Lead contamination in food consumed and produced in Brazil: Systematic review and meta-analysis

Journal Pre-proof Lead contamination in food consumed and produced in Brazil: Systematic review and meta-analysis

Milton Cabral de Vasconcelos Neto, Thales Brendon Castano Silva, Vânia Eloísa de Araújo, Scheilla Vitorino Carvalho de Souza PII:

S0963-9969(19)30557-5

DOI:

https://doi.org/10.1016/j.foodres.2019.108671

Reference:

FRIN 108671

To appear in:

Food Research International

Received date:

25 April 2019

Revised date:

30 August 2019

Accepted date:

9 September 2019

Please cite this article as: M.C. de Vasconcelos Neto, T.B.C. Silva, V.E. de Araújo, et al., Lead contamination in food consumed and produced in Brazil: Systematic review and meta-analysis, Food Research International (2018), https://doi.org/10.1016/ j.foodres.2019.108671

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© 2018 Published by Elsevier.

Journal Pre-proof Review

Lead contamination in food consumed and produced in Brazil: Systematic review and meta-analysis Milton Cabral de Vasconcelos Netoa,c, Thales Brendon Castano Silvad, Vânia Eloísa de Araújob,d, Scheilla Vitorino Carvalho de Souzac,* [email protected] a

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Ezequiel Dias Foundation, Health Public Laboratory of Minas Gerais State, Belo Horizonte, Minas Gerais, 30.5010-010, Brazil. ORCID 0000-0002-8930-5171 b Pontifical Catholic University of Minas Gerais, Belo Horizonte, Minas Gerais, 30531901, Brazil. ORCID 0000-0002-0345-8522 c Postgraduate Program in Food Science, Department of Food Science (ALM), Faculty of Pharmacy (FAFAR), Federal University of Minas Gerais (UFMG), Av. Antônio Carlos, 6627, Campus da UFMG, Pampulha, 31270-010, Belo Horizonte, Minas Gerais, Brazil. ORCID, 0000-0003-0256-3782 d Postgraduate Program in Medicines and Pharmaceutical Assistance, Faculty of Pharmacy (FAFAR), Federal University of Minas Gerais (UFMG),, Belo Horizonte, Minas Gerais, Brazil, ORCID 000-0030196-8884, 0000-0002-0345-8522 * Corresponding author.

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ABSTRACT

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This systematic review (SR) evaluated evidence of lead (Pb) levels in foods consumed or produced in Brazil. Seventy-seven publications were included in this review,

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corresponding to a total of 8,466 food samples that were grouped into 12 food categories with similar characteristics (infant food; sugar; beverages; meat and meat

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products; nuts, cocoa and products; fruits and fruit products; grains, cereals and products; milk and milk products; eggs; oil and fat spreads; vegetables and vegetable products and other foods). The random model was used to establish levels of Pb in food categories. We used the software R to perform the meta-analysis. The overall occurrence of Pb was estimated at 0.0541 mg/kg, and ranged from 0.0004mg/kg to 0.4842 mg/kg. The SR and meta-analysis presented relevant results about Pb contamination on foods, despite the high heterogeneity. They were understood as a viable strategy to answer questions regarding prevalence of Pb which is necessary for the risk assessment of Pb intake in foods. Keywords: heavy metals, lead poisoning, lead-204, food safety.

1. Introduction

Journal Pre-proof Much is discussed about the effect of lead (Pb) on human health and the different sources of exposure, with Pb intake through contaminated food as the main nonoccupational exposure route. In this way, studies related to dietary Pb intake that have been reviewed (WHO, 2011a) suggest the adoption of new global and national regulatory practices in food safety (CAC, 2019a; CAC, 2019b; CAC, 2019c). Pb is considered a rare metal compared to iron (Fe) and aluminum (Al). It generally occurs in the Earth's crust, in descending order, in the combined form of thorium (Th) 208Pb, uranium (U) 206Pb, actone 207Pb, and

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Pb isotopes (Vecchia et al.,

2014). However, environmental levels have increased over centuries as a result of

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human activities in the environment and in the industrial sector (Panel & Chain, 2013). Pb acts by the affinity with thiol and sulfhydryl protein groups, interfering with the functioning of cell membranes and enzymes (Panel & Chain, 2013; Caldas et al.,

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2016). Exposure to Pb may cause a reduction in the intelligence quotient, joint weakness, accelerated skeletal maturation, increased incidence of cavities, increased

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blood pressure, anemia, spontaneous abortion, impairment of renal function, changes in hormone levels, and an increase in immunoglobulin E (IgE) levels and, consequently, in

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allergic diseases (EPA, 2014; Wani et al., 2015). Thus, Pb was included in the list of poisonous and deleterious substances and identified as one of the ten chemicals of

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greatest concern to public health, suggesting the need for protective measures for specific population groups (WHO, 2010).

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Depending mainly on the concentration of Pb in food, levels of exposure through food intake vary between countries (EPA, 2014; Panel & Chain, 2013). Thus, the most

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recent Joint FAO/WHO Expert Committee on Food Additives (JECFA) assessment related to Pb exposure by food, published in 2011, resulted in the annulment of the weekly provisional safety dose (PTWI; 0.025mg/kg.bw) and indicated the need to identify the main sources of food for the adoption of appropriate methods for risk reduction (WHO, 2011a). The SR, whether associated with meta-analysis or not, is considered a robust source of evidence in various fields of science. However, its application in the area of food safety is not frequently observed. The EFSA (2010) prepared a guide suggesting the application of an SR in the food industry, considering its potential applicability in obtaining answers to questions related to the process of risk assessment. No studies related to the estimation of the occurrence of Pb in Brazilian food based on an SR with meta-analysis are reported in the literature, and there is little global evidence from SRs

Journal Pre-proof to respond to the various questions generated by risk assessment. In this context, the main goal of this article was to estimate the Pb content in foods consumed or produced in Brazil.

