Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
권호 표지
DOI QR코드

DOI QR Code

Investigation of Various Pesticide Residues in Commercial Bee Pollen Products Sold in South Korea

한국에서 유통되는 화분식품의 잔류농약 함량 분석

  • Byeong-Tae Kim (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Jae-Gwan Kim (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Mi-Hui Son (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Young-Sun Cho (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Na-Eun Han (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Jong-Cheol Choi (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Seong-Nam Lee (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Myoung-Ki Park (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment) ;
  • Yong-Bae Park (Ansan Agricultural and Fishey Products Inspection Center, Gyeonggi Province Institute of Health and Environment)
  • 김병태 (경기도보건환경연구원 안산농수산물검사부) ;
  • 김재관 (경기도보건환경연구원 안산농수산물검사부) ;
  • 손미희 (경기도보건환경연구원 안산농수산물검사부) ;
  • 조영선 (경기도보건환경연구원 안산농수산물검사부) ;
  • 한나은 (경기도보건환경연구원 안산농수산물검사부) ;
  • 최종철 (경기도보건환경연구원 안산농수산물검사부) ;
  • 이성남 (경기도보건환경연구원 안산농수산물검사부) ;
  • 박명기 (경기도보건환경연구원 안산농수산물검사부) ;
  • 박용배 (경기도보건환경연구원 안산농수산물검사부)
  • Received : 2023.02.07
  • Accepted : 2023.06.19
  • Published : 2023.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

To analyze the pesticide residues in commercial bee pollen products in South Korea, 61 samples were collected and screened for 339 pesticides. Results revealed that approximately 34% (>LOQ) of samples were contaminated with at least one pesticide. The pesticide residue detection rates of domestic and imported samples were 31% and 44%, respectively. Furthermore, the pesticide residue detection rate of online distribution (60%) was higher than that of offline distribution (27%). Fifteen pesticides were discovered in bee pollen, and pendimethalin, chlorfenvinphos, chlorpyrifos, and fluazinam were detected in 7, 6, 3, and 2 order of frequency, respectively. Even though its concentration was low, chlorfenvinphos which is banned in food crops in the United States, European Union, and Korea, was detected in bee pollen samples commonly. Therefore, continuous investigation of pesticide residues in bee pollen products and their acceptance criteria is required for safety.

현재까지 한국 벌화분 잔류농약 함량 조사는 벌이 농약에 노출된 정도를 파악하기 위한 목적으로 분석되어 왔고, 식품의 관점에서 벌화분의 잔류농약 함량 연구는 보고된 바 없었다. 본 연구는 화분가공품으로서 식용으로 판매되는 벌화분 제품의 잔류농약 함량 모니터링을 통해 한국에서 유통되는 벌화분에서 잔류농약이 얼마나 검출되는지를 파악하였다. 조사 결과 다양한 농약 성분들이 벌화분에 잔류되어 있었고, 그 중에서 Chlorfenvinphos, Chlorpyrifos 같이 식용작물에서 사용금지된 농약들이 포함되어 있었다. 벌의 활동범위는 식용작물에 국한되어 있지 않기 때문에, 식용작물에만 제한적 농약사용 등의 인위적 관리만으로는 식용 벌화분의 유해물질로부터 안전성을 확보하는 것이 불가능하다는 것을 파악할 수 있었다. 따라서, 식용 벌화분의 잔류농약 안전성에 대한 연구 및 기준 설정이 필요할 것으로 보인다. 또한, 벌화분 원료와 완제품의 성상적 차이가 미미하고 주로 완제품 형태로 유통된다는 것을 고려하였을 때, 원료에만 기준을 두어 잔류농약 검사를 하는 것이 아니라 벌화분의 완제품에서도 잔류농약 검사가 필요할 것으로 보인다.

Keywords

References

  1. Jung, C.E., Integrated Pollinator-Pest Management (IPPM) Strategy as Future Apple IPM. Korean J. Appl. Entomol., 60, 145-154 (2021). 
  2. Jung, S.M., Relation between the honey bee mortality and the pesticide residue detected during the pear and apple blooming season. PhD thesis, Andong National University, Andong, Korea (2017). 
  3. Vanengelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B.K., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Underwood, R., Tarpy, D.R., Pettis, J.S. Colony Collapse Disorder: A Descriptive Study. PLoS One., 4, e6481 (2009). 
  4. Lee, K.Y., Lee, S.G., Lee, Y.B., Kim, N.J., Kim, J.H., Choi, Y.S., Kang, P.D., Yoon, H.J., Current status of honeybee production for pollination service in 2013. Korean J. Apic., 29, 245-256 (2014). 
  5. Bohme, F., Bischoff, G., Zebitz, C.P.W., Rosenkranz, P., Wallner, K., Pesticide residue survey of pollen loads collected by honeybees (Apis mellifera) in daily intervals at three agricultural sites in South Germany. PLoS One, 13, e0199995 (2018). 
  6. Brittain, C., Potts, S.G., The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl. Ecol., 12, 321-331 (2011).  https://doi.org/10.1016/j.baae.2010.12.004
  7. Vegh, R., Csoka, M., Soros, C., Sipos, L., Food safety hazards of bee pollen - A review. Trends Food Sci. Technol., 114, 490-509 (2021).  https://doi.org/10.1016/j.tifs.2021.06.016
  8. Muli, E., Kilonzo, J., Dogley, N., Monthy, G., Kurgat, J., Irungu, J., Raina, S., Detection of pesticide residues in selected bee products of honeybees (Apis melllifera L.) colonies in a preliminary study from seychelles archipelago. Bull. Environ. Contam. Toxicol., 101, 451-457 (2018).  https://doi.org/10.1007/s00128-018-2423-4
  9. Niell S, Jesus F, Perez C, Mendoza Y, Diaz R, Franco J, Cesio V, Heinzen H., QuEChERS adaptability for the analysis of pesticide residues in beehive products seeking the development of an agroecosystems sustainability monitor. J. Agric. Food Chem., 63, 4484-4492 (2015).  https://doi.org/10.1021/acs.jafc.5b00795
  10. de Oliveira, R.C., Queiroz, S.C.D.N., da Luz, C.F.P., Porto, R.S., Rath, S., Bee pollen as a bioindicator of environmental pesticide contamination. Chemosphere, 163, 525-534 (2016).  https://doi.org/10.1016/j.chemosphere.2016.08.022
  11. Fulton, C.A., Huff Hartz, K.E., Fell, R.D., Brewster, C.C., Reeve, J.D., Lydy, M.J., An assessment of pesticide exposures and land use of honey bees in Virginia. Chemosphere, 222, 489-493 (2019).  https://doi.org/10.1016/j.chemosphere.2019.01.156
  12. Mullin, C.A., Frazier, M., Frazier, J.L., Ashcraft, S., Simonds, R., Vanengelsdorp, D., Pettis, J.S., High levels of miticides and agrochemicals in north American apiaