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Contamination level, distribution and health risk assessment of heavy and toxic metallic and metalloid elements in a cultivated mushroom Pleurotus florida (Mont.) singer

Abstract

There are great concentrations of toxic metallic and metalloid elements such as lead, arsenic, mercury, cadmium or silver in many species of mushrooms comparative to other fruits and vegetables. In this study, contamination with heavy and toxic metallic and metalloid elements in the cultivated mushroom of (Pleurotus florida (Mont.) Singer) is investigated. P. florida was cultivated on different substrates; wheat straw (as blank), wheat straw + pine cone, wheat straw + soybean straw and wheat straw + urea and the effects of these substrates on contamination levels of Mn, Fe, Cu, Zn, As, Cd, and Pb were analyzed. The results showed that the concentrations of essential elements (Mn, Fe, Cu, and Zn) in the target mushroom are at the typical levels. The estimated daily intakes of studied metallic and metalloid elements were below their oral reference dosage mentioned by the international regulatory bodies. Health risk index (HRI) was calculated to evaluate the consumer’s health risk assessment from the metal intake that contaminated in the cultivated mushroom of P. florida on the different nutrient sources. In this study, the individual HRIs were less than 1, which indicates insignificant potential health risk associated with the consumption of target mushroom from the studied substrates. Based on the HRIs values among the toxic metallic and metalloid elements, As in the target mushroom in the substrate of the wheat straw + pine cone is the main sources of risk, and it may cause severe health problems. Thus, this study suggests that the concentrations of heavy and toxic elements should be periodically monitored in cultivated mushrooms.

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References

  1. Adebayo GJ, Omolara BN, Toyin AE (2009) Evaluation of yield of oyster mushroom (Pleurotus pulmonarius) grown on cotton waste and cassava peel. Afr J Biotechnol 8:215–218

    CAS  Google Scholar 

  2. Agrahar-Murugkar D, Subbulakshmi G (2005) Nutritional value of edible mushrooms collected from the Khasi hills of Meghalaya. Food Chem 89:599–603. doi:10.1016/S0308-8146(04)00257-2

    CAS  Article  Google Scholar 

  3. Alam N, Amin R, Khan A, Ara I, Shim MJ, Lee MW, Lee TS (2008) Nutritional analysis of cultivated mushrooms in Bangladesh - Pleurotus ostreatus, Pleurotus sajor-caju, Pleurotus florida and Calocybe indica. Mycobiology 36:228–232. doi:10.4489/MYCO.2008.36.4.228

    CAS  Article  Google Scholar 

  4. Alananbeh KM, Bouqellah NA, Al Kaff NS (2014) Cultivation of oyster mushroom Pleurotus ostreatus on date-palm leaves mixed with other agro-wastes in Saudi Arabia. Saudi J Biol Sci 21:616–625. doi:10.1016/j.sjbs.2014.08.001

    Article  Google Scholar 

  5. Amin R, Khair A, Alam N, Lee TS (2010) Effect of different substrates and casing materials on the growth and yield of Calocybe indica. Microbiology 38:97–101. doi:10.4489/MYCO.2010.38.2.097

    Google Scholar 

  6. Bernas E, Jaworska G, Lisiewska Z (2006) Edible mushrooms as a source of valuable nutritive constituents. Acta Sci Pol Technol Aliment 5:5–20

    CAS  Google Scholar 

  7. Bobek P, Galbavy S (2001) Effect of pleuran (beta-glucan from Pleurotus ostreatus) on the antioxidant status of the organism and on dimethylhydrazine-induced precancerous lesions in rat colon. Br J Biomed Sci 58:164–168

    CAS  Google Scholar 

  8. Brzezicha-Cirocka J, Mędyk M, Falandysz J, Szefer P (2016) Bio- and toxic elements in edible wild mushrooms from two regions of potentially different environmental conditions in eastern Poland. Environ Sci Pollut Res 23:21517–21522. doi:10.1007/s11356-016-7371-0

    CAS  Article  Google Scholar 

  9. Busuioc G, Elekes CC, Stihi C, Iordache S, Ciulei SC (2011) The bioaccumulation and translocation of Fe, Zn, and Cu in species of mushrooms from Russula genus. Environ Sci Pollut R 18:890–896. doi:10.1007/s11356-011-0446-z

