Antimicrobial Residues and Food Safety: A Public Health Crisis of Concern in Tanzania. A Review

ABSTRACT

Background

Antimicrobial resistance (AMR) along the food supply chain is a global challenge affecting both developed and developing countries. Globally, antimicrobial residues have been a growing problem of both food safety and public health concern. The irrational use of antimicrobial agents in the food industry significantly contributes to antimicrobial residues in the food supply chain and ultimately leading to AMR.

Aim

This review aims to highlight the intertwined connection of antimicrobial residues in food products and the burden of AMR globally, the situation in Tanzania, and the way forward through informed interventions in the area of food safety and security.

Methodology

A literature search was done in PubMed, Science Direct, and Google Scholar databases with a predefined search strategy. A literature review of published articles between 2005 and 2023 on antimicrobial residues, AMR, antimicrobial uses in livestock production, and food safety, especially from Tanzania, was considered.

Results

Antimicrobial residues in commercial livestock production are a big problem in Tanzania. Antimicrobial‐resistant organisms and harmful levels of antimicrobial residues have been reported in beef (35%–71.1%), milk (1.7%–42.7%), eggs (100%), chicken meat (50%–90.5%), and fish samples obtained from formal and informal settings in Tanzania, while the key concern in crop food products being the exposure to insecticides. Improper treatment documentation, nonadherence to the withdrawal period, and limited awareness among farmers are the factors to irrational and indiscriminate uses of antimicrobials that fuel AMR in Tanzania.

Conclusion

Antimicrobial residues in food products is a serious growing public health problem globally and in Tanzania of food safety concern. Multidisciplinary close monitoring and routine evaluation of the antimicrobial residues are imperative to ensure food safety. Awareness to the public, implementation of integrated surveillance programs, and enforcement of legislations by respective government organs in collaboration with stakeholders might be both cost and time‐effective approaches to address the issue.

1. Introduction

Antimicrobial resistance (AMR) is among the major emerging public health problems that can be managed through one health approach. The world continuously observes an increase in population, rigorous climate changes, and emerging global health threats, while in contrast, the food supply chain is likely not to cope with these challenges. In response to these challenges, the agricultural sector is forced to intensify production so as to cope with the ever‐increasing demand for food, and this has been cited to be among the propelling factors to use of antimicrobial agents in livestock production [1]. The irrational use of antimicrobial agents in the food industry threatens public health through compromised food safety and increased AMR [1, 2, 3].

Antimicrobial residues along the food supply chain is a global challenge affecting both developed and developing countries. It is more prevalent in commercial poultry production; however, other livestock production, aquaculture, and food processing industries are also affected [4, 5, 6, 7]. Annually, Tanzania uses more than 1.2 million kg of antibiotics to support poultry production [8]. Antimicrobial agents are used in agriculture for treatment, prophylaxis, and growth promotion [9].

It is worth noting that Tanzania has a large population of livestock, which are mostly managed under an extensive production system characterized by minimal control of diseases by vaccination, pesticide use, and biosecurity measures. This kind of livestock production exposes livestock to disease‐causing agents that consequently propel towards irrational uses of antimicrobial agents in the treatment and control of diseases in livestock [8]. Studies show that there is a continuous increase in the use of antimicrobial agents in food animals in Tanzania, which has been associated with an increase in the number of food animals [10]. It is predicted that by 2030, antimicrobial use in livestock will rise by 8% and 25% globally and in Africa, respectively [11]. The use of antimicrobials in animals remains higher in Africa and other developing countries, including Tanzania, because, unlike in humans, antimicrobials are frequently used in animals for treatment, prophylaxis, increase production, and promote growth [11, 12]. Globally, this is also accompanied by the possibility of an increased burden of AMR secondary to irrational use and low awareness regarding the emergence, spread, and effect of AMR in agricultural food products [13, 14]. The antimicrobial‐resistant microorganisms can spread from domestic, wild, and aquatic animals to humans and vice versa through contaminated food, water, and environment; hence, the solution of this complex health challenge network needs one health approach [14, 15, 16]. According to the global burden of bacterial antimicrobial resistance 1990–2021, It was found that the global human deaths due to AMR are expected to increase from 4.71 million in 2021 to 8.22 million in 2050 [17]. The challenges of AMR are more evident in the developing countries, including Africa, where the burden of diseases both in humans and in animals is high [18].

This review aims to highlight the intertwined connection of antimicrobial residues in food products and the burden of AMR globally and their consequences. Moreover, it expounds the situation in Tanzania and the way forward in addressing such a global health crisis of public health concern through informed interventions in the area of food safety and security.

