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Arsenic contribution of poultry manure towards soils and food plants contamination and associated cancer risk in Khyber Pakhtunkhwa, Pakistan

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Abstract

Exposure to high level of arsenic (As) through the ingestion of contaminated soil, dust and food plants can pose health risk to humans. This study investigates the total arsenic (As), arsenobetaine (AsB), monomethylarsenate (MMA), dimethylarsenate (DMA), arsenite (As3+) and arsenate (As5+) concentrations in poultry feed, manure, agricultural soils and food plants collected from Khyber Pakhtunkhwa Province, Pakistan. The total mean As concentrations in the edible parts of food plants ranged from 0.096 mg kg−1 to 1.25 mg kg−1 with percentile (P) values (P25-0.039, P50-0.0765, P75-0.165 1 mg kg−1 to P25-0.95, P50-1.23, P75-1.6 1 mg kg−1) and exceeded the food safety limit (0.1 mg kg−1) of Food & Agriculture Organization (FAO) and World Health Organization (WHO) in all plant species except Pisum sativum (pea) and Mentha arvensis (mint). The risk to human health was assessed through the average daily intake (ADI), hazards quotient (HQ), health risk index (HRI) and lifetime cancer risk (LTCR). The highest average daily intake of As via the ingestion of Malva neglecta (mallow, a leafy plant) was observed for adults and children. The ADI for adults and children (2.36 × 10−4 mg kg−1 day−1 and 6.33 × 10−4 mg kg−1 day−1) was about 13% and 5%, respectively, of the Bench Mark Dose Limit (BMDL0.5) of 3.00 × 10−3 mg kg−1 day−1 set by WHO. The HRI was 3 times more in the children (2.1) than the adults (0.79), posing non-cancer health risks (health risk index > 1) for children. The LTCR values were slightly higher (1.53 × 10−4) relative to USEPA and WHO limits (1 × 10−6 to 1 × 10−4) for children whereas a minimal cancer risk was observed for adults via consumption of selected food plants. The results showed that poultry manure can contaminate food plants that may lead to cancer and non-cancer risks in agricultural areas, Pakistan. Thus, it is important to minimize As concentration in poultry feed to safeguard human health and environment from adverse effects.

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References

  • Acosta, J. A., Arocena, J. M., & Faz, A. (2015). Speciation of arsenic in bulk and rhizosphere soils from artisanal cooperative mines in Bolivia. Chemosphere, 138, 1014–1020.

    CAS  Google Scholar 

  • Adekiya, A. O., Aboyeji, C. M., Dunsin, O., Asamu, F., Owolabi, A. O., Aremu, C. O., Oyetunji, D. A., Oloye, A. D., & Owolabi, I. O. (2019). Poultry manure addition affects production, plant nutritional status and heavy metals accumulation in green Amaranth (Amaranthus hybridus). International Journal of Agriculture & Biology, 22(5), 993–1000.

    CAS  Google Scholar 

  • Ali, W., Rasool, A., Junaid, M., & Zhang, H. (2019). A comprehensive review on current status, mechanism, and possible sources of arsenic contamination in groundwater: A global perspective with prominence of Pakistan scenario. Environmental Geochemistry and Health, 41(2), 737–760.

    CAS  Google Scholar 

  • Alvarez-Ayuso, E., Abad-Valle, P., Murciego, A., & Villar-Alonso, A. (2016). Arsenic distribution in soils and rye plants of a cropland located in an abandoned mining area. Science of the Total Environment, 542, 238–246.

    CAS  Google Scholar 

  • Anawar, H. M., Rengel, Z., Damon, P., & Tibbett, M. (2018). Arsenic-phosphorus interactions in the soil-plant-microbe system: Dynamics of uptake, suppression and toxicity to plants. Environmental Pollution, 233, 1003–1012.

    CAS  Google Scholar 

  • Augustsson, A., Uddh-Söderberg, T., Filipsson, M., Helmfrid, I., Berglund, M., Karlsson, H., & Alriksson, S. (2018). Challenges in assessing the health risks of consuming vegetables in metal-contaminated environments. Environment International, 113, 269–280.

    CAS  Google Scholar 

  • Aysha, M. I. J., Zakir, H. M., Haque, R., Quadir, Q. F., Choudhury, T. R., Quraishi, S. B., & Mollah, M. Z. I. (2017). Health risk assessment for population via consumption of vegetables grown in soils artificially contaminated with arsenic. Archive of Current Research International, 10(3), 1–12.

    Google Scholar 

  • Baig, J. A., Kazi, T. G., Arain, M. B., Afridi, H. I., Kandhro, G. A., Sarfraz, R. A., Jamal, M. K., & Shah, A. Q. (2009). Evaluation of arsenic and other physico-chemical parameters of surface and groundwater of Jamshoro, Pakistan. Journal of Hazardouse Material, 166, 662–669.

    CAS  Google Scholar 

  • Baig, J. A., & Kazi, T. G. (2012). Translocation of arsenic contents in vegetables from growing media of contaminated areas. Ecotoxicology & Environmental Safety, 75, 27–32.