    CAS  Article  Google Scholar 

  10. Chen XH, Zhou HB, Qiu GZ (2009) Analysis of several heavy metals in wild edible mushrooms from regions of China. Bull Environ Contam Toxicol 83:280–285. doi:10.1007/s00128-009-9767-8

    CAS  Article  Google Scholar 

  11. Cocchi L, Vescovi L, Petrini LE, Petrini O (2006) Heavy metals in edible mushrooms in Italy. Food Chem 98:277–284. doi:10.1016/j.foodchem.2005.05.068

    CAS  Article  Google Scholar 

  12. Cohen R, Persky L, Hadar Y (2002) Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Appl Microbiol Biotechnol 58:582–594. doi:10.1007/s00253-002-0930-y

    CAS  Article  Google Scholar 

  13. Das N (2005) Heavy metals biosorption by mushrooms. Nat prod radiance 4:454–459

    Google Scholar 

  14. Deepalakshmi K, Mirunalini S (2014) Pleurotus ostreatus: an oyster mushroom with nutritional and medicinal properties. J Biochem Tech 5:718–726

    Google Scholar 

  15. Demirbaş A (2000) Accumulation of heavy metals in some edible mushrooms from Turkey. Food Chem 68:415–419. doi:10.1007/s10661-010-1728-5

    Article  Google Scholar 

  16. Demirbas A (2001) Concentrations of 21 metals in 18 species of mushrooms growing in the east Black Sea region. Food Chem 75:453–457. doi:10.1016/S0308-8146(01)00236-9

    CAS  Article  Google Scholar 

  17. Demirer T, Ock-Okuyucu BR, Ozer I (2005) Effect of different types and doses of nitrogen fertilizers on yield and quality characteristics of mushrooms (Agaricus bisporus (Lange) sing) cultivated on wheat straw compost. J Agr Rural Dev Trop 106:71–77

    Google Scholar 

  18. Falandysz J, Borovička J (2013) Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol 97:477–501. doi:10.1007/s00253-012-4552-8

    CAS  Article  Google Scholar 

  19. Falandysz J, Drewnowska M (2015) Distribution ofmercuryin Amanita fulva (Schaeff.) Secr. Mushrooms: accumulation, loss in cooking and dietary intake. Ecotoxicol Environ Saf 115:49–54. doi:10.1016/j.ecoenv.2015.02.004

    CAS  Article  Google Scholar 

  20. Falandysz J, Rizal LM (2016) Arsenic and its compounds in mushrooms: a review. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. doi:10.1080/10590501.2016.1235935

    Google Scholar 

  21. Falandysz J, Szymczyk K, Ichihashi H, Bielawski L, Gucia M, Frankowska A, Yamasaki S (2001) ICP/MS and ICP/AES elemental analysis (38 elements) of edible wild mushrooms growing in Poland. Addit Contamin 18:503–513. doi:10.1080/02652030119625

    CAS  Article  Google Scholar 

  22. Falandysz J, Saba M, Liu HG, Li T, Wang JP, Wiejak A, Zhang J, Wang YZ, Zhang D (2016) Mercury in forest mushrooms and topsoil from the Yunnan highlands and the subalpine region of the Minya Konka summit in the eastern Tibetan plateau. Environ Sci Pollut Res. doi:10.1007/s11356-016-7580-6

    Google Scholar 

  23. Fanadzo M, Zireva DT, Dube E, Mashingaidze AB (2010) Evaluation of various substrates and complements for biological efficiency of Pleurotus sajor-caju and Pleurotus ostreatus. Afr J Biotechnol 9:2756–2761. doi:10.5897/AJB09.1259

    Google Scholar 

  24. Fang Y, Sun X, Yang W, Ma N, Xin Z, Fu J, Hu Q (2014) Concentrations and health risks of lead, cadmium, arsenic, and mercury in rice and edible mushrooms in China. Food Chem 147:147–151. doi:10.1016/j.foodchem.2013.09.116

