DOI: https://doi.org/10.21203/rs.3.rs-2277306/v1
Ochratoxin A is one of the most important toxic metabolites of fungi that can be found in agricultural products. This study aimed to estimate the prevalence and concentration of OTA in spices through meta-analysis. Therefore, online databases including PubMed, Web of Science, and Scopus were screened systematically from 1995 to 2022 to collect the related data. After assessing for eligibility, 36 articles with 1686 samples were included in the study. According to findings, the global pooled prevalence of OTA was counted as 50% (95% CI: 47–52%). Moreover, the highest and lowest concentrations of OTA in spices were noted in paprika (50.66 ng/g) and cinnamon (3.4 ng/g), respectively. The outcome of this meta-analysis can be used for risk assessment model development, aiming to help the government and industries for finding a specific way to reduce the prevalence of OTA spice products.
Spices are generally derived from the non-leafy parts of the source plants including the seeds, bark, root, flowers, or fruits (Viuda-Martos et al. 2010). They are widely used to enhance aroma, taste, color, smell, and flavor in daily food preparations (Kabak and Dobson 2017). Due to their preservative characteristics, spices have potential applications in food industry. On the other hand, these products are among the most efficient plant species for medical purposes because of their treatment effects on acute and chronic diseases. In this context, spices are rich sources of various phytochemicals (Srinivasan 2014). Phytochemicals are a large group of bioactive compounds found in plants that have potential protective effects on the health of human (Shan et al. 2005; Srinivasan 2014). These natural compounds are consists of flavonoids and other phenolic chemicals, thus provide protection against oxidation by reacting with free radicals or form complexes with metal ions. For example, several antioxidants from spices, such as gingerol (ginger), eugenol (red pepper), and curcumin (turmeric), coumarin (cumin), were experimentally evidenced to control cellular oxidative stress due to render antioxidant activity and their ability to scavenge free radicals (Embuscado 2015). Besides, antimicrobial, antidiabetic, and immunomodulatory effects of some spices have been confirmed, such as cinnamon. In addition, curcumin as a spice compound is able to act like an anti-inflammatory agent by interacting with various inflammatory processes (Nilius and Appendino 2013). Spices can contribute to the prevention and treatment of some cancers due to their anti-oxidative characteristics (Zheng et al. 2016). In terms of trade value, red chilli, black pepper, paprika, turmeric, cumin, coriander, cumin, nutmeg and ginger are the most important spices used all over the world. spice crops are cultivated worldwide, but most of them originated in India (74%), Bangladesh (6%), Turkey (5%) and China (5%). In recent years, there have been increasing concerns over the food safety of consumers. Several factors including poor harvesting practices, improper storage, processing, packaging, drying method and distribution influence fungal growth responsible for spoilage and mycotoxin production (Thanushree et al. 2019). All the steps during production and storage have critical effects on spice quality. Fungal contamination of spices is one of the main issues may occur at all the steps during production and storage and is very important from human health perspectives. Fungal contamination of spices leads to serious consequences for animal and human health by production of mycotoxins (Richard 2007). Mycotoxins are a limited group of toxic secondary metabolites, mainly synthesized by some fungal species belong to the genera Aspergillus, Penicillium and Fusarium (Almela et al. 2007). To date, over 400 mycotoxins have been identified among these metabolites, ochratoxin A (OTA) is one of them and can contaminate a wide range of agricultural commodities including cereal, coffee, cocoa, nuts, and spices under certain environmental conditions (Trucksess and Diaz-Amigo 2011). OTA is the most studied mycotoxin in spices that its prevalence depends on many specific factors which among them, temperature, storage conditions and processing are the most described factors. Humans are exposed to this metabolite through consumption of contaminated food products (Jalili 2016). Exposure to this mycotoxin is a life threatening problem and can have many toxicological effects on consumers. OTA intake through the consumption of contaminated crops can cause some adverse effects such as kidney and liver diseases, as well can target the nervous system, and immune system in test animals (da Rocha et al. 2014; Ringot et al. 2006). In addition, this molecule has been classified as a possible human carcinogen (group 2B) by the International Agency for Research on Cancer (IARC). To avoid such outcomes, processing protocols and storing conditions must be controlled to obtain a good quality product. However, given the health risks of exposure to OTA, regulatory agencies or commissions, have imposed national standards on its contamination in agricultural products, which may vary in different countries. For instance, the European Commission has established levels up to 15 ng/g for OTA in the spices. Meta-analysis refers to the statistical analysis of collected data from multiple independent studies in order to investigate the integration of results.
To the best of our knowledge, no systematic reviews have been conducted to assess the prevalence and concentration of ochratoxin A in spices; however, some assessments were carried out to measure the mycotoxin levels in different food commodities. Therefore, for the first time, the current investigation aimed to estimate the prevalence and concentration of ochratoxin A in various spices (pepper, paprika, chili, cinnamon, turmeric, nutmeg, ginger, cayenne and curry) via a systematic review and meta-analysis approach.
A systematic literature search was carried out to investigate the prevalence and concentration of ochratoxin A in spices. In this regard, Relevant articles were collected from international databases including PubMed, Scopus, and Web of Science between 1995 to January 2022. Search keywords used included spice; mycotoxins; and OTA. Besides, the references list of all articles was also screened in order to collect other suitable studies.
After first screening by the title and abstract, the eligible articles were obtained. Two authors read and cheeked the screened articles based on the following research criteria independently.
Each author reviewed the titles, abstracts, and full texts of the papers to select the articles with the inclusion criteria, and any differences were resolved by dispute and consensus. The inclusion criteria were: (1) Full-text available; (2) reporting prevalence and/or concentration data of OTA; (3) only spice samples; (4) cross-sectional research; studies conducted from 1995 to January 2022; only published in the English language. Additionally, the following items were adopted as exclusion criteria: (1) Books, theses, and review articles; (2) OTA contamination in other agricultural products; (3) any other mycotoxins prevalence.
The data were extracted by one of the authors and checked by another author. All the required data such as first author, publication year, country, total sample size, type of spice, number of positive samples, the prevalence of OTA, the mean and standard deviation of OTA, the limit of detection (LOD), and limit of quantification (LOQ) were included in the Microsoft Excel software (Microsoft Corporation, WA, US).
In the present study, the random effect model (REM) was used to estimate the pooled concentrations and prevalence of OTA in spices with 95% confidence intervals for all evaluated articles. This test was also applied to calculate the overall prevalence in subgroups such as country, continent and type of spice products. The heterogeneity of data was determined by Chi-square (I2) index and Cochrane Q test with P < 0.05. The range of the I2 index was between 0 and 100%, and when I2 index ≥ 50 values indicate that considered heterogeneous. Meta-regression was used to determine the effects of sample size, year, and country on the prevalence of OTA in spices using the method of moment model (Borenstein et al. 2021). Publication bias among the included studies was detected statistically by using the Egger's test (Egger et al. 1997). As publication bias among studies was significant (P-value < 0.05), the Meta Trim test was performed to estimate the pooled prevalence of OTA in the spices to eliminate the publication bias (White 2009). All data were analyzed using STATA 14.0 (2015; STATA 14.0 Statistical Software, College Station, TX, USA). Statistical difference was significant at p < 0.05.
The flow diagram of the systematic search in Scopus, PubMed, Embase and Web of Science databases is outlined in Fig. 1. After the removal of duplicates (n = 635) a total of 490 articles were obtained for further investigation. Considering the titles and abstracts, 402 that did not meet our inclusion criteria were excluded. Full texts of 88 remained articles were assessed and based on the eligibility criteria 36 articles with 65 studies were included in the current meta-analysis.