    CAS  Google Scholar 

  • Bashir, S., Hussain, Q., Shaaban, M., & Hu, H. (2018). Efficiency and surface characterization of different plant derived biochar for cadmium (Cd) mobility, bioaccessibility and bioavailability to Chinese cabbage in highly contaminated soil. Chemosphere, 211, 632–639.

    CAS  Google Scholar 

  • Bellows, B.C. (2005). Arsenic in poultry litter: organic regulations. ATTRA the National Sustainable Agriculture Information Service. (available at http://www.attra.org/attra-pub/PDF/ arsenic-poultry-litter.pdf).

  • Bhowmick, S., Pramanik, S., Singh, P., Mondal, P., Chatterjee, D., & Nriagu, J. (2018). Arsenic in groundwater of West Bengal, India: A review of human health risks and assessment of possible intervention options. Science of the Total Environment, 612, 148–169.

    CAS  Google Scholar 

  • Bibi, I., Hussain, K., Amen, R., Hasan, I. M. U., Shahid, M., Bashir, S., & Ali, W. (2021). The potential of microbes and sulfate in reducing arsenic phytoaccumulation by maize (Zea mays L.) plants. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-021-00902-5

    Article  Google Scholar 

  • Bui, A. T., Nguyen, H. T., Nguyen, M. N., Tran, T. H. T., Vu, T. V., Nguyen, C. H., & Reynolds, H. L. (2016). Accumulation and potential health risks of cadmium, lead and arsenic in vegetables grown near mining sites in Northern Vietnam. Environmental Monitoring Assessment, 188(9), 525.

    Google Scholar 

  • Carlin, D. J., Naujokas, M. F., Bradham, K. D., Cowden, J., Heacock, M., Henry, H. F., & Waalkes, M. P. (2015). Arsenic and environmental health: State of the science and future research opportunities. Environmental Health Perspective, 124(7), 890–899.

    Google Scholar 

  • Chen, H., Teng, Y., Lu, S., Wang, Y., Wu, J., & Wang, J. (2016). Source apportionment and health risk assessment of trace metals in surface soils of Beijing metropolitan, China. Chemosphere, 144, 1002–1011.

    CAS  Google Scholar 

  • China MEP, M.M.o.E.P.o.t.P.s,R,o.C. (2014). The Ministry of Land Resources Report on the National Soil Contamination Survey, China.

  • Chung, C. J., Huang, C. J., Pu, Y. S., Su, C. T., Huang, Y. K., Chen, Y. T., & Hsueh, Y. M. (2008). Urinary 8-hydroxydeoxyguanosine and urothelial carcinoma risk in low arsenic exposure area. Toxicology & Applied Pharmacology, 226(1), 14–21.

    CAS  Google Scholar 

  • Ciminelli, V. S., Gasparon, M., Ng, J. C., Silva, G. C., & Caldeira, C. L. (2017). Dietary arsenic exposure in Brazil: The contribution of rice and beans. Chemosphere, 168, 996–1003.

    CAS  Google Scholar 

  • Clemens, S., & Ma, J. F. (2016). Toxic heavy metal and metalloid accumulation in crop plants and foods. Annual Review Plant Biology, 67, 489–512.

    CAS  Google Scholar 

  • Cortinas, I., Field, J. A., Kopplin, M., Garbarino, J. R., Gandolfi, A. J., & Sierra-Alvarez, R. (2006). Anaerobic biotransformation of roxarsone and related N-substituted phenylarsonic acids. Environmental Science & Technology, 40(9), 2951–2957.

    CAS  Google Scholar 

  • Cubadda, F., Jackson, B. P., Cottingham, K. L., Van Horne, Y. O., & Kurzius-Spencer, M. (2017). Human exposure to dietary inorganic arsenic and other arsenic species: State of knowledge, gaps and uncertainties. Science of the Total Environment, 579, 1228–1239.

    CAS  Google Scholar 

  • Cui, Y. J., Zhu, Y. G., Zhai, R. H., Chen, D. Y., Huang, Y. Z., Qiu, Y., & Liang, J. Z. (2004). Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China. Environment International, 30, 785–791.

    CAS  Google Scholar 

  • Dahlawi, S., Naeem, A., Iqbal, M., Farooq, M. A., Bibi, S., & Rengel, Z. (2018). Opportunities and challenges in the use of mineral nutrition for minimizing arsenic toxicity and accumulation in rice: A critical review. Chemosphere, 194, 171–188.

    Google Scholar 

  • Dai, Y., Lv, J., Liu, K., Zhao, X., & Cao, Y. (2016). Major controlling factors and prediction models for arsenic uptake from soil to wheat plants. Ecotoxicology & Environmental Safety, 130, 256–262.

    CAS  Google Scholar 

  • Datta, R., Sarkar, D., Sharma, S., & Sand, K. (2006). Arsenic biogeochemistry and human health risk assessment in organo-arsenical pesticide-applied acidic and alkaline soils: An incubation study. Science of the Total Environment, 372(1), 39–48.

    CAS  Google Scholar 

  • Davis, M. A., Signes-Pastor, A. J., Argos, M., Slaughter, F., Pendergrast, C., Punshon, T., Gossai, A., Ahsan, H., & Karagas, M. R. (2017). Assessment of human dietary exposure to arsenic through rice. Science of the Total Environment, 586, 1237–1244.

