Spices and herbs as source of Salmonella-related foodborne diseases
Claudio Zweifel , Roger Stephan Institute for Food Safety and Hygiene, Vetsuisse Faculty University of Zurich, 8057 Zurich, Switzerland a b s t r a c t a r t i c l e i n f o Article history: Received 24 December 2010 Accepted 13 February 2011 Keywords: Spices and herbs Salmonella Serovars Outbreaks Prevalence Salmonella is a leading cause of foodborne diseases and the role of ready-to-eat products including plant- derived food is increasingly recognized. The present survey reviewed recent literature on Salmonella-related outbreaks caused by spices and herbs and on the occurrence of Salmonella in these food matrices. Spices and herbs contaminated with Salmonella were responsible for a variety of foodborne outbreaks in Europe and North America. Identied serovars did often not belong to those predominating in human illness. Moreover, in different survey studies, Salmonella belonging to a broad diversity of serovars were found in a variety of spices and herbs. The proportion of Salmonella-positive samples ranged from 0% to 8.4%, albeit detection rates were rather lowin most studies. Higher prevalence rates were often obtained with regard to a specic spice or herb type. Due to high desiccation tolerance, Salmonella can survive for an extended period of time in spices and dried herbs. Thus, by the use of untreated spices and herbs for production of foods not subjected to a heat treatment or for seasoning of ready-to-eat products, Salmonella might be introduced and in this way might pose a threat to consumers. 2011 Elsevier Ltd. All rights reserved. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 765 2. Salmonella-related outbreaks caused by spices and herbs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 766 3. Occurrence of Salmonella spp. in spices and herbs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 767 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768 1. Introduction Worldwide, Salmonella is a leading cause of acute human bacterial gastroenteritis. In the European Union, a total of 131,468 conrmed cases of human salmonellosis were reported in 2008 (EFSA, 2010). The notication rate for salmonellosis was 26.4 cases per 100,000 population, ranging from 2.9 in Romania to 126.8 conrmed cases per 100,000 population in Slovakia. As in previous years, Salmonella Enteritidis and Salmonella Typhimurium were the most frequently reported serovars (79.9% of all known serovars in human cases). With regard to foodborne outbreaks within the European Union, Salmonella spp. were responsible for 35.4% of all 5733 reported outbreaks and for 55.1% of the veried outbreaks (EFSA, 2010). The great majority of sporadic cases and outbreaks of salmonel- losis is caused by contaminated food (Scallan et al., 2011). Beside frequently mentioned foods like poultry, pork, or egg products, the role of ready-to-eat products is increasingly recognized. This is of particular concern when contamination with Salmonella cannot be excluded and the food is consumed without further heat treatment. In recent years, increased numbers of foodborne outbreaks were related to plant-derived matrices (Doyle & Erickson 2008; Lynch, Tauxe, & Hedberg 2009; Sivapalasingam, Friedman, Cohen, & Tauxe 2004). In this context, spices and herbs used all over the world for their avor properties must also be mentioned. Spices and herbs are frequently traded internationally and they are used as ingredients in manyways. Thereby it is alsoof importance that due to the globalization of food production and trade, almost every product is nowadays available year-round in developed countries and associated outbreaks are often characterized by a wide geographic distribution of cases (Sobel, Grifn, Slutsker, Swerdlow, & Tauxe 2002). If spices or herbs are contaminated with bacterial pathogens like Salmonella, such pathogens might enter the food chain (McKee 1995). Due to high tolerance to desiccation stress, Salmonella spp. can thereby survive for an extended period of time in dried products such as spices (Hiramatsu, Matsumoto, Sakae, &Miyazaki 2005; Lehmacher, Bockemhl, &Aleksic 1995; Ristori, dos Santos Pereira, &Gelli 2007). The contamination of spices and herbs Food Research International 45 (2012) 765769 Corresponding author. Tel.: +41 44 635 8651; fax: +41 44 635 8908. E-mail address: zweifelc@fsafety.uzh.ch (C. Zweifel). 