERTIES

100 Muscles
600 Kidney
Sipromycin 200 Meat Codex Alimentarius Commission [74]
1437
1438 M. D. MUND ET AL.

intestines of chicken and are transported through the whole body via blood plasma where it reaches
the ovaries (follicles and oviducts) responsible for formation and secretion of egg contents, thus
upsurges the risks of deposition of drug residues in the yolk and albumen.[28,55] Drugs have been
reported to deposit more rapidly in both yolk and albumen.[1,45,56] However, the distribution and
deposition pattern of residues varies depending upon the composition, physiochemical properties of
antimicrobial agents, physiology of hen, egg formation, and nature of egg compartments.[57,58]
Studies have provided evidence of contamination of poultry eggs with various concentrations of
drug residues. For example, the deposition of nitrofuran residues (3-amino-2-oxazolidone)
employed for treating salmonellosis and other bacterial infections, in eggs has been confirmed by
Al-Ghamdi et al.[59] and Amiri et al.[60] The eggs were found to be contaminated with 268.25 ng kg−1
of amino-2-oxazolidone metabolite and indicated extensive use of furazolidone drugs.[60] Similarly,
contamination of eggs with 103–230 ng g−1 of sulfonamide residues (sulfadiazine) exceeding MRLs
has also been reported by Mehtabuddin et al.[25] Moreover, deposition of various drug residues
including amprolium, furaltadone, furaprol (nitrofuran-amprolium combination), oxytetracycline,
soluvite (vitamins and minerals supplement), tylosin, streptomycin, and sulfaquinoxaline within eggs
has also been ascertained by Kabir et al.[42] Likewise, deposits of dinitrocarbanilide in egg samples
have indicated prevalence of nicarbazin residues.[61]
Additionally, the transmission of administered amoxicillin from egg-laying hens to the eggs and
its accumulation in the yolk as well as the egg white has been ascertained by Khattab et al.[28] Even
storage at room temperature, refrigeration (4°C) and boiling for 10 mins was not found helpful in
minimizing the effect of these residues.[28] Similarly, the administration of gentamycin in different
doses either subcutaneously or intramuscularly showed variations in the deposition of residues
between egg whites and yolks even after the cessation of drug dosing. These residues accumulated
in significantly higher concentrations (90%) within the yolk in contrast to the albumen.[45,56] On the
other hand, high levels of chlortetracycline and sulfanilamide residues (above MRLs) in egg whites as
compared to yolks have also been predicted.[57] Hence, it is evident that drug residues (exceeding
MRL values) get deposited within various egg compartments and the consumption of such con-
taminated eggs can cause serious consumer health hazards.

Drug residues in meat

Poultry meat offers a better substitution for mutton and beef based on nutritional specifications and
affordability. But uncontrolled drug usage and lack of proper biosafety measures for their withdrawal
has resulted in a decreased quality of meat.[25] For instance, the deposition of significantly higher
concentrations of various antibiotic residues in edible tissues of chickens receiving therapeutic, or
prophylactic without observance of recommended withdrawal times have been demonstrated by
Kabir et al.[42] and Hind et al.[62] Likewise, the accumulation of oxytetracycline (88.217 ng g−1)
enorfloxacin (18.32 ng g−1),[61–64] quinolones (30.81 μg kg−1),[65] chloramphenicol (0.021 and 0.008
µg kg−1,[66] and 89.33–223.05 µg kg−1),[48] and oxytetracycline (670–1816 µg kg−1)[48] residues also
been reported leaving residues in chicken meat. In addition to this, considerably higher concentra-
tions of enrofloxacin (due to lipophilic nature) in the broilers’ meat have also been reported by
Amjad et al.[31] Sattar et al.[67] also reported the deposition of ciprofloxacin (34%), enorfloxacin
(22%), and tetracycline (20%) residues in meat along with amoxicillin (26%) in thigh muscles,
ciprofloxacin (30%), tetracycline (24%), amoxicillin (22%), and enorfloxacin (18%) residues in breast
muscles of egg-layers and broilers. Furthermore, Karmi[68] also confirmed the presence of amino-
glycoside, tetracycline, quinolone, and sulfonamide residues in fresh, local frozen, and imported
frozen samples from chickens (breast and thighs) sold for human consumption, while the contam-
ination of poultry meat samples with β-lactam and/or tetracycline (75.81%), macrolide and/or β-
lactam (44.35%), sulfonamide (36.29%), and aminoglycoside (13.71%) residues has also been con-
firmed by Hakem et al.[69] Similarly, widespread misuse of antimicrobial agents due to non-
 INTERNATIONAL JOURNAL OF FOOD PROPERTIES 1439

compliance of withdrawal periods also has revealed detectable levels of oxytetracycline residues in
chicken fillets.[70]