    CAS  Article  Google Scholar 

  25. Garcia MA, Alonso J, Fernández MI, Melgar MJ (1998) Lead content in edible wild mushrooms in Northwest Spain as indicator of environmental contamination. Arch Environ Contam Toxicol 34:330–335. doi:10.1007/s002449900326

    CAS  Article  Google Scholar 

  26. Gebrelibanos M, Megersa N, Taddesse AM (2016) Levels of essential and non-essential metals in edible mushrooms cultivated in Haramaya, Ethiopia. Int J Food Contamin 3:1–12. doi:10.1186/s40550-016-0025-7

    Article  Google Scholar 

  27. Gonzalez P, Labarere J (2000) Phylogenetic relationships of Pleurotus species according to the sequence and secondary structure of the mitochondrial small-subunit rRNA V4, V6 and V9 domains. Microbiology 146:209–221

    CAS  Article  Google Scholar 

  28. Govil PK, Sorlie JE, Murthy NN, Sujatha D, Reddy GL, Rudolph-Lund K, Krishna AK, Rama Mohan K (2008) Soil contamination of heavy metals in the Katedan industrial development area, Hyderabad, India. Environ Monit Assess 140:313–323. doi:10.1007/s10661-007-9869-x

    CAS  Article  Google Scholar 

  29. Granero S, Domingo JL (2002) Levels of metals in soils of Alcalá de Henares, Spain: human health risks. Environ Int 28:159–164. doi:10.1016/S0160-4120(02)00024-7

    CAS  Article  Google Scholar 

  30. Gupta N (2014) Preliminary phytochemical screening of different extracts of Pleurotus florida. Columbia. J Pharm Sci 1:23–26

    Google Scholar 

  31. Hoa HT, Wang CL, Wang CH (2015) The effects of different substrates on the growth, yield, and nutritional composition of two Oyster mushrooms (Pleurotus ostreatus and Pleurotus cystidiosus). Mycobiology 43:423–434. doi:10.5941/MYCO.2015.43.4.423

    Article  Google Scholar 

  32. Huang SS, Liao QL, Hua M, XM W, Bi KS, Yan CY, Chen B, Zhang XY (2007) Survey of heavy metal pollution and assessment of agricultural soil in Yangzhong district, Jiangsu Province, China. Chemosphere 67:2148–2155

    CAS  Article  Google Scholar 

  33. Jafarpour M, Eghbalsaeed S (2012) High protein complementation with high fiber substrates for oyster mushroom cultures. Afr J Biotechnol 11:3284–3289. doi:10.5897/AJB11.1473

    CAS  Google Scholar 

  34. Jafarpour M, Jalali Zand A, Dehdashtizadeh B, Eghbalsaied SH (2010) Evaluation of agricultural wastes and food complements usage on growth characteristics of Pleurotus ostreatus. Afr J Agric Res 5:3291–3296. doi:10.5897/AJAR10.623

    Google Scholar 

  35. Jan FA, Ishaq M, Khan S, Ihsanullah I, Ahmad I, Shakirullah M (2010) A comparative study of human health risks via consumption of food crops grown on wastewater irrigated soil (Peshawar) and relatively clean water irrigated soil (lower Dir). J Hazard Mater 179:612–621. doi:10.1016/j.jhazmat.2010.03.047

    CAS  Article  Google Scholar 

  36. Jarzyńska G, Falandysz J (2012) Trace elements profile of slate bolete (Leccinum durisculum) mushroom and associated upper soil horizon. J Geochem Explor 121:69–75. doi:10.1016/j.gexplo.2012.07.001

    Article  Google Scholar 

  37. Jarzyńska G, Chojnacka A, Dryżałowska A, Nnorom IC, Falandysz J (2012) Concentrations and Bioconcentration factors of minerals in yellow-cracking bolete (Xerocomus Subtomentosus) mushroom collected in Noteć Forest, Poland. J Food Sci 77:202–206. doi:10.1111/j.1750-3841.2012.02876.x

    Article  Google Scholar 

  38. Kalač P, Svoboda L (2000) A review of trace element concentrations in edible mushrooms. Food Chem 69:273–281. doi:10.1016/S0308-8146(99)00264-2

