Antibiotic Residues in Food: History
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Carmen PETCU
,
Jeachul Jang
,
Margarita Ghimpeteanu
,
Elena Pogurschi
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,
Nela Dragomir
,
Oana Mihai

The usage of antibiotics has been, and remains, a topic of utmost importance; on the one hand, for animal breeders, and on the other hand, for food safety. Although many countries have established strict rules for using antibiotics in animal husbandry for the food industry, their misuse and irregularities in compliance with withdrawal periods are still identified. In addition to animal-origin foods that may cause antibiotic residue problems, more and more non-animal-origin foods with this type of non-compliance are identified. 

  • antibiotic residues
  • food safety
  • antimicrobial resistance
  • public health

1. Products of Non-Animal Origin

Although food products of animal origin are considered to be the major source of antibiotic residues, studies in the literature have shown that even non-animal origin products represent an important problem regarding this type of contamination. The main sources of these compounds in agriculture are irrigation water with antibiotics traces due to inappropriate recycling processes or the use of manure as soil amendments, which leads to spreading antibiotics through the food chain [1]. As a result of these agricultural practices, antibiotics in soil can be taken up by plants, entering the food chain. Due to the fact that plants are considered to be a minor source of antibiotic residues, studies have focused on few compounds [2][3][4]. The most common vegetables that accumulate antibiotics are considered to be cereals, such as wheat, rice, and oat, and coarse grains, such as maize and barley. In this field, studies have focused on antibiotic detection in different matrices or were conducted as experiments in a hydroponic environment [5][6][7][8][9].
In recent years, research has been conducted in order to study the relation between intake of antibiotics in edible crops due to poorly management of wastewater used in irrigations and from manure [5][7][10][11][12][13]. Pan and Chu (2017) studied the influence of some antibiotics (tetracycline, sulfamethazine, norfloxacin, erythromycin, and chloramphenicol) on crops in relation to two types of contamination, irrigation with wastewater and soil amendment with animal manure. Findings showed that the distribution of tetracycline, norfloxacin, and chloramphenicol in crop tissues were as follows: fruit > leaf/shoot > root; an opposite order was found for sulfamethazine (SMZ) and erythromycin (ERY), i.e., root > leaf/shoot > fruit [10]. Research also revealed that the uptake of antibiotics in crops was higher in the case of wastewater use and it was lower in the case of manure fertilization, argued by the fact that crops are more likely to absorb residues during the continuous process of irrigation. However, the levels of antibiotics ingested through the consumption of edible crops under the different treatments were much lower than acceptable daily intake (ADI) levels.
In Northern China, studies have shown that oxytetracycline, tetracycline, chlortetracycline, sulfamethoxazole, sulfadoxine, sulfachloropyridazine, chloramphenicol, ofloxacin, pefloxacin, and lincomycin were found in vegetables. In the same geographical area, relatively high concentrations of norfloxacin, ciprofloxacin, and enrofloxacin were found in vegetables, such as tomato, cucumber, pepper, spinach, eggplant, and crown daisy [14]. Other studies have shown that parts of vegetables, such as the roots of carrot and leaves of lettuce, as well as cabbage and spinach, the stem of celery, and fruits of cucumber, bell pepper, and tomato had 64% pharmaceutical residues, including antibiotics, due to the wastewater used for irrigation [15]. Bassil et al. (2013) evaluated the uptake of gentamicin and streptomycin in carrot (Daucus carota), lettuce (Lactuca sativa), and radish (Rhaphanus sativus) due to the same type of fertilization. The conclusion of the study was that three crops absorbed relatively higher amounts of gentamicin (small molecule) than streptomycin (large molecule), and that the levels of antibiotics in plant tissues increased when increasing the antibiotic concentration in manure [16]. The intake of antibiotics into vegetables seedlings was also studied by Ahmed et al. (2015), who showed that cucumber (Cucumis sativus), cherry tomato (Solanum lycopersicum), and lettuce had relatively high levels of tetracyclines and sulfonamides in the non-edible parts, but lower concentrations in fruit parts and were within acceptable daily intake levels [13].

