Antibiotic-Resistant Staphylococcus spp.: History
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Siwalee Rattanapunya

The application of antibiotics to orange trees in open production environments to halt the spread of bacterial disease presents risks to the environment and creates health concerns for Thai farmers using those agents. ARB on crops such as oranges may enter the global food supply and adversely affect public health. 

  • antimicrobial resistance
  • Staphylococcus spp.
  • orange orchards

1. Introduction

Multidrug-resistant bacteria rank among the world’s most important public health problems of the 21st century. The World Health Organization (WHO) suggests that if the world neglects taking action, then we are heading to a post-antibiotic era, in which common infections and minor injuries will result in death [1]. Currently, antimicrobial resistance (AMR) trends support the perspective of the WHO that worldwide, at least 700,000 people die each year from common diseases, including respiratory tract infections, sexually transmitted infections, urinary tract infections, and foodborne illnesses [2]. Annually, more than two million people in the United States suffer from illnesses caused by antibiotic-resistant bacteria [ARB] [3]. A wealth of literature suggests that the ARB crisis is accelerated by the overuse and misuse of antibiotics in human medicine. Considerable attention has focused on the prevalence of ARB associated with food-producing animals and their environment, including commercial farms, feedlots, processing plants, and packing plants, since antibiotics are directly used for growth promotion and the prevention of diseases in food-producing animals [4][5][6][7][8]. The use of antibiotics and the spread of ARB associated with fruits (whether treated with antibiotics) through the global food supply is often overlooked [9]. ARB and antibiotic residues may also accumulate in the agriculture production environment, potentially adversely affecting farmworkers and consumer health.
According to regulatory agencies in the US and Britain, certain antibiotics (streptomycin, oxytetracycline) are permissible for use on production crops, including oranges, stone tree fruit, and pome fruit [10]. Gentamicin is used in the treatment of animal and human diseases but has been used to control plant diseases [11]. This is particularly true in Brazil, Korea, Thailand, and China for the control of citrus greening disease or Huanglongbing (HLB) and lettuce diseases [11][12]. In the United States, an alarm was raised for the spraying of antibiotics in open production environments to halt the spread of crop associated bacterial disease [13]. Indeed, from 1970 to the present, antibiotics such as ampicillin, amoxicillin, and tetracycline have been permitted for the prophylactic treatment of bacterial diseases in plants by Candidatus Liberibacter asiaticus or HLB in citrus via a graft-based chemotherapy method [14][15][16]. In Thailand, farmers or orchard operators regularly use capsule forms of ampicillin, amoxicillin, and tetracycline for the treatment of HLB. The recommended treatment dose of ampicillin is 12,500–25,000 ppm (i.e., achieved by adding 50 ampicillin 250 mg or 500 mg capsules per 1 L of water) through injection into tree trunks approximately three to four times per year [17][18]. Uncontrolled use of various antibiotics to treat HBL was encouraged by some orchard operators, academics, and government agencies. Orchard owners purchased the antibiotics directly from retail pharmacies or agrochemical suppliers [19]. Prevalence of ARB in animal production has been reported [19][20][21][22], an absence of literature is available on ARB associated with orange orchards.
Staphylococci are Gram-positive bacteria associated with the respiratory tract and skin of humans and animals. Staphylococcus aureus and members of the S. intermedius group are the clinically most important coagulase-positive staphylococci in human and veterinary medicine, respectively. Dozens of coagulase-negative staphylococcal species have been described as colonizers of the skin and mucous membranes and as food- associated saprophytes [23][24]. Most of them are less frequently involved in clinically manifested infections; however, in particular species of the S. epidermidis group account significantly for foreign body-related infections [24][25]. Multidrug-resistant (MDR) Staphylococcus spp. exhibited resistance rates to penicillin, ampicillin, and erythromycin of 96.6%–00%, 96.6%–8%, and 50%–7.1%, respectively [26][27][28]. A study in Thailand showed that the prevalence of community-acquired bacteraemia, healthcare-acquired bacteraemia, and hospital-acquired bacteraemia caused by MDR S. aureus was 8%, 28%, and 50%, respectively [29]. Antibiotic-resistant staphylococci have been isolated from the soil, surface water, wastewater, household surface dust, air, and a variety of crops intended for human consumption, as well as orange and apple juice products [30][31][32]. Antibiotic use in orange crop production may result in antibiotic residues in the environment and an increase in ARB entering the global food supply chain.

2. Current Insights

There is a significant knowledge gap concerning the use of antibiotics on edible fruit crops and the occurrence of ARB on those fruits. In the present study, Staphylococcus spp. resistant to erythromycin and ampicillin were only recovered from samples collected from orange orchards applying ampicillin to trees for the control of HLB. Staphylococcus spp. are associated with diseases of humans and animals and have been recovered from the environment (e.g., water and soil); therefore, isolation from an orange production environment is not unexpected. The recovery of antibiotic-resistant staphylococci from oranges and orange orchard environments raises concern for the spread of ARB through the food supply chain. The occurrence of antimicrobial-resistant microorganisms associated with fresh fruits or their production environment is of human health importance. For example, Aspergillus fumigatus resistance to all triazole antifungals recovered from patients likely originated in the environment [33].
The unregulated application of antibiotics may result in increased populations of ARB and antibiotic residues on crops intended for human consumption resulting in the spread of antimicrobial resistance (AMR) and exacerbating a global health crisis. Thai mandarin orange growers indicated they adjusted HLB antibiotic treatment, antibiotic concentration, volume, frequency, route of administration, and combination of antibiotics based on outcomes rather than following science-based recommendations [18]. Orange growers participating in the present study used ampicillin for the treatment of HLB, which is not approved for use, for example, in the United States and Britain. Very few studies have addressed the issues of antibiotic use on food crops and ARB on antibiotic-treated crops or the surrounding environment. Parameters influencing the mobility and stability of antimicrobials in the environment must be addressed to protect the global food supply and human health.
The Staphylococcus spp. isolated in the present study are classified as coagulase-negative staphylococci (CoNS) and are associated with nosocomial infections [24]. The results of this study are consistent with previous reports in which S. epidermidis, S. arlettae, S. haemolyticus, and S. saprophyticus recovered from non-healthcare settings [34][35] and healthcare settings [36][37] were often resistant to multiple antibiotics (e.g., penicillin, erythromycin, amoxicillin, and ampicillin). Unlike meat and poultry, which are thermally processed prior to cooking, oranges are consumed raw, and therefore ARB is not inactivated. ARB on the orange surface can cross-contaminate the edible portion of the orange during peeling. The present study did not investigate the potential dissemination of antibiotic residues associated with oranges exposed to antibiotics. Although coagulase-negative staphylococci are not considered foodborne pathogens, they may play an important role in the spread of antibiotic resistance genes in community and hospital environments.

3. Conclusions

The ramifications of the direct application of antibiotics to food crops such as oranges and the emergence and spread ARB on human health are not fully appreciated. The application of antibiotics to orange trees in open production environments to halt the spread of the bacterial disease of a crop presents risks to the environment and creates health concerns for farmers using those agents. The present study focused on Gram- positive bacteria exhibiting multi-antibiotic resistance. Gram-negative bacteria are commonly isolated from fresh fruits and vegetables and therefore should be included in future investigations of ARB. ARB and antibiotic residues on crops such as oranges may enter the global food supply and adversely impact human health. The presence of ARB on foods that will not undergo a process to inactivate the bacteria prior to consumption may represent a greater risk for the spread of ARB and antibiotic resistance genes.

This entry is adapted from the peer-reviewed paper 10.3390/ijerph19010246

References

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