As blood lead levels of children and adults in the United States continue to decline,1 the epidemiological evidence of adverse health effects from lower levels of lead exposure continues to grow. It has now been widely acknowledged that there is no known level of lead exposure that can be considered safe.2 In children, a particularly vulnerable group due to their behavior and neurological development,3 the adverse effects of lead exposure on learning and behavior have been well documented.4–8 In adults, lead exposure can increase risk of hypertension, peripheral neuropathy, renal dysfunction, and adverse reproductive outcomes.9–11 Pregnant women present a unique concern because lead exposure can affect the health of both the woman and the fetus.3 Since symptoms of lead poisoning are often not observed, and many adverse health effects are irreversible, preventing exposure is the only effective way to avoid the health consequences of lead poisoning for children and adults.
The average blood lead levels of New York City's (NYC's) children and adults follow the pattern of national decline1; however, lead poisoning continues to be an important public health concern. In 2017, there were more than 5000 children and 2000 adults with blood lead levels at or above the Centers for Disease Control and Prevention's reference level of 5 μg/dL.12 , 13 While lead-based paint and occupational lead hazards remain the primary sources of lead exposure among NYC children and men, respectively, these are not the only possible lead sources. Consumer products, such as certain supplements or remedies, cosmetics, religious powders, and spices, are often identified as potential lead sources associated with elevated blood lead levels.14 Between 2008 and 2017, the NYC Department of Health and Mental Hygiene (DOHMH) tested more than 3000 samples of consumer products during investigations of lead poisoning cases and surveys of local stores. Of these samples, spices were the most frequently tested—more than 40% of all analyzed samples were spices.
The potential for lead exposure from spices has been previously documented. However, the few published reports either focused on a single spice type or a single country of origin or presented limited case studies.15–17 The purpose of this article is to describe the characteristics of a variety of spices tested by DOHMH during the 10-year period between 2008 and 2017. Given the diversity of NYC's population, the spice samples analyzed by DOHMH provided a unique opportunity to examine spices commonly available and used around the world.
Case investigations and sample collection
DOHMH receives all blood lead test results for NYC residents and routinely conducts investigations of child and adult lead poisoning cases.14 During these investigations, DOHMH collects samples of products suspected to contain lead and reportedly placed in the mouth or ingested by the lead-poisoned individual. Samples are analyzed for lead by an accredited laboratory using the Environmental Protection Agency (EPA) Inductively Coupled Plasma Mass Spectrometry Method SW6020 or Atomic Absorption Method SW7420 following acid digestion via EPA Method 3050. If a product is found to contain elevated lead concentrations, DOHMH visits local stores to determine availability and purchase samples of the implicated product, or similar products, for lead testing.14 Laboratory results for each sample collected during case investigations and store surveys, along with a description of each sample, as reported by the family or retrieved from product packaging, such as the product name, origin, amount used, and frequency of use, are documented electronically in a proprietary SQL Server database. This public health activity is not subject to DOHMH Institutional Review Board review, as the scope is limited to public health practice, and all activities are authorized and conducted by DOHMH, a public health authority.
We calculated descriptive statistics for lead concentration in spices. Chi-square tests were used to compare frequencies of samples of different origin exceeding guideline lead levels; the Mann-Whitney U test was used to compare distributions of lead concentrations for spices purchased abroad and in the United States, and independent-samples t tests were used for mean comparisons of log-transformed concentrations of samples with detectable levels purchased abroad and in the United States. All analyses were conducted using IBM SPSS version 23.