2. Material and methods

This SR was conducted according to the guidelines of the items of Preferential Reports for Systematic Reviews and Meta-Analyses (PRISMA) (Moher et al., 2009). The protocol was registered, Centre of Reviews Dissemination (CRD) number

(PROSPERO)

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42017060069, in the International Prospective Register of Systematic Reviews (www.crd.york.ac.uk/prospero,

CRD42017060069)

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(Supplementary Table 1).

protocol

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2.1. Information sources, search strategy and study selection

An extended search with indexed terms and synonyms was performed through

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June 2018 in the following databases: MEDLINE (PubMed), Cochrane Library, CINAHL, Web of Science, Food Science and Technology (FSTA), Latin American and

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Caribbean Literature in Health (LILACS) (Virtual Health Library, VHL), São Paulo State Secretary (SESSP) (Virtual Health Library, VHL), Scopus and AGRICultural

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OnLine Access (Agricola) from the National Agricultural Library. A complementary search was made, as well as a manual search of unpublished literature. Two independent

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reviewers carried out the evaluation of the studies for inclusion in the review, assessment of bias risk and data collection. In cases of disagreement, a third evaluator was recruited for consensus (Supplementary Table 2).

2.2. Eligibility criteria: inclusion and exclusion criteria

Cross-sectional studies of Pb in foods samples randomly selected were included. The level of Pb must have been expressed in mg/kg or a similar unit, and when the results were not detectable (ND) or not quantifiable (NQ), the limits of quantification (LOQ) and limits of detection (LOD) must have been reported. We excluded studies with nonprimary data; results expressed in other noncomparative units; missing information (i.e., LOD, LOQ, number of samples,

Journal Pre-proof amplitude of results and deviation); food produced in Brazil in an area known to be unsuitable for food production or consumption; spiked foods for method validation and other products; and investigation of parameters other than Pb.

2.3. Data collection and evaluation of methodological quality

The instrument for quality evaluation of cross-sectional studies proposed by Loney et al. (1998) was used, with adaptations. Each item was assigned a score of 1 point, making 8 the maximum score possible. High-quality studies were those with

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scores of 7 and 8; moderate studies were those with scores between 4 and 6; and lowquality studies were those with scores equal to or less than 3. The established criteria were 1) random sampling or total population; 2) impartial sampling; 3) sample size

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adequate for identifying the analyte; 4) objective criteria adequate for measuring the outcome; 5) results measured by impartial evaluators; 6) results adequately expressed

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and parameters established; 7) occurrence levels given with deviation and for each type of food or food category, if appropriate; and 8) the subject of the study described in

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detail and similar to the subject of interest.

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2.4. Data processing and statistical analysis

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The prevalence of Pb was expressed as mg/kg, and an arithmetic mean was established for all food categories. The prevalence results corresponded to wet weight.

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Data expressed as dry weight were converted to wet weight, and a TACO Table (TACO, 2011) was used as the reference for the moisture content. The value of the LOD of the analytical method was considered as a deviation when the reported results were equal to zero. The deviations were estimated in the studies that presented only the amplitude of the results. Foods were grouped by similarity based on the IBGE (IBGE, 2011) and GEMS/Food (WHO, 2011b) classification lists, allowing for prospective association between Pb prevalence and food consumption, for the evaluation of exposure to chemical compounds in Brazil. In order to avoid the effects of confounders, the confounding bias was controlled in the planning, since random sampling or total sampling was considered in the inclusion criteria (Meuli & Dick, 2018). The endpoint was the concentration of Pb in food with a 95% confidence interval (95% CI). The data were combined using the metamean command of the

Journal Pre-proof software package R, version 3.4.3. The heterogeneity was investigated by the Chisquared test with a significance level of p<0.01 and magnitude ascertained by the Isquared (I²) statistic, which describes the variation among studies (Higgins & Green, 2011). A subgroup analysis (by food category) was conducted to explore the heterogeneity. Each subgroup was established grouping foods of similar characteristics. The random effect model was applied to incorporate heterogeneity among studies (Atamaleki et al., 2019). Sensitivity analysis was carried out to evaluate the extent to which inferences might depend on studies that presented small sampling size (Hamidiyan et al., 2018).

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The effect measure overall means and ranges for foods and subgroups (food categories) were estimated. Considering that the Pb level variable tends to present values between undetectable/unquantifiable and infinity, negative values in the CI were

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assumed to be left censored, below the limits of the methods, and therefore were

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considered to be zero.

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3.1. Selection of the studies

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3. Results and discussion

We retrieved 1171 publications from the electronic databases. After elimination

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of the duplicates, using Endnote software, 1009 studies were selected for reading titles and abstracts and 108 for a full reading. Using the inclusion and exclusion criteria, we

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selected 77 studies for inclusion in the meta-analysis. Although all of the included studies adopted random sampling, only 3 of them were based on statistical approaches. Only 15 studies reported the results adequately (e.g., declared no conflicts of interest, reported negative results), and 59 studies provided confidence intervals with Pb levels. All of the included studies provided Pb levels for food (Figure 1).

The concordance between the reviewers was considered satisfactory (0.85) when applying the KAPPA test (Higgins & Green, 2011). From the total quantity of included studies, thirty-five studies (46%) were published in food-related journals. The other articles were published in journals specialized in the environment and identification of chemical elements. The dissertations and theses belonged to the areas of food science, chemistry and toxicology. Approximately 20% of the studies reported no conflicts of

Journal Pre-proof interest. The quality of the studies presented a mean score of 5.6 points, with 9% (n=7) of them being high-quality, with a score of 7; 90% (n=69) being moderate-quality, with scores between 4 and 6; and 1% (n=1) being low-quality, with a score of 3. The excluded studies and the characteristics of the eligible studies are shown in Supplementary Tables 1 and 2, respectively.

3.2. Population

A total of 8,466 results of Pb concentration on foods consumed and produced in

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Brazil, covering the period 1989 to 2017, were suitable for calculating Pb concentrations, once all results met the inclusion criteria. In general, the foods covered in this study corresponded to those foods identified in food consumption studies

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conducted by the Brazilian Institute of Geography and Statistics (IBGE) (IBGE, 2011). Most of the samples were collected in Brazil and from the retail market. However, for

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meats and meat products, the samples were predominantly obtained from the environment (e.g., fishing sites) and from the place of production (e.g., slaughterhouses

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and farms).