2. Methodology

A literature search was done in different databases, including PubMed, Science Direct, and Google Scholar. A predefined search strategy included the following key terms “Agriculture,” “Antibiotic,” “Antibiotic Resistance,” “Antibiotic Resistance,” “Antibiotic Residues,” “Antimicrobial Residues,” “Food,” “Food safety,” “Poultry,” “livestock,” and “Tanzania.” All articles considering antimicrobial residues and food safety, public health issues globally, and those from Tanzania were included. A total of 63 articles from 2005 to 2023 written in English were retrieved and reviewed.

2.1. Food Safety and Security Dilemma

Food safety is the assurance of taking foodstuff that does not cause harm to the consumer. Food will be considered safe if the biological and chemical components it comprises cannot physically harm the consumer. Food security is a state where all people have access to nutritious food that meets their dietary needs without facing any physical or economic barriers at any time [19]. The two terms are strongly connected as they share a common fundamental basis. Consumers are likely to use unsafe food when there are challenges in the food supply, thus aggravating the chances of malnutrition and foodborne infections, which largely affect children, pregnant women, elderly people, and other immunocompromised groups [20]. While farmers are forced to use antimicrobial agents in production to meet the food demands, failure to adhere with the withdrawal period endangers the quality and safety of food produced because of antimicrobial residues [21, 22].

3. AMR Crisis, Global Burden, and Food Safety

According to the World Health Organization 2019 report on AMR, globally, 4.95 million deaths were associated with AMR, and 1.27 million deaths were attributed to AMR. Regionally, sub‐Saharan Africa had the highest proportion, and Australia bore the lowest burden [23]. In Europe, 541,000 deaths are associated with AMR, of which intra‐abdominal infections are second to bloodstream infections contributing to death that is associated with resistance. The dominant resistant bacteria are Escherichia coli, Staphylococcus aureus, and Enterococcus faecium [24].

The risk of foodborne AMR is determined by the severity and incidence rate of foodborne infections [1]. One meta‐analysis review showed that, globally, the prevalence of AMR foodborne pathogens in food samples and human clinical specimens was greater than 10% and 19%, respectively [25]. The challenges of AMR and residues in food products on human health are evident due to the prevalence of residues at different levels and increased resistance to foodborne infections. For instance, Campylobacter infections, which are common foodborne infections, have shown a reduced susceptibility to macrolides, gentamicin, and tetracyclines at different rates and settings since the 1980s [26, 27, 28]. One study reported the significant prevalence of Salmonella, E. coli, and Campylobacter as the most common foodborne infections. The same author reported an emergency of vancomycin‐resistant Enterococcus faecalis, which is becoming common in clinical settings [29]. Overall, if AMR in food animals and products is not addressed appropriately, there will be an increased frequency of bloodstream and gastrointestinal infections, disease severity, and mortality [30].

AMR and residues along the food chain are continually a topic of focus due to the increased irrational use of antimicrobial agents in agriculture, which interferes with food safety and security. In overview, the developed countries have the highest consumption of antimicrobial agents in agriculture, which is expected to double by 2030 [31]. One study found that the use of tetracycline and oxytetracycline drugs in animal farming was high globally [32]. Another finding from the study included high levels of antimicrobial residues in milk, poultry, and cattle, and the least in mutton. The most striking results in another study describe Africa to hold a high proportion of residues in food products despite observing a decrease in consumption of antimicrobial agents in agriculture [4, 32].

Entry points of resistant bacteria and antibiotics in the food chain range from farm practices like drug administration, poor adherence to withdrawal periods, and contamination from the environment. The other routes are postharvest, which include food processing, preservation, and management practices like additions of bio‐preservatives, probiotics, and cross contamination [33]. A study by Innes et al. found that 20% of AMR bacterial infections in humans rose from food or animals. These findings suggested a mutual relationship in the genetic determinants of resistance between humans and animals [34]. The food system owes an important environment for the development, persistence, amplification, and transfer of resistance, which is complicated by the ability of bacteria to form biofilms [35].