Drug residues in offals

Various researchers have investigated the presence of drug residues in treated animals’ edible tissues
and/or offals including heart, liver, kidneys, and gizzard through different techniques.[31,60,71–76]
Studies have conferred the prevalence of higher concentrations of levamisole residues in liver of
broiler chickens as compared to other body tissues, including thigh muscles, due to the lipid-soluble
nature of the drug.[30] Moreover, the deposition of oxytetracycline and chloramphenicol residues in
substantially higher amounts within the liver and kidney samples of broilers confirmed by
Salehzadeh et al.[63] and Shahid et al.[71] indicated non-compliance of established MRLs. Similarly,
higher concentrations of ciprofloxacin and enorfloxacin residues in livers and kidneys of broiler
chickens along with relatively lower concentrations of flumequine have also been detected.[31] The
contamination of liver and kidney samples with enrofloxacin and chloramphenicol residues exceed-
ing MRL values has been reported, respectively, by Salehzadeh et al.[64] and Mehdizadeh et al.[72]
Correspondingly, highest concentrations of tetracycline (48%), ciprofloxacin (44%), amoxicillin
(42%), and enorfloxacin (40%) residues have been found in boilers and egg-layers livers, whereas
kidneys contained 24, 42, 30, and 34% residue of the respective antibiotic substances.[67]
Furthermore, the occurrence of high levels of nicarbazin residues (dinitrocarbanilide) in boilers’
livers has been reported.[37,61]
Sipramycin isolated from Streptomyces ambofaciens is a macrolid antibiotic and is used as a
growth promoter in poultry. Amro et al.[75] examined the presence of residual sipramycin in treated
chicken tissues. Their results revealed the contamination of liver, thigh, and gizzard samples with
sipramycin residues. However, the highest concentration of residues were observed in liver (40%)
and with lowest found in gizzard and muscle (10%) samples. Another study reported the contam-
ination of chicken giblets with amoxicillin and sulphaquinoxaline residues. The study reported that
out of 90 samples of heart, liver, and gizzard (30 each) examined, were around 3.33, 13.33, and 10%
heart, liver, and gizzard samples were containing higher levels of amoxicillin residues, whereas only
10 and 13.33% of gizzard and liver samples were found to be contaminated with higher concentra-
tions of sulphaquinoxaline residues (exceeding MRLs).[76] Similarly, a study conducted by Morshdy
et al.[74] showed the incidence of liver and gizzard samples contaminated with tilmicos. Abiola
et al.[77] also have reported the contamination of gizzard samples with nitrofuran (41%), tetracycline
(14%), sulfamids (8%), and chloramphenicol (5%) residues collected from market and poultry farms.
A study conducted by Barbosa et al.[78] concerning the accumulation and distribution of furaltadone,
nifursol, and their metabolites (3,5-dinitrosalicylic acid hydrazine [DNSAH] and 3-amino-5-mor-
pholinomethyl-2-oxazolidinone [AMOZ]) in liver and gizzard samples ascertained the prevalence of
furaltadone and nifursol residues in animals medicated for 5 weeks without observing withdrawal
periods. However, the analysis of treated birds after 3 weeks along with observed withdrawal periods
showed no accumulation of furaltadone and nifursol residues, but ascertained a quick conversion of
these compounds into respective metabolites (AMOZ and DNSAH) which persisted for longer
durations as compared to parent compounds. The AMOZ concentrations in liver and gizzard
samples were estimated as 80 and 331 µg kg−1, while for liver and gizzard observed DNSAH
concentrations were 6.4 and 10.3 µg kg−1, respectively.[78]

Human health risks associated with drug residues

The veterinary drug residues in poultry products can potentially be transmitted to humans via
consumption of contaminated edible tissues and may lead to several pathological implications that
are considered as major health issues. Chicken meat contaminated with drug residues may pose
serious public health hazards in the form of antibiotic resistant bacterial formation, allergic
1440 M. D. MUND ET AL.