The use of statistical methods in the sampling plans was not noted in the studies

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chosen from the proportionality of positive results. Only one study reported the use of a statistical method to establish sample size. However, it was not clearly understood

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whether it adopted the proportion of positive samples to estimate the sample size. The most prevalent analytical techniques in this review were inductively coupled

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plasma optical emission spectrometry (ICP-OES) and atomic absorption spectrometry with graphite furnace (GF-AAS), which together corresponded to 44% of the studies. One study did not report the technique used (Seixas et al., 2005). The analytical methods commonly used and reported in other studies included mainly atomic absorption spectrometry (AAS), flame atomic absorption spectrometry (FAAS), inductively coupled plasma mass spectrometry (ICP-MS), GF-AAS and ICP-OES (Panel & Chain, 2013; WHO, 2011a). The samples were grouped into 12 food categories. Each category contained a number of foods with similar characteristics. It is important to consider that the diversity of food obtained in our study was greater than that presented by Brazil to JECFA to conduct the risk assessment (WHO, 2011a). The other foods category included supplements and pollen. Table 3 presents the composition of foods by category, the

Journal Pre-proof reported analytical techniques and the different reported LOD and LOQ that were presented in intervals. The categories meat and meat products, beverages, and vegetables and vegetable products were those with more studies and larger samples, while the categories fruits, eggs and infant food were those with less studies and smaller samples.

3.3. Lead levels

Most of the studies that reported ND or NQ results declared the respective limits

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of the methods. Only one study did not present the LOD and reported outcomes as ND (Souza et al., 2011). This study was excluded. From the total eligible studies, 77% reported at least one of the limits (LOD or LOQ), and 23% did not declare either of

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them. Twenty-eight studies (36%) declared both limits. Only 28% of the studies declared LOD only and 13% LOQ only. In addition, the studies did not inform if they

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were applicable to concentrations near the regulatory maximum limits (LMs) for each studied food.

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The meta-analysis pointed to an estimate of prevalence that reinforces the contamination of food with Pb in all categories of foods (Table 4). In Supplementary

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Figure 1 we present a graphical representation of the results of the meta-analysis for all food categories, with the results from the test of heterogeneity (chi-squared test), the

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measurement of inconsistency and the hypothesis test. Lastly, the estimated mean level

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of Pb and the range are shown.

Since the revocation of PTWI (0.025mg/kg.bw), efforts have been made by the Codex Alimentarius Commission and Brazilian regulatory bodies to minimize the impact of Pb exposure (ANVISA, 2013, CAC 2019c). In this review, concentrations ranged from 0.0004 mg/kg (95% CI [-0.0073 – 0.0082]; I2=0% p=0.41; weight 2.6%) for nuts and cocoa products to 0.4842 mg/kg (95% CI [-0.5548 – 1.5233]; I2=87%; p<0.01; weight 2.2%) for infant food. The food categories for food destined for consumption by the general population that presented the highest mean levels of Pb in our study were meat and meat products with 0.1248 mg/kg (95% CI 0.1202 – 0.1294; I2 = 100%; p = 0; weight 29.3%), vegetables and vegetable products with 0.1671 mg/kg (95% CI 0.1072 – 0.2279;, I2 = 100%; p = 0; weight 17%), and other food with 0.1485

Journal Pre-proof mg/kg (95% CI 0.0134 – 0.2836; I2 = 98%; p = 0; weight 3.7%). The mean concentration of Pb estimated for all foods was 0.0541 mg/kg (95% CI 0.0529 – 0.0554; I2 = 100%). Approximately 23% of the samples had Pb levels below the limits of the respective methods, which is lower than the 55% observed by Panel and Chain (2013). Among the studies, different analytical techniques were used within and among categories, implying different LOD and LOQ (Table 3). The mean proportion of positive samples was 77%. Thus, except for the categories eggs, infant food, and fruits and fruit products, the categories met the sample size (69 samples) suggested for the 95% CI criteria, 10% accuracy and 77% positive

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samples (Sargeant, 2018). However, a detailed investigation of the proportion of different types of food in the categories, specifically in the categories with the highest prevalence and the greatest impact on consumption, might be necessary to assess the

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quantity of food.

Food categories with the highest level of detectable Pb included meat;

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vegetables; grains, cereals and products (WHO, 2011a). The Pb levels occurring for food categories obtained in the present study show similarity to the general levels of Pb

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in food observed in other countries, as well a wide range of Pb concentrations in food groups that have been investigated. However, we observed a difference between the

2014; Jin et al., 2014).

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types of relevant categories among the studies (Panel & Chain, 2013; Taylor et al.,

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The mean levels of Pb in different food groups investigated in China, Europe, the United States, Singapore and Australia ranged from 0.0001 mg/kg to 1.029 mg/kg

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between 1999 and 2009 (WHO, 2011a). According to Panel and Chain (2013), in evaluating levels of Pb in the diet, values between 0.0030 mg/kg and 0.456 mg/kg were observed in 15 food categories, i.e., had similar amplitude to that reported in the present study. In Germany, mean levels of Pb between 0.004 mg/kg and 0.0421 mg/kg were obtained in different food groups analyzed between 2000 and 2009, as reported by Taylor et al. (2014). In this study, the highest levels of contamination were observed for meat, fish, vegetables, cereals and oil seeds (Taylor et al., 2014). Mean values for Pb between 0.025 mg/kg and 1.937 mg/kg for 11 food groups were obtained by Jin et al. (2014). Among these 11 groups, lower values were obtained for fruits (0.025 mg/kg) and milk and derivatives (0.026 mg/kg), when compared with the values of 0.0472 mg/kg and 0.1073 mg/kg, respectively, estimated in the present study.

Journal Pre-proof According to Mendes (2015), the average level of Pb for some foods, evaluated in Brazil, ranged from 0.0005 mg/kg (mineral water) to 0.3 mg/kg (fish and seafood and vegetables). Pb levels obtained in the present study for most of the food categories, such as beverages (0.0483 mg/kg), fruits and fruit products (0.0472 mg/kg), vegetables and vegetable products (0.1671 mg/kg), and meat and meat products (0.1248 mg/kg), were within the ranges reported by Mendes (2015) for foods. The number of samples in the category meat and meat products (n=5891) corresponded to approximately 70% of the total food investigated in our study. This entire food group was composed of meat and nonindustrially processed viscera of

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specific species (i.e., bovine, porcine, poultry, fish and seafood), canned fish and food products based on meat. In the present study, the mean Pb level was 0.1248 mg/kg, one of the highest Pb levels among the investigated food groups. This contamination level

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was within the range for worldwide Pb contamination (ND to 5309 mg/kg) obtained from the GEMS/Food database for the meat category (including hunting meat), based

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on analyzed samples until 2018, by country and region (e.g., Australia, Canada, China, France, Japan, the African Region, the European Region, the United States of America,

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Singapore, Thailand) (WHO, 2019).