4. Situation in Tanzania

The magnitude of AMR and residues along the food chain is significantly rising in Tanzania. The problem has been demonstrated by different authors addressing different perspectives. In Tanzania, the rates of multidrug resistance in clinical settings were found to range from 25% to 50% [36]. Harmful levels of antimicrobial residues have been found to exist in beef (35%–71.1%) of which 68% had above acceptable antimicrobial residues regulatory levels [37, 38], milk (1.7%–42.7%) [39, 40, 41, 42], eggs (100%) [43, 44], chicken meat (50%–90.5%) [45, 46, 47], and fish which was extracted from formal and informal settings [37, 39, 43, 45, 47] (Table 1). Antimicrobials access food crops through different means, including application of insecticides and fungicides, animal‐sourced manure with residues, and antimicrobial residues in effluents used for irrigation [48, 49, 50, 51].

Table 1.

Prevalence of antibiotic residues in animal‐derived food products in Tanzania.

Sample source	Region	Year	Antibiotic residue (%)	Proportion above accepted residue safety levels (%)	Ref.
Beef	Morogoro	2015	71.1	68.3a	[38]
	Dodoma	2017	35	NR	[37]
Chicken	Morogoro	2009	70	NR	[45]
	Zanzibar	2014	76.4	NR	[46]
	Dar es Salaam	2022	100	13.1%a/90.5b	[47]
Eggs	Morogoro	2010	100	NR	[44]
	Dar es Salaam	2017	100	80.4a	[43]
Milk	Morogoro	2006	1.7	NR	[39]
	Multiple regions in Tanzania	2006	36	NR	[40]
	Tanga	2008	42.70	NR	[42]
	Pwani	2015	10	100a	[41]

Abbreviation: NR, not reported.

^a MRL, maximum residual level.

^b ADI, acceptable daily intake.

From 2010 to 2017, Tanzania imported a total of 12,147,491 kg of antibiotics for veterinary use. Among the imported antibiotics, tetracycline, sulfonamides, and trimethoprim had the highest proportion of use, while others were used in combinations. Annually, Tanzania uses about 2 million kg of antibiotics in animals, out of which 80% is used in commercial chicken production [8, 52]. This trend was thought to be secondary to increased resistance among animals that required the use of a last‐resort regimen [8]. Further studies in Tanzania have shown high levels of microbial resistance to the majority of the commonly used veterinary antimicrobials, including tetracyclines, sulphonamides, penicillins, and fluoroquinolones [53, 54, 55]. In contrast to the magnitude of the problem, the majority of consumers were found to be unaware of the risk of contracting antimicrobial residues and resistant microorganisms in animal and crop products [56]. However, consuming unsafe food has been associated with acquiring not only resistance but also foodborne infections and zoonotic infections [40, 57, 58]. The farmers' antimicrobial use practices are highly dependent on the level of education and experience in poultry or livestock keeping. These factors determine the farmers' choice of medication, disease management, source of veterinary services, and record keeping [59, 60, 61].

Evidence from Tanzania indicated a lack of treatment documentation and nonadherence to withdrawal periods as unfavorable practices that promote AMR, with the low‐educated farmers having a greater contribution than their counterparts [59]. One study found that 95% of farmers slaughtered their chicken before the withdrawal period because they were afraid of losses and were unaware of the effects of antimicrobial residues in humans [45]. In Tanzania, significant harmful levels of antimicrobial residues have been reported in eggs, broiler meat, beef, and milk across the markets [52]. The exposure to tetracyclines, cephalosporins, aminoglycosides, Sulphonamides, and macrolides residues subjects the consumers to health risks. In the spread of resistant strains along the food chain, Salmonella spp., Staphylococcus spp., E. coli, Enterococcus, and Streptococcus spp. have of significant impact on human health in Tanzania [62].

5. Discussion

Several studies have shown that most of the food of animal origin is of high risk, likely to expose consumers to antimicrobial residues and AMR [63]. The situation of antimicrobial residues and resistant strains in food in Tanzania does not vary greatly from those found in other places in Africa and the world; however, Tanzania appears to hold high concentrations [64]. These findings raise a concern regarding the health effects that are associated with long‐term exposure to antimicrobial residues and resistant bacteria in the Tanzanian population. The fact that up to 90% of farmers self‐prescribe antimicrobials to their livestock and chickens, and the medicines are accessible over the veterinary shops with no restrictions; this might have significantly contributed to the irrational uses of antimicrobials in animals [65].

The veterinary antimicrobial agents' misuse probably was further escalated by a lack of food inspection for residues and poor legislation enforcement by the responsible government organs like the Tanzania Bureau of Standards (TBS), Tanzania Meat Board (TMB), and Tanzania Dairy Board (TDB). Moreover, the reason for the increased irrational use of antibiotics in food production in Tanzania might be similar to Kenyan poultry keepers, who are influenced by labels on antibiotics that claim to promote production, growth, and prevent infections, and poor agricultural practices that promote infections [66]. High consumption of tetracyclines in agriculture has been reported in Ethiopia, and the reason for this is that tetracyclines are broad‐spectrum antibiotics and are used as growth promoters; this might be the same also in Tanzania [67].

