Microbial Safety and Sanitary Quality of Strawberry Primary Production in Belgium: Risk Factors for Salmonella and Shiga Toxin-Producing Escherichia coli Contamination

Abstract

Strawberries are an important fruit in Belgium in both production and consumption, but little information is available about the presence of Salmonella and Shiga toxin-producing Escherichia coli (STEC) in these berries, the risk factors in agricultural production, and possible specific mitigation options. In 2012, a survey was undertaken of three soil and three soilless cultivation systems in Belgium. No Salmonella spp. were isolated. No STEC was detected in the strawberry samples (0 of 72), but STEC was detected by PCR in 11 of 78 irrigation water and 2 of 24 substrate samples. Culture isolates were obtained for 2 of 11 PCR-positive irrigation water samples and 2 of 2 substrate samples. Multivariable logistic regression analysis revealed elevated generic E. coli numbers (the odds ratio [OR] for a 1 log increase being 4.6) as the most important risk factor for STEC, together with the berry-picking season (elevated risk in summer). The presence of generic E. coli in the irrigation water (>1 CFU per 100 ml) was mainly influenced by the type of irrigation water (collected rainfall water stored in ponds was more often contaminated than groundwater pumped from boreholes [OR ‫؍‬ 5.8]) and the lack of prior treatment (untreated water versus water subjected to sand filtration prior to use [OR ‫؍‬ 19.2]). The follow-up study in 2013 at one of the producer locations indicated cattle to be the most likely source of STEC contamination of the irrigation water.

Occurrence of Escherichia coli, Campylobcter, Salmonella and Shiga-Toxin Producing E. coli in Norwegian Primary Strawberry Production

“…Delbeke et al . [10] enumerated E. coli in two of 72 samples in a study similar to ours, whereas in Yoon et al . [9] and Muherjee et al .…”

“…Delbeke et al . [10] detected E. coli in approximately 30% of the substrate samples and 56% of the water samples. The higher prevalence of E.coli in water samples in our study can be explained by the fact that the Norwegian producers used surface water without treatment, while in Belgium borehole water and collected rainfall water stored in ponds with or without barriers were used.…”

“…Another source for STEC would be the irrigation water, but the farmer informed us that no irrigation had been applied this season. Delbeke et al [10] isolated STEC O26 from strawberry irrigation water and substrate on one farm that also had cattle. In a follow-up study on the particular farm one year later, fecal samples from the cattle were PCR positive for STEC O26, but no isolates were obtained for further comparison.…”

“…In a survey carried out by the US Food and Drug Administration (FDA), Salmonella was detected in one of a total of 143 samples of imported strawberries [7]. Only a few studies have been found in the literature regarding primary production of strawberries, and the results from these surveys also indicate low occurrence of fecal indicators and typical pathogens on strawberries [8,9,10]. …”

Contamination of Fresh Produce by Microbial Indicators on Farms and in Packing Facilities: Elucidation of Environmental Routes

“…Ultimately, there are no comprehensive prospective studies directly linking microbial contamination of fresh produce to that of hands, soil, water, or surfaces in the natural setting of the agricultural production environment. This may be due to logistical constraints in setting up a matched study design (6,17), resource constraints in acquiring large sample sizes (18), application of the appropriate statistical analyses to account for multivariable factors affecting microbial contamination (6,(19)(20)(21), and data variability from diverse microbial distributions on produce and environmental samples (22)(23)(24). Because of the low rate of detection of pathogen contamination (25)(26)(27)(28), populations of microbial-indicator organisms, including organisms that indicate filth (coliforms) and/or fecal contamination (Escherichia coli, Enterococcus spp., and somatic coliphage), can be monitored (reviewed in references 29 to 31).…”