key: cord-0960273-9l4f6nay
authors: Ngweme, Georgette N.; Al Salah, Dhafer Mohammed M.; Laffite, Amandine; Sivalingam, Periyasamy; Grandjean, Dominique; Konde, Joel N.; Mulaji, Crispin K.; Breider, Florian; Poté, John
title: Occurrence of organic micropollutants and human health risk assessment based on consumption of Amaranthus viridis, Kinshasa in the Democratic Republic of the Congo
date: 2020-09-02
journal: Sci Total Environ
DOI: 10.1016/j.scitotenv.2020.142175
sha: b46e8463849d50f76f5985f15e3f443d643b89e1
doc_id: 960273
cord_uid: 9l4f6nay

The contamination of water resource and food chain by persistent organic pollutants (POPs) constitutes a major environmental and human health concern worldwide. The aim of this study was to investigate the levels of POPs in irrigation water, soil and in Amaranthus viridis (A. viridis) from different gardening sites in Kinshasa to evaluate the potential environmental and human health risks. A survey study for the use of pesticides and fertilizers was carried out with 740 market gardeners. The levels of POPs (including organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and polycyclic aromatic hydrocarbons (PAHs)) were analyzed in irrigation water and 144 vegetable samples collected from different gardening sites. The assessment of potential human health risk was estimated by calculating daily intake and toxic equivalency to quantify the carcinogenicity. The results show highest PAH levels in A. viridis from all studied sites. The concentrations of the sum of seven PCBs (Σ7PCBS) congeners in analyzed plants ranged between 15.89 and 401.36 ng g−1. The distributions of OCPs in both water and A. viridis were congener specific, chlorpyrifos-ethyl and p,p′-DDE were predominantly detected. Among PBDEs, only BDE47 was quantified with noticeable concentration in A. viridis, while no PBDEs were detected in irrigation water. Higher estimated daily intake values indicate that consuming leafy vegetables might associate with increased human health risks. However, calculated incremental lifetime cancer risk values indicates no potential carcinogenic risk for the local population. The results of this study provide important information on A. viridis contamination by POPs and strongly recommend implementing the appropriate measures to control the use of chemicals used in studied gardening areas. Thus in Kinshasa, urban agriculture control programs for POPs and fertilizers is very important in order to protect the public health through direct and dietary exposure pathways.

Persistent organic pollutants (POPs) are toxic, persistent, with strong hydrophobicity, non-degradable, can accumulate in fauna and flora, and have the potential to long-range transport through the atmosphere (Olatunji, 2019; Olisha et al., 2019; Cindoruk et al., 2020) .

Due to their properties, contamination of environments with POPs is of great public health concern. As a result, the occurrence, and toxicological effects on the human and environmental health of these organic pollutants have been widely investigated in different environmental compartments (air, soil, aquatic environment) and food chains (e.g., Poté et al., 2008; Doong et al., 2008; Montuori et al., 2016; Combi et al., 2016; Babut et al., 2019; Shen et al., 2013) . In sub-Saharan African countries, some studies have been conducted to assess the POPs contamination levels in sediments from rivers, lakes, stream and groundwater (e.g., Verhaert, 2013; Kilunga et al., 2017; Mwanamoki et al., 2014; Bruce-Vanderpuije et al., 2019) , and their accumulation in fish (Ssebugere et al., 2014a,b) , fruits and vegetables (e.g., Adeleye et al., 2019; Lehmann et al., 2017; Ibrahim et al., 2018; Kolani et al., 2016) .

Three major types of POPs are commonly reported in the environment for many years.

They were mostly anhropogenically derived compounds including polychlorinated biphenyls (PCBs), polyaromatic hydrocarbons (PAHs), and organochlorine pesticides (OCPs).

