This study provides data for the first time on the prevalence of resistant Escherichia coli and Salmonella enterica from lettuce and cabbages sources in the Tamale metropolis of Ghana. It also provides baseline information by which other studies can be compared. Resistance of foodborne pathogens including Escherichia coli and Salmonella enterica to multiple antibiotics has become an emerging public health issue worldwide. The use of antibiotics in agricultural practices have contributed immensely to the development of resistant foodborne pathogens (Cohen 2000; Adams and Moss 2008; Golly et al. 2016; Jongman and Korsten 2016). Antibiotics are mostly used for treatment of animals and humans against bacterial infections. This can lead to some bacteria developing resistance against the antibiotics being used to control them. Subsequently, animals and humans share these pathogens which find their way into water bodies some of which are used to irrigate vegetables. The results of this is that vegetables get contaminated with these resistant pathogens which can also be easily transferred to other food sources. A number of sources including application of manures to the farm from slaughter houses, in vitro propagation of crops (tissue cultured plants), antibiotics spray on the crops in the orchard, soil and water contamination with fecal material and effluent from farm animals at the field, and genetic engineering causing increased antibiotic resistance have noted as sources by which antibiotic resistances are incorporation into fruits and vegetables (Rashmi et al. 2017). In Nigeria, Afolabi and Oloyede (2010) found irrigation water as possible source of food borne pathogens in raw vegetables. In South Africa, Jongman and Korsten (2016) indicated that there is a link between the Escherichia coli isolates from irrigation water sources and leafy green vegetables in their phenotypic (antimicrobial) and genotypic (DNA fingerprinting) analyses. Schwaiger et al. (2011) suggested that expressing resistance by bacteria isolated from vegetables is at the expense of bacterial viability, since vegetables purchased directly at the farm are probably fresher than at the supermarket, and they have not been exposed to stress factors. Mąka and Popowska (2016) reported that the use of a single antibiotic might result in the development of resistance to other antimicrobial compounds of the same or different classes.
Antibiotic resistance of Escherichia coli isolates of lettuce and cabbage samples in the present study is comparable. The overall resistance (54.55% vs 52.59%), intermediate resistance (9.09% vs 10.37%) and susceptibility (36.36% vs 37.04%) for cabbage and lettuce, respectively were similar. Rodloff et al. (2008) indicated that intermediate resistance is associated with an uncertain therapeutic effect. Escherichia coli from both sources showed high resistance to the penicillin (ampicillin), macrolide (erythromycin) and ofloxacin (quinolone) but showed susceptibility to the quinolone (ciprofloxacin). Susceptibility to the cephalosporin (ceftriaxone), aminoglycoside (gentamicin) and sulfonamide (suphamethoxazole/trimethoprim) were also similar among the Escherichia coli lettuce and cabbage isolates. Intermediate resistances were more prevalent in Escherichia coli of cabbage source than that of lettuce (5 vs 3, respectively). Golly et al. (2016) reported that Escherichia coli from cabbage, lettuce and carrot sources were resistant to ampicillin (90.9%), tetracycline (54.5%), gentamicin (18.2%), chloramphenicol (63.6%) and ceftriaxone (54.5%), which were relatively similar to that of the present study. Contrarily to this study, Jongman and Korsten (2016) found that Escherichia coli isolates from green leafy vegetables were susceptible to ceftriaxone (100%) and gentamicin (100%).
All Escherichia coli isolates from lettuce and cabbage samples were resistant to at least 3 different antibiotics, thus 100% multidrug resistant was observed among the Escherichia coli isolates. Furthermore, cabbage Escherichia coli isolates were resistant to seven (9.09%), six (27.27%), five (27.27%) and four (18.18%) different antibiotics, while lettuce Escherichia coli isolates were resistant to six (20%), five (40%) and four (20%) different antibiotics. Jongman and Korsten (2016) found that 19 (14.6%) of Escherichia coli isolates from leafy green vegetables (n = 70) and water (n = 60) sources were resistant to one antibiotic (tetracycline) and 92 (70.7%) were resistant to various antibiotics (including ampicillin, cefoxitin, and nalidixic acid).
Antibiotic resistance of Salmonella enterica from lettuce and cabbage samples revealed some similarities and differences in resistance percentages and patterns. The overall resistance (48.77% vs 35.80%), intermediate resistance (11.11% vs 10.49%) and susceptibility (40.12% vs 53.70%) for cabbage and lettuce, respectively were quite dissimilar. Resistance to the penicillin (ampicillin), macrolide (erythromycin) and quinolone (ofloxacin) were similar but not resistance to the chloramphenicol (chloramphenicol), quinolone (ciprofloxacin), cephalosporin (ceftriaxone), aminoglycoside (gentamicin), tetracycline (tetracycline) and sulfonamide (suphamethoxazole/trimethoprim). Susceptibility followed similar trend except for resistance to erythromycin. Intermediate resistances were also similar between lettuce and cabbage Salmonella enterica isolates. Intermediate resistance has been suggested to be those isolates which are not clearly resistant or susceptible, and such isolates have the tendency to easily become resistant (Adzitey et al. 2012; Adzitey et al. 2015). Generally, Salmonella enterica isolates from cabbage were more resistant than those from lettuce sources. Golly et al. (2016) found that Salmonella species isolated from cabbage, lettuce and carrot sources were resistant to ampicillin (100%), tetracycline (63.6%), gentamicin (9.1%), chloramphenicol (72.7%) and ceftriaxone (63.6%), which was relatively dissimilar to the present study.
The lettuce and cabbage Salmonella enterica isolates were resistant to at least 2 different antibiotics. Resistance to seven (5.56%), six (5.56%), and four (5.56%) different antibiotics occurred for lettuce Salmonella enterica isolates. Resistance to seven (11.11%), six (22.78%) and five (16.67%) antibiotics was found for cabbage Salmonella enterica isolates. This indicates that cabbage and lettuce samples harboured high levels of multidrug resistant Salmonella enterica isolates. The resistance pattern ampicillin-ofloxacin-erythromycin (AmpOfxE) was the commonest considering all Salmonella enterica isolates of both lettuce and cabbage sources. Seven and twelve resistance patterns were found for lettuce and cabbage Salmonella enterica isolates, respectively. Golly et al. (2016) reported that their Salmonella isolates showed seven resistance patterns to eight commonly used antibiotics. They also reported that all their isolates exhibited multidrug resistance.
Antibiotics and their resistant patterns by foodborne pathogens have evolved over the years. Differences and similarities in resistance patterns can occur among foodborne isolates from the same or different sources. These differences have been reported to be widely due to the differences in in geographical locations, the bacteria species involved, the animal production systems employed, the extent to which antibiotics are used, sampling techniques and period of sampling (Adzitey 2015b). Rashmi et al. (2017) stated that, the presence of residual antibiotics in foods constitute an important health risk because of the increased microbial resistance detected in latest years.