The main characteristics of the included studies are displayed in Table 1. According to the methods used for detection and quantification, the presence of OTA was determined by HPLC, TLC, LC-MS/MS, enzyme-linked immunosorbent assay (ELISA) and UHPLC. Eleven studies were conducted in Asia (Jalili 2016; Jalili and Jinap 2015; Jalili et al. 2010; Jeswal and Kumar 2015; Zareshahrabadi et al. 2020; Cao et al. 2013; Salari et al. 2012; Ozbey and Kabak 2012; Thirumala-Devi et al. 2001; Tosun and Ozden 2016; Zhao et al. 2014), sixteen in Europe (Yogendrarajah et al. 2013; Yogendrarajah et al. 2014; Santos et al. 2010b; Santos et al. 2011; Waśkiewicz et al. 2013; Hernandez Hierro et al. 2008; El Darra et al. 2019; El-Kady et al. 1995; Fazekas et al. 2005; Boonzaaijer et al. 2008; Skarkova et al. 2013; Goryacheva et al. 2007; Molnár et al. 2018; Reinholds et al. 2016; Reinholds et al. 2017; Skrbic et al. 2013), six in Africa (Zaied et al. 2010; Lippolis et al. 2017; Manda et al. 2016; Motloung et al. 2018; Nguegwouo et al. 2018; Aziz et al. 1998), three in America (Kolakowski et al. 2016a; Garcia et al. 2018; Shundo et al. 2009). These studies were published between 1995 and 2020. The selected articles reported OTA prevalence data in different countries globally. Among all studies 20 (30.3%) studies were related to black pepper; 14 (21.2%) studies were paprika; 8 (12.1%) studies were cinnamon; 7 (10.6%) studies were tumeric; 8 (12.1%) studies were ginger; 9 (13.6%) studies were red pepper. The data of black pepper, parpika, tumeric, ginger and red pepper was entered to the present study. As shown in Table 1 the prevalence of OTA contamination in the included studies ranged from 0 to 100 for spices. Totally, collected data from 1686 spice samples were pooled for this meta-analysis.
| Author (year) | Country | Continent | Type of spice | Sample size | Positive | Prevalence (%) | Concentration mean (ng/g) | Method of detection | Reference |
|---|---|---|---|---|---|---|---|---|---|
| Jalili et al. (2015) | Iran | Asia | Black pepper | 20 | 8 | 40 | 1.5 | HPLC | (Jalili and Jinap 2015b) |
| Yogendrarajah et al. (2013) | Belgium | Europe | Black pepper | 10 | 1 | 10 | 48 | HPLC–MS/MS | (Yogendrarajah et al. 2013) |
| Santos et al. (2010) | Spain | Europe | Paprika | 64 | 63 | 98 | HPLC | (Santos et al. 2010a) | |
| Waśkiewicz et al. (2013) | Poland | Europe | Black pepper | 5 | 4 | 80 | 9.46 | LC/MS/MS | (Waśkiewicz et al. 2013b) |
| Waśkiewicz et al. (2013) | Poland | Europe | Cinnamon | 4 | 3 | 75 | 2.14 | LC/MS/MS | (Waśkiewicz et al. 2013b) |
| Waśkiewicz et al. (2013) | Poland | Europe | Turmeric | 1 | 1 | 100 | 11.72 | LC/MS/MS | (Waśkiewicz et al. 2013b) |
| Hierro et al. (2008) | Spain | Europe | Paprika | 21 | 14 | 67 | 11.9 | HPLC-MS | (Hernandez Hierro et al. 2008) |
| Zaied et al. (2010) | Tunisia | Africa | Black pepper | 20 | 13 | 65 | 274 | HPLC | (Zaied et al. 2010b) |