A wide range of Pb levels was seen in the main groups meat and fish, as

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observed by Taylor et al. (2014). For meat (excluding fish and seafood), the highest values were obtained in animals slaughtered by the State Inspection Service in the state

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of Goiás (n=60) during an experiment with a variation from 0.392 mg/kg to 6.030 mg/kg (Gonçalves, 2007). Lower levels were obtained in samples of chicken meat

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collected from the market in different regions of the country and whose values were less than the LOD for the analytical method used (Batista et al., 2012). For edible viscera, the values ranged from 0.06 mg/kg (Caldas et al., 2016) to 2.20 mg/kg (Gonçalves, 2007), both related to bovine viscera. In an SR conducted in China, the observed Pb levels for meats and edible viscera varied from 0.003 mg/kg to 0.349 mg/kg and from 0.025 mg/kg to 0.719 mg/kg, respectively (Jin et al., 2014). In Norway, hunting meat presented an average level of 5.6 mg/kg (LindBoe et al., 2012). In edible viscera investigated in Korea, in 2016, values between 0.00432 mg/kg and 0.0477 mg/kg were observed (Kim et al., 2015). In a study published in Italy, in 2007, mean Pb levels in edible viscera of animals aged less than one year old ranged from 0.004 mg/kg to 0.0318 mg/kg (Forte & Bocca, 2007). In Nigeria, the results showed for Pb range between <0.04 – 501.79 mg/kg in edible offals

Journal Pre-proof (Ihedioha & Okoye, 2012). In samples from bovine livers and kidneys collected from slaughterhouses in Brazil, the values obtained were 0.12 mg/kg and 0.13 mg/kg, respectively (Aranha et al., 1994). This study was not included in this review because it did not meet the inclusion criteria established. The range of Pb levels for fish, seafood and canned fish was from ND to 73.11 mg/kg d.w. Overall individual results for Pb levels for fish, seafood and fish products, analyzed around the world until 2018, from the GEMS/Food database ranged between ND and 17 mg/kg (WHO, 2019). Of the total samples, 888 corresponded to fresh fish, including 17 species:

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Caranx crysos, Cynoscion leirachus, Salmo salar, Genypterus brasiliensis, Lopholatilus villarii, Priacanthus arenatus, Lile pequitinga, Macrodon ancylodon, Mugil liza, Micropogonias furnieri, Sardinella brasiliensis, Pangasius spp, Bryconamericus

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iheringii, Pseudoplatystoma corruscans, Chichia spp, Oreochromis niloticus and Tuna (Dalzochio et al., 2017; Silva et al., 2017; Arantes et al., 2016; Araújo et al., 2016;

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Hauser-Davis et al., 2016; Molognoni et al., 2016; Santos et al., 2013; Guimarães, 2013; Medeiros et al., 2012; Morgano et al., 2011a; Morgano et al., 2011b; Tajiri et al.,

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2011; Niekraszewick, 2010). The levels for fish in these studies ranged from ND to 3.31 mg/kg. Higher values were obtained for carnivorous fish of the species

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Pseudoplatystoma corruscans collected in the wild (Arantes et al., 2016). The worldwide range (ND to 1 mg/kg) for fish analyzed until 2018 from the GEMS/Food

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database was lower than that observed in the present study (WHO, 2019). A wide range of variation among Pb concentrations (0.02 - 2.02 mg/kg d.w) among 17 fish species

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was seen by Tong et al. (2016). Furthermore, in fish samples collected between 2009 and 2010 in the market of Granada, Spain, average levels of Pb in fresh and frozen fish ranged from 0.004 mg/kg to 0.544 mg/kg (Olmedo et al., 2013). Lower average Pb levels for fish were observed in most previous studies involving these food matrices. In marine fish analyzed in Italy, Pb levels between 0.013 mg/kg and 0.269 mg/kg were reported (Miedico et al., 2015; Pastoreli et al., 2012). The average levels of Pb contamination for fish investigated in China have historically varied between 0.027 mg/kg and 0.115 mg/kg (Hu et al., 2016; Jin et al., 2014; Liu et al., 2010). The range of levels of Pb for canned fish (0.19 mg/kg to 2.15 mg/kg) obtained in a study included in this review (Tarley et al., 2001) was similar to the Pb contamination observed by Iwegbue et al. (2015) for canned fish samples (0.05 mg/kg to 2.98 mg/kg)

Journal Pre-proof in Nigeria. However, a lower range of Pb levels was estimated in other studies. For example, Olmoedo et al. (2013) established median Pb levels between 0.004 mg/kg and 0.584 mg/kg for canned fish. The mean Pb content determined in canned fish in Ghana was 0.72 mg/kg, ranging from <0.01 mg/kg to 1.44 mg/kg (Okyere et al., 2015). The mean Pb level reported for canned fish in Serbia was 0.048 mg/kg (Popovic et al., 2018), and the mean Pb level reported by Storelli et al. (2010) in Italy was 0.06 mg/kg wet wt. The difference between the Pb levels for canned fish could have resulted from the advances in packaging technology, which eliminated the leaching of Pb into the food (ANVISA, 2007).

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Although the Pb levels for the category vegetables and vegetable products had been considered the second most concerning in the present study, the mean level of 0.1833 mg/kg (95% CI 0.1187 – 0.2487; I2 = 100%) was lower than that reported in

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Singapore (0.402 mg/kg) and the United States (0.3 mg/kg) (WHO, 2011a). This mean level is within the ranges reported by Mendes (2015) related to the Brazilian monitoring

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programs (0.083 mg/kg and 0.2 mg/kg for beans and roots and tuber vegetables, respectively) and that reported by Sakuma et al. (1989) related to leafy vegetables

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collected in São Paulo (from 0.17 mg/kg to 0.41 mg/kg). The levels of Pb of 20 species of edible vegetables investigated in Spain in the 1980s ranged from 0.021 mg/kg to

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0.581 mg/kg (Bosque et al., 1990). In Jordan, in 2011, when investigating 16 species of edible vegetables, the average level ranged from ND (eggplant) to 1.950 mg/kg d.w.

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(caruru) (Massadeh et al., 2011).