    Article  Google Scholar 

  39. Kazemi Jeznabadi E, Jafarpour M, Eghbalsaied S (2016) King oyster mushroom production using various sources of agricultural wastes in Iran. Int J Recycl Org Waste Agricult 5:17–24. doi:10.1007/s40093-015-0113-3

    Article  Google Scholar 

  40. Khan MA (2010) Nutritional composition and hypocholesterolemic effect of mushroom: Pleurotus sajor-caju and Pleurotus florida. LAP Lambert Academic publishing Gmbh & co. KG, Saarbrucken, Germany, pp. 1–11

    Google Scholar 

  41. Kiaei M (2011) Anatomical, physical, and mechanical properties of eldar pine (Pinus eldaricamedw.) grown in the Kelardasht region. Turk J Agric For 35:31–42. doi:10.3906/tar-1001-552

    Google Scholar 

  42. Li Y, Gou X, Wang G, Zhang Q, Su Q, Xiao G (2008) Heavy metal contamination and source in arid agricultural soil in Central Gansu Province. China. J Environ Sci 20:607–612. doi:10.1016/S1001-0742(08)62101-4

    CAS  Article  Google Scholar 

  43. Mallikarjuna SE, Ranjini A, Haware DJ, Vijayalakshmi MR, Shashirekha MN, Rajarathenam S (2013) Mineral composition of four edible mushrooms. Hindawi J Chem 2013:1–5. doi:10.1155/2013/805284

    Article  Google Scholar 

  44. Manzi P, Aguzzi A, Pizzoferrato L (2001) Nutritional value of mushrooms widely consumed in Italy. Food Chem 73:321–325. doi:10.1016/S0308-8146(00)00304-6

    CAS  Article  Google Scholar 

  45. Manzi P, Marconi S, Aguzzi A, Pizzoferrato L (2004) Commercial mushrooms: nutritional quality and effect of cooking. Food Chem 84:201–206. doi:10.1016/S0308-8146(03)00202-4

    CAS  Article  Google Scholar 

  46. Mattila P, Konko K, Eurola M, Pihlava JM, Astola J et al (2001) Contents of vitamins, mineral elements and some phenolic compounds in cultivated mushrooms. J Agric Food Chem 49:2343–2348. doi:10.1021/jf001525d

    CAS  Article  Google Scholar 

  47. Mattila P, Suonpa K, Pilronen V (2006) Functional properties of edible mushroom. Nutr J 16:694–696. doi:10.1016/S0899-9007(00)00341-5

    Article  Google Scholar 

  48. Menaga D, Mahalingam P, Rajakumar S, Ayyasamy P (2012) Evaluation of phytochemical characteristics and antimicrobial activity of Pleurotus florida mushroom. Asian J Pharm Clin Res 5:102–106

    Google Scholar 

  49. Mleczek M, Niedzielski P, Siwulski M, Rzymski P, Gąsecka M, Goliński P, Kozak L, Kozubik T (2016) Importance of low substrate arsenic content in mushroom cultivation and safety of final food product. Eur Food Res Technol 242:355–362. doi:10.1007/s00217-015-2545-4

    CAS  Article  Google Scholar 

  50. Moraditochaee M (2012) Evolution energy indices of soybean production in north of Iran. ARPN J Agric Biol Sci 7:554–557

    Google Scholar 

  51. Nnorom IC, Jarzyńska G, Falandysz J, Drewnowska M, Okoye I, Oji-Nnorom Ch G (2012) Occurrence and accumulation of mercury in two species of wild grown Pleurotus mushrooms from southeastern Nigeria. Ecotoxicol Environ Saf 84:78–83. doi:10.1016/j.ecoenv.2012.06.024

    CAS  Article  Google Scholar 

  52. Nnorom IC, Jarzyńska G, Drewnowska M, Dryżałowska A, Kojta A, Pankavec S, Falandysz J (2013) Major and trace elements in sclerotium of Pleurotus tuber-regium (Ósū) mushroom—dietary intake and risk in southeastern Nigeria. J Food Comp Anal 29:73–81. doi:10.1016/j.jfca.2012.10.001