    CAS  Google Scholar 

  • Dixon, L. M., Sparks, N. H. C., & Rutherford, K. M. D. (2015). Early experiences matter: A review of the effects of prenatal environment on offspring characteristics in poultry. Poultry Science, 95(3), 489–499.

    Google Scholar 

  • Dradrach, A., Karczewska, A., & Szopka, K. (2020). Arsenic accumulation by red fescue (Festuca rubra) growing in mine affected soils-findings from the field and greenhouse studies. Chemosphere, 248, 126045.

    CAS  Google Scholar 

  • El-Kady, A. A., & Abdel-Wahhab, M. A. (2018). Occurrence of trace metals in foodstuffs and their health impact. Trends in Food Science & Technology, 75, 36–45.

    CAS  Google Scholar 

  • FAO/WHO Joint expert committee on food additives. Meeting, & World Health Organization. (2011). Evaluation of certain contaminants in food: seventy-second report of the Joint FAO/WHO Expert Committee on Food Additives (Vol. 72). World Health Organization.

  • Farooqi, A., Masuda, H., Siddiqui, R., & Naseem, M. (2009). Sources of arsenic and fluoride in highly contaminated soils causing groundwater contamination in Punjab, Pakistan. Archives of Environmental Contamination & Toxicology., 56, 693–706.

    CAS  Google Scholar 

  • Farooq, M. A., Islam, F., Ali, B., Najeeb, U., Mao, B., Gill, R. A., & Zhou, W. (2016). Arsenic toxicity in plants: Cellular and molecular mechanisms of its transport and metabolism. Environental & Experimental Botany, 132, 42–52.

    CAS  Google Scholar 

  • Fisher, D. J., Yonkos, L. T., & Staver, K. W. (2015). Environmental concerns of roxarsone in broiler poultry feed and litter in Maryland, USA. Environmental Science & Technology, 49, 1999–2012.

    CAS  Google Scholar 

  • Gao, S., Mostofa, M. G., Quamruzzaman, Q., Rahman, M., Rahman, M., Su, L., & Christiani, D. C. (2019). Gene-environment interaction and maternal arsenic methylation efficiency during pregnancy. Environment International, 125, 43–50.

    CAS  Google Scholar 

  • Garbarino, J. R., Bednar, A. J., Rutherford, D. W., Beyer, R. S., & Wershaw, R. L. (2003). Environmental fate of roxarsone in poultry litter. I. Degradation of roxarsone during composting. Environmental Science & Technology, 37, 1509–1514.

    CAS  Google Scholar 

  • Garcia, K. O., Teixeira, E. C., Agudelo-Castaneda, D. M., Braga, M., Alabarse, P. G., Wiegand, F., Kautzmann, R. M., & Silva, L. F. O. (2014). Assessment of nitro-polycyclic aromatic hydrocarbons in PM1 near an area of heavy-duty traffic. Science of the Total Environment, 479, 57–65.

    Google Scholar 

  • Geng, A., Wang, X., Wu, L., Wang, F., Chen, Y., Yang, H., & Zhao, X. (2017). Arsenic accumulation and speciation in rice grown in arsanilic acid-elevated paddy soil. Ecotoxicology & Environmental Safety, 137, 172–178.

    CAS  Google Scholar 

  • González-Martínez, F., Sánchez-Rodas, D., Cáceres, D. D., Martínez, M. F., Quiñones, L. A., & Johnson-Restrepo, B. (2018). Arsenic exposure, profiles of urinary arsenic species, and polymorphism effects of glutathione-s-transferase and metallothioneins. Chemosphere, 212, 927–936.

    Google Scholar 

  • Gupta, S. K., Le, X. C., Kachanosky, G., Zuidhof, M. J., & Siddique, T. (2018). Transfer of arsenic from poultry feed to poultry litter: A mass balance study. Science of the Total Environment, 630, 302–307.

    CAS  Google Scholar 

  • Haberecht, S., Bajagai, Y. S., Moore, R. J., Van, T. H., & Stanley, D. (2020). Poultry feeds carry diverse microbial communities that influence chicken intestinal microbiota colonisation and maturation. AMB Express, 10(1), 1–10.

    Google Scholar 

  • Hartley, W., Edwards, R., & Lepp, N. W. (2004). Arsenic and heavy metal mobility in iron oxide-amended contaminated soils as evaluated by short-and long-term leaching tests. Environmental Pollution, 131, 495–504.

    CAS  Google Scholar 

  • Hu, J., Wu, F., Wu, S., Sun, X., Lin, X., & Wong, M. H. (2013). Phytoavailability and phytovariety codetermine the bioaccumulation risk of heavy metal from soils, focusing on Cd-contaminated vegetable farms around the Pearl River Delta, China. Ecotoxicology & Environmental Safety, 91, 18–24.

    CAS  Google Scholar 

  • Hu, Y., Cheng, H., & Tao, S. (2017). Environmental and human health challenges of industrial livestock and poultry farming in China and their mitigation. Environment International, 107, 111–130.