Moreover, according to the Stockholm Convention 2004 regulations, protection of environment and human health risk from POPs is a high priority (Stockholm Convention, 2004) . For instance, through a variety of food matrices (e.g., vegetables, eggs, fish, meat, oils, and milk) consumption, these contaminants were reported to induce health effects such as neurotoxicity, endocrine disruption, cancer, reproductive disorders, leukemia, asthma and health risks to fetal development (Lü et al., 2014; UNEP/WHO, 2013; Gilden et al., 2010; Kima et al., 2017; Fernandes et al., 2019) . POPs are very persistence in soil and can affect crop quality and yield. Consequently, many studies propose the organic pollutant degradation J o u r n a l P r e -p r o o f Journal Pre-proof mechanism pathways (such as photocatalytic degradation) and the remediation efficiency of multi-element contaminated soil in order to reduce exposure, guarantee food safety and protection of human health (e.g. Venny et al., 2012; Ye et al., 2020; 2019a,b; Weber et al., 2019) .

Vegetable is an essential part of the human healthy diet and considered as a source of many essential nutrients to maintain normal physiological functions, antioxidants, dietary fiber metabolites and to prevent several diseases (Boeing et al., 2012; FAO/WHO, 2017; Azi et al., 2018) . Vegetables also attract a wide range of pests and affected by diseases, and therefore need intensive pest management (Dinham, 2003) . Leafy Amaranthus spp. are very important to the human diet because its constitute excellent sources of magnesium, manganese, phosphorus and vitamin C, its contain higher mineral levels than many common leafy vegetables, have a calorific value of 43.35 kcal, crude protein 2.11%, moisture content 87.90%, carbohydrate content 7.67%, crude fiber 1.93%, crude fat 0.47%, and ash content 1.85% (Sharma et al., 2012; Mota et al., 2016; Jiménez-Aguilar and Grusak, 2017) .

Amaranthus spp. are among of the most domestic vegetables consumed in south of Asian and sub-Saharan African countries, and currently imported and sold in African and Asian shops located in many EU countries. The local population consumes daily and during the big festivals A. viridis leaf generally cooked and favors it for taste and tradition. The plant is mainly cultivating in peri-urban market gardening (Akinola and Eresama, 2009; Islam and Hoque, 2014; Azi et al., 2018; Bashri et al., 2016) .

In the DRC, particularly in Kinshasa its Capital City, the urban agriculture (market gardeners) plays an economic and social role in daily life of the population and provides more than 60% of the consumed fresh produce supply of the city. After cassava leaf, A. viridis has been identified to be a second most consumed leaf vegetable in the DRC. The A. viridis cultivation is mainly performed in the peri-urban municipalities near riverbanks. This activity J o u r n a l P r e -p r o o f Journal Pre-proof supports many families in Kinshasa and employs more than ten thousands of people. It can therefore contribute to the sustainable development of the city under certain conditions, especially through its professionalization, the non-use of chemical inputs and the equitable distribution of arable land (Musibono et al., 2011) . intake data in order to assess the local consumer health risks.

The survey study for the use of pesticides and fertilizers was performed in 8 studied sites as a questionnaire. A total of 740 gardeners (100/site except for the Kimpoko site (40)) were interviewed concerning the types and practices of pesticides and fertilizers use (pesticides and fertilizers use practices, application interval and water method used, preharvest packaging and feeling of discomfort related to the application of pesticides). All interviewed gardeners are working in sampled sites; 54.6% males and 45.4% females, with an average age of 47 years.

This research was performed in 8 gardening sites located in Kinshasa, the capital city of DRC and immediately transported to the laboratory for pre-treatment and analysis within 72h.

Before analysis, edible plant parts (leaf) were washed with deionized water, weighted, lyophilized and water content was calculated. Soil samples were sieved through a 1 mm mesh size sieve, weighted, lyophilized and water content was calculated.

Chlorinated pesticides, PCBs, PAHs and PBDEs analysis in water, soil and plant samples was performed using gas chromatography with triple mass spectrometry detection Mwanamoki et al., 2014; Thevenon et al., 2013 (SD) ). The validation of the used analytical methods was performed by calculating the limit of detection (LOD), the limit of quantification (LOQ), and recovery values as performed by Lehmann et al. (2018) . The limits of quantification (LOQ) for the selected target analytes, material and chemical sources, purity as well as operating parameters for GC-MS and UPLC-MS/MS are described in

Supplementary Data (sections S1 and S2, Tables S2-S5).

