Fresh Produce with Antibiotic-Resistant Bacteria: Comparison
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Fresh produce, when consumed raw, can be a source of exposure to antimicrobial residues, antimicrobial-resistant bacteria (ARB) and antimicrobial resistance genes (ARGs) of clinical importance. The most commonly observed ARB were E. coli (42.5%) followed by Klebsiella spp. (22.5%), and Salmonella spp. (20%), mainly detected on lettuce.

  • antimicrobial resistance
  • antibiotic-resistant bacteria
  • agriculture
  • fresh agriculture products

1. Introduction

The World Health Organization (WHO) and Food and Agriculture Organization (FAO) promote the daily consumption of fruits and vegetables as part of a healthy diet, due to their high nutritional value [1][2]. Raw consumption of many fresh leafy and non-leafy vegetables, root vegetables, sprouts, and fruits results in the exposure of humans to foodborne bacterial pathogens, including antibiotic-resistant bacteria (ARB) [3][4][5][6]. In recent decades, exposure to antimicrobial-resistant pathogens through the food chain has increasingly been reported to cause foodborne disease outbreaks [7].
Studies have reported the presence of ARB and antibiotic resistance genes (ARGs) on fresh produce. For example, in Japan, extended-spectrum β-lactamase (ESBL)-producing pathogens have been found on fresh produce [8]. Multidrug-resistant E. coli and Salmonella spp. on vegetables have been linked with disease outbreaks in Germany, the United States, Canada, Australia and Finland [9][10][11][12][13]. Additionally, opportunistic microorganisms previously considered non-pathogenic are present in fresh produce, and can cause serious infections in an immune-compromised host. For example, opportunistic bacteria, such as Klebsiella spp. and Enterobacter spp., have been found on vegetables (e.g., cabbage, capsicum and tomatoes) in retail markets in different settings [14][15][16]. Consumption of vegetables contaminated with Klebsiella spp. can cause acute bronchopneumonia and labor pneumonia in immunocompromised individuals [17].
Fresh produce can be contaminated with bacterial pathogens at multiple points throughout its production and supply chain by direct contact with fecal waste during farming, such as wastewater irrigation and the use of biosolids or animal manure as fertilizer [18][19]. Contamination can also happen during the transport and handling of produce [20]. While these potential contamination pathways have been studied well for traditional pathogens, their relative contributions to the contamination of fresh produce with ARB, ARGs and antimicrobial residues have not been quantified. Such information could potentially inform interventions to reduce human exposure to ARB/ARGs through fresh produce.