    CAS  Google Scholar 

  • Huang, K., Chen, C., Shen, Q., Rosen, B. P., & Zhao, F. J. (2015). Genetically engineering Bacillus subtilis with a heat-resistant arsenitemethyltransferase for bioremediation of arsenic-contaminated organic waste. Applied Environmental Microbiology, 81(19), 6718–6724.

    CAS  Google Scholar 

  • Huang, K., Chen, C., Zhang, J., Tang, Z., Shen, Q., Rosen, B. P., & Zhao, F. J. (2016). Efficient arsenic methylation and volatilization mediated by a novel bacterium from an arsenic-contaminated paddy soil. Environmental Science & Technology, 50, 6389–6396.

    CAS  Google Scholar 

  • IARC (International Agency for Research on Cancer). (2004). Monographs on the evaluation of carcinogenic risk to human. Some Drinking Water Disinfectants and Contaminants, including Arsenic, Lyons, France, 84, 39–270.

    Google Scholar 

  • IARC (International Agency for Research on Cancer). (2012). Arsenic, metals, fibres and dust. IARC Monogrphs on the Evaluation of Carcinogenic Risks on Human, 100C, 1–501.

    Google Scholar 

  • Jackson, B. P., & Bertsch, P. M. (2001). Determination of arsenic speciation in poultry wastes by IC-ICP-MS. Environmental Science & Technology, 35, 4868–4873.

    CAS  Google Scholar 

  • Jackson, B. P., Bertsch, P. M., Cabrera, M. L., Camberato, J. J., Seaman, J. C., & Wood, C. W. (2003). Trace element speciation in poultry litter. Journal of Environmental Quality, 32, 535–540.

    CAS  Google Scholar 

  • Jiang, Y., Wen, H., Zhang, Q., Yuan, L., & Liu, L. (2021). Source apportionment and health risk assessment of potentially toxic elements in soil from mining areas in northwestern China. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-021-00907-0

    Article  Google Scholar 

  • JECFA (Joint FAO/WHO Expert Committee on Food Additives), (2011). Evaluation of certain contaminants in food. The seventy-second report, WHO, 1-115.

  • Kaise, T., Watanabe, S., & Itoh, K. (1985). The acute toxicity of arsenobetaine. Chemosphere, 14, 1327–1332.

    CAS  Google Scholar 

  • Kloke, A., Sauerbeck, D. R., Vetter, H. (1984). The contamination of plants and soils with heavy metals and the transport of metals in terrestrial food chains. In Changing metal cycles and human health (pp. 113–141). Springer, Berlin, Heidelberg.

  • Khalid, S., Shahid, M., Dumat, C., Niazi, N. K., Bibi, I., GulBakhat, H. F. S., & Javeed, H. M. R. (2017). Influence of groundwater and wastewater irrigation on lead accumulation in soil and vegetables: Implications for health risk assessment and phytoremediation. International Journal of Phytoremediation, 19, 1037–1046.

    CAS  Google Scholar 

  • Khan, A., Khan, S., Khan, M. A., Qamar, Z., & Waqas, M. (2015a). The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: A review. Environmental Science & Pollution Research, 22, 13772–13799.

    CAS  Google Scholar 

  • Khan, S., Cao, Q., Zheng, Y. M., Huang, Y. Z., & Zhu, Y. G. (2008). Health risks of heavy metals in contaminated soils and food-crops irrigated with wastewater in Beijing, China. Environmental Pollution, 152, 686–692.

    CAS  Google Scholar 

  • Khan, S., Rehman, S., Khan, A. Z., Khan, M. A., & Shah, M. T. (2010). Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, Northern Pakistan. Ecotoxicology & Environmental Safety, 73, 1820–1827.

    CAS  Google Scholar 

  • Khan, S., Reid, B. J., Li, G., & Zhu, Y. G. (2014). Application of biochar to soil reduces cancer risk via rice consumption: A case study in Miaoqian village, Longyan, China. Environment International, 68, 154–161.

    CAS  Google Scholar 

  • Khan, S., Waqas, M., Ding, F., Shamshad, I., Arp, H. P. H., & Li, G. (2015b). The influence of various biochars on the bioaccessibility and bioaccumulation of PAHs and potentially toxic elements to turnips (Brassica rapa L.). Journal of Hazardouse Material, 300, 243–253.

    CAS  Google Scholar 

  • Khan, M. A., Ding, X., Khan, S., Brusseau, M. L., Khan, A., & Nawab, J. (2018). The influence of various organic amendments on the bioavailability and plant uptake of cadmium present in mine-degraded soil. Science of the Total Environment, 636, 810–817.

    CAS  Google Scholar 

  • Knapp, C. W., Callan, A. C., Aitken, B., Shearn, R., Koenders, A., & Hinwood, A. (2017). Relationship between antibiotic resistance genes and metals in residential soil samples from Western Australia. Environmental Science & Pollution Research, 24, 2484–2494.

    CAS  Google Scholar 

  • Kołodyńska, D., Wnętrzak, R., Leahy, J. J., Hayes, M. H. B., Kwapiński, W., & Hubicki, Z. (2012). Kinetic and adsorptive characterization of biochar in metal ions removal. Chemical Engineering Journal, 197, 295–305.

