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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
Spices and herbs
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.
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.
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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
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
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
United States (California) Fresh cilantro Campbell et al., 2001
1993 Various Salmonella serovars
N1000 Germany Paprika and paprika-powdered potato chips Lehmacher et al., 1995
Outbreak due to enterotoxigenic Escherichia coli and Salmonella Anatum.
Thirty-ve sporadic cases and a restaurant-associated outbreak of 41 cases.
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
Retail, United Kingdom 18/3760 (0.5%) Agona, Anatum, Durban, Javiana, Mgulani,
Montevideo, Newport Senftenberg, Virchow
Elviss et al., 2009
Dried spices and herbs
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
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
Retail, London 5/298 (1.7%) Newport, Uphill, Virchow, Weltevreden Surman-Lee et al., 2008
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
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
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
Retail, Vienna 1/160 (0.6%) Arizonae Kneifel & Berger 1994
Detection of Salmonella spp. in basil, cilantro, curry leaves, mint, parsley, and walleria.
Detection of Salmonella spp. in all spice, black pepper, cayenne, chili, coriander, cinnamon, cumin, curry, fennel, fenugreek, garam masala, mint, okra, sage, and turmeric.
Detection of Salmonella spp. in black pepper, and cumin.
Detection of Salmonella spp. in basil, cilantro, and curry leaves.
Detection of Salmonella spp. in black and red pepper.
Detection of Salmonella spp. in ginger, and poppy seeds.
Detection of Salmonella spp. in cilantro, culantro, and parsley.
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.
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