Veterinary antibiotics in animal manure and manure laden soil: Scenario and challenges in Asian countries

1 Introduction

In the past decades, worldwide utilization of antibiotics for both human and animals are on the climb. The production of total antibiotics in China in 2009 was nigh on 1.47 million tonnes (Yang et al., 2009), while in the US, veterinary antibiotics used in animal feeds solely was increased to 130,000 tons in 2009 from 9300 tons (FDA, 2012). Globally, the consumption of antibiotics in animal feeds was increased by 8% from 2009 to 2011 (FDA, 2009, 2011). Approximately 80.5% of the total antibiotics consumed in the US were used on farmed animals (FDA, 2011). Veterinary antibiotics are used on a regular basis for treatment and prevention of diseases in animals in commercial livestock farming. Substantial amount of antibiotics is used in livestock for prophylactic, metaphylactic and therapeutic purposes as well as feed addictives. Veterinary antibiotics are also extensively adopted for subtherapeutic use with the intention of preventing disease and promoting growth. Despite the fact that incorporation of antibiotics in animal feed for the purpose of growth promotion (as antimicrobial growth promoters) is fully banned in European Union under Regulation (Regulation 1831/2003/EC) (EC, 2005), nonetheless, many countries still permit such practice.

Animals are not able to effectively metabolize antibiotics. Depends on antibiotics, they may be either completely metabolized or a portion may be excreted via urine or feces in either its original state or as active/non-active metabolites. Incomplete metabolization will lead to the presence of high concentration of antibiotics in animal waste. In fact, up to 72% of the active principle in tetracycline, one of the most commonly used veterinary antibiotics is excreted via faeces and urine (Winckler and Grafe, 2001). Antibiotic residues were recurrently detected in animal manures such as swine and poultry (Awad et al., 2014; Chen et al., 2012; Geng et al., 2013; Hou et al., 2015; Zhao et al., 2010), as well as soil amended with animal manure for fertilizing purpose in Canada (Aust et al., 2008), China (An et al., 2015; Hou et al., 2015; Zhang et al., 2015), and Malaysia (Ho et al., 2014).

Wang and Tang (2010) had reported the total amount of antibiotic use annually including both medical and veterinary antibiotics has attained 100,000–200,000 tonnes worldwide. The quantity is in rising trend as the usage of VA guarantees the production outcome. This is not an all-inclusive review, but as an endeavour to present and add new information to previously published researches. Key questions that will be addressed in this paper are: 1) The prevalent occurrence of antibiotics in animal manure and manure laden agricultural soil in Asia region. 2) The current policy available (FDA and EC) and the lack of regulations controlling antibiotics used as animal growth promoter in other countries. Hence, the primary intention of this paper is to reveal the extent of antibiotics use on farm animals and its significant linkage to soil “pollution” attributable to common agriculture practise in selected countries, and at the same time, heightening awareness for the need of proper handling of antibiotics-containing manure.

2 Veterinary antibiotics

Prevalence of antibiotic consumption in livestock production, in correlation to the rising pervasiveness of antibiotic resistance in our environment, points towards the call for the strict directive on antibiotic usance in agriculture.

Fig. 1 shows the utilization of antibiotics in food producing animals in 29 European countries (EMA, 2012), with tetracyclines, penicillin and sulphonamides as the top three most consumed antibiotics. Prevalence studies of antibiotics in manure laden soil are also in line with the consumption as reported in Fig. 1. As stated by Van Boeckel et al. (2015), top five countries with largest shares of antibiotics consumption in food animal in 2010 were China (23%), United States (13%), Brazil (9%), India (3%) and Germany (3%). However, the projected ranking by 2030 has revealed increment; estimated China will remain possessing the highest share of global antibiotics consumption (30%), following by United States (10%), Brazil (8%), India (4%) and Mexico (2%). Projected findings also revealed three out of the top five countries that are expected to have greatest percentage increases in antibiotics consumption by 2030 are from Asia. Each year, estimated more than 20,000 tonnes of sulphonamides, with bacteriostatic properties, are introduced into biosphere, exclusive of drugs that introduced to the environment as herbicides (Baran et al., 2011). Regardless of the above-mentioned findings, data on antibiotics used on animal farming in these developing countries are still not widely available. Antibiotics can enter the environment via multiple routes (Fig. 2), encompassing emission from factory, disposal of unused medicine and container, pharmaceutical manufacturing effluents, livestock husbandry effluents and animal waste, excretory products from pasture-reared animals, aquaculture and sewage treatment plant. Fig. 2 illustrated the major entry pathways for antibiotics to enter our environment.

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Fig. 1

Consumption of antibiotics for food producing animals by classes in 29 European countries (EMA, 2012).

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Fig. 2

Multiple entry pathways of antibiotics into environment.

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Fig. 1 Utilization of antibiotics for food producing animals by classes in 29 European countries (EMA, 2012)

These antibiotics are added into livestock feed for three core purposes: to treat disease (therapeutic levels), to preclude disease (subtherapeutic levels), and to boost growth (subtherapeutic levels). Morton (1989) defined “subtherapeutic” use of antibiotics as concentration less than 2 gt⁻¹ feed for a period longer than two weeks, or as mentioned by Cohen (1998), lower than 0.2 g kg⁻¹. Yet, in most countries, antibiotics are used as prophylactic measures (for example in extenuating infection and disease widespread), and for growth boosting (WHO, 2014). In general, antibiotics are presented to livestock via feed or water, nonetheless, a faction are administered by intramammary, oral, or direct application (Van Epps and Blaney, 2016) (Table 1).