| Zaied et al. (2010) | Tunisia | Africa | Paprika | 23 | 15 | 70 | 203 | HPLC | (Zaied et al. 2010b) |
| Kolakowski et al. (2016) | Canada | America | Paprika | 100 | 100 | 100 | 149 | HPLC | (Kolakowski et al. 2016b) |
| Kolakowski et al. (2016) | Canada | America | Turmeric | 100 | 90 | 90 | 1.92 | HPLC | (Kolakowski et al. 2016b) |
| Jeswal et al. (2015) | India | Asia | Black pepper | 42 | 33 | 78.5 | 154.1 | ELISA | (Jeswal and Kumar, 2015) |
| Jeswal et al. (2015) | India | Asia | Turmeric | 35 | 20 | 57.1 | 125.9 | ELISA | (Jeswal and Kumar 2015) |
| Jeswal et al. (2015) | India | Asia | Ginger | 36 | 20 | 55.5 | 82.8 | ELISA | (Jeswal and Kumar 2015) |
| Zareshahrabadi et al. (2020) | Iran | Asia | Turmeric | 20 | 2 | 10 | 1.07 | HPLC | (Zareshahrabadi et al. 2020) |
| Zareshahrabadi et al. (2020) | Iran | Asia | Red pepper | 20 | 11 | 55 | 1.52 | HPLC | (Zareshahrabadi et al. 2020) |
| Zareshahrabadi et al. (2020) | Iran | Asia | Black pepper | 20 | 20 | 100 | 49.29 | HPLC | (Zareshahrabadi et al. 2020) |
| Zareshahrabadi et al. (2020) | Iran | Asia | Cinnamon | 20 | 15 | 75 | 18.5 | HPLC | (Zareshahrabadi et al. 2020) |
| Cao et al. (2013) | China | Asia | Ginger | 20 | 6 | 30 | UPLC-FLR | (Cao et al. 2013) | |
| Darra et al. (2019) | Italy | Europe | Black pepper | 4 | 1 | 25 | 2.3 | LC-MS/MS | (El Darra et al. 2019) |
| Darra et al. (2019) | Italy | Europe | Paprika | 3 | 2 | 66.66 | 11.4 | LC-MS/MS | (El Darra et al. 2019) |
| Darra et al. (2019) | Italy | Europe | Turmeric | 2 | 1 | 50 | 2.4 | LC-MS/MS | (El Darra et al. 2019) |
| Darra et al. (2019) | Italy | Europe | Cinnamon | 3 | 0 | 0 | 0 | LC-MS/MS | (El Darra et al. 2019) |
| Darra et al. (2019) | Italy | Europe | Ginger | 3 | 0 | 0 | 0 | LC-MS/MS | (El Darra et al. 2019) |
| El-Kady et al. (1995) | Egypt | Europe | Black pepper | 5 | 0 | 0 | TLC | (El-Kady et al. 1995a) | |
| El-Kady et al. (1995) | Egypt | Europe | Red pepper | 5 | 0 | 0 | TLC | (El-Kady et al., 1995a) | |
| Fazekas et al. (2005) | Hungary | Europe | Red pepper | 70 | 32 | 45.7 | HPLC | (Fazekas et al. 2005) | |
| Fazekas et al. (2005) | Hungary | Europe | Black pepper | 6 | 0 | 0 | 0 | HPLC | (Fazekas et al. 2005) |
| Garcia et al. (2018) | Brazil | America | Cinnamon | 13 | 0 | 0 | 0 | HPLC | (Garcia et al. 2018) |
| Garcia et al. (2018) | Brazil | America | Black pepper | 15 | 0 | 0 | 0 | HPLC | (Garcia et al. 2018) |
| Jalili et al. (2010) | Malaysia | Asia | Black pepper | 30 | 17 | 56.7 | 2.167 | HPLC | (Jalili et al. 2010) |
| Lippolis et al. (2017) | Nigeria | Africa | Ginger | 89 | 33 | 37 | 2.76 | HPLC | (Lippolis et al. 2017) |
| Manda et al. (2016) | Côte d'Ivoire | Africa | Ginger | 30 | 15 | 50 | 0.12 | HPLC | (Manda et al. 2016b) |
| Salari et al. (2012) | Iran | Asia | Red pepper | 36 | 6 | 17 | TLC | (Salari et al. 2012a) | |
| Motloung et al. (2018) | South Africa | Africa | Paprika | 7 | 1 | 14 | 11 | LC-MS/MS | (Motloung et al. 2018a) |
| Ozbey et al. (2012) | Turkey | Asia | Black pepper | 23 | 4 | 17.4 | 1.82 | HPLC-FD | (Ozbey and Kabak 2012) |
