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

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

  1. 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.

    Article  CAS  Google Scholar 

  2. 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 

  3. 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.

    Article  CAS  Google Scholar 

  4. 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.

    Article  CAS  Google Scholar 

  5. 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.

    Article  CAS  Google Scholar 

  6. 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.

    Article  CAS  Google Scholar 

  7. 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.

    Article  Google Scholar 

  8. 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.

    Article  CAS  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. 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.

    Article  CAS  Google Scholar 

  11. 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).

  12. 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.

    Article  CAS  Google Scholar 

  13. 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 

  14. 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.

    Article  CAS  Google Scholar 

  15. 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.

    Article  CAS  Google Scholar 

  16. 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.

    Article  CAS  Google Scholar 

  17. 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.

  18. 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.

    Article  CAS  Google Scholar 

  19. 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.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. 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.

    Article  CAS  Google Scholar 

  22. 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.

    Article  CAS  Google Scholar 

  23. 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.

    Article  CAS  Google Scholar 

  24. 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.

    Article  CAS  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. 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.

    Article  CAS  Google Scholar 

  27. 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.

    Article  CAS  Google Scholar 

  28. 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.

    Article  Google Scholar 

  29. 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.

    Article  CAS  Google Scholar 

  30. 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.

    Article  CAS  Google Scholar 

  31. 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.

  32. 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.

    Article  CAS  Google Scholar 

  33. 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.

    Article  CAS  Google Scholar 

  34. 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.

    Article  CAS  Google Scholar 

  35. 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.

    Article  CAS  Google Scholar 

  36. 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.

    Article  CAS  Google Scholar 

  37. 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.

    Article  CAS  Google Scholar 

  38. 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.

    Article  CAS  Google Scholar 

  39. 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.

    Article  CAS  Google Scholar 

  40. 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.

    Article  CAS  Google Scholar 

  41. 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.

    Article  CAS  Google Scholar 

  42. 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.

    Article  CAS  Google Scholar 

  43. 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.

    Article  CAS  Google Scholar 

  44. 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.

    Article  CAS  Google Scholar 

  45. 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.

    Article  CAS  Google Scholar 

  46. 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.

    Article  CAS  Google Scholar 

  47. 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 

  48. 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 

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

    Article  CAS  Google Scholar 

  50. 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.

    Article  CAS  Google Scholar 

  51. 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 

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

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

    Article  CAS  Google Scholar 

  54. 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.

  55. 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.

    Article  CAS  Google Scholar 

  56. 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.

    Article  CAS  Google Scholar 

  57. 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.

    Article  CAS  Google Scholar 

  58. 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.

    Article  CAS  Google Scholar 

  59. 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.

    Article  CAS  Google Scholar 

  60. 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.

    Article  CAS  Google Scholar 

  61. 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.

    Article  CAS  Google Scholar 

  62. 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.

    Article  CAS  Google Scholar 

  63. 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.

    Article  CAS  Google Scholar 

  64. 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.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  66. 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.

    Article  CAS  Google Scholar 

  67. 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.

    Article  CAS  Google Scholar 

  68. 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.

    Article  CAS  Google Scholar 

  69. 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.

    Article  CAS  Google Scholar 

  70. 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.

    Article  CAS  Google Scholar 

  71. 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.

    Article  CAS  Google Scholar 

  72. 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.

    Article  CAS  Google Scholar 

  73. 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.

    Article  CAS  Google Scholar 

  74. 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.

    Article  CAS  Google Scholar 

  75. 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.

    Article  CAS  Google Scholar 

  76. 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.

    Article  CAS  Google Scholar 

  77. 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.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  79. 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.

    Article  CAS  Google Scholar 

  80. 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.

    Article  CAS  Google Scholar 

  81. 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.

    Article  Google Scholar 

  82. 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.

    Article  CAS  Google Scholar 

  83. 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.

    Article  CAS  Google Scholar 

  84. 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 

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

    Google Scholar 

  86. 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.

    Chapter  Google Scholar 

  87. 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.

    Article  CAS  Google Scholar 

  88. 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.

    Article  CAS  Google Scholar 

  89. 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.

    Article  CAS  Google Scholar 

  90. 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.

    Article  CAS  Google Scholar 

  91. 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.

    Article  CAS  Google Scholar 

  92. 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.

    Article  CAS  Google Scholar 

  93. 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.

    Article  CAS  Google Scholar 

  94. 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.

    Article  CAS  Google Scholar 

  95. 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.

    Article  Google Scholar 

  96. 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.

    Article  CAS  Google Scholar 

  97. 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.

    Article  CAS  Google Scholar 

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

  99. 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.

    Article  CAS  Google Scholar 

  100. 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.

    Article  CAS  Google Scholar 

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

  102. 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.

    Article  CAS  Google Scholar 

  103. 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 

  104. 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.

    Article  CAS  Google Scholar 

  105. 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.

    Article  CAS  Google Scholar 

  106. 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.

    Article  CAS  Google Scholar 

  107. 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.

    Article  CAS  Google Scholar 

  108. 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.

    Article  CAS  Google Scholar 

  109. 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 

  110. 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.

    Article  CAS  Google Scholar 

  111. 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/

  112. 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

  113. 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.

    Article  CAS  Google Scholar 

  114. 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.

    Article  CAS  Google Scholar 

  115. 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 

  116. 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.

    Article  CAS  Google Scholar 

  117. 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.

    Article  CAS  Google Scholar 

  118. 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.

  119. 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.

    Article  CAS  Google Scholar 

  120. 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 

  121. 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.

    Article  CAS  Google Scholar 

  122. 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.

    Article  CAS  Google Scholar 

  123. 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.

    Article  CAS  Google Scholar 

  124. 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.

    Article  CAS  Google Scholar 

  125. 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.

    Article  CAS  Google Scholar 

  126. 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.

    Article  CAS  Google Scholar 

  127. 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.

    Article  CAS  Google Scholar 

  128. 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.

    Article  CAS  Google Scholar 

  129. 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.

    Article  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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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 (2021). https://doi.org/10.1007/s10653-021-01096-6

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Keywords

  • Poultry manure
  • Arsenic
  • Agricultural soils
  • Food plants
  • Health risk assessment