    Google Scholar 

  • Li, G., Sun, G. X., Williams, P. N., Nunes, L., & Zhu, Y.-G. (2011). Inorganic arsenic in Chinese food and its cancer risk. Environment International, 37, 1219–1225.

    CAS  Google Scholar 

  • Li, N., Wang, J., & Song, W. Y. (2015). Arsenic uptake and translocation in plants. Plant Cell Physiology, 1, 4–13.

    Google Scholar 

  • Li, L., Hang, Z., Yang, W. T., Gu, J. F., & Liao, B. H. (2017). Arsenic in vegetables poses a health risk in the vicinity of a mining area in the southern Hunan Province, China. Human & Ecological Risk Assessment, an International Journal, 23, 1315–1329.

    CAS  Google Scholar 

  • Li, G., Khan, S., Ibrahim, M., Sun, T. R., Tang, J. F., Cotner, J. B., & Xu, Y. Y. (2018). Biochars induced modification of dissolved organic matter (DOM) in soil and its impact on mobility and bioaccumulation of arsenic and cadmium. Journal of Hazardouse Material, 348, 100–108.

    CAS  Google Scholar 

  • Liao, N., Seto, E., Eskenazi, B., Wang, M., Li, Y., & Hua, J. (2018). A comprehensive review of arsenic exposure and risk from rice and a risk assessment among a cohort of adolescents in Kunming, China. International Journal of Environmental Research and Public Health, 15(10), 2191.

    CAS  Google Scholar 

  • Liu, X. M., Song, Q. J., Tang, Y., Li, W. L., Xu, J. M., Wu, J. J., Wang, F., & Brookes, P. C. (2013). Human health risk assessment of heavy metals in soil-vegetable system: A multimedium analysis. Science of the Total Environment, 463, 530–540.

    Google Scholar 

  • Liu, Q., Peng, H., Lu, X., Zuidhof, M. J., Li, X.-F., & Le, X. C. (2016a). Arsenic species in chicken breast: Temporal variations of metabolites, elimination kinetics, and residual concentrations. Environmental Health Perspective, 124, 1174–1181.

    CAS  Google Scholar 

  • Liu, Q., Leslie, E. M., & Le, X. C. (2016b). Accumulation and transport of Roxarsone, Arsenobetaine, and inorganic arsenic using the human immortalized Caco-2 cell line. Journal of Agriculture & Food Chemistry, 64, 8902–8908.

    CAS  Google Scholar 

  • Llobet, J. M., Falco, G., Casas, C., Teixido, A., & Domingo, J. L. (2003). Concentrations of arsenic, cadmium, mercury, and lead in common foods and estimated daily intake by children, adolescents, adults, and seniors of Catalonia, Spain. Journal of Agriculture & Food Chemistry, 51, 838–842.

    CAS  Google Scholar 

  • Luo, L., Ma, Y., Zhang, S., Wei, D., & Zhu, Y. G. (2009). An inventory of trace element inputs to agricultural soils in China. Journal of Environmental Management., 90, 2524–2530.

    CAS  Google Scholar 

  • Ma, L., Wang, L., Jia, Y., & Yang, Z. (2017). Accumulation, translocation and conversion of six arsenic species in rice plants grown near a mine impacted city. Chemosphere, 183, 44–52.

    CAS  Google Scholar 

  • Marchiol, L., Assolari, S., Sacco, P., & Zerbi, G. (2004). Phytoextraction of heavy metals by canola (Brassica napus) and radish (Raphanussativus) grown on multi contaminated soil. Environmental Pollution, 132, 21–27.

    CAS  Google Scholar 

  • Martinello, K., Oliveira, M. L. S., Molossi, F. A., Ramos, C. G., Teixeira, E. C., Kautzmann, R. M., & Silva, L. F. O. (2014). Direct identification of hazardous elements in ultra-fine and nanominerals from coal fly ash produced during diesel co-firing. Science of the Total Environment, 470, 444–452.

    Google Scholar 

  • Marwa, E.M.M., Meharg, A.A., Andrew, A., & Clive, M. (2012). Risk assessment of potentially toxic elements in agricultural soils and maize tissues from selected districts in Tanzania. Science of the Total Environment 416, 180–186.

    CAS  Google Scholar 

  • Meharg, A. A. (2004). Arsenic in rice understanding a new disaster for South-East Asia. Trend in Plant Sciences, 9, 415–417.

    CAS  Google Scholar 

  • Moreno-Jiménez, E., Manzano, R., Esteban, E., & Peñalosa, J. (2010). The fate of arsenic in soils adjacent to an old mine site (Bustarviejo, Spain): Mobility and transfer to native flora. Journal of Soil & Sediment, 10, 301–312.

    Google Scholar 

  • Mudhoo, A., Sharma, S. K., Garg, V. K., & Tseng, C. H. (2011). Arsenic: An overview of applications, health, and environmental concerns and removal processes. Critical Reviews in Environmental Science & Technology, 41(5), 435–519.