Lead concentration by type of spice
Table 1 presents lead concentrations by type of spice. Between 2008 and 2017, DOHMH analyzed 1496 samples of more than 50 types of spices. More than half of the samples (n = 797) had detectable lead concentrations, and 31% exceeded the reference limit of 2 ppm—a permissible limit for lead in certain food additives that is used by DOHMH as a guidance value (for information on spices exceeding other reference limits, see Supplemental Digital Content Table 1, available at http://links.lww.com/JPHMP/A524).18 , 19 The highest lead concentration (48 000 ppm) was observed for the Georgian spice kviteli kvavili, also known as yellow flower or Georgian saffron. All samples of kviteli kvavili had detectable lead levels (geometric mean [GM] = 240 ppm; geometric standard deviation [GSD] = 63 ppm); 84% exceeded the reference level of 2 ppm. Other spices and spice mixes typically used in Georgian cuisine, such as khmeli suneli or kharcho suneli, svanuri marili or svaneti salt, utskho suneli or fenugreek, adjika and kvliavi, also known as dzira or caraway, measured high as well, with maximum lead concentrations ranging from 1400 ppm (kvilavi) to 17 000 ppm (khmeli suneli). The majority of Georgian spice samples had detectable lead levels, with average concentrations ranging from 8.9 to 291 ppm (kvilavi and svanuri marili, respectively). Between 49% (khmeli suneli) and 78% (kvilavi and svanuri marili) of the samples exceeded the reference level of 2 ppm. Spices and spice mixes commonly used in South Asian cuisine such as curry, masala, and turmeric were also found to contain elevated lead levels, with maximum concentrations ranging from 2700 ppm (turmeric and masala) to 21 000 ppm (curry). About half of these spices had detectable lead, with average concentrations exceeding the reference level of 2 ppm. Various other spices and seasonings used widely in different cuisines, such as bouillon cubes and powders, broth, or soup spices, as well as hot pepper, chili powder, and paprika, were also found to have detectable levels of lead exceeding the reference limit of 2 ppm.
Qualitative data on frequency and quantity of use of spices were analyzed. The daily use of 1 teaspoon of spices in food preparation was most frequently reported. On average, 3 different spice samples were collected from each home.
Lead concentration in spices by country of purchase
The purchase country was reported for 88% (n = 1 311) of the samples (Table 2). More than half of the spices were purchased outside the United States (n = 792), altogether representing spices from 41 different countries. Bangladesh (n = 275) and Georgia (n = 210) were the most commonly reported countries of purchase; spices purchased in these 2 countries represented 61% of all samples purchased abroad. South Asian countries India, Pakistan, and Nepal were also frequently reported countries of purchase, as were Mexico, Morocco, and Jamaica. The majority of the spices purchased abroad were in unmarked packaging without brand name information.
Lead was more commonly found in spices purchased abroad than in those purchased in the United States (66% vs 40% with detectable lead concentrations, respectively; P < .001). This difference was even greater for the proportion of samples exceeding the reference level of 2 ppm. The spices purchased abroad were more than 3 times as likely to exceed this value compared with the spices purchased in the United States (45% vs 13%, respectively; P < .001). Spices purchased in Georgia were most likely to exceed the reference level of 2 ppm (70% of samples were above the limit), followed by spices from Bangladesh (54%), Morocco (48%), Nepal (30%), and Pakistan (25%). Spice samples from Georgia measured up to 48 000 ppm, from Pakistan up to 7100 ppm, from Nepal up to 2700, from Bangladesh up to 2000 ppm, and from Morocco up to 120 ppm. Samples purchased in India, Mexico, and Jamaica were less likely to exceed the reference level of 2 ppm, although some extreme concentrations were found in samples obtained in India (maximum = 690 ppm). Among other countries, an extreme concentration of 33 000 ppm was found in an unlabeled spice purchased in Belarus; however, spices from Belarus were not frequently sampled. Although a maximum of 21 000 ppm was found in a spice reportedly purchased in the United States, similar levels were never observed in spice samples purchased in local store surveys (maximum = 21 ppm), indicating a possible case of misreported country of purchase.