0963-9969/$ see front matter 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2011.02.024 Contents lists available at ScienceDirect Food Research International j our nal homepage: www. el sevi er. com/ l ocat e/ f oodr es with Salmonella can occur at all stages including growing, harvesting, processing, storage, packaging, and sale (McKee 1995). The mainte- nance of good manufacturing and hygiene practices, together with appliance of HACCP principles, is therefore of great importance during growing, harvesting, and processing. Additionally, decontamination procedures might be applied for dried spices and herbs to reduce the level of contamination. The aimof the present reviewwas to elucidate the role of spices and herbs as source of Salmonella-related foodborne diseases based on published data. For this purpose, PubMed (http://www.pubmed.com) andScienceDirect (http://www.sciencedirect.com) were searched using combinations of the keywords Salmonella, spices, herbs, and outbreaks. Moreover, literature inselectedstudies was crosschecked. Basedontitles and abstracts, studies covering Salmonella-related outbreaks caused by spices and herbs as well as studies on the occurrence of Salmonella spp. in/on spices and herbs published since 1994 were selected. 2. Salmonella-related outbreaks caused by spices and herbs Selected Salmonella outbreaks caused by spices and herbs are shown in Table 1. Specied is thereby the number of conrmed cases. These numbers represent only a small proportion of the total illness in the outbreaks, as many patients either do not seek care or do not have a stool culture performed. On the other hand, spices and herbs that are typically consumed in small quantities as ingredients of other dishes can be difcult to implicate. Nevertheless, the selected examples show that spices and herbs contaminated with Salmonella of various serovars (commonly not predominating in human illness) might be responsible for foodborne outbreaks. In the United States, two Salmonella outbreaks related to spices occurred in 2009 and 2010 (CDC, 2010; Kennelly 2010). Identication of the most probable causative products was accomplished only after extensive epidemiological and microbiological investigations. In the nationwide Salmonella Montevideo outbreak (CDC, 2010), which comprised 272 patient-cases in 44 states and DC, preliminary analysis suggested salami as possible source (Table 1). Intensied examina- tions identied black and red pepper as most likely source of contamination. In the course of this outbreak, more than 640,000 kg of ready-to-eat salami products were recalled. Additionally, Salmonella Senftenberg was found in food samples from retail and a patient household during this outbreak investigation, but the related 11 cases were not included in the case count reported above. The other multistate outbreak was caused by the consumption of white pepper contaminated with Salmonella Rissen (Kennelly 2010 2010). This outbreak comprised at least 85 conrmed cases in ve different states (California, Idaho, Nevada, Oregon, Washington). Interestingly, pepper was already associated with a Salmonella outbreak in Norway years ago (19811982) (Gustavsen&Breen1984). This outbreak comprising 126 patient-cases was caused by Salmonella Oranienburg and black pepper imported from Brazil was the implicated product. Besides, the nationwide Salmonella Saintpaul outbreak during the summer of 2007 (CDC, 2008) is also worth mentioning, although fresh jalapeo and serrano peppers are regarded fresh produce. This outbreak comprised 1442 patient-cases from 43 states, DC, and Canada. At least 286 persons were hospitalized and the infection might have contributed to two deaths. The initial casecontrol study identied an association between illness and eating rawtomatoes. Although tomatoes possibly were a source of contamination early in the outbreak, subsequent epidemiological and microbiological investigations supported the conclusion that Mexican jalapeo and serrano peppers were major vehicles. In 2006 and 2007, two outbreaks were associated with Salmonella- contaminated fresh basil (Table 1). While fresh herbs are unusual products to be consumed alone, they are frequently used as ingredients in