    CAS  Article  Google Scholar 

  53. Nunes MD, da Luz JMR, Paes SA, Ribeiro JJO, da Silva MCS, Kasuya MCM (2012) Nitrogen supplementation on the productivity and the chemical composition of oyster mushroom. J Food Res 1:113–119. doi:10.5539/jfr.v1n2p113

    Article  Google Scholar 

  54. Oyetayo VO, Ariyo OO (2013) Micro and macronutrient properties of Pleurotus ostreatus (Jacq: fries) cultivated on different wood substrates. Jordan J Biol Sci 6:223–226. doi:10.12816/0001537

    Article  Google Scholar 

  55. Patel Y, Naraian R, Singh VK (2012) Medicinal properties of Pleurotus species (oyster mushroom): a review. World J Fun Plant Bio 3:1–12. doi:10.5829/idosi.wjfpb.2012.3.1.303

    CAS  Google Scholar 

  56. Patil SS, Ahmed SA, Telang SM, Baig MM (2010) The nutritional value of Pleurotus ostreatus (Jacq.: Fr) Kumm cultivated on different lignocellulosic agro-wastes. Innov rom. Food Biotechnol 7:66–76

    CAS  Google Scholar 

  57. Peksen A, Yakupoglu G (2009) Tea waste as a complement for the cultivation of Ganoderma lucidum. World J Microbiol Biotechnol 25:611–618

    CAS  Article  Google Scholar 

  58. Prabu M, Kumuthakalavalli R (2014) Nutritional and phytochemical studies on Pleurotus florida (Mont.) singer and Calocybe indica P&C. World J Pharm Res 3:4907–4913

    Google Scholar 

  59. Radulescu C, Stihi C, Busuioc G, Popescu IV, Gheboianu AI, Cimpoca VG (2010) Evaluation of essential elements and heavy metal levels in fruiting bodies of wild mushrooms and their substrate by EDXRF spectrometry and FAA spectrometry. Rom. Biotech Lett 15:5444–5456

    CAS  Google Scholar 

  60. Royse DJ (2014) A global perspective on the high five: Agaricus, Pleurotus, Lentinula, Auricularia & Flammulina. In: Singh M (ed) Proceedings of the 8th international conference on mushroom biology and mushroom products, New Delhi, India, pp 1–6

  61. Royse DJ, Fales SL, Karunanandaa K (1991) Influence of formaldehyde-treated soybean and commercial nutrient complementation on mushroom (Pleurotus sajor-caju) yield and invitro dry matter digestibility of spent substrate. Appl Microbiol Biotechnol 36:425–429. doi:10.1007/BF00208169

    Article  Google Scholar 

  62. Royse DJ, Rhodes TW, Ohga S, Sanchez JE (2004) Yield, mushroom size and time to production of Pleurotus cornucopiae (oyster mushroom) grown on switch grass substrate spawned and complemented at various rates. Bioresour Technol 91:85–91. doi:10.1016/S0960-8524(03)00151-2

    CAS  Article  Google Scholar 

  63. Saba M, Falandysz J, Nnorom IC (2016a) Accumulation and distribution of mercury in fruiting bodies by fungus Suillus luteus foraged in Poland, Belarus and Sweden. Environ Sci Pollut Res 23:2749–2757. doi:10.1007/s11356-015-5513-4

    CAS  Article  Google Scholar 

  64. Saba M, Falandysz J, Nnorom IC (2016b) Mercury bioaccumulation by Suillus bovinus mushroom and probable dietary intake with the mushroom meal. Environ Sci Pollut Res 23:14549–14559. doi:10.1007/s11356-016-6558-8

    CAS  Article  Google Scholar 

  65. Sales-Campos C, Fereira DA, Eira A, Teixeira DE, Almeida M, Noguieira DE, Andrade MC (2009) Mineral composition of raw material, substrate and fruiting bodies of Pleurotus ostreatus in culture. Interciencia 34:432–436

    Google Scholar 

  66. Sanchez C (2010) Cultivation of Pleurotus ostreatus and other edible mushrooms. Appl Microbiol Biotechnol 85:1321–1337. doi:10.1007/s00253-009-2343-7