    CAS  Google Scholar 

  • Muhammad, J., Khan, S., Lei, M., Khan, M. A., Nawab, J., Rashid, A., Ullah, S., & Khisro, S. B. (2020a). Application of poultry manure in agriculture fields leads to food plant contamination with potentially toxic elements and causes health risk. Environmental Technology & Innovation, 19, 100909.

    Google Scholar 

  • Muhammad, J., Khan, S., Su, J. Q., Hesham, A. E. L., Ditta, A., Nawab, J., & Ali, A. (2020b). Antibiotics in poultry manure and their associated health issues: A systematic review. Journal of Soils and Sediments, 20(1), 486–497.

    CAS  Google Scholar 

  • Nachman, K. E., Baron, P. A., Raber, G., Francesconi, K. A., Navas-Acien, A., & Love, D. C. (2013). Roxarsone, inorganic arsenic, and other arsenic species in chicken: A US-based market basket sample. Environmental Health Perspectives, 121, 818.

    Google Scholar 

  • Nguyen, M. H., Pham, T. D., Nguyen, T. L., Vu, H. A., Ta, T. T., Tu, M. B., & Chu, D. B. (2018). Speciation analysis of arsenic compounds by HPLC-ICP-MS: application for human serum and urine. Journal of Analytical Methods in Chemistry. https://doi.org/10.1155/2018/9462019

    Article  Google Scholar 

  • Pal, P. (2015). Groundwater arsenic remediation: Treatment technology and scale UP. Butterworth-Heinemann.

    Google Scholar 

  • Pandey, S., Rai, R., & Rai, L. C. (2015). Biochemical and molecular basis of arsenic toxicity and tolerance in microbes and plants. Handbook of arsenic toxicology (pp. 627–674). Elsevier.

    Google Scholar 

  • Pigna, M., Caporale, A. G., Cavalca, L., Sommella, A., & Violante, A. (2015). Arsenic in the soil environment: Mobility and phytoavailability. Environmental Engineering Science, 32(7), 551–563.

    CAS  Google Scholar 

  • Pizarro, I., Gómez, M., Cámara, C., & Palacios, M. A. (2003). Arsenic speciation in environmental and biological samples: Extraction and stability studies. Analytica Chimica Acta, 495, 85–98.

    CAS  Google Scholar 

  • Rahman, M. M., Owens, G., & Naidu, R. (2009). Arsenic levels in rice grain and assessment of daily dietary intake of arsenic from rice in arsenic-contaminated regions of Bangladesh—implications to groundwater irrigation. Environmental Geochemistry & Health, 31, 179–187.

    CAS  Google Scholar 

  • Rahman, M. A., Rahman, A., Khan, M. Z. K., & Renzaho, A. M. (2018). Human health risks and socio-economic perspectives of arsenic exposure in Bangladesh: A scoping review. Ecotoxicology & Environmental Safety, 150, 335–343.

    CAS  Google Scholar 

  • Rasheed, H., Slack, R., & Kay, P. (2016). Human health risk assessment for arsenic: A critical review. Critical Reviews in Environmental Science & Technology, 46, 1529–1583.

    CAS  Google Scholar 

  • Rasheed, H., Kay, P., Slack, R., & Gong, Y. Y. (2018). Arsenic species in wheat, raw and cooked rice: Exposure and associated health implications. Science of the Total Environment, 634, 366–373.

    CAS  Google Scholar 

  • Rashid, A., Khan, S., Ayub, M., Sardar, T., Jehan, S., Zahir, S., Khan, M. S., Muhammad, J., Khan, R., Ali, A., & Ullah, H. (2019). Mapping human health risk from exposure to potential toxic metal contamination in groundwater of Lower Dir, Pakistan: Application of multivariate and geographical information system. Chemosphere, 225, 785–795.

    CAS  Google Scholar 

  • Rehman, Z. U., Khan, S., Qin, K., Brusseau, M. L., Shah, M. T., & Din, I. (2016). Quantification of inorganic arsenic exposure and cancer risk via consumption of vegetables in southern selected districts of Pakistan. Science of the Total Environment, 550, 321–329.

    CAS  Google Scholar 

  • Rehman, Z. U., Sardar, K. H. A. N., Shah, M. T., Brusseau, M. L., Khan, S. A., & Mainhagu, J. (2018). Transfer of heavy metals from soils to vegetables and associated human health risks at selected sites in Pakistan. Pedosphere, 28, 666–679.

    Google Scholar 

  • Rocco, C., Seshadri, B., Adamo, P., Bolan, N. S., Mbene, K., & Naidu, R. (2018). Impact of waste-derived organic and inorganic amendments on the mobility and bioavailability of arsenic and cadmium in alkaline and acid soils. Environmental Science & Pollution Research, 25, 25896–25905.

    CAS  Google Scholar 

  • Rutherford, D. W., Bednar, A. J., Garbarino, J. R., Needham, R., Staver, K. W., & Wershaw, Rl. (2003). Environmental fate of roxarsone in poultry litter. Part II. Mobility of arsenic in soils amended with poultry litter. Environmental Science & Technology, 37(8), 1515–1520.