manifestations, or alteration of useful microflora of digestive tract to no microflora and/or harmful

or non-healthy microflora.[79] For instance, residual β-lactams, including cephalosporin and peni-
cillin, have been reported to cause dermatitis, cutaneous eruptions, anaphylaxis, and gastro-intestinal
symptoms in humans via ingestion of contaminated poultry products.[80] Penicillin residues are
considered as the most problematic because of the vulnerability of a large proportion of people,
many are allergic.[81] Moreover, penicillin residues in poultry can lead to severe anaphylactic
reactions while eggs containing residues of sulfonamides in higher concentrations cause skin
allergies upon consumption.[42,82]
The residual levels of tetracycline in a diet intended for human consumption have been reported
to lead to poor development of fetuses, staining of teeth in young children, gastrointestinal disorders,
and pro-inflammatory, cytotoxic, and immuno-pathological effects.[13,82,83] Similarly, residual
amounts of tilmicosin affect hematological (white blood cell [WBC], red blood cell [RBC]) and
biochemical parameters such as total protein, albumen, cholesterol, and triglyceride concentrations.-
[84]
Likewise, the persistence of sulphamethazine, oxytetracycline, and furazolidone residues in
humans is known to pose immuno-pathological effects (such as autoimmunity, carcinogenicity),
while that of gentamicin and chloramphenicol may be mutagenic, nephropathic, and hepatotoxicor
they may lead to reproductive abnormalities or bone marrow toxicity.[51]
Similarly, intake of nitrofuran metabolites as residues via poultry products may produce toxic,
mutagenic, or carcinogenic side effects and may transmit antibiotic resistance among human
microflora, hence the application of nitrofurans in poultry has been banned.[60] While some drug
residues such as nitroimidazole and 3-nitrofuran cause different cancers in humans.[85–88]
Continuous doses of ciprofloxacin residues to humans is also known to cause toxicity, impede
cytochrome (CYP1A2) mediated metabolism, and can result in increased concentration of drug in
systemic circulation due to reduced renal clearance.[38] Moreover, the consumption of drug residues
via chicken products may result in the production and proliferation of drug-resistant bacteria in
human beings, which could lead to therapeutic failures among such infected individuals.[51,68]

Risks of Dissemination of antimicrobial resistant microbes in humans

Though the applications of antimicrobial agents in poultry feed has lowered disease incidences, but their
prolonged and intensive uses in low doses as growth enhancers has resulted in stimulation and
emergence of antimicrobial resistant strains. For example, the emergence of resistance in Salmonella
and Campylobacter species against fluoro-quinolones and third-generation cephalosporin’s (used to
treat human diseases) has been reported by Anderson et al.[88] Similarly, S. intermedius strains (221),
isolated from the canine family, exhibited different rates of resistance to cephalotin, mupirocin,
ciprofloxacin, clindamycin, gentamicin, chloramphenicol, and amoxicillin/clavulanic acid, which
could lead to difficulties in effective treatment in human diseases. [89] Moreover, there are several
reports on the prevalence of antimicrobial resistant bacteria within on-farm broiler chickens. Around
525 avian E. coli strains isolated from broiler have been reported to be resistant to various antimicrobial
agents including trimethoprim-sulfamethoxazole and ciprofloxacin. Additionally, the prevalence rate of
resistant E.coli to ciprofloxacin and erythromycin in broiler with colibacillosis was reported to be
significantly higher as compared to that of controls.[90]Avian E. coli strains (468) isolated by Blanco
and co-workers[91] displayed significantly higher resistance levels to trimethoprim-sulfamethoxazole
and fluoroquinolones, moreover, these antimicrobials were suggested to lead to cross-resistance in
human enteric pathogens. A total of 293 strains isolated from chicken farms and slaughter houses,
characterized as S. enterica Indiana, were found to be resistant to norfloxacin, enrofloxacin, and
ciprofloxacin, moreover, gene mutations were also detected in these strains.[92] Similarly E. tenella,
isolated from poultry fields, also exhibited a development of resistance against salinomycin.[93] These
researches suggest that uninterrupted and indiscriminate employment of these antimicrobial agents is
increasing the dissemination of resistance against multiple drugs in foodborne-bacteria and/or human
pathogens[94] and is leading to loss of effectiveness of antibiotics against poultry and human ailments.
 INTERNATIONAL JOURNAL OF FOOD PROPERTIES 1441