a variety of retail-prepared or homemade ready-to- eat products. The Salmonella Senftenberg outbreak (Pezzoli et al., 2008) comprised 51 patient-cases in England, Wales, Scotland, Denmark, the Netherlands, and the United States. By using molecular techniques, the same genotype of Salmonella Senftenberg was identied in human isolates and in pre-packed fresh basil for sale in the United Kingdom and grown in Israel. The second outbreak (Pakalniskiene et al., 2009) caused by the consumption of pasta salad with pesto affected about 200300 of 750 students and teachers attending a high-school dinner in Greater Copenhagen, November 2006. The pesto was prepared about 48 h prior to consumption. The fresh basil used as ingredient for the pesto was the most likely source of contamination. This outbreak was primary due to enterotoxigenic Escherichia coli, but Salmonella Anatum also played a role as a certain strain was found in the pasta salad and some patients. Furthermore, a Salmonella Agona outbreak affecting infants in Germany (20022003) was caused by aniseed-containing herbal tea imported from Turkey (Koch et al., 2005) and a Salmonella Thompson outbreak in California (1999) was associated with fresh cilantro (Campbell et al., 2001). A large outbreak of salmonellosis caused by contaminated spices occurred in Germany in 1993 (Table 1). Due to the consumption of contaminated paprika-powdered potato chips more than 1000 persons, especially children under the age of 14 fell ill (Lehmacher et al., 1995). The spice mixtures were thereby applied to the roasted chips at the end of the production where the temperature had already dropped to about 60 C. Striking about this outbreak was the great variety of detected rare Salmonella serovars and monophasic or non- motile strains. Salmonella Saintpaul, Salmonella Rubislaw, and Salmo- nella Javiana predominated and these serovars were found in patients, paprika powder imported from South America, and paprika-avored products. Interestingly, results of Lehmacher et al. (1995) suggested that very low numbers of Salmonella (less than 50 organisms in a person who had consumed 100 g of chips) were able to cause illness in this outbreak. Due to cross-resistance, desiccation stress occurring in dry food matrices might trigger up-regulated acid (and heat) resistance contributing to the observed low infectious dose. Table 1 Selected Salmonella-related outbreaks caused by spices and herbs. Year Pathogen No. of cases Affected country Implicated products References 20092010 Salmonella Montevideo 272 United States (44 states, DC) Black and red pepper CDC, 2010 2009 Salmonella Rissen 87 United States (5 states) White pepper Kennelly 2010 2007 Salmonella Senftenberg 51 United Kingdom, Denmark, Netherlands, United States Fresh basil Pezzoli et al., 2008 2006 Salmonella Anatum a N200 Denmark (Greater Copenhagen) Fresh basil (pesto) Pakalniskiene et al., 2009 20022003 Salmonella Agona 42 Germany Aniseed-containing herbal tea Koch et al., 2005 1999 Salmonella Thompson 76 b United States (California) Fresh cilantro Campbell et al., 2001 1993 Various Salmonella serovars c N1000 Germany Paprika and paprika-powdered potato chips Lehmacher et al., 1995 a Outbreak due to enterotoxigenic Escherichia coli and Salmonella Anatum. b Thirty-ve sporadic cases and a restaurant-associated outbreak of 41 cases. c In particular Salmonella Saintpaul, Rubislaw, and Javiana. 766 C. Zweifel, R. Stephan / Food Research International 45 (2012) 765769 3. Occurrence of Salmonella spp. in spices and herbs In the European Union, a wide range of foodstuffs including different kinds of plant-derivedproducts was testedfor Salmonellabythemember states in 2008 (EFSA, 2010). Within these monitoring examinations, seven studies from six countries (Austria, Hungary, Ireland, the Netherlands, Romania, Slovakia) addressed the occurrence of Salmonella in spices and herbs. Salmonella spp. were detected in three of these studies and the proportion of positive samples accounted for 1.0% (2/198), 3.9% (69/1768), and 6.7% (3/45) in Hungary, the Netherlands, and Slovakia, respectively. Except for spices, herbs, and sprout seeds, Salmonella were rarely detected in plant-derived products within these monitoring investigations (EFSA, 2010). Additional surveillance data fromGermany showed that