Probabilistic health risk assessment of heavy metals in honey, Manihot esculenta, and Vernonia amygdalina consumed in Enugu State, Nigeria

  • Orish Ebere OrisakweEmail author
  • Harrison Anezi Ozoani
  • Ify Lawerence Nwaogazie
  • Anthonet Ndidi Ezejiofor


Honey is a nutritive fluid product of bees with an array of pharmacological/medicinal effects. As a natural product from honeybees, honey is regarded to be safe and free from any contaminants. Cassava tuber (Manihot esculenta)–based meal, Vernonia amygdalina (bitter leaf soup), and honey are common local cuisine in Nigeria. This is a human health risk assessment of heavy metals associated with the consumption of honey (Apis mellifera scutellata), cassava (Manihot esculenta), and bitter leaf (Vernonia amygdalina) in Enugu State, Nigeria. Concentrations of lead (Pb), Cd, As, Cu, Ni, Mn, Fe, Cr, and Fe in honey, soil, Manihot esculenta, and Vernonia amygdalina were determined using an atomic absorption spectrophotometer (AAS). The principal component analysis (PCA) was performed as a factor reduction technique among 12 factors (3 locations against 4 sources of heavy metals). The mean concentration of metals in honey, soil, Manihot esculenta, and Vernonia amygdalina ranged from 0.001 to 4.28 mg kg−1, from 0.0026 to 170.52 mg kg−1, from 0.012 to 80.63 mg kg−1, and from 0.0016 to 126.48 mg kg−1, respectively. Pb showed the highest carcinogenic risk with values of 3.18E−04–1.43E−01 in Vernonia amygdalina and 1.69E−04–3.47E−04 in Manihot esculenta for adults and children, respectively. In honey, Cd showed the highest carcinogenic risk with values of 1.26E−02–1.07E−01. About 51.5% of total cancer risk (TCR) was below 1E−04. Consumption of honey, Vernonia amygdalina, and Manihot esculenta in some urban parts of Enugu may pose some adverse health effects.


Heavy metal risk assessment Honey Manihot esculenta Vernonia amygdalina Public health Nigeria 