| Ozbey et al. (2012) | Turkey | Asia | Cinnamon | 17 | 0 | 0 | 0 | HPLC-FD | (Ozbey and Kabak 2012) |
| Boonzaaijer et al. (2008) | Netherland | Europe | Paprika | 3 | 3 | 100 | 4.5 | LC-MS/MS | (Boonzaaijer et al. 2008a) |
| Nguegwouo et al. (2018) | Cameroon | Africa | Black pepper | 20 | 2 | 10 | 3.30 | ELISA | (Nguegwouo et al. 2018b) |
| Santos et al. (2011) | Spain | Europe | Paprika | 17 | 17 | 100 | HPLC | (Santos et al. 2011a) | |
| Santos et al. (2011) | Spain | Europe | Paprika | 4 | 4 | 100 | HPLC | (Santos et al. 2011a) | |
| Shundo et al. (2009) | Brazil | America | Paprika | 70 | 60 | 85.7 | 7 | HPLC-FLD | (Shundo et al. 2009a) |
| Skarkova et al. (2013) | Czech Republic | Europe | Red pepper | 12 | 12 | 100 | 19 | HPLC-FD | (Skarkova et al. 2013) |
| Skarkova et al. (2013) | Czech Republic | Europe | Black pepper | 12 | 11 | 92 | 0.83 | HPLC-FD | (Skarkova et al. 2013) |
| Thirumala-Devi et al. (2001) | India | Asia | Black pepper | 26 | 14 | 53.84 | ELISA | (Thirumala-Devi et al. 2001a) | |
| Thirumala-Devi et al. (2001) | India | Asia | Ginger | 25 | 2 | 8 | ELISA | (Thirumala-Devi et al. 2001a) | |
| Thirumala-Devi et al. (2001) | India | Asia | Turmeric | 25 | 9 | 36 | ELISA | (Thirumala-Devi et al. 2001a) | |
| Tosun et al. (2016) | Turkey | Asia | Red pepper | 75 | 71 | 94.7 | 3.5 | HPLC-FLD | (Tosun and Ozden 2016b) |
| Yogendrarajah et al. (2014) | Belgium | Europe | Black pepper | 82 | 7 | 8.53 | 30.9 | UPLC | (Yogendrarajah et al. 2014a) |
| Zhao et al. (2014) | China | Asia | Cinnamon | 80 | 4 | 5 | 1.1 | HPLC-FLD | (Zhao et al. 2014) |
| Goryacheva et al. (2007) | Russia | Europe | Paprika | 6 | 2 | 33 | ELISA | (Goryacheva et al. 2007) | |
| Goryacheva et al. (2007) | Russia | Europe | Red pepper | 7 | 3 | 43 | ELISA | (Goryacheva et al. 2007) | |
| Goryacheva et al. (2007) | Russia | Europe | Black pepper | 5 | 0 | 0 | ELISA | (Goryacheva et al. 2007) | |
| Goryacheva et al. (2007) | Russia | Europe | Ginger | 5 | 0 | 0 | ELISA | (Goryacheva et al. 2007) | |
| Molnár et al. (2018) | Hungary | Europe | Paprika | 53 | 21 | 39.6 | HPLC | (Molnár et al. 2018) | |
| Reinholds et al. (2017) | Latvia | Europe | Paprika | 50 | 2 | 4 | 7.5 | UHPLC | (Reinholds et al. 2017b) |
| Škrbić et al. (2013) | Serbia | Europe | Red pepper | 13 | 0 | 0 | UHPLC | (Škrbić et al. 2013) | |
| Škrbić et al. (2013) | Serbia | Europe | Black pepper | 2 | 0 | 0 | UHPLC | (Škrbić et al. 2013) | |
| Aziz et al. (1998) | Egypt | Africa | Ginger | 5 | 2 | 40 | TLC | (Aziz et al. 1998a) | |
| Aziz et al. (1998) | Egypt | Africa | Cinnamon | 5 | 0 | 0 | TLC | (Aziz et al. 1998a) | |
| Reinholds et al. (2016) | Latvia | Europe | Black pepper | 50 | 0 | 0 | HPLC | (Reinholds et al. 2016) | |
| Jalili et al. (2016) | Iran | Asia | Black pepper | 23 | 10 | 43.5 | 3.31 | HPLC | (Jalili 2016) |
| Jalili et al. (2016) | Iran | Asia | Red pepper | 23 | 4 | 17.4 | 5.66 | HPLC | (Jalili 2016) |