3 Occurrence of veterinary antibiotics in soil animal manure and soil in selected Asian countries.

4 Policy on veterinary antibiotics use on animal and aquaculture production

Despite the banning of antibiotics use in animal growth, the usage of antibiotics in livestock industries is still on the rise globally. Currently, only Food and Drug Administration (FDA) and EU have clear regulations on prohibiting the application of selected antibiotics as growth promoter. According to FDA, 18 classes of antimicrobials are authorizedto be employed in livestock (FDA, 2011). China follows agricultural industry standards (NY525-2012) which only control and regulate pH, worm mortality, the number of fecal coliforms of manure-based commercial organic fertilizers. However, antibiotics uses on animal are presently not regulated under any standards in China (Zhou et al., 2017).

Veterinary feed directive (VFD) regulations were pronounced by Food and Drug Administration (FDA) in 2015, altering classification of certain antimicrobial drugs and banning animal production application of VFD drugs (CFR, 2015, FDA, 2015). An order of VDF has to be issued by a licensed veterinarian before being fed to animal. This system helps in governing the distribution and use of certain drugs (VFD drugs) that can be only used in animal feed with explicit approval of a licensed veterinarian. The more detailed breakdown of these regulations summarized into five major points on tackling antibiotic usage. First, it requires of several previously approved antimicrobial drugs into VFD drugs which will require order in black and white issued by licensed veterinarian. Second, medicated feeds that carry VFD drug can no longer be used for improving weight fain and feed efficiency. Third, a VFD order can only be issued if anofficial veterinarian-client-patient relationship with the animal and the customer (owner of animal) is established. Fourth, acknowledgment and the administering of all medicated animal feeds that carry VFD listed drug must be properly recorded for two years. Fifth, veterinarian may be charged with adulterating or misbranding the VDF drug if a VFD is issued without complying with regulations (CFR, 2015).

Regulation of antibiotics application in aquaculture is broadly regulated, with great differences from country to country, and little to no enforcement in many countries of major aquaculture production (Pruden et al., 2013). Discrepancies between regulations on antibiotics usage in both agriculture and aquaculture have led to frequent detection of antibiotics occurrences in Asia region. Aquaculture is mentioned here as the practise of integrated farming is also common in Asia region (reusing of aquaculture water on farmland), hence indirectly affects the situation at some point. Table 2 supported the importance of antibiotics that shared between animal and human health. The prevalence of veterinary antibiotics in agricultural soil revealed the objective of this work as the effectiveness of such antibiotics in human health industry may be affected in long term.

5 Conclusion

Reusing animal manures in agriculture industry is not a brand new practise and it has been carried out for a very long time. However, this only came under spot light of researchers after the raising concern on antibiotics usage hike in food animals and its risk, particularly associated with occurrences of antibiotic resistance gene in the environment and its potential fallout. This manuscript has brought out the major findings on veterinary antibiotics detected in agricultural soil, as well as in the environment. Even though findings mentioned above are mainly focused on Asia region (as Asia is the region with rising veterinary antibiotics use), but be cognizant that these findings are actually reflecting a worldwide scenario. Some results reported on antibiotics concentration detected were said to be argumentatively low (not high enough to pose any current threat), but the major point of this review lies towards the long term usage and the accumulation potential of such recalcitrant and hazardous environmental pollutant, especially when veterinary antibiotics usage is still unavoidable for now.

Veterinary antibiotics from few groups (tetracyclines and sulphonamids) of antibiotics were commonly detected in the environment. Though other groups of veterinary antibiotics are also widely used and detected. Different regions may have different practises in selecting which veterinary antibiotics to be used. Apart from that, elimination mechanism of tetracyclines, which have been widely in used for the past decades are mainly via urine, unlike the newer derivatives such as doxycycline, which is excreted via feces (Szatmári et al., 2012). Hence, with the shift from older antibiotics to newer veterinary antibiotics for greater effectiveness, risk in reutilising animal waste for food crops fertilisation is ever-increasing. It is apparent that policies on controlling veterinary antibiotics usage on food animals still need to be strengthened in many countries, as well as be introduced in countries in Asia. Chung et al. (2017) revealed that EU (European Union) has set maximum residue limits (MRL) for antibiotics (tetracyclines and fluoroquinolones) in foods of animal origin (EU Commission, 2010), but there was no MRL set for food crops. Antibiotics sales and usage are not regulated in India (Ganguly et al., 2011; NICD, 2011), and there is no current regulation to regulate the antibiotics usage on animals in China (Zhou et al., 2017). It is important to understand that antibiotics sales do not always represent the antibiotic usage as most of the information regarding antibiotic usage is not readily available. Antibiotics are prone to be more persistent once released into soil and sediment (Wang and Yates, 2008) and this observable fact was in a manner corresponding to soil characteristics, antibiotics sorption capacity, distribution coefficient and hydrophobicity (Tolls, 2001). Apart from that, antibiotics are also likely to stay in soil with high acidity and clay content (Awad et al., 2014) and soil pH also play an important role in determining sorption capacity of antibiotics in soil (Sassman and Lee, 2005).

Risk assessment on veterinary antibiotics towards soil microbial communities is still in lacking. Available data and results from current available research are often too vague to have definitive conclusion, hence, leading to the lack of regulations and control of antibiotics usage in many countries, especially in Asia. More research attention should be focus on such issue to bring greater understanding on current antibiotics “pollution” scenario. If such heavy veterinary antibiotic usage trend continues, no doubt we are to face the severe consequences in near future, and environment is the one paying the price.