  1. Abboud, P., & Wilkinson, K. J. (2013). Role of metal mixtures (Ca, Cu and Pb) on Cd bioaccumulation and phytochelatin production by Chlamydomonas reinhardtii. Environmental Pollution, 179, 33–38.Google Scholar
  2. Adedokun, O. M., Kyalo, M., Gnonlonfin, B., Wainaina, J., Githae, D., Skilton, R., & Harvey, J. (2016). Mushroom: molecular characterization of indigenous species in the Niger Delta Region of Nigeria. European Journal of Horticultural Science, 81(5), 273–280.Google Scholar
  3. Adelekan, B. A. (2010). Investigation of ethanol productivity of cassava crop as a sustainable source of biofuel in tropical countries. African Journal of Biotechnology, 9, 5643–5650.Google Scholar
  4. Altun, S. K., Dinç, H., Paksoy, N., TemamoLullar, F. K., & Savrunlu, M. (2017). Analyses of mineral content and heavy metal of honey samples from south and east region of Turkey by using ICP-MS. International Journal of Analytical Chemistry, 2017, 1–6. Scholar
  5. Amadi, C. N., Igweze, Z. N., & Orisakwe, O. E. (2017). Heavy metals in miscarriages and stillbirths in developing nations. Middle East Fertility Society Journal, 22(2), 91–100.Google Scholar
  6. Bamuwamye, M., Ogwok, P., & Tumuhairwe, V. (2015). Cancer and non-cancer risks associated with heavy metal exposures from street foods: evaluation of roasted meats in an urban setting. Journal of Environment Pollution and Human Health, 3(2), 24–30.Google Scholar
  7. Bellinger, D. C., Stiles, K. M., & Needleman, H. L. (1992). Low-level lead exposure, intelligence and academic achievement: a long-term follow-up study. Pediatrics, 90(6), 855–861.Google Scholar
  8. Calderon, J., Ortiz-Perez, D., Yanez, L., & Díaz-Barriga, F. (2003). Human exposure to metals. Pathways of exposure, biomarkers of effect, and host factors. Ecotoxicology and Environmental Safety, 56, 93–103.Google Scholar
  9. Cao, H., Qiao, L., Zhang, H., & Chen, J. (2010). Exposure and risk assessment for aluminum and heavy metals in Puerh tea. Science of the Total Environment, 408, 2777–2784.Google Scholar
  10. Costanza, R., d’Arge, R., De Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O’Neill, R. V., Paruelo, J., & Raskin, R. G. (1997). The value of the world’s ecosystem services and natural capital. Nature, 387(6630), 253–260.Google Scholar
  11. EFSA. (2008). Scientific opinion of the panel on contaminants in the food chain on a request from the European Commission on polycyclic aromatic hydrocarbons in food. EFSA Journal, 724, 1–114.Google Scholar
  12. FAO/WHO. (2011). Evaluation of certain contaminants in food: seventy-second report of the joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series No. 959. Geneva: World Health Organization.Google Scholar
  13. Gallmann, P., Stefan, B., Tomislav, J., & Robert, S. (2009). Honey for nutrition and health: a review. Journal of the American College of Nutrition, 27, 677–689. Scholar
  14. Hague, T., Petroczi, A., Andrews, P. L., Barker, J., & Naughton, D. P. (2008). Determination of metal ion content of beverages and estimation of target hazard quotients: a comparative study. Chemistry Central Journal, 2(1), 13.Google Scholar
  15. Hernández, O. M., Fraga, J. M. G., Jiménez, A. I., Jimenez, F., & Arias, J. J. (2005). Characterization of honey from the Canary Islands: determination of the mineral content by atomic absorption spectrophotometry. Food Chemistry, 93(3), 449–458.Google Scholar
  16. Hu, X., Zhang, Y., Ding, Z. H., Wang, T. J., Lian, H. Z., & Sun, Y. Y. (2012). Bio accessibility and health risk of arsenic and heavy metals (Cd, Co, Cr, Cu, Ni, Pb, Zn and Mn) in TSP and PM2. Atmospheric Environment (Vol. 57, pp. 146–152).Google Scholar
  17. Igbiri, S., Udowelle, N. A., Ekhator, O. C., Asomugha, R. N., Igweze, Z. N., & Orisakwe, O. E. (2017). Polycyclic aromatic hydrocarbons in edible mushrooms from Niger Delta, Nigeria: carcinogenic and non-carcinogenic health risk assessment. Asian Pacific Journal of Cancer Prevention, 18(2), 437.Google Scholar
  18. Ioannidou, M. D., Zachariadis, G. A., Anthemidis, A. N., & Stratis, J. A. (2005). Direct determination of toxic trace metals in honey and sugars using inductively coupled plasma atomic emission spectrometry. Talanta, 65, 92–97.Google Scholar
  19. Iwegbue, C. M., Obi-Iyeke, G. E., Tesi, G. O., Obi, G., & Bassey, F. I. (2015). Concentrations of selected metals in honey consumed in Nigeria. International Journal of Environmental Studies, 72(4), 713–722.Google Scholar
  20. Jarup, L., (2003). Hazards of heavy metal contamination. Br. Med. Bull. 68, 167–182.\Google Scholar
  21. Jolly, Y. N., Islam, A., & Akbar, S. (2013). Transfer of metals from soil to vegetables and possible health risk assessment. SpringerPlus, 2(1), 385.Google Scholar
  22. Kalia, K., & Flora, S. J. (2005). Strategies for safe and effective therapeutic measures for chronic arsenic and lead poisoning. Journal of Occupational Health, 47, 1–21.Google Scholar
  23. Komosinska-Vassev, K., Olczyk, P., Kaźmierczak, J., Mencner, L., & Olczyk, K. (2015). Bee pollen: chemical composition and therapeutic application. Evidence-Based Complementary and Alternative Medicine, 1–7.Google Scholar