2. Products of Animal Origin

The use of antibiotics that may lead to the accumulation of residues in meat, milk, eggs, and honey should not be allowed in foods intended for human consumption. If the use of antibiotics is necessary in the treatment or prevention of various animal diseases, a withholding period must be respected until antibiotic residues are no longer detected [17]. The presence of antibiotic residues in meat from various species of economic interest is considered a significant danger to public health.
The results of the study conducted by Al-Mashhadany in 2020 on sheep meat harvested from supermarkets in Iraq showed that samples contained antibiotic residues at a level higher than the maximum allowed limits. Cooling and freezing, as preservation methods, slightly reduce antibiotic residues in meat. The same study showed that thermal processing of lamb meat (cooking for about 45 min) leads to a transformation of antibiotic residues into inactive residues against bacteria [18].
Another study conducted by Babapour. et al. in 2012 on meat samples collected from Iran obtained similar results in terms of the incidence rate of antibiotic residues in meat [19]. A higher incidence of antibiotic residue has been reported in Nigeria in beef samples [20]. In contrast, the lowest incidence rates were reported in sheep samples analyzed in Spain [21]. The presence of fluoroquinolone residues (enrofloxacin and ciprofloxacin) in some Indonesian chicken samples indicated that it were used by farmers in poultry feed [22][23].
Milk with antibiotic residues significantly influences the technological process of obtaining dairy products, which includes the technology used for dairy yeasts. Antibiotics can get into milk from treatments applied to sick animals or (less often and not recommended) through the use of preservatives. Milk with antibiotic residues is considered a rigged food on the market. By consuming unpasteurized milk, antibiotic-resistant bacteria can be transmitted to consumers, especially in areas with a dense population and a lower degree of development, where there is a risk of improper storage of milk and dairy products [24][25]. Milk and dairy products are exposed to contamination by antibiotics and other drug residues, but also to neutralizing and preserving substances [26][27][28]. Analysis of antibiotic residues in dairy products (pasteurized drinking milk, yogurt, sour cream, whipped milk, cheese) leads to the identification of the gentamicin/neomycin group, especially in sour cream. Macrolides sometimes appear in cheese, and tetracyclines in sour cream and cheese. Here discuss about milk samples subject to confirmatory investigations, used for human consumption. Moghadam et al. (2016) identified that 38.5% of raw milk samples collected from the Iranian province of Khorasan Razavi had penicillin residues, while Ghanavi et al. (2013) reported identification of residues of 11% antibiotics of cow milk samples collected from different regions of Iran [29][30]. Studies conducted by Vinu, (2021) showed that there is a direct correlation between the stage of lactation and the presence of antibiotic residues in milk; 34.3% of positive samples came in the lactation stage of 0–70 days, 20% between 70–140 days of lactation, and 45.7% between 140–305 days of lactation [31]. Additionally, Knappstein et al. (2004) highlighted a direct correlation between milk production and the presence of antibiotic residues (cefquinomas), their level not being influenced by the frequency with which milking was performed [32].
In most countries, eggs are the main product generated from backyard poultry production systems due to the fact that they can be quickly consumed or sold to meet essential family needs. In a study by Cornejo et al. (2020), in Chile, the presence of antimicrobial residues in eggs, such as tetracyclines, beta-lactams, aminoglycosides, and macrolides, was analyzed. The survey showed that all samples were positive for at least one of the four antimicrobials tested [33]. Another recent study from China concluded that careful monitoring should be imposed on antibiotic residues in poultry eggs, after detecting 30% positive egg samples for quinolones, tetracyclines, and sulphonamides [34].
The most common contaminations of honey can be explained by treatments in order to control honeybee diseases and contaminants coming from procedures applied in agriculture [35]. The European Union has forbidden the use of antibiotics for bees, this aspect is strictly enforced by recent legislation [36][37]. The most common and important antibiotics found in honey are beta-lactams (penicillin, ampicillin, cloxacillin, amoxicillin for bacterial infections), amphenicols (thiamphenicol, florfenicol, chloramphenicol which are carcinogenic antimicrobials), tetracyclines (oxytetracycline, chlortetracycline, tetracycline for bacterial diseases), macrolides (erythromycin, tylosin, oleandomycin and spiramycin), and aminoglycoside, fluoroquinolones (ciprofloxacin, enrofloxacin, norfloxacin—growth enhancing) [38][39][40].

This entry is adapted from the peer-reviewed paper 10.3390/foods11101430

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