    CAS  Google Scholar 

  • Saritha, P. (2011). Degradation of some USEPA listed recalcitrant compounds using Advanced Oxidation Processes (AOPS).

  • Sarwar, T., Khan, S., Yu, X., Amin, S., Khan, M. A., Sarwar, A., & Nazneen, S. (2021). Analysis of Arsenic concentration and its speciation in rice of different markets of Pakistan and its associated health risk. Environmental Technology & Innovation, 21, 101252.

    CAS  Google Scholar 

  • Sawut, R., Kasim, N., Maihemuti, B., Hu, L., Abliz, A., Abdujappar, A., & Kurban, M. (2018). Pollution characteristics and health risk assessment of heavy metals in the vegetable bases of northwest China. Science of the Total Environment, 642, 864–878.

    CAS  Google Scholar 

  • SEPA. (1995). Environmental quality standards for soils. State environmental protection administration; China.GB15618–1995

  • Shah, A. H., Shahid, M., Khalid, S., Shabbir, Z., Bakhat, H. F., Murtaza, B., & Niazi, N. K. (2020). Assessment of arsenic exposure by drinking well water and associated carcinogenic risk in peri-urban areas of Vehari, Pakistan. Environmental Geochemistry and Health, 42(1), 121–133.

    CAS  Google Scholar 

  • Shahid, M., Khalid, S., & Saleem, M. (2021). Unrevealing arsenic and lead toxicity and antioxidant response in spinach: A human health perspective. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-021-00818-0

    Article  Google Scholar 

  • Sharifi, R., Moore, F., Keshavarzi, B., & Badiei, S. (2017). Assessment of health risks of arsenic exposure via consumption of crops. Exposure Health, 10, 129–143.

    Google Scholar 

  • Steffan, J. J., Brevik, E. C., Burgess, L. C., & Cerdà, A. (2018). The effect of soil on human health: An overview. European Journal of Soil Science, 69, 159–171.

    CAS  Google Scholar 

  • Su, Y. H., McGrath, S. P., & Zhao, F. J. (2010). Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant and Soil, 328, 27–34.

    CAS  Google Scholar 

  • Sun, H. J., Rathinasabapathi, B., Wu, B., Luo, J., Pu, L. P., & Ma, L. Q. (2014). Arsenic and selenium toxicity and their interactive effects in humans. Environment International, 69, 148–158.

    CAS  Google Scholar 

  • Taylor, V., Goodale, B., Raab, A., Schwerdtle, T., Reimer, K., Conklin, S., & Francesconi, K. A. (2017). Human exposure to organic arsenic species from seafood. Science of the Total Environment, 580, 266–282.

    CAS  Google Scholar 

  • Torre, L. A., Bray, F., Siegel, R. L., Ferlay, J., Lortet-Tieulent, J., & Jemal, A. (2015). Global cancer statistics. CA: A Cancer Journal for Clinicians, 65, 87–108.

    Google Scholar 

  • Uddh-Söderberg, T. E., Gunnarsson, S. J., Hogmalm, K. J., Lindegard, M. B. G., & Augustsson, A. L. (2015). An assessment of health risks associated with arsenic exposure via consumption of homegrown vegetables near contaminated glassworks sites. Science of the Total Environment, 536, 189–197.

    Google Scholar 

  • USEPA. (2005).Human health risk assessment protocol for hazardous waste combustion facilities. USEPA, Integrated risk information system (IRIS), 2012. Available at: http://www.epa.gov/IRIS/

  • USEPA. Exposure Factors Handbook. (2011). Edition (Final) US Environmental Protection Agency; Washington, DC: 2011. EPA/600/R09/052F. Available at: http://cfpub.epa.gov/ncea/risk/recordisplay.cfm?deid=236252#Download

  • Wang, N., Zhang, S., & He, M. (2018). Bacterial community profile of contaminated soils in a typical antimony mining site. Environmental Science & Pollution Research, 25(1), 141–152.

    CAS  Google Scholar 

  • Wang, G., Kennedy, S. P., Fasiludeen, S., Rensing, C., DasSarma, S. (2004). Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. Journal of Bacteriology, 186(10), 3187–3194.

    CAS  Google Scholar 

  • Wang, Y., Xu, W., Li, J., Song, Y., Hua, M., Li, W., & He, X. (2021). Assessing the fractionation and bioavailability of heavy metals in soil–rice system and the associated health risk. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-021-00876-4

    Article  Google Scholar 

  • Waqas, M., Khan, S., Chao, C., Shamshad, I., Qamar, Z., & Khan, K. (2014). Quantification of PAHs and health risk via ingestion of vegetable in Khyber Pakhtunkhwa Province, Pakistan. Science of the Total Environment, 497, 448–458.

    Google Scholar 

  • Waqas, M., Li, G., Khan, S., Shamshad, I., Reid, B. J., Qamar, Z., & Chao, C. (2015). Application of sewage sludge and sewage sludge biochar to reduce polycyclic aromatic hydrocarbons (PAH) and potentially toxic elements (PTE) accumulation in tomato. Environmental Science & Pollution Research, 22, 7071–7081.