The daily intake of PAH (DI-PAH) through consumption of PAH-contaminated vegetable was determined using the following equation:

Where CPAH, C factor , V intake and B weight represent the PAH concentration in vegetables (g kg -1 ), conversion factor, daily intake of vegetables, and average body weight, respectively. To convert fresh weight of vegetable into dry weight, a conversion factor (0.085) was used (Rattan et al., 2005) . Average daily vegetable intake for adults were considered as 0.067 kg person -1 day -1 (PNUD-SOCOGEM, 2000; Bonkena et al., 2018) , while the average adult body weight was considered as 57.8 kg (Mbenza et al., 2006) . 

Where TEF i is the corresponding toxic equivalency factor for PAHs and C i is the concentration of the individual PAH.

Incremental lifetime cancer risk (ILCR) of PAHs from vegetable consumption was calculated using the following equation:

Where ILCR refers to the incremental lifetime cancer risk of the dietary exposure, IR is the daily PAH exposure level (g day -1 ), EF (365 days year -1 ) is the exposure frequency, BW = the average body weight of population (57.8 kg), SF is the oral cancer slope factor of ben(a)pyrene (7.3 mg kg -1 day -1 ), CF is a conversion factor (10 -6 mg ng -1 ), AT=average time (equal to 75 years for carcinogens) and ED is the exposure duration (70 years) (USEPA, 1993; 2002) .

The statistical treatment of the data has been realized using SigmaStat 11.0 (Systat Software, Inc., USA). The data were subjected to the Spearman's Rank Correlation test to investigate the possible positive and negative relationships among variables. Principal Component Analysis (PCA), a multivariate statistical analysis was performed using R (R Core Team, 2015) in order to understand relationship among analyzed compound and their potential sources. Prior to performing PCA analysis, data were centered in order to maximize the dispersion (Kilunga et al., 2017).

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We have surveyed the use of commonly used pesticides and fertilizers in the study sites. Based on the survey, the use of pesticides is as follows: Thiodan endosulfan sulfate (94.6%) >dithiocarbamate (37.2%) >rhodiatox (4.7%) >cypermethrine (4.5%) >coga 80 WPmancozebe (2.7%) >ivory-mancozebe (2%) >karate-lambda cyhalothrine (1.5%) >pacha- Table 1a and Among analyzed PAHs, low molecular weight (LM) chemicals such as naphthalene and phenanthrene were predominantly detected in water samples could probably be linked to the urban land use. Regarding the OCPs targeted in this study, only chlorpyrifos-ethyl, p,p'-DDE, and p,p'-DDD were detected in some sites. p,p'-DDE, was found to be the most dominantly occurring pesticide in irrigation water. The levels of analyzed POPs in irrigation water from our study sites were generally higher in comparison with the data obtained in a control site (Lake Ma Vallée), where the values of POPs and toxic metals in the water column and sediments are in many cases below detection limit (Mwanamoki et al., 2014; Laffite et al., 2020) .

The sum of twelve congener PCBs (Σ 12PCBs) in A. Viridis is presented in Table 2a .

The concentrations of PCBs were reported in ng g -1 dry weight. The occurrence similar to those of irrigation water was also observed for POPs in A. viridis. 

The concentrations of PCBs, PAHs, OCPs, DDTs and PBDEs in soils from eight garden areas were shown in Table 3a and 

The dominating presence of higher chlorinated PCBs could be attributed to the local input sources and the impact of urban activities in receiving river ecosystems to the gardening land.

Individual and total PAHs levels (ng g -1 ) in soil samples are presented in Table 3a . All analyzed PAHs congeners were detected in soil samples except the congener acenaphthylene.

The concentration of total PAHs (Σ16PAHs) ranged between 93.5 and 469.0 ng g -1 in soils.