C. jejuni, Salmonella sp., and Verotoxigenic Escherichia coli have been recognized as major emerging
foodborne pathogens among human beings.[97] Luber et al.[98] and Chuma et al.[99] have ascertained
contamination of poultry meat available in supermarkets with antimicrobial resistant C. jejuni, which
upon consumption may lead to compylobacteriosis. C. jejuni strains isolated from poultry samples were
found to be resistant to multiple antibiotics including ampicillin, cephalothin, sulfamethoxizole
+trimethoprim.[100] Moreover, exhibition of resistance against ampicillin following ciprofloxacin, tetra-
cycline, erythromycin, and gentamicin by Campylobacter strains (C. coli and C. jejuni) isolated from
fresh chicken meat has also been documented by Sison.[101] This reflects emergence of resistance to
multiple antibiotics through misuse or overuse of antibiotics. Similarly, C. jejuni, S. enterica, serotype
Enteritidis, L. monocytogenes, and E. coli from chicken carcasses showed higher resistance percentages
against multiple drugs including tetracycline, sulfonamides, and quinolones.[102] Idrees et al.[103] and
Nsofor et al.[104] ascertained the presence of multi-drug resistant E. coli in chickens; being commensal,
these can lead to serious public health issues. Ali et al.[105] reported the prevalence of high-level
vancomycin, kanamycin, clarithromycin, ampicillin, gentamicin, and erythromycin resistant non-enter-
ococci and enterococci in poultry feed, water, litter/manure, and air. Additionally, the occurrence of
streptomycin-, ampicillin-, kanamycin-, neomycin-, tetracycline-, erythromycin-, cefotaxime-, novo-
biocin-, nalidixic acid-, bacitracin-, and spectinomycin-resistant Salmonella serovars in chicken meat
has been confirmed by Shah and Korejo[106] and indicated that these multiple drug resistance isolates
may cause human infections upon consumption of contaminated meat. Several strains of E. coli isolated
from poultry carcass have shown resistance to extended-spectrum β-lactamase. These strains are of
main concern due to their potential transferability to humans via the consumption of meat.[107]
Numerous detailed evidences of linkage between extended animal in-feed antimicrobials applications
and escalation in transmission of drug-resistant microbial infections among humans have been cited by
Marshell and Levy.[12] Hence, there must be strict legislation for determination of safer drug levels and
withdrawal times (to reduce prolonged use of drugs) and implementation for following drug withdrawal
periods for safe consumer consumption by health authorities.[84]
Although significant reductions in mortality have occurred due to bacterial infection by the use of
antibiotics, some diseases are on the rise because of continuous acquisition of resistance against all
available antibiotics.[5,95] Acquisition of multi-drug resistance is now becoming a widespread issue
and is of major concern among poultry veterinarians and food microbiologists due to their severe
implications on public health. Studies have described that there exists a linkage between applications
of antimicrobials in poultry and subsequent transmission of resistant genes in human pathogens.
This may be because of the fact that numerous human and animal pathogens treated with identical
or related classes of antibiotics are developing diverse resistance mechanisms and ultimately sharing
and spreading them within other microbial populations.[15,17] The mechanisms of acquisition of
resistance against antibiotics and dissemination of these resistant genes among other microorgan-
isms have been described in detail by Poole and Sheffield.[96]

Conclusion
The deposition and subsequent detection of residual amounts of these antimicrobial substances
exceeding MRLs in poultry products is really a matter of concern. Furthermore, emergence and co-
occurrence of resistance to various and/or multiple antibiotics in commensal, pathogenic, and
mutualistic microbes is also threatening human health. Therefore, strict legislations and control
measures at national and local levels should be established for production, sale, and use of veterinary
drugs in treatment or as feed supplements. Additionally, the recommended withdrawal periods
between administration of drugs and slaughtering must be instigated and enforced by the respective
food and drug administration, other regulatory authorities, and professional veterinarians. There
should be regular monitoring and assessments for the presence of drug residues in edible tissues of
poultry to ensure the consumers safety.
1442 M. D. MUND ET AL.

Funding
No particular funding or grant was received for this work

ORCID
Uruj Tahir http://orcid.org/0000-0002-5393-5278

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