examination of spices for Salmonella yielded positive results in1.3%(2008) and0.5%(2009) of morethan600samples tested in each year (Hartung 2009; Hartung 2010). Further recently performed investigations on the occurrence of Salmonella spp. in spices and herbs are summarized in Table 2. The column sample location also lists the region/country where examinations were performed. Yet it must be mentioned that a considerable proportion of the implicated spices and herbs were imported from various countries distributed throughout the world. Based on the evaluated studies examining spices and herbs (Table 2), Salmonella spp. were detected in 11 studies, whereas four surveys yielded negative results. The latter comprised studies performed in Spain (Cosano et al., 2009), the United States (Johnston et al., 2006), Mexico (Garca, Iracheta, Galvn, & Heredia 2001), or Norway (Johannessen, Loncarevic, & Kruse 2002). Johnston et al., (2006) investigated the microbial quality of fresh produce of domestic and Mexican origin. Of the 466 samples collected at packing sheds, 222 originated from fresh herbs (cilantro, dill, parsley), but Salmonella were not detected. Similarly, Garca et al. (2001) did not nd Salmonella in 304 samples from retail herbs and spices (bay leaves, black pepper, cumin seeds, garlic powder, oregano) collected at Mexican markets. In Norway, Johannessen et al. (2002) analyzed the microbial quality of fresh produce (including 230 samples of growing herbs, dill, and parsley) but failed to detect Salmonella. Later however, Salmonella were found in 28% (2007) and 15% (2007) of fresh herbs and leafy vegetables imported from South-East Asia (NSCFS, 2008). Isolated strains thereby belonged to 18 different serovars. The main ndings of the 11 studies yielding Salmonella-positive results in spices and herbs are briey summarized below (Table 2). Four of them were performed in the United Kingdom (Elviss et al., 2009; Little, Omotoye, & Mitchell 2003; Sagoo et al., 2009; Surman- Lee, Murphy, Pathak, Clements, & de Pinna 2008). Sagoo et al. (2009) assessed the microbial status of dried spices and herbs fromretail and production premises in 2004. Salmonella spp. were detected in 31 (1.1%) of 2833 retail samples. Thereby, 1.0% of 2090 spice samples and 1.4% of 743 herb samples tested positive. Besides, two (1.5%) of 132 production batches were positive for Salmonella. In this study, Salmonella spp. were found in many different spices and herbs with contamination rates ranging from 0.6% to 14%. Moreover, a great variety of Salmonella serovars was obtained (Table 2), whilst 20% of the serotyped isolates were identied as Salmonella Senftenberg. An earlier study by Little et al. (2003) revealed that Salmonella were present in one (0.1%) of 750 spices and spice ingredients examined. On the other hand, in the study of Elviss et al. (2009), 3760 ready-to- eat fresh herbs of different varieties were sampled across the United Kingdom in 2007. Eighteen (0.5%) samples of six different herb types were thereby contaminated with Salmonella spp. at retail premises. Comparable to the ndings of Sagoo et al. (2009), different Salmonella serovars were obtained from the contaminated herb samples (Table 2). Eight samples of pre-packed basil produced by a grower in Israel were all contaminated with Salmonella Senftenberg. Following the isolation of Salmonella Senftenberg from basil, a multinational outbreak caused by the same strain was recognized (Pezzoli et al., 2008). Furthermore, a pan-London retail study of fresh herbs in 2006 showed that 1.7% (5/298) of the samples tested positive for Salmonella and the isolates belonged to four different serovars (Surman-Lee et al., 2008). In the United States, a Food and Drug Administration survey of domestic fresh produce in 2000 and 2001 reported that 0.6% of fresh herbs (parsley, cilantro) were contaminated with Salmonella (FDA, 2003), whereas another surveyof importedfreshproduce in1999found Table 2 Selected studies on the occurrence of Salmonella in spices and herbs. Products Sample location Positive samples/ total samples (%positive) Salmonella serovars References Fresh herbs a Retail, United Kingdom 18/3760 (0.5%) Agona, Anatum, Durban, Javiana, Mgulani, Montevideo, Newport Senftenberg, Virchow Elviss et al., 2009 Dried spices and herbs b Production / Retail, United Kingdom 2/132 (1.5%) / 31/2833 (1.1%) Aequatoria, Agona, Caracas, Clifton, Derby, Edinburg, Friedenau, Hato, Hvittingfoss, Infantis, Mbandaka, Montevideo, Poona, Saintpaul, Schwarzengrund, Senftenberg, Tennessee, Typhimurium Sagoo et al., 2009 Spices c Retail, So Paulo 13/233 (5.6%) Serovars not determined Moreira et al., 2009 Saffron Spain 0/79 (0%) No Salmonella detected Cosano et al., 2009 Fresh herbs d Retail, London 5/298 (1.7%) Newport, Uphill, Virchow, Weltevreden Surman-Lee et al., 2008 Spices e Retail, Tokyo 2/259 (0.8%) Senftenberg, Weltevreden Hara-Kudo et al., 2006 Fresh herbs Southern United States 0/222 (0%) No Salmonella detected Johnston et al., 2006 Spices f Retail, India 2/154 (1.3%) Serovars not determined Banerjee & Sarkar 2003 Spices United Kingdom 1/750 (0.1%) Enteritidis PT11 Little et al., 2003 Fresh herbs g United States 1/175 (0.6%) / 23/273 (8.4%) Serovars not determined FDA, 2003 / FDA, 2001 Fresh herbs Norway 0/230 (0%) No Salmonella detected Johannessen et al., 2002 Spices and herbs Retail, Mexico 0/304 (0%) No Salmonella detected Garca et al., 2001 Spices and condiments Retail, Trinidad 1/200 (0.5%) Derby Rampersad et al., 1999 Spices and herbs h Retail, Vienna 1/160 (0.6%) Arizonae Kneifel & Berger 1994 a Detection of Salmonella spp. in basil, cilantro, curry leaves, mint, parsley, and walleria. b Detection of Salmonella spp. in all spice, black pepper, cayenne, chili, coriander, cinnamon, cumin, curry, fennel, fenugreek, garam masala, mint, okra, sage, and turmeric. c Detection of Salmonella spp. in black pepper, and cumin. d Detection of Salmonella spp. in basil, cilantro, and curry leaves. e Detection of Salmonella spp. in black and red pepper. f Detection of Salmonella spp. in ginger, and poppy seeds. g Detection of Salmonella spp. in cilantro, culantro, and parsley. h Detection of Salmonella spp. in black pepper. 767 C. Zweifel, R. Stephan / Food Research International 45 (2012) 765769 8.4% of fresh herb samples (cilantro, culantro, parsley) to be contam- inated (FDA, 2001). Although the intent was not to draw quantitative comparisons between the prevalence of contamination of domestic and importedproduce, the different detectionrates might reect differences in conditions during pre- and post-harvest operations. Based on the studies included in the present review (Table 2), Salmonella-contaminated spices and herbs were also detected in surveys from Brazil (Moreira, Loureno, Pinto, & Rall 2009), Japan (Hara-Kudo et al., 2006), India (Banerjee & Sarkar 2003), Trinidad (Rampersad et al., 1999), and Austria (Kneifel & Berger 1994). In the study of Moreira et al. (2009) examining the microbial status of various commodities (basil, bay leaves, black pepper, cinnamon, clove, cumin, dehydrated green onion, dehydrated parsley, oregano) marketed in So Paulo, 13 (5.6%) of 233 samples were positive for Salmonella. Salmonella spp. were isolated from12 (18.2%) of 66 black pepper samples and from one of 12 cumin samples, but not from the other commodities. Interestingly, in another Brazilian study, Salmonella Typhimurium was found in Brazil nut kernels (Freire & Offord 2002). Hara-Kudo et al. (2006) investigated the prevalence of Salmonella in spices imported to Japan and purchased at retail shops in Tokyo. Of the 259 samples comprising 40 product types, two (0.8%) were contaminated with Salmonella, although at low concentrations. The two positive samples originated from black pepper (2.4%, n=42) and red pepper (1.7%, n=59). Salmonella isolates belonged to serovars Weltevreden (black pepper) and Senftenberg (red pepper). In the study of Banerjee and Sarkar (2003) examining the microbial status of 27 types of spices (154 samples) from retail stores distributed over 20 Indian states, Salmonella spp. were only found in two (1.3%) samples, one each of ginger and poppy seeds. Rampersad et al. (1999) primarily investigated the microbial quality of oysters sold in Western Trinidad, but the occurrence of Salmonella in condiments/spices was also determined. One (0.5%) of the 200 samples fromcondiments/spices was positive for Salmonella and the isolate belonged to the serovar Derby. Finally, the survey of Kneifel and Berger (1994) showed that one black pepper sample out of 160 samples from 55 different spice and herb types retailed