    Google Scholar 

  • WHO (World Health Organization) Joint FAO (Food and Agriculture Organization)/WHO (2012). Food standards programme codex committee on contaminants in foods sixth session Maastricht, 2012. The Netherlands, pp. 26–30 March 2012 Proposed Draft Maximum Levels for Arsenic in Rice.

  • Williams, P. N., Villada, A., Deacon, C., Raab, A., Figuerola, J., Green, A. J., & Meharg, A. A. (2007). Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environmental Science & Technology, 41, 6854–6859.

    CAS  Google Scholar 

  • Xiao, X. Y., Chen, T. B., Liao, X. Y., Yan, X. L., Xie, H., Wu, B., & Wang, L. X. (2009). Comparison of concentrations and bio concentration factors of arsenic in vegetables, grain and oil crops in China. Acta Scientiae Circumstantiae, 29, 291–296.

    CAS  Google Scholar 

  • Yañez, L. M., Alfaro, J. A., & Mitre, G. B. (2018). Absorption of arsenic from soil and water by two chard (Beta vulgaris L.) varieties: A potential risk to human health. Journal of Environmental Management, 218, 23–30.

    Google Scholar 

  • Yang, X., Li, Q., Tang, Z., Zhang, W., Yu, G., Shen, Q., & Zhao, F. J. (2017). Heavy metal concentrations and arsenic speciation in animal manure composts in China. Waste Management, 64, 333–339.

    CAS  Google Scholar 

  • Zabin, S. A., Foaad, M. A., & Al-Ghamdi, A. Y. (2008). Non-carcinogenic risk assessment of heavy metals and fluoride in some water wells in the Al-Baha Region, Saudi Arabia. Human & Ecological Risk Assessment, 14, 1306–1317.

    CAS  Google Scholar 

  • Zeng, F., Wei, W., Li, M., Huang, R., Yang, F., & Duan, Y. (2015). Heavy metal contamination in rice-producing soils of Hunan province, China and potential health risks. International Journal of Environmental Research Public Health, 12, 15584–15593.

    CAS  Google Scholar 

  • Zhang, S. Y., Williams, P. N., Luo, J., & Zhu, Y. G. (2017). Microbial mediated arsenic biotransformation in wetlands. Frontiers in Environmental Science & Engineering., 11, 1.

    Google Scholar 

  • Zhang, S., Song, J., Cheng, Y., Liu, G., & Wallace, A. R. (2018). Trace metal (loid)s exposure through soil–tobacco–human pathway: Availability in metal-contaminated agricultural soils, transfer models and health risk assessment. Ecotoxicology & Environmental Safety, 148, 1034–1041.

    CAS  Google Scholar 

  • Zhao, F. J., Zhu, Y. G., & Meharg, A. A. (2013). Methylated arsenic species in rice: Geographical variation, origin and uptake mechanisms. Environmental Science & Technology, 47, 3957–3966.

    CAS  Google Scholar 

  • Zhou, H., Yang, W. T., Zhou, X., Liu, L., Gu, J. F., Wang, W. L., & Liao, B. H. (2016). Accumulation of heavy metals in vegetable species planted in contaminated soils and the health risk assessment. International Journal of Environmental Research & Public Health, 13, 289.

    Google Scholar 

  • Zhu, Y. G., Williams, P. N., & Meharg, A. A. (2008). Exposure to inorganic arsenic from rice: A global health issue. Environmental Pollution, 154, 169–171.

    CAS  Google Scholar 

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Funding

This study was supported by Planning and Development Department, Government of Khyber Pakhtunkhwa, Pakistan under program of Piloting Innovative Ideas (PII) to Address Key Issues of Khyber Pakhtunkhwa.

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Authors and Affiliations

  1. Department of Environmental Sciences, University of Peshawar, Peshawar, 25120, Pakistan

    Juma Muhammad, Sardar Khan, Tasneem Sarwar & Shahla Nazneen

  2. Department of Environmental Sciences, Shaheed Benazir Bhutto University, Sheringal, Dir Upper, Pakistan

    Juma Muhammad

  3. Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China

    Juma Muhammad & Jian Qiang Su

  4. China National Rice Research Institute, Hangzhou, 310006, China

    Ping Xu

  5. Department of Forestry, Shaheed Benazir Bhutto University, Sheringal, Dir Upper, Pakistan

    Alamgir Khan

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  1. Juma Muhammad
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  2. Ping Xu
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  3. Sardar Khan
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  4. Jian Qiang Su
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  5. Tasneem Sarwar
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  6. Shahla Nazneen
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  7. Alamgir Khan
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Contributions

JM: Investigation, writing-original draft. PX: Software, data curation. SK: Funding acquisition, supervision, project administration, conceptualization, methodology. JQS: Visualization, writing-review and editing. TS: data curation. SN: writing-review and editing. AK: Software, data curation.

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Correspondence to Sardar Khan.

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Muhammad, J., Xu, P., Khan, S. et al. Arsenic contribution of poultry manure towards soils and food plants contamination and associated cancer risk in Khyber Pakhtunkhwa, Pakistan. Environ Geochem Health 44, 3321–3342 (2022). https://doi.org/10.1007/s10653-021-01096-6

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