Comparison of lead concentration in select spices purchased during local store surveys and abroad
A comparison of select spices purchased during local store surveys (n = 88) and the same spice types purchased abroad (n = 466) showed significantly lower concentrations of lead in the spices obtained locally (GM = 31.6 ppm vs 1.1 ppm, respectively; P < .001; Table 3). Samples of khmeli suneli or kharcho suneli spices with detectable lead levels purchased in the United States had significantly lower average lead concentrations than those purchased in Georgia or Russia (GM = 0.8 ppm vs 82.9 ppm, respectively; P < .001). Maximum lead concentration for the samples of khmeli suneli or kharcho suneli purchased in local stores did not exceed 10 ppm, whereas a sample of the same spice purchased abroad had a maximum lead concentration of 17 000 ppm. Turmeric samples with detectable lead levels bought in local stores had a significantly lower average lead concentration than turmeric purchased abroad in Bangladesh, India, Nepal, Pakistan, and Morocco (GM = 1.0 ppm vs 152.3 ppm; P < .001). The maximum lead concentration of turmeric purchased abroad was 2700 ppm, whereas turmeric purchased locally did not exceed 10 ppm. Hot pepper, chili powder, and paprika samples purchased locally also had significantly lower lead concentrations than similar spices purchased abroad (GM = 0.4 ppm vs 8.0 ppm; P < .001). The maximum lead concentration for the locally purchased samples of hot pepper, chili powder, and paprika never exceeded the permissible level of 2 ppm, whereas the maximum concentration of lead for samples purchased abroad was 2400 ppm. Similarly, the maximum lead concentration for the locally purchased kviteli kvavili (21 ppm), utskho suneli (3.6 ppm), and curry (20 ppm) were much lower than the maximum lead concentrations for the same spices purchased abroad (48000 ppm, 1883 ppm, and 570 ppm, respectively), although the number of samples purchased locally were too small for reliable statistical comparisons (data not shown in Table 3).
Discussion and Conclusion
To our knowledge, this is the first time such an extensive database of spices, systematically collected over a decade-long period as part of lead poisoning investigations, has been analyzed for lead content. These samples provided a unique insight into spices of diverse origins and types.
One of our main findings was that spices purchased abroad were more likely to have elevated lead concentrations compared with similar spices purchased locally in the United States. The greatest proportion of spices exceeding reference limits were those purchased in the countries Georgia, Bangladesh, Pakistan, Nepal, and Morocco. Earlier studies have described the potential of foods and spices from Georgia and South Asia to contain elevated lead levels, and cases of lead poisoning associated with spices obtained in Georgia and South Asia have also been documented.15 , 17 , 20 In NYC, Georgians and South Asians are disproportionately represented among lead-poisoned children and pregnant women,21 , 22 and although spices may not be the only source of lead exposure for these populations, it is an important risk factor to consider during lead poisoning investigations of these at-risk groups.
Adulteration of spices can occur at any point along the supply chain due to the intentional or inadvertent addition of lead. Lead may be added as a coloring agent, or to add weight for products sold by weight, or it can be introduced because of poor processing equipment; the presence of lead in air, dust, or soil where food is grown or processed can also contribute toward contamination.23 In addition, poor regulatory controls in some countries can further impact the safety of food supplies. Although some of the countries have established guidelines for allowable lead concentration in foods, our findings show that a large proportion of the spices purchased in these countries may surpass the country's regulatory limits. For example, in Georgia, the permissible limit for lead in food is 5 ppm (National Food Agency of Ministry of Agriculture of Georgia, e-mail communication, 2017), which was exceeded in our study by more than 60% of the spices purchased there (see Supplemental Digital Content Table 2, available at http://links.lww.com/JPHMP/A525), indicating a need for tougher quality control and enforcement of standards.