However, smaller values were observed by Liu et al. (2010), who obtained

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average levels varying from 0.036 mg/kg to 0.018 mg/kg for vegetables and 0.098 mg/kg for tuber vegetables, in their investigation in China. In China, Pb levels of 0.096 mg/kg were seen in the plant category (Jin et al., 2014). Although only two types of foods had been studied in Bangladesh, the levels of Pb ranged from 0.005 mg/kg for tomatoes to 0.057 mg/kg for beans (Shaheen et al., 2016). According to Higgins & Green (2011), in a SR heterogeneity is expected due to the grouping of distinct studies that present methodological diversity. In this review, there were observed some inconsistencies. Significant heterogeneity was present in most of subgroups (food categories), possibly not only due to questions regarding individual characteristics of the different types of food, proportion of food group composition and sampling but also due to the differences between the analytical techniques used in the studies to identify Pb in the same type of food and the lack of the

Journal Pre-proof evaluation of the applicability of the analytical methods to the LMs, as already reported in this work. Grouping by category was an adequate investigative strategy for the subgroups analysis because it allowed, even with limitations, to group foods with similar characteristics and analytical methods. Heterogeneity (I2) estimated for the fruits and fruit products (0%) and for nuts, cocoa and products (45%) were smaller than those calculated for the other categories and also presented less variability in the adopted analytical techniques (Table 3). Mendes (2015) reported that it is possible to identify, in a single food category, LODs

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reported by an author that are superior to LOQs adopted by another author, which could interfere with the mean concentration of the analyte. According to the FAO & WHO (2009), the selection of applicable sampling procedures and methods of analysis is

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critical for obtaining data on chemical concentrations in consistent and comparable foods.

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Despite the variety of analytical methods observed in the review and in other studies (Panel & Chain, 2013; WHO, 2011a), there is no sanitary standard in Brazil that

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establishes which analytical method should be used (ANVISA, 2013). However, analytical methods should be validated to be applied to the analyte and matrix,

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complying with the LMs, which could result in a reduction in the effect of the analytical method on the heterogeneity of the results (Codex Alimentarius Commission, 2016).

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Thus, in the case of Pb, an environmental contaminant, the use of low sensitivity methods may Pb to the lack of real concentrations, negatively interfering with the

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establishment of prevalence levels and evaluation of the proportion of positive samples within the sampled food groups and therefore the evaluation of the correct sampling and prioritization of the exposure sources. In addition, sensitive and applicable methods could minimize the heterogeneity of the results. These assumptions are based on the wide variety of analytical methods and amplitude of the limits observed in the present study. The interference of the year of the study in the Pb levels established within the categories was also investigated. However, it was not possible to establish a pattern of contamination by periods. Although sanitary standards were reissued in Brazil during the period of the studies (ANVISA, 2013), robust evidences about the impact of the regulation on levels of contamination were not observed.

Journal Pre-proof There was identified a little reduction in the overall and subgroup prevalence due to the sensitivity analysis, based on the exclusion of studies with small samples. However, no significant effects were observed in the heterogeneity of the meta-analysis (Supplementary Figure 2).

4. Conclusions To provide food contamination data, as an official risk assessment, it is recommended to use only analytical results obtained by monitoring and surveillance

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programs. However, this first report of SR about Pb contamination in food in Brazil was considered an applicable screening strategy to synthesize analytical data from studies reporting a broad and variable contamination of food. The SR included 77 studies which overall occurrence of Pb was estimated at 0.0541 mg/kg, ranging between 0.0004 mg/kg

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and 0.4842 mg/kg. Additionally, the subgroup analysis by food categories was

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considered an interesting strategy applied to heterogeneity investigation. Relevant uncertainties were identified due to the high heterogeneity, lack of prevalence data for

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some food categories (infant food, fruits and fruit products, eggs and oils and fat spreads), sampling procedures and variability in the analytical methods. To address

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these gaps some recommendations are appointed. Firstly, more high-quality studies should be conducted to provide satisfactory evidence about Pb levels in food and further

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validate these methods. Secondly, Pb levels should be stablished by analytical methods more sensible as possible, and validated to be applied to analyte and matrix, complying

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with the maximum regulated levels.

Conflict of interest: The authors declare that they have no conflicts of interest.

Acknowledgments: The authors are grateful to, the Ezequiel Dias Foundation (FUNED), the Food Science Department of the Faculty of Pharmacy (FAFAR) at the Federal University of Minas Gerais (UFMG), and the librarian and health specialist, Maria do Rosário de Fátima Rodrigues Vasconcelos.

Funding:

Journal Pre-proof This work was supported by the Foundation for Research Support of the State of Minas Gerais (FAPEMIG)

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Journal Pre-proof

Identification

Identified studies through database searching (n=1171) Medline(PubMed) (n=208), Cochrane (n=89), CINAHL (n=21), Web of Science (n=63), Food Science and Technology Abstract (n=126), AGRIcola (n=80), SCOPUS (n=143), LILACS (n=351), São Paulo State Secretary (n= 16), IBCIT (74)

Studies identified through other sources (3) Screening

Full-text articles assessed (n=108)

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Excluded studies by applying exclusion criteria (n=901)

Excluded studies by applying exclusion criteria (n=31) Type of study: 12 Population: 19

na

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Type of study: 11 Population: 692 Outcome : 192 Duplicated: 6

Included studies (77)

Jo

ur

Included

Titles and abstracts screened (n=1009)

Elegibility

Excluded studies by Endnote (n=162)

Figure 1. PRISMA – Studies identification, inclusion and exclusion.

Journal Pre-proof

Jo

ur

na

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Figure 2. Graphical representation of the results of the meta-analysis for all food categories

Jo

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Journal Pre-proof

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Journal Pre-proof

Journal Pre-proof Table 1. Excluded studies and respective reasons for exclusion. Studies

Reasons for exclusion

Macedo et al., 2017; Souza et al., 2017; Xie et al., 2016; Amato-Lourenco et al., 2016; Cardoso et al., 2014; Ettinger

Population

et al., 2014; Izário-Filho et al., 2014; Islam et al., 2014; Magna et al., 2014; Mataveli et al., 2013; Gonçalves et al., 2011; Antonious et al., 2010; Koyashiki et al., 2010a; Koyashiki et al., 2010b; Segura-Muñoz et al., 2006; Zenebon et al., 2004; Okada 1997; Lima et al.,1996. Borges et al., 2015; Mendes, 2015; Rosa et al., 20 ; T šić et al., 2015; Barros & Barbieri, 2012; Silva et al., 2010a;

Type of study

Seixas et al., 2005; Santos et al., 2002; Cunha et al., 2001; Aranha et al., 1994; Sakuma et al., 1989; Rocha et al., 1985.