2. Prevalence of Antimicrobial-Resistant Bacteria on Fresh Produce

The included studies detected bacteria of more than twenty different genera on vegetables (leafy, non-leafy, root), fruits, sprouts consumed raw, and ready to eat (RTE) salad. The most frequently observed bacteria were E. coli, found in 17 out of 40 (42.5%) included articles. E. coli, including pathogenic strains, was mainly detected on lettuce, cabbage, cucumbers, and tomatoes. For example, among 260 samples of leafy, non-leafy and root vegetables investigated in Pakistan, approximately one-third of E. coli strains isolated from lettuce samples were identified as diarrheagenic E. coli pathotypes (DEPs) [21]. Pathogenic E. coli strains, such as Shiga toxin-producing E. coli (STEC), enteropathogenic E. coli (EPEC), and enterotoxigenic E. coli (ETEC) were detected in two studies, from nopalitos samples in Mexico [22] and from cucumber, lettuce and spinach samples in Pakistan [21]. DEPs in both studies reported resistance to multiple antibiotics including tetracycline (TET), ampicillin (AMP), ciprofloxacin (CIP), and gentamicin (GEN). The study in Pakistan tested 50 DEPs isolates and found that 92% of the isolates were resistant to TET, 87% to AMP and 82% to efotaxime (CTX) [21]. E. coli (not DEPs) isolated from fresh produce showed varying resistance to amoxicillin (AMX), AMP, GEN, erythromycin (ERY), colistin (CST), amikacin (AMK), cefotaxime (CTX) and ceftazidime (CAZ). The resistance profiles for E. coli were diverse between the studies.
The second most common bacteria were Klebsiella spp. And Salmonella spp. Klebsiella spp., which were detected on produce in nine out of 40 articles (22.5%). Among these, Klebsiella pneumoniae was the most common; six out of nine articles (66.6%) detected this species from produce samples. For example, a study in China recovered 175 Klebsiella pneumoniae isolates from 216 samples of leafy, non-leafy, root vegetables and sprouts [23]. Another study in Algeria found 13 third-generation cephalosporin-resistant Klebsiella pneumoniae strains from 310 samples of fruits, leafy and non-leafy vegetables. Leafy vegetable lettuce was frequently contaminated. Klebsiella spp. was often resistant to aztreonam (ATM) and CTX [24]. CTX resistant Klebsiella spp. were also detected on onion, cucumber, tomato, chili pepper and ginger in India [25]. In Italy, K. ozaenae resistant to AMP, cefoxitin (FOX), CTX were detected in ready to eat (RTE) salad samples [26].
Salmonella spp. were found in nine out of 40 articles (22.5%). Lettuce samples were observed to be highly contaminated with Salmonella spp. followed by coriander, spinach, parsley, and sprouts. More than 100,000 samples of various types of fresh produce were investigated in the United States from 2002 to 2012, resulting in the detection of Salmonella spp. in 51 different serotypes of 152 samples [27]. Of the 51 Salmonella serotypes, 10 were resistant to different antibiotics [27]. The identified Salmonella serotypes were Oranienburg, Montevideo, Agona, Havana, Thompson, Poona, Kentucky, Tucson, Veneziana and one was unknown, with Tucson being the more prevalent. Antibiotic-resistant Salmonella serotypes Thompson, Poona, and Kentucky, were found on lettuce samples (23.1%), whereas the Oranienburg serotype was found on cantaloupe sample (6.7%) [27]. Another study in Malaysia isolated multidrug-resistant S. enteritidis from carrots that were resistant to AMP, AMX, trimethoprim (TMP) nalidixic acid (NA), trimethoprim-sulfamethoxazole (SXT), and chloramphenicol (CHL) [28]. In a study in Thailand, S. Stanley, S. Schwarzengrund and S. Rissen were isolated from lettuce samples, among which S. Schwarzengrund was resistant to AMP, CHL, NA, while S. Rissen was resistant to AMP, SXT and TET, and S. Stanley was resistant to NA [29]. Two studies in Malaysia found other Salmonella serotypes, such as S. Corvallis, S. Typhimurium and S. Enteritidis, detected from leafy vegetables, water dropwort, and long bean samples, which were accordingly resistant to multiple antibiotics [9][30]. A study in Mexico observed multidrug-resistant Salmonella in lettuce and carrot samples with resistance to AMP, cephalotin (CHT), CHL, TET, CIP, NA, streptomycin (STR), and SXT [31]. Resistance profiles of Salmonella isolates varied between studies and could not be compared, due to the detection of different serotypes. However, most of the studies (87.5%) found Salmonella isolates to be resistant to AMP.
Eight out of 40 articles (20%) reported the detection of Pseudomonas spp. in produce samples, and six of these studies reported isolates resistant to AMP. Pseudomonas spp. were frequently recovered from lettuce, carrots, and spinach. A study in Jamaica found that, among 88 P. aeruginosa isolates recovered from 95 vegetable samples, all were resistant to imipenem (IMP) (100%), followed by 97% to GEN, 93% to CIP, and 79% to CAZ [32].
Other ARBs that were often detected on leafy and non-leafy vegetables, fruits, and sprouts, were B. cereus, Enterobacter spp. [33] and Listeria spp. (predominantly L. monocytogenes), Rahnella aquatilis [34], Staphylococcus spp., Shigella spp. and Citrobacter spp. In addition, Acinetobacter spp. (predominantly A. baumannii), Sphingobacterium multivorum, Pseudomonas putida, Erwinia persicina, Pantoea agglomerans, Serratia fonticola, and Enterococcus spp. (E. faecalis and E. casseliflavus) were also found on fresh produce. Rahnella aquatilis was infrequently isolated from spinach, whereas Listeria spp. was isolated from carrot and cabbage samples. Enterococcus spp. were also detected on produce. A study that tested 112 fruit samples in the USA found 16% of samples contaminated with enterococci [35]. Another study conducted in Germany found that all B. cereus strains isolated from 137 fresh vegetables were resistant against PEN G and CTX, and 99.3% were resistant to amoxicillin-clavulanic acid (AMC) [36]. For Enterobacter spp., one study in South Africa found that E. cloacae isolated from spinach, tomato and cucumber were resistant to aminoglycoside, CHL and TET, whereas another study from Italy reported E. cloacae strains isolated from frisée salad and RTE salad were resistant to AMP, AMC and CTX [26][37]. Two studies reported penicillin resistant L. monocytogenes in fresh produce, one in Malaysia which showed all 58 L. monocytogenes strains isolated from 301 vegetable samples were resistant to PEN G and 71% (n = 41) of isolates were resistant to meropenem [28]. Another study conducted in Brazil found that L. monocytogenes from raw and RTE salad vegetable samples were resistant to PEN G and TET [38]. RTE salads consisting of leafy and non-leafy vegetables without salad dressings were contaminated with antibiotic-resistant E. coli [21][26][39], K. pneumoniae [39], L. monocytogenes [38], E. faecalis and E. faecium [40] and E. cloacae [26].

3. Antibiotic Resistance Genes on Fresh Produce

Ten articles presented findings on ARGs. Of these, seven studies detected ARGs in E. coli isolated from fresh produce. For instance, a study conducted in the Czech Republic detected the ampicillin resistance gene blaTEM, and tetracycline resistance genes tetA and tetB in E. coli isolated from asparagus, rucola, leek and raddish samples [41]. In a study from China, plasmid-mediated mobile colistin resistance (mcr-1) gene was detected in E. coli isolated from an apple sample, which also carried ten more resistance genes including aadA2, aadA1, floR, cmlA1, sul2, sul3, tetA, tetM, dfrA12, mdfA [42]. Mcr-1 positive E. coli were also isolated from carrot, pak choi, lettuce, tomato, spinach and cucumber, and were resistant to colistin (CST), AMP, GEN, NA, TET, CIP, cefotaxime (CTX), kanamycin (KAN), levofloxacin (LVX), doxycycline (DOX) and fosfomycin (FOS) [43][44][45]. A study in the Czech Republic found that the majority of E. coli isolates (13 of 15) from 108 raw vegetable samples were positive for one or multiple ARGs, including qac, sul1, tetA, int, sul1, sul3, mer and tetB [10]. One study in Germany reported that 7 out of 245 vegetable samples were positive for extended-spectrum β-lactamase (ESBL)-producing E. coli, and all ESBL-producing isolates were positive for blaCTX-M genes conferring resistance to third generation cephalosporins (3GC) [11].
ESBL-producing K. pneumoniae recovered from vegetable and fruit samples in Algeria were positive for multiple beta-lactamase genes, including blaCTX-M-15, blaOXA-1, and bla SHV-101, as well as genes that confer resistance to sulfonamides (sul1, sul2), tetracyclines (tetA), fluoroquinolones (qnrS1, aac(6′)Ib-cr, qnrB66), trimethoprim (dfrA12, dfrA14), aminoglycosides (aph(3′)-Ia, aadA2, strB, strA, aac(6′)Ib-cr, aac(3)-IIa), phenicols (catA2) and macrolides lincosamides streptogramins (MLS) (mph(A)) [24]. In addition, a study in China found that K. pneumoniae isolated from an orange sample was positive for nine ARGs, including mcr-1, blaSHV-110, qnrS1 and fosA6 [42]. Pseudomonas spp. harboring two ESBL-genes, blaTEM-116 and blaSHV-12, were detected from vegetable samples in a Japanese study [8].