  24. Leblebici, Z. E. L. I. H. A., & Aksoy, A. H. M. E. T. (2008). Determination of heavy metals in honey samples from Central Anatolia using plasma optical emission spectrofotometry (ICP-OES). Polish Journal of Environmental Studies, 17(4), 549–555.Google Scholar
  25. Li, Z., Zhuanga, P., McBride, M. B., Xiaa, H., & Lia, N. (2009). Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. Science of the Total Environment, 407(5), 1551–1561.Google Scholar
  26. 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 Agricultural and Food Chemistry, 51(3), 838–842.Google Scholar
  27. NEPAC. (2005). Maximum levels of contaminants in food. Beijing, China: National Environmental Protection Agency of China.Google Scholar
  28. Nwaogazie, I. L. (2011). Probability and statistics for science and engineering practice (pp. 125–126). Enugu: De-Adroit Innovation.Google Scholar
  29. Oluwole, S. O., Makinde, O. S. C., Yusuf, K. A., Fajana, O. O., & Odumosu, A. O. (2013). Determination of heavy metal contaminants in leafy vegetables cultivated by the road side. International Journal of Engineering Research and Development, 7(3), 1–5.Google Scholar
  30. Orisakwe, O. E., Nduka, J. K., Amadi, C. N., Dike, D. O., & Bede, O. (2012). Heavy metals health risk assessment for population via consumption of food crops and fruits in Owerri, South Eastern, Nigeria. Chemistry Central Journal, 6, 77.Google Scholar
  31. Orisakwe, O. E., Blum, J. L., Sujak, S., & Zelikoff, J. T. (2014). Metal pollution in Nigeria: a biomonitoring update. Journal of Health Pollution, 4(6), 40–52.Google Scholar
  32. Orisakwe, O. E., Igweze, Z. N., & Udowelle, N. A. (2019). Candy consumption may add to the body burden of lead and cadmium of children in Nigeria. Environmental Science and Pollution Research, 26(2), 1921–1931.Google Scholar
  33. Osu, S. R., Solomon, M. M., Abai, E. J., & Etim, I. G. (2015). Human health risk assessment of heavy metals Intake via cassava consumption from crude oil impacted soils with and without palm bunch ash additive. International Journal of Technical Research and Applications, 3(4), 140–148.Google Scholar
  34. Ozoani, H. A.. (2018). Human health risk assessment of heavy metal and polycyclic aromatic hydrocarbons (PAHs) in honey, cassava and bitter leaf from Enugu State, Nigeria. MSc thesis. Faculty of Pharmacy, University of Port Harcourt. NigeriaGoogle Scholar
  35. Rehman, K., Fatima, F., Waheed, I., & Akash, M. S. H. (2018). Prevalence of exposure of heavy metals and their impact on health consequences. Journal of Cellular Biochemistry, 119(1), 157–184.Google Scholar
  36. Silici, S., Uluozlu, O. D., Tuzen, M., & Soylak, M. (2008). Assessment of trace element levels in Rhododendron honeys of Black Sea Region, Turkey. Journal of Hazardous Materials, 156(1–3), 612–618.Google Scholar
  37. Singh, A., Sharma, R. K., Agrawal, M., & Marshall, F. M. (2010). Risk assessment of heavy metal toxicity through contaminated vegetables from waste water irrigated area of Varanasi, India. Tropical Ecology, 51(2), 375–387.Google Scholar
  38. Sitarz-Palczak, E., Kalembkiewicz, J., & Galas, D. (2015). Evaluation of the content of selected heavy metals in samples of Polish honeys. Journal of Ecological Engineering, 16(3), 130–138.Google Scholar
  39. Steenland, K., Boffetta, P. (2000). Lead and cancer in humans: where are we now? Am. J. Ind. Med. 38, 295–299Google Scholar
  40. Underwood, E. J. (1977). Trace elements in human and animal nutrition (4th ed.). New York: Academic.Google Scholar
  41. US EPA (1989) (United States Environmental Protection Agency)Risk assessment guidance for superfund. Human Health Evaluation Manual (Part A). Interim Final, vol. I, United States Environmental Protection Agency, Washington (DC) EPA/540/1-89/002Google Scholar
  42. USEPA (2000) Supplementary guidance for conducting health risk assessment of chemical mixtures. Risk Assessment Forum Technical Panel [EPA/630/R-00/002].Google Scholar
  43. USEPA. (2005). The limits of pollutants in food. China: State Environmental Protection Administration.Google Scholar
  44. WHO (1991) International Programme on Chemical Safety. Environmental Health Criteria, Vol. 108, Geneva, p. 286.Google Scholar
  45. WHO (1992). Cadmium. Environmental Health Criteria, Geneva. Vol. 134.Google Scholar
  46. Xia, Z. H., Duan, X. L., Qiu, W. X., Liu, D., Wang, B., Tao, S., Jiang, Q. J., Lu, B., Song, Y. X., & Hu, X. X. (2010). Health risk assessment on dietary exposure to polycyclic aromatic hydrocarbons (PAHs) in Taiyuan, China. Science of the Total Environment, 408, 5331–5337.Google Scholar
  47. Zhan, X., Liang, X., Jiang, T., & Xu, G. (2013). Interaction of phenanthrene and potassium uptake by wheat roots: a mechanistic model. BMC Plant Biology, 13(1), 1–9.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Experimental Pharmacology & Toxicology, Faculty of PharmacyUniversity of Port HarcourtPort HarcourtNigeria
  2. 2.Department of Civil & Environmental Engineering, Faculty of EngineeringUniversity of Port HarcourtPort HarcourtNigeria

Personalised recommendations