| Jalili et al. (2016) | Iran | Asia | Turmeric | 23 | 7 | 30.4 | 2.77 | HPLC | (Jalili 2016) |
| Jalili et al. (2016) | Iran | Asia | Cinnamon | 23 | 8 | 3.5 | 5.46 | HPLC | (Jalili 2016) |
| Location of study | Number of study | ES*(%) | Lower ES (%) | Upper ES (%) | Relative Weight (%) | P-value | I2 (%) |
|---|---|---|---|---|---|---|---|
| Iran | 10 | 0.43 | 0.23 | 0.64 | 16.33 | 0 | 89.54 |
| Belgium | 2 | 0.07 | 0.02 | 0.14 | 3.24 | 0 | 0 |
| Spain | 4 | 0.96 | 0.76 | 1.00 | 6.26 | 0 | 80.93 |
| Poland | 3 | 0.84 | 0.46 | 1.00 | 3.63 | 0 | 0 |
| Tunisia | 2 | 0.65 | 0.50 | 0.79 | 3.26 | 0 | 0 |
| Canada | 2 | 0.97 | 0.94 | 0.99 | 3.41 | 0 | 0 |
| India | 6 | 0.48 | 0.28 | 0.68 | 9.94 | 0 | 87.69 |
| China | 2 | 0.08 | 0.03 | 0.15 | 3.32 | 0 | 0 |
| Italy | 5 | 0.21 | 0.00 | 0.53 | 6.20 | 0.31 | 16.11 |
| Egypt | 4 | 0.05 | 0.00 | 0.26 | 5.56 | 0.27 | 24.33 |
| Hungary | 3 | 0.33 | 0.16 | 0.53 | 4.82 | 0 | 0 |
| Brazil | 3 | 0.20 | 0.00 | 0.94 | 4.86 | 0 | 0 |
| Malaysia | 1 | 0.57 | 0.37 | 0.75 | 1.66 | 0 | 0 |
| Nigeria | 1 | 0.37 | 0.27 | 0.48 | 1.70 | 0 | 0 |
| Côte d'Ivoire | 1 | 0.50 | 0.31 | 0.69 | 1.66 | 0 | 0 |
| South Africa | 1 | 0.14 | 0.00 | 0.58 | .47 | 0 | 0 |
| Turkey | 3 | 0.35 | 0.00 | 0.99 | 4.94 | 0 | 0 |
| Netherland | 1 | 1.00 | 0.29 | 1.00 | 1.25 | 0 | 0 |
| Cameroon | 1 | 0.10 | 0.01 | 0.32 | 1.62 | 0 | 0 |
| Czech Republic | 2 | 0.97 | 0.85 | 1.00 | 3.12 | 0 | 0 |
| Russia | 4 | 0.15 | 0.00 | 0.44 | 5.68 | 0.13 | 46.57 |
| Latvia | 2 | 0.01 | 0.00 | 0.05 | 3.37 | 0 | 0 |
| Serbia | 2 | 0.00 | 0.00 | 0.08 | 2.70 | 0 | 0 |
| Continent | Number of study | ES*(%) | Lower ES (%) | Upper ES (%) | Relative Weight (%) | P-value | I2 (%) |
|---|---|---|---|---|---|---|---|
| Asia | 22 | 0.41 | 0.26 | 0.57 | 36.19 | 0 | 94.06 |
| Europe | 30 | 0.37 | 0.18 | 0.59 | 43.04 | 0 | 93.81 |
| Africa | 8 | 0.36 | 0.21 | 0.53 | 12.49 | 0 | 75.15 |
| America | 5 | 0.58 | 0.19 | 0.92 | 8.28 | 0 | 97.71 |
The overall prevalence of OTA in spices was 50% (95% CI: 47–52%) (Fig. 2). The prevalence of OTA in the black pepper, paprika, cinnamon, turmeric, ginger and red pepper was 31% (95% CI: 14–51%), 73% (95% CI: 44–95%), 15% (95% CI: 0–42%), 50% (95%CI: 16–84%), 29% (95% CI: 15–45%) and 42% (95% CI: 14–72%), respectively (Fig. 3). The rank order of spices based on prevalence of OTA was paprika (73%) > turmeric (50%) > red pepper (42%) > black pepper (31%) > ginger (29%) > cinnamon (15%). Furthermore, based on locations the highest prevalence of OTA in spices was noticed in Netherland 100% (95% CI: 29–100%) and the lowest prevalence rate was in Serbia 0% (95% CI: 0–0.08%) (table. 2). Moreover, the rank of countries regarding the occurrence of OTA in spices was ordered as Netherland > Czech Republic = Canada > Spain > Poland > Tunisia > Malaysia > Côte d'Ivoire > India > Iran > Nigeria > Turkey > Hungary > Italy > Brazil > Russia > South Africa > Cameroon > China > Belgium > Egypt > Latvia > Serbia.