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Table 2. Characteristics of the included studies which determined lead concentration in food and food products. Study Year (surname of of first author the and year of study publication)

State or country

-p

Objective

Sampling locality

Lead levels

Score of quality

2014

Development of analytical method for determination of metals, including lead, in honey

Paraná

Market

141 ng/g - 228 ng/g

6

Andrade et al., 2018b Santos et al., 2018

NI

Determine trace and toxic elements in yogurt

Paraná

< 35.4 - 210 ± 16ng/g

7

NI

Bahia

< LQ

5

Costa et al., 2017

2016

Bahia

Market

0.05 mg/kg - 2.84 mg/kg

7

Dalzochio et al., 2017 França et al., 2017 Mandlate et al., 2017 Oliveira et al., 2017

NI

Evaluate the effect of the heat treatment on trace elements in three legume species, including lead, and bioaccessibility Determine lead content in crab, including- fresh tissue and culinary preparations Analysis of water and bioaccumulation of metals in capture fish Determine metals concentrations, including lead, in lettuce. Evaluate of soft drink parameters

Food producer Market

Rio Grande do Sul Pernambuco

In nature

0.09 ± 0.05mg/kg - 0.34 ±0.19mg/kg
6

44 ng/L - 115 ng/L

6

Food producer

0.00212 mg/L - 0.03736 mg/L

5

lP

re

Andrade et al., 2018a

na

2013 2017

Rio Grande do Sul Paraná

Food producer Market

6

Development of analytical methods to determine cadmium and lead content in milk

Santos et al., 2017

NI

Determine and compare the metals concentrations in mate herbal in different South states in Brazil

Rio Grande do Sul

Market

0.015 mg/kg - 0.15 mg/kg

6

Silva et al., 2017

2013

Determine metals concentrations, including lead, in seafood.

Rio de Janeiro

Market

< 1.9 ng/g

6

Arantes et al., 2016

2010 2012

Determine the metals concentrations, including lead, in seafood.

Minas Gerais

In nature

0.94 ± 0.98 mg/kg - 3.31 ± 4.64 mg/kg

5

Araújo et al., 2016

2013 2014

Cadmiun and lead levels and risk of consumption in seafood

Bahia

Market


6

Caldas et al., 2016

2014

Determine the metals concentrations, including lead, in meat and edible offals

Rio de Janeiro

Market

0.06 ±0.03 mg/kg - 0.10 ± 0.08 mg/kg

6

Hauser-Davis et al., 2016

2016

Metals bioacumulation in fish

Rio de Janeiro

In nature

< LQ

4

Lino et al., 2016

2009 2010 2016

Bioaccumulation of metals in bivalve mollusks

Rio de Janeiro São Paulo

In nature

< 0.6 mg/kg

5

Market

<0.030 mg/kg - 0.245 ± 0.007 mg/kg

7

Mataveli et al., 2016

Jo

ur

NI

Develop analytical methods to determine cadmium and lead content in rice

Morena-Piñeiro et al., 2016

NI

Bioavailability of essential and toxic metals in almonds

Spain

Market

< LQ - 80.2 ± 10.2 ng/g

6

Pedron et al., 2016

2014 2015

Determine essential elements concentration in rice and non-rice infant food

São Paulo

Market


7

dos SantosAraujo & Alleoni, 2016 Sattler et al., 2016 Schunk et al., 2016

2016

Evaluate the relationship between the soil and the concentration of metals including lead in vegetables

São Paulo

Market

0.93 ± 2.12 mg/kg

5

2011

Determine the concentrations of essentials and no essential elements in pollen Determine the metals concentrations , including lead, in tea

Rio Grande do Sul Espirito Santo

Food producer Market

0.015 ± 0.001 mg/100g

5 6

Silva et al., 2016

2011 2012

Determine the metals concentrations, including lead, in seafood.

Bahia

Market

0.01 mg/L - 0.02 mg/L for infusion and 0.42 mg/kg 0.55 mg/kg for chamomile tea < 0.144 mg/kg d.w

2015

6

Journal Pre-proof Evaluate the metals levels, including lead, in different parts of vegetable cultivated in Brazil areas which use fertilization Develop analytical methods to determine cadmium and lead contents in ice-cream packing

Minas Gerais

Kiyataka et al., 2015

2014

Lima et al., 2015

NI

Molognoni et al., 2016

NI

Pozebon et al., 2015

Determine the metals concentrations, including lead, in rice Development of analytical method for determination of metals including lead in fish

Rio Grande do Sul Brasil

2015

Toxic elements and nutrients in mate herb

Alkmim Filho et al., 2014a

2002 2008

Alkmim Filho et al., 2014b

2002 2008

Araújo et al., 2014

2011

De Jesus et al., 2014 Kiyataka et al., 2014

2011 2012 2013

Development of analytical method for determination of metals, including lead, in fish Development of analytical methods to determine cadmium and lead content in yogurt packing

Morgano et al., 2014 Nacano et al., 2014 Villa et al., 2014

NI

2010

Determine the metals concentrations, including lead, in sashimi Assess the exposure to metals including lead for school food Evaluate the cadmium and lead concentrations in chocolate commercialized in Brazil Development of analytical methods to determine cadmium and lead content in nuts Determine inorganic contaminants in honey

2013

Risk assessment of lead ingestion in manioc

Welma et al., 2014 Leme et al., 2014

2011 2014 NI

Experimental agriculture area Market

<0.040 mg/kg - 0.106 mg/kg

6


6

Market

<0.04 mg/kg

4

Food producer

< 0.0284 mg/kg

6

Rio Grande do Sul

Market

6

Determine the metals concentrations, including lead, in chicken and swine meat between 2002 and 2008

Minas Gerais

Food producer

0.407 ± 0.230 mg/kg for Brazil and 0.222 ± 0.107 mg/kg - 0.314 ± 0.178 mg/kg for other countries 0.191 mg/kg - 0.281 mg/kg

