Prevalence, serotype diversity, and antimicrobial resistance of Salmonella in imported shipments of spice offered for entry to the United States, FY2007–FY2009

Abstract

In response to increased concerns about spice safety, the U.S. FDA initiated research to characterize the prevalence of Salmonella in imported spices. Shipments of imported spices offered for entry to the United Sates were sampled during the fiscal years 2007–2009. The mean shipment prevalence for Salmonella was 0.066 (95% CI 0.057–0.076). A wide diversity of Salmonella serotypes was isolated from spices; no single serotype constituted more than 7% of the isolates. A small percentage of spice shipments were contaminated with antimicrobial-resistant Salmonella strains (8.3%). Trends in shipment prevalence for Salmonella associated with spice properties, extent of processing, and export country, were examined. A larger proportion of shipments of spices derived from fruit/seeds or leaves of plants were contaminated than those derived from the bark/flower of spice plants. Salmonella prevalence was larger for shipments of ground/cracked capsicum and coriander than for shipments of their whole spice counterparts. No difference in prevalence was observed between shipments of spice blends and non-blended spices. Some shipments reported to have been subjected to a pathogen reduction treatment prior to being offered for U.S. entry were found contaminated. Statistical differences in Salmonella shipment prevalence were also identified on the basis of export country.

Introduction

In 2006, FDA reported that Salmonella contamination of spices was the cause of 95% of the U.S. food recalls associated with spices over the period 1980–2000 (Vij et al., 2006). Between 2007 and 2010, three large-scale salmonellosis outbreaks in the United States were attributed to consumption of Salmonella-contaminated spices/seasonings (Sotir et al., 2009; CDC, 2010; Higa, 2011). Since that time, FDA established the Reportable Food Registry (RFR), an early warning system that enables industry and public health officials to report hazards in foods before the food reaches the consumer (USFDA, 2012a, USFDA, 2012b). In its first two years of reporting (Sept. 2009–Sept 2011; USFDA, 2012c, USFDA, 2012d), “spices and seasonings” led nearly all human food categories in total number of RFR primary entries (ranked 2nd in years 1 and 2) and number of primary entries associated with Salmonella (ranked 1st in year 1 and 2nd in year 2). The present study is a part of a larger effort by the United States Food and Drug Administration (FDA) to conduct spice safety research to assess the salmonellosis public health risk posed by spice consumption in the U.S. and to assist the agency in identifying options to mitigate the risk (USFDA, 2010).

The U.S. is one of the largest importers of spices, on the basis of both volume and value (Buzzanell et al., 1995), with more than 80% of the total U.S. spice supply provided by imports (USDA/ERS, 2011). The present study examines FDA Salmonella surveillance sampling and testing results for a variety of imported spices offered for entry to the U.S. over a three year period. In addition to determining an average Salmonella prevalence value for spices sampled, this study examines whether Salmonella prevalence is strongly dependent on the type of spice, extent of processing, and country of export. Subtype and antimicrobial resistance information provide insights into the diversity of Salmonella found in spices. This is the first comprehensive study of Salmonella contamination of spices imported into the United States, updating a very limited study in 1987–8 (Satchell et al., 1989) and complementing the examination of recall events from 1980 to 2000 (Vij et al., 2006).