in Vienna contained Salmonella (Salmonella Arizonae). Summing up these results, it can be stated that Salmonella spp. were found in a variety of spices and herbs, albeit detection rates were rather low in most studies. In particular (black) pepper, cilantro, or basil repeatedly tested positive for Salmonella. Overall, the proportion of Salmonella-positive samples ranged from 0% to 8.4%. Yet it must be considered that the results listed in Table 2 refer to all spice or herb samples examined. With regard to specic spice or herb types, higher prevalence rates of Salmonella were frequently obtained. For example, in the survey of Moreira et al. (2009) examining various commodities, 18.2% of the black pepper samples tested positive. Moreover, the diversity of Salmonella serovars identied among the positive samples must be emphasized, especially the great diversity obtained in the extensive studies of Elviss et al. (2009) and Sagoo et al. (2009). This diversity might also be associated with the growing international trade of spices and herbs. Furthermore, a review performed by Vij, Ailes, Wolyniak, Angulo, and Klontz (2006) showed that between 1973 and 2003 20 of 21 recalls involving spices in the United States were due to contamination with Salmonella spp. (the exception was a recall of bay leaves contaminated with Listeria monocytogenes). Sixteen of the 21 recalls occurred during the last 4 years of the study period, whereas the remaining ve recalls were distributed over the preceding 30 years. Overall, these recalls involved 12 spice types. Cumin, oregano, paprika, sage, sesame seeds, and thyme were thereby responsible for two or more recalls. Information about Salmonella serovars was available for 10 recalls and the serovars Bispebjerg, Derby, Gaminara, Haifa, Karlshamn, Ohio, Onderstepoort, Salford, and Senftenberg were identied (Vij et al., 2006). The country of origin of the spice was known for 14 of the Salmonella-related recalls: 12 involved imported spices (Egypt, India, Jamaica, Mexico, Spain, Taiwan, Turkey), whereas the remaining recalls comprised domestically produced spices (Vij et al., 2006). 4. Conclusions The present data on Salmonella-related outbreaks and on the occurrence of Salmonella spp. emphasize that spices and herbs might constitute a threat for the contamination of various food products with Salmonella. In the European Union, Salmonella is currently not dened as a food safety criterion for spices and herbs (Anonymous 2005). But Regulation (EC) No 178/2002 lays down general food safety requirements, according to which food must not be placed on the market if it is unsafe (Anonymous 2002). Food business operators are therefore also testing spices and herbs for Salmonella. By the use of untreated spices for the production of e.g. meat products as cured rawproducts or rawsausages that are not subject to a heating step (at least pasteurization) during production or by the use of untreated spices for the seasoning of ready-to-eat products, Salmonella might be introduced. Even if growth is not expected due to intrinsic factors and process parameters, Salmonella will be present in the nal product. The nding of Salmonella spp. is a reason for complaint, might result in large recalls or changed buying behavior of consumers, and under certain circumstances can pose a threat for consumer's health. Hence, in terms of the production of ready-to-eat products, food business operators should also monitor the microbi- ological status of spices and herbs. But because such randommicrobial testing is not sufcient to warrant control of Salmonella, the use of products subjected to decontamination treatments (as e.g. irradiation, steam, high pressure) to enhance the microbial safety and quality is recommended. However, potential affection of avor characteristics by such treatments remains to be elucidated for each particular matrix. Seen this way, the use of spice extracts also needs to be considered, in particular if taking into account that spices might be added to foods that are not further processed. References Anonymous (2002). Regulation (EC) No 178/2002 of the European Parliament and the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Ofcial Journal of the European Union, L31. Anonymous (2005). 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