Determine the metals concentrations, including lead, in cattle meat and edible offals between 2002 and 2008 Compare the metals concentrations, minerals and pesticides residues in vegetables

Minas Gerais

Food producer


6

Pernambuco

Agriculture area / crop area In nature

0.18 ±0.007 mg/L - 0.32 ± 0.014 mg/L

5

< LQ

6

Food producer


5


6

<21 ng/g - 138.4 ng/g

7

NI

Determine the lead concentration in eggs

2011 2012 2009

Mazon, 2013

2013

Migues et al., 2013 Nedzarek et al., 2013 Santos et al., 2013 Silvestre & Nomura, 2013 Medeiros et al., 2012 Batista et al., 2012

2011 2012 2013

Determine the metals concentrations, including lead, in milk. Determine the metals concentrations, including lead, in ish ri er’s sediments nd hair Development of analytical method for determination of metals, including lead, in wine Envirommental impact in shrimp

Bragança et al., 2012 Vieira, 2012

2011

Wilson et al., 2012 Dessuy et al., 2011

lP

na

Determine the metals concentrations, including lead, in cattle, chicken and swine meat

Jo

2011

Determine the minerals concentrations in coffee beverage Determine the metals concentrations, including lead, in seafood. Development of analytical methods for determination of cadmium and lead content in rice Assess levels of metals, including lead, in fish

ur

2009

2005 2009 2012 2011

Jesus et al., 2011

2010

Morgano et al., 2011a

2010

Morgano et al., 2011b Rodrigues, 2011

2011

Souza et al., 2011 Tajiri et al., 2011 Arcari, 2010

2006 2010 2006 2007 2010

De Castro, 2010

2007

NI

Bahia São Paulo

São Paulo

São Paulo Poland

Market


6

Food producer Food producer Market

Without contaminantion for lead 0.34 mg/kg

7

0.010 mg/kg - 0.089 mg/kg

5

Food producer In nature

0.034 ± 0.004 mg/L - 0.467 ± 0.306 mg/L 0.03 𝜇g/g - 0.1𝜇g/g

6

Amazonas São Paulo

Market

< 0.15 mg/L

6

Bahia

In nature

< LQ

6

Polônia

Market

0.71 mg/kg ± 0.13 mg/kg

4

Bahia

Market

0.1 mg/kg - 5.4 mg/kg

6

São Paulo

Market

ND - 0.06 mg/kg

6

Rio de Janeiro São Paulo

Market

0.04 ±0.03mg/kg - 0.3 ±0.3 mg/kg 7.3 ±4.5 ng/g - 15.3± 8.8 ng/g for chicken; 12.6± 30 ng/g for pork and 9.3± 7.7 ng/g for cattle
6


6

0.2 ppb - 0.4 ppb for Brazil

5


6

São Paulo

Mato Grosso do Sul Amazonas Brazil

Paraná

Determine trace elements, including lead, in fruit juice Development of analytical method for determination of metals, including lead, in honey Determine the arsenic and lead concentrations in fruit juice Development of analytical method for determination of metals, including lead, in alcoholic beverages and vinegar after leaching from pewter cups Development of analytical method for determination of metals, including lead, in vegetable Determine the metals concentrations, including lead, in fish

Mato Grosso do Sul Minas Gerais United States Rio Grande do Sul

Determine the metals concentrations, including lead, in fish Determine the metals concentrations, including lead, in milk. Determine the metals concentrations, including lead, in fish Determine the metals concentrations, including lead, in fish (Oreochromis niloticus) Characterization of fortified wine produced in Brazil Determine toxic metals (cadmiun and lead) in milk and infant formula commercialized in Brasilia

6

Food producer Food producer Market

re

Carneiro et. al., 2013 Freitas et al., 2013 Gomes et al., 2013 Guimarães, 2013

2010 2011 2013

Brazil

ro of

2010 2011

-p

Corguinha et al., 2015

Food producer

Market Food producer Market Market

6

5

5

6

5

Bahia

Ni

São Paulo

Market

0.101 ± 0.097 mg/kg - 0.228 ± 0.127 mg/kg

6

São Paulo

Market

<0.02 - 2.92mg/kg

6

Goiás

Food producer In nature

1.50 ± 0.70 mg/kg - 40 ± 7.07 mg/kg
5

0.00338 ± 0.0008 mg/kg 0.004936 ± 0.0007 mg/kg 0.084 mg/kg - 0.109 mg/kg

5

Bahia Paraná Florianópolis Brasília

Food producer Food producer Market

3

5 7

5

Journal Pre-proof Morgano et al., 2010 Niekraszewicz, 2010 Silva et al., 2010b Caldas et al., 2009 Vulcano, 2008

2007 2008 NI

Gonçalves, 2007

2006

Dias & Cardoso,2006 Mattos et al., 2006 Oliveira & GomesNeto,2006 Salazar et al., 2006 Mirlean et al., 2005 Santos, 2005

2006

2004 NI NI

2003 2004 2006

2005 1997

Tarley et al., 2001 Mantelatto et al., 1999 Elpo & Freitas, 1995 Moura-Costa et al., 1989

1999 2000 1995

1989

0.12 ± 0.13 mg/kg

6

< LD

5

Food producer Market

3 – 1,050 𝜇g/kg

6

0.0018 mg/L - 0.216 mg/L

6

Market

0.42 mg/kg - 0.53 mg/kg

6

Food producer NI

0.392 mg/kg - 6.030 mg/kg

6

<0.01 mg/kg

5

Rio Grande do Sul São Paulo

Market


6

Market

2.8 ± 0.3µg/L - 32.4 ± 2.6 µg/L

4

São Paulo

Market


5

Rio Grande do Sul São Paulo

Market

0.005 mg/L - 0.290 mg/L

5

Food producer In nature


5


5

Market

0.19 mg/kg - 2.15 mg/kg

6

São Paulo

In nature

5

Paraná

Market

21.15± 4.55 mg/kg - 73.11 ± 33.80 mg/kg d.w 0.05 mg/kg - 0.56 mg/kg < 0.08 mg/kg - 0.4±0.5 mg/kg

5

São Paulo Minas Gerais Goiás Brasil

Determine the metals concentrations, including lead, in polen. Biomonitoring of trace elements including lead in oysters Determine the metals concentrations, including lead, in canned fish. Determine the metals concentrations, including lead, in shrimp Evaluate the metal levels, including lead, in staple food Development of analytical methods to determine cadmium and lead content in maize

Rio Grande do Norte Paraná

-p

Silva et al., 2001

Food producer Market

Rio Grande do Sul Pernambuco

Determine the metals concentrations, including lead, in vegetable Evaluate the contamination in grape products

2005

1993

São Paulo

ro of

2006

Determine the metals concentrations, including lead, in polen. Elemental concentration in canned tuna and interaction between canned and food Determine the lead concentration in milk and milk products. Development of analytical method for determination of metals, including lead, in cachaça Development of analytical method for determination of metals, including lead, in tea Determine the metals concentrations, including lead, in meat Determine the lead concentration in sugar and candies Determine the metals concentrations, including lead, in supplement. Determine the metals concentrations, including lead, in vegetable

Minas Gerais

Agriculture area / crop area

6

re

LD: limit of detection; LQ: limit of quantification; NI: not informed. In nature: river, bay, sea.