4. Potential for Adverse Health Outcomes from the Consumption of Fresh Produce Contaminated with ARB/ARGs

Researchers found 25 articles that discussed health risks from consuming fresh produce contaminated with pathogens resistant to one or more antibiotics. However, the articles did not conduct any risk assessment of potential foodborne diseases due to the consumption of contaminated fresh produce. Instead, these articles broadly mentioned that consuming raw or minimally processed leafy and non-leafy vegetables can be a potential source of foodborne illnesses and invasive bacterial diseases. Moreover, the consumption of contaminated vegetables without any heat treatment or cooking may allow ARB to survive in the food, and reach the human gastrointestinal passage. Multiple studies reported that raw produce could be a vector for transmitting ARGs to the human commensal intestinal flora [21][26][38][39][40]. One article mentioned that the consumption of raw vegetables contaminated with multidrug-resistant pathogens such as Klebsiella pneumoniae increased the risk of sharing ARGs (ESBL/AmpC gene) with resident microorganisms in the gut by horizontal gene transfer [24]. Another article mentioned that Rahnella aquatilis, P. agglomerans, E. cloacae, and C. freundii might contribute to the spread of ARGs to resident bacteria [26]. The public health risks associated with exposure to ARB, especially 3GC-resistant Enterobacteriaceae are diverse, ranging from risk of difficult-to-treat diseases, to colonization and asymptomatic carriage, to mere passage through human intestines by environmental species [6][10]. Only three articles discussed the fact that gut colonization by resistant bacteria can pose a risk of complicated infection among infants, the elderly or individuals with weakened immune systems [24][30][36].
Diarrheagenic E. coli strains isolated from contaminated cucumber, lettuce and spinach were found to cause diarrhoea and other foodborne gastrointestinal diseases [21]. Consumption of contaminated fruits was also associated with diarrhea diseases, and enterotoxigenic E. coli positive for heat-stable enterotoxin-1 gene astA was identified as a causative agent [42]. Another article pointed out that the presence of the mobile colistin resistance (mcr 1) gene in E. coli isolates from lettuce samples is a serious public health concern, considering that colistin is a last-resort antibiotic used for the treatment of infections caused by multidrug-resistant bacteria. Similarly, Salmonella infection (salmonellosis) is one of the consequences of consuming fresh leafy vegetables reported in a study conducted in Malaysia [9]. Both S. Weltevreden and S. Paratyphi were isolated from leafy vegetables. S. Weltevreden causes diarrhoea in tropical regions of low-income countries, and Salmonella Paratyphi B. also causes enteric fever and gastroenteritis in humans [9]. A few articles (3 out of 40) mentioned that the emergence of drug resistant Salmonella infections linked with the consumption of raw vegetables is alarming since multidrug resistance limits the effectiveness of therapeutic treatments [28][30][46].
Antibiotic resistance in E. coli is of particular concern because it is the most common Gram-negative bacterial pathogen causing intestinal and extra-intestinal infections in humans [47]. Apart from Gram-negative bacterial pathogens, fresh produce contaminated with Gram-positive bacteria, such as Listeria spp. and Staphylococcus spp. could be potential sources of foodborne illnesses [46]. Listeriosis caused by L. monocytogenes is dangerous for vulnerable individuals; pregnant women and their fetuses, the young, and the elderly, are susceptible to invasive listeriosis, with fatality rates ranging between 20% and 40% [38]. Moreover, uncooked vegetables contaminated with P. agglomerans, P. fluorescens and Rahnella aquatilis could be possible sources of nosocomial infections in vulnerable patients in the hospital [26].

5. Pathways of Contamination of Fresh Produce with ARB

Researchers found 22 articles that discussed the potential pathways of contamination of fresh produce with ARB. The most common pathways included cross-contamination both during the pre- and post-harvesting periods.
Sources of fresh produce contamination with bacterial pathogens during pre-harvesting are diverse, including but not limited to, soils, irrigation water, or animal manure. E. coli, Salmonella spp. and Staphylococcus spp. have been detected in agricultural soils [42]. Pseudomonas species, due to their presence in environmental reservoirs (e.g., soil and water), are frequently found on vegetables. Leafy and non-leafy vegetables such as carrots are at high risk of contamination with soil-borne bacteria, either from the natural microbiota of the soil, or the manure fertilizer used in soil [32]. Untreated animal manure was the most common cause of pre-harvest spread of ARB in fresh produce [9][12][23][40][41][48]. Leafy vegetables such as parsley and water spinach that grow around swamps or riverbanks can be contaminated with wastewater released into these waterbodies by industries, slaughterhouses, or processing plants [9]. Runoff from cattle farms which contains ARB and ARGs, due to the heavy use of antibiotics in animal feed and treatment, may contaminate irrigation water, which can subsequently transfer ARB to fresh produce. Treated or untreated municipal wastewater is used for irrigation in many parts of the world; the absence of wastewater treatment facilities is a major reason for using untreated wastewater in agricultural farms in low-income countries, increasing the potential risk of contamination of produce with ARB [21].

Improper handling of fresh produce during post-harvest processing, including cutting, washing or sanitizing, transporting, packaging or storing, can also create opportunities for microbial cross-contamination [8][26]. The use of contaminated water during post-harvest washing, and the reuse of wash water, were mentioned as reasons for the contamination of fresh produce with bacterial pathogens [41]. Presence of contaminated soil particles that remain as residues on the fresh produce after harvest were mentioned as a potential source of contamination of vegetables with Arcobacter spp. [48]. Poor hygiene and sanitation practices of food handlers are often overlooked when it comes to handling vegetables and fruits in retail markets, although these can also be major sources of contamination [42]. One article mentioned that Staphylococcal contamination of fresh produce has been linked to carriage in nasal cavities of infected food handlers, or agricultural workers [49]. L. monocytogenes from animal foods can also cross-contaminate fresh produce during processing or display at marketplaces [38].

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