    CAS  Article  Google Scholar 

  67. Sarikurkcu C, Tepe B, Solak MH, Cetinkaya S (2012) Metal concentrations of wild edible mushrooms from Turkey. Ecol Food Nutr 51:346–363. doi:10.1080/03670244.2012.674448

    Article  Google Scholar 

  68. Svoboda L, Zimmermannova K, Kalač P (2000) Concentrations of mercury, cadmium, lead and copper in fruiting bodies of edible mushrooms in an emission area of copper smelter and a mercury smelter. Sci Total Environ 246:61–67. doi:10.1016/S0048-9697(99)00411-8

    CAS  Article  Google Scholar 

  69. Tchounwou PB, Patlolla AK, Centeno JA (2003) Carcinogenic and systemic health effects associated with arsenic exposure-a critical review. Toxicol Pathol 31:575–588. doi:10.1080/714044691

    CAS  Google Scholar 

  70. US-EPA IRIS (2006) United States, Environmental Protection Agency, Integrated Risk Information System. <http://www.epa.gov/iris/substS>.

  71. Vetter J (1994) Mineral elements in the important cultivated mushrooms Agaricus bisporus and Pleurotus ostreatus. Food Chem 50:277–279. doi:10.1016/0308-8146(94)90132-5

    CAS  Article  Google Scholar 

  72. Vetter J, Hajdú J, Györfi J, Maszlavér P (2005) Mineral composition of the cultivated mushrooms Agaricus bisporus, Pleurotus ostreatus and Lentinula eodes. Acta Alim 34:441–451. doi:10.1556/AAlim.34.2005.4.11

    CAS  Article  Google Scholar 

  73. Wang H, Ng TB (2000) Isolation of a novel ubiquitin-like protein from Pleurotus ostreatus mushroom with anti-human immune deficiency virus, translation-inhibitory and ribonuclease activities. Biochem Biophys Res Commun 276:587–593. doi:10.1006/bbrc.2000.3540

    CAS  Article  Google Scholar 

  74. Wang D, Sakoda A, Suzuki M (2001) Biological efficiency and nutritional value of Pleurotus ostreatus cultivated on spent beet grain. Bioresour Technol 78:293–300. doi:10.1016/S0960-8524(01)00002-5

    CAS  Article  Google Scholar 

  75. Watanable T, Tsuchinasi N, Takai Y, Tanaka K, Suzuki A (1994) Effect of ozone exposure during cultivation of oyster mushroom Pleurotus ostreatus on chemical components of the fruit bodies. J Jpn Soc. Food Sci Technol 41:705–708. doi:10.3136/nskkk1962.41.705

    Article  Google Scholar 

  76. Yang X, Zhao HT, Wang J, Meng Q, Zhang H, Yao L, Zhang YC, Dong AJ, Ma Y, Wang ZY, DC X, Ding Y (2010) Chemical composition and antioxidant activity of essential oil of pine cones of Pinus armandii from the southwest region of China. J Med Plants Res 4:1668–1672. doi:10.5897/JMPR10.217

    CAS  Google Scholar 

  77. Zhang D, Frankowska A, Jarzyńska G, Kojta AK, Drewnowska M, Wydmańska D, Bielwaski L, Wang J, Falandysz J (2010) Metals of king bolete (boletus edulis) bull.: Fr. Collected at the same site over two years. Afr J Agric Res 5:3050–3055

    Google Scholar 

  78. Zhu F, Qu L, Fan W, Qiao M, Hao H, Wang X (2011) Assessment of heavy metals in some wild edible mushrooms collected from Yunnan Province, China. Environ Monit Assess 179:191–199. doi:10.1007/s10661-010-1728-5

    CAS  Article  Google Scholar 

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Acknowledgements

We are grateful to the research council of the University of Birjand for financial support.

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Correspondence to Rouhollah Khani.

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Khani, R., Moudi, M. & Khojeh, V. Contamination level, distribution and health risk assessment of heavy and toxic metallic and metalloid elements in a cultivated mushroom Pleurotus florida (Mont.) singer. Environ Sci Pollut Res 24, 4699–4708 (2017). https://doi.org/10.1007/s11356-016-8222-8

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Keywords

  • Heavy metal content
  • Cultivated mushroom
  • Toxic metals
  • Health risk assessment
  • Food safety