Beverage Meat and meat products

Nuts, cocoa and products Fruits and fruit products Grains, cereals and products Milk and milk products Eggs

Banana, jam fruit and grape vinegar, meals based on fruit Rice, mayze, wheat, soya, flour, pasta and bread Raw milk, processed milk, yogurt, cheese Eggs

Min - Max mg/kg

Analytical techniques

LOD

LOQ

FAAS, HPL-ICP-MS

3 x 10-5 - 0.00271

0.009

ETAAS, ICP-MS, TS-FF-FS-AAS, FAAS ICP-MS, ICP-OES, GF-AAS, AAS

9.2 x 10-5 - 0.1

0.0003 - 0.095

na

Sugar

Milk and cereal infant food (solid) Honey, sugarcane, syrup and candy Wine, beers, chachaça, juice, soft drink, coffee, tea and herbal tea Meat, pork, chicken, fish, edible offals, seafood and canned fish, meals based on (Meat, pork, chicken, fish) Brazil nuts and chocolate

ur

Infant food

Food (examples)

Jo

Category

lP

Table 3. Analytical characteristics observed by food category

-9

7.2 x 10 - 0.05 -5

0.001 - 0.0045

ICP-MS, GF-AAS, AAS, ETAAS, FAAS, ICP-OES, Spectroscopy PIXE

5.0 x 10 - 4.7

0.0003 - 0.9597

ICP-MS, ICP-OES, GF-AAS

0.0063 - 0.0375

0.021 - 0.042

FAAS

0.05 - 0.1

NI

GF-AAS, HPL-ICP-MS, ICP-OES

0.007 - 0.080

0.064

GF-AAS, FAAS, ICP-OES

0.00064 - 0.0136

0.00214 - 0.035 0.09

ICP-MS

NI

Oils and fat spreads

Vegetable oil, and margarine

FAAS

0.005

NI

Other foods Vegetables and vegetable products

Calcium supplement, pollen Vegetables, potato, tomato, beans, manioc, flour,meals based on vegetables -

ICP-OES ICP-MS, ICP-OES, AAS, ETAAS, GF-AAS, FAAS

0.0005 - 0.01 0.0004 - 0.06

0.02 - 0.06 0.0014 - 0.5

-

7.2 x 10-9 - 4.7

0.003 - 0.9597

TOTAL

Min: minimum; Max: maximum; LOD: limit of detection; LOQ: limit of quantification; NI: not informed; AAS: atomic absorption spectrometry; ICP-MS: inductively coupled plasma mass spectrometry; ICP-OES: inductively coupled plasma optical emission spectrometry; GF-AAS: atomic absorption spectrometry with graphite furnace; FAAS: flame atomic absorption spectrometry; ETAAS: electrothermal atomic absorption spectrometry; HPLC-ICP-MS: inductively coupled plasma mass spectrometry coupled to high performance liquid chromatography; TS-FF-FS-AAS: atomic absorption spectrometry in fast sequential mode with flame furnace and thermal aerosol.NI: not informed

Table 4. Lead levels in mg/kg for the different food categories. Category

Number

Prevalence

Heterogeneity

Journal Pre-proof

Studies

Samples

Mean levels of lead mg/kg

95%CI

I2 (%)

p (chisquare)

Weight (%)

2 5 15 30

66 150 535 5891

0.4842 0.0683 0.0483 0.1248

[-0.5548 ;1.5233] [0.0116; 0.1249] [0.0444 ; 0.0522] [0.1202 ; 0.1294]

87% 97% 100% 100%

<0.01 <0.01 0 0

2.2 2.4 20.9 29.3

3

105

0.0065

[-0.0098 ; 0.0228]

45%

0.16

2.6

3

51

0.0004

[-0.0073 ;0.0082]

0%

0.41

1.5

8

452

0.0562

[0.0303 ; 0.0821]

99%

<0.01

12.4

9

270

0.1073

[0.0532; 0.1615]

100%

0

7.7

1 4 1 12

56 150 7 733

0.0414 0.1485 0.0786 0.1671

[0.0150; 0.0678] [0.0134 ; 0.2836] [-0.0304; 0.1875] [0.1072 ; 0.2270]

NA 97% NA 100%

NA <0.01 NA 0

0.2 3.7 0 17

TOTAL

93

8466

0.0541

[0.0529; 0.0554]

100%

0

100

ro of

Infant food Sugar Beverage Meat and meat products Nuts, cocoa and products Fruits and fruit products Grains, cereals and products Milk and milk products Eggs Other foods Oils and fat spreads Vegetables and vegetable products

95% CI: 95% confidence interval; I²: I-squared (I²); p: probability; NA: not applied.

-p

Graphical Abstract

Levels of lead in Brazilian food

re

Vegetables and vegetables products Oils and fat spreads

lP

Other foods

Milk and milk products

Grains, cereals and products

na

Food categories

Eggs

Fruits and fruits products

Nuts, cocoa and products

ur

Meat and meat products

Jo

Beverage Sugar

Infant food 0.00

0.10

0.20

0.30

0.40

0.50

0.60

Lead (mg/kg)

Highlights     

This paper is the first systematic review on food contamination with Pb in Brazil. Contamination with Pb was observed in basic Brazilian food. Higher levels of Pb were observed in infant food, vegetables, meat and meat products. More studies are necessary for eggs, fruits, infant food, oils and fat spreads. A systematic review was considered an applicable strategy for risk assessment.