Irrational use of antibiotics in food products exposes consumers to several long‐term consequences, including cancer, allergies, and gut dysbiosis‐related complications, apart from contributing to the AMR crisis. Antimicrobial residues in foods can cause adverse side effects with different severities on human health that involve multiple body tissues, organs, and systems. Antimicrobial residues can serve as carcinogens, mutagens, and teratogens. Quinoxaline, nitrofurans, and nitroimidazoles, which are common veterinary drugs, have carcinogenic potential. Vaginal adenocarcinoma and benign abnormalities of the uterus may arise due to long‐term exposure to low doses of nitroimidazoles and 3‐nitrofurans [68]. Recurrent exposure to penicillin is associated with an elevated risk of esophageal, gastric, pancreatic, and bladder malignancies [69]. The common allergic manifestations involve skin rashes, hematological (hemolytic anemia, thrombocytopenia), and vascular allergies (vasculitis) [63].

The alimentary canal comprises a diversity of microorganisms forming an ecosystem of microorganisms that are responsible for homeostasis, and metabolic and physiological processes [70]. Abuse of antimicrobial agents can result in an irreversible homeostatic imbalance of gut microbiota, which results in the blooming of opportunistic pathogens. Gut microbiota dysbiosis can progress to inflammatory bowel syndrome, rheumatoid arthritis obesity, and diabetes [71]. In clinical settings, dysbiosis has been linked to affect the severity and prognosis of patients in the intensive care unit (ICU) [72]. Despite inadequate evidence, alteration of the gut microbiota is likely to increase the chances of obesity, which results from low‐dose antibiotic consumption [73]. Generally, gut microbiota dysbiosis is a risk factor for metabolic syndrome diseases, allergic effects, and developing noncommunicable diseases in consumer victims.

The government of Tanzania has demonstrated a positive initiative in combating AMR. Part of these efforts is the development of the national AMR surveillance framework, and participating in the Global Antimicrobial Surveillance System (GLASS). However, the usefulness of these systems is limited due to poor data reporting, quality, and the use of data to inform policy and decision‐makers [74]. Moreover, the government has not yet established an integrated AMR surveillance framework that supports combined reporting analysis of AMR in foodborne microorganisms like bacteria, which has already been adopted in Zambia [75, 76].

6. Conclusion and Recommendation

Despite remarkable milestones that have been achieved as part of efforts to control AMR and residues in the food chain, the problem still exists globally and in Tanzania. Technical problems in data collection, quality, utilization, laboratory infrastructures, enforcement of the law, low awareness of the effects of AMR, and irrational use of antibiotics in agriculture are the major drivers of the burden. Poor community involvement is outlined as the major setback in this review, which augments the effect of low awareness, irrational use of antibiotics, and poor farming practices among farmers. Generally, the existing gap is the execution of evidence obtained from research and surveillance into practice at different levels.

To address the main challenges of irrational use of antimicrobial agents in food production, Tanzania's agricultural system should implement and emphasize several approaches, including extension services on good livestock husbandry practices, disease prevention by vaccination, and biosecurity and biosafety measures in farms. These approaches will open a door for adopting technologies in Tanzanian settings, which will improve the monitoring of antimicrobial usage (AMU) at the farm level. Monitoring of food safety at different levels along the food chain especially through the farmers' cooperative societies could help to improve the quality and safety of different agricultural food products. Proper utilization of cooperative societies could serve as a platform to educate farmers, conducting surveillance and screening for residues in food products. To fully capture data about AMR in agricultural food production, Tanzania should hasten to use integrated AMR surveillance programs to address the burden holistically.

Author Contributions

Harold L. Mashauri: conceptualization, data curation, writing – original draft, methodology, project administration, supervision, writing – review and editing. Baraka L. Max: methodology, writing – original draft, data curation, conceptualization. Sarah M. Makweba: conceptualization, writing – original draft, methodology, data curation. Hezron E. Nonga: data curation, writing – review and editing, supervision, methodology, conceptualization.

Ethics Statement

The authors have nothing to report.

Conflicts of Interest

The authors declare no conflicts of interest.

Transparency Statement

The lead author Harold L. Mashauri affirms that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.

Data Availability Statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.