Results also declared that considering the OTA prevalence in spices based on continents, the maximum level was found in America, 58% (95% CI: 19–92%). Also, prevalence rates of 41% (95% CI: 26–57%) and 37% (95% CI: 19–58%) were observed in Asia and Europe, respectively (table. 3). Given the continent prevalence of OTA in spices, Africa showed the lowest value of 36% (95% CI: 21–53%).
The rank order of spices based on mean concentration of OTA was paprika (50.66) > black pepper (30.57) > turmeric (24.29) > ginger (17.13) > red pepper (4.94) > cinnamon (3.4). The overall concentration of OTA in spices was 24.51 ng/g. The highest concentration of OTA in black pepper was noticed in Tunisia (274 ng/g); paprika in Tunisia (203 ng/g); turmeric in India (125.9 ng/g); ginger in India (82.8 ng/g); red pepper in Czech Republic (19 ng/g); and cinnamon in Iran (18.5 ng/g) (Table 4).
| Type of spice | Number of study | Mean concentration |
|---|---|---|
| black pepper | 19 | 30.57 |
| Cinnamon | 8 | 3.4 |
| Turmeric | 6 | 24.29 |
| Paprika | 8 | 50.66 |
| Ginger | 5 | 17.13 |
| Red pepper | 6 | 4.94 |
Meta-regression showed that the association between prevalence of OTA with sample size (p-value = 0.052), year of study (p-value = 0.56) and continent (p-value = 0.29) were not significant )p-value > 0.05) (Fig. 4). According to the publication bias test, publication bias among studies was not significant (P-value = 0.084).
OTA content is one of the most important factors for evaluating the quality of spices. These products such as paprika, black pepper, turmeric, ginger, red pepper, and cinnamon have been used in daily diets for many years. Unfortunately, despite their benefits, may pose risks due to OTA contamination. The contamination by OTA in the food chain is a serious worldwide issue that can lead to a wide range of health problems (Hajok et al. 2019). Therefore, due to its toxicity and carcinogenic related effects, a quite number of studies have reported the concentration of this compound in agricultural food crops. However, to the author’s knowledge, this is the first quantitative analysis elucidating the overall prevalence and concentration of OTA in different spices. According to our result, the overall prevalence of OTA in the spices was 50%. Moreover, The highest prevalence of OTA was in paprika (73%), while the lowest prevalence was related to cinnamon (15%). There are many studies that evaluated the content of OTA in spice samples. In a study conducted by Tančinová D et al. (2014) OTA was present in 27.3% of the spice samples (Tančinová et al. 2014). In Tunisia, 57.1% of the spices were contaminated with OTA, with an average concentration of 3.5 ng/g (Ghali et al. 2008). In another study, Ahmad-Zaidi et al. (2019) reported that 70% of spice samples were positive for OTA, which was higher than the obtained result from this study (Ahmad-Zaidi et al. 2020). Spices are known as plant products with food flavoring, antioxidant, and anti-microbial properties, as well as are susceptible to fungal spoilage. According to the European Commission Regulation No. 1137/2015, the maximum limits of 15 ng/g has been set for spices. Among the analyzed studies, 21% (11 out of 52) of the conducted studies exceeded the European standard contamination level for OTA in spices, the highest and the lowest levels were observed in paprika (50.66 ng/g) and cinnamon (3.4 ng/g), respectively. However, none of the investigated red pepper samples had concentration more than the permitted levels by the EC. Fazekas et al. (2005) and Santos et al. (2010) investigated the ochratoxin A content of different spices. Their finding showed that 11.4% of red pepper and 37% of paprika samples had OTA concentration higher than the guideline level, respectively (Fazekas et al. 2005; Santos et al. 2010a). On the other hand, samples of spice presented a mean OTA contamination of 6.18 ng/g, in a study carried out in Italy (Prelle et al. 2014). As seen in these studies, there are some differences in our results and other reports about contamination of OTA in spices. The differences in the prevalence and concentration of this mycotoxin can be associated with some factors including climate conditions, geographic location, inappropriate packaging, and improper harvesting procedure which pose an important effect on the OTA production in the final product (Cherkani-Hassani et al. 2016). In this context, several