In general, Σ16PAHs concentrations in soil samples were higher and more or less showed similar trend except for the sites MON and CF. The sum concentrations of (Σ16PAHs) respectively. However, results show that the levels of Phenanthrene and Fluoranthene were higher than at the sites KI and CF, respectively. The result can be explained that these regions are associated with intensive anthropogenic activities and high road traffic. Therefore, it is crucial to monitor the levels of Phenanthrene and Fluoranthene in these sites at regular intervals. The PAHs sources were identified using several diagnostic ratios, as described previously (Budzinski et al. (1997; Yunker et al., 2002; Manneh et al., 2016) . The results of diagnostic ratios are presented in 

The estimated DI-PAH used to assess the human health risk of the selected PAH associated with consumption of PAH-contaminated A. viridis are given in (USEPA, 1993; 2002) , an ILCR less than 10 -6 indicates acceptable or negligible risk, while an ILCR greater than 10 -4 represents the serious risk (Bahrami et al., 2019; Nie et al. 2014; Zhao et al. 2014; Xia et al. 2010; USEPA, 1993; 2002) . The ILCR for PAH dietary exposure calculated in this study were found in the following order CE (1.24 10 -5 )> KI (1.18 10 -5 )> SA (9.8 10 -6 )> LI (9.5 10 -6 )> MO (5.2 10 -6 )> TS (4.6 10 -6 )> MON (4.3.10 -6 ) > RF (1.21 10 -6 ). For all sites the ILCR are less the priority risk level of 10 -4 and relatively higher than the acceptable risk level of 10 -6 .

Attention should be paid for CE and KI sites where ILCR indicates values around 10 -5 .

Principle component analysis (PCA) was performed to illustrate the contributions of total PCBs, PAHs, and DDTs in water, soil and A. viridis (Fig. 2) . Fig. 2A demonstrates the impact of each variable and the relative correlations between them. All of the variables seem to have relevant significant impact (9-17%) on the total variance with the exception of the total PAHs in water and soil (3-5%), and total PCBs in water (0%). The reason that the total PCBs in water have no impact is that it remained below the detection limit at all the sites. Fig.   2B illustrates a total variance of 65.1%. The samples seem to cluster according to their physical proximity. Cluster 2 is less changing compared to cluster 1 because RF, LI, and CE are on the same river. 

Data on POPs (including organochlorine pesticides ( -OCPs, such as p,p'-DDD and p,p'-DDT were detected in irrigation water and A. viridis samples. These results suggest that the sites investigated have been exposed by agricultural misuse of DDTs.

-DI-BaP through consumption of vegetables for adults were relatively higher than the safe dose for the sampling sites KI, SA, RF and LI.

-The ILCR do not indicates a significant potential for carcinogenicity.

POPs and PAHs and recommend strongly the control of pesticide use in studied gardening areas.

-Thus in Kinshasa, urban agriculture control programs for POPs and fertilizer are very important in order to protect the consumer health.

-The authors also ascertain that need for future epidemiological studies among the residents in the study area to assess the cancer incidence, kidney disease, and endocrine disease possibly from the dietary exposure to POPs.

This research warrants that further study on POPs should be conducted at regular intervals in others consumable vegetables cultivating and selling in studied areas. Based on our results, the authors ascertained to implement suitable measures and efforts by policymakers to reduce these contaminants to improve the quality of this one of the most consumed and exported plant in order to minimize human risks.

The research presented in this paper represents the first report regarding the POPs contaminating vegetable in studied region. It provides baseline information not only on the extent of water, soil and vegetable contamination by POPs as well as evaluation of potential human health risk in a tropical area, but also represents useful tools which can be applied to the similar regions. J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f

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DG performed research: sampling and laboratory analysis; All authors analyzed data and wrote the paper

We are grateful to financial support from the Swiss National Science Foundation (grant n° IZSEZO_188357 / 1). Authors thank Professor Jérôme Lacour (Dean of Faculty of Science, University of Geneva) and Professor Marie Besse (Head of the Department F.-A. Forel for environmental and aquatic sciences, University of Geneva) for financial support to Georgette

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.J o u r n a l P r e -p r o o f