In the United States, local and national surveillance and regulatory controls are in place to curtail the sale and distribution of contaminated products (eg, routine surveillance and enforcement conducted by DOHMH, New York State Department of Agriculture and Markets, US Customs and Border Protection, and the US Food and Drug Administration [FDA]).14 , 24 , 25 These actions have led to national alerts and recalls and, in some cases, investigative and auditing activities in the products' countries of origin.26 , 27 The finding that spices purchased in the United States were less likely to have elevated lead concentrations compared with similar spices purchased abroad further speaks to the effectiveness of existing processes. Nevertheless, the regulatory structure could always be strengthened. For instance, although FDA routinely monitors levels of heavy metals in certain food items through the Total Diet Study, a market basket survey of foods representative of the diet of the US consumer, the list of foods typically does not incorporate spices.28 In addition, although FDA has established a federally recommended maximum level for lead in candy, a similar limit has not been set for lead in spices; providing such a guidance may enhance regulatory procedures.29 Current surveillance and border control protocols are also ineffective when addressing transfer of contaminated spices brought into the United States by travelers for personal use. In this study, the spices purchased abroad were often in unmarked packaging, without any brand name information, and many times reported to be either custom-ground or from an open market. The purchase of spices from open markets presents a challenge, as trace-back mechanisms to stop the sale of these contaminated products may not be easily employed. Farmers and processors play a key role in the spice production supply chain. It is critical to engage these stakeholders by providing not only information about the health risks of spice adulteration and food safety challenges, but also access to modern, low-cost technologies that may help reduce inadvertent introduction of contaminants. On the regulatory end, routine monitoring and auditing of these nonconventional outlets, along with an emphasis on good agricultural practices, may also help curb both intentional and unintentional contaminations.30
In addition to regulatory controls, raising awareness about the possibility for lead contamination in spices among at-risk populations is critical. DOHMH has implemented a multifaceted, data-driven approach incorporating both local enforcement and education and dissemination of information nationally and internationally by engaging foreign consulates and regulatory authorities.14 DOHMH has also developed linguistically and culturally appropriate educational materials for routine dissemination of health messages through respected and trusted entities such as community- and faith-based organizations and continues to work with community stakeholders to identify innovative and practical avenues to reach target populations. DOHMH's approach has been instrumental in triggering national and international investigations around lead hazards in spices and other consumer products. This process hinges on the identification of hazardous products during lead poisoning case investigations and systematic cataloguing of relevant data about these products. A similar approach can be adopted by other jurisdictions, which will improve the capacity to effectively address emerging and existing hazardous products.
Our findings had several limitations. The absence of product labeling introduced uncertainty into the data due to possible errors in reporting of spice names and origin. The spices in this study may not be representative of the spices available in the US marketplace, nor of the spices available in the countries mentioned here. They may represent worst-case scenarios since they were collected and tested as part of lead poisoning investigations. A small sample size for some spices purchased during store surveys was also a limitation in our comparison of lead concentrations between spices purchased abroad versus those purchased locally in the United States, although this difference holds for spice types with larger sample sizes, as well as across sample types overall. Despite the limitations, this study provides an informative snapshot of the various types of spices that have been found to contain elevated lead concentrations and were associated with lead-poisoned children and adults in NYC.
Our findings clearly suggest that users of spices purchased in Georgia, Bangladesh, Pakistan, Nepal, and Morocco may be at an increased risk for lead exposure. This is of concern, as previous studies have shown high bioaccessibility of lead from contaminated spices15 , 26 and that chronic ingestion of such spices can lead to increased blood lead levels.16 Although further evaluation of the association between spice ingestion and blood lead levels in children and adults is needed, our findings underscore the need to develop comprehensive intervention efforts that engage local, state, federal, and international governmental entities to implement stricter regulations, quality control, and enforcement of standards that safeguard the integrity of global food supplies.
Implications for Policy & Practice
- Our findings highlight the importance of communicating the risks for lead contamination in spices purchased abroad, particularly to individuals who recently traveled to or emigrated from Georgia, Bangladesh, Pakistan, Nepal, or Morocco and may have obtained their spices in these countries.
- Public health professionals and medical providers should also be aware of spices as a potential risk factor for lead exposure and screen at-risk populations, especially those with Georgian, Moroccan, or South Asian ancestry.
- Adopting a comprehensive approach to identify hazardous products and documenting findings systematically can help lead poisoning prevention programs effectively respond to emerging and existing lead hazards.14
- Overall, a solely localized or national approach to address spice contamination will not be adequate, as the problem is global. Our results demonstrate the need for more stringent quality control and enforcement of standards globally. Although local authorities cannot mandate another country to impose stricter regulations for reducing lead contamination in spices, intergovernmental efforts can be effectively initiated by a local government agency.31 Improving food safety standards and ensuring their effective implementation through a regulatory framework are paramount to address the issue of lead-contaminated spices.
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