studies evaluated the effects of different factors on mycotoxin production in contaminated spices. They noticed that the temperatures ranging from 25 to 30°C and moisture contents about 16% at a water activity of 0.70 can lead to OTA production in these products (Adams et al. 2011; Vickers 2017). Among various parameters, storage temperature and the moisture content of the spice are the most important abiotic factors (Moses et al. 2013). Subgroup analysis was performed to check the possible effects of country, continent and type of spices on the prevalence of OTA. Subgroup analysis revealed that the incidence of OTA in Netherland 100% (95% CI: 29–100%) was higher than other countries. Among the countries that presented studies related to OTA contamination in spices, America had a higher prevalence with 58% (95% CI: 19–92%) and it was more prevalent in paprika samples with 73% (95% CI: 44–95%). Based on the conducted studies, OTA concentration was vary in different countries. For example, in studies performed in Italy, Turkey and Malaysia, the average level of OTA in black pepper was 2.3, 1.82, and 2.16 ng/g, respectively (El Darra et al. 2019; Ozbey and Kabak 2012; Jalili et al. 2010). In Canada, the OTA concentration was found to be 149 ng/g in paprika (Kolakowski et al. 2016b). The differences in the concentration and prevalence of OTA in different countries can be due to several reasons such as climates conditions, geographical origin of spice and storage conditions (Kamika and Tekere 2016). Alkadri et al. (2014) demonstrated that weather conditions are a critical parameter in the prevalence of mycotoxins in food products (Alkadri et al. 2014). In addition, several researchers have concluded that global warming as one of the main affected factors has increased the prevalence of mycotoxins (Juan et al. 2016; Stanciu et al. 2017). According to Bayman and Baker (2006), Strains that produce OTA differ between crops and geographical location (Bayman and Baker 2006). The observed year of study and region influences can be correlated to weather conditions, in another word, the dry weather and warm seem to lead to increase OTA producing fungi in spices.
Considering the Fig. 4, the results of meta-regression revealed a positive association between prevalence of OTA with year of study, country, and sample size, yet these were not statistically significant (P > 0.05). Given the frequency of OTA in spices and the stability of this toxin, consumption of such products could be a matter of health concern due to their possible toxic effects.
The main strength of the present study was that this is the first meta-analysis to evaluate the prevalence and concentration of OTA in spices. Prior to this meta-analysis, the evidence base was not uniform and needed a quantitative investigation which we have performed. However, there are some limitations such as small samples size that need to be addressed in this meta-analysis.
In the current study, the prevalence and concentration of OTA in spices were investigated based on defined subgroups such as country, continent and type of spice products. Meta-regression was also conducted between the prevalence of OTA in spice with year of study, sample size and country. The highest prevalence and concentration of OTA were observed in the paprika samples, while the lowest values were attributed to cinnamon. Meta-regression indicated that the year of study, sample size and country can affect the incidence of OTA in spices. The outcome of this meta-analysis can be used for risk assessment model development, aiming to help the government and industries for finding a specific way to reduce the exposure to this mycotoxin through the consumption of spice products.
Ethical approval
Not applicable because it is a review article and has no experiments.
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Author contribution
Payam Safaei, Afsaneh Mohajer and Parisa Sadighara: conceptualization, data curation, formal analysis, investigation, methodology, visualization, writing— original draft. Kiandokht Ghanati: conceptualization, investigation, methodology, project administration, supervision, visualization, writing—review and editing.
Funding
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Competing interests
The authors declare that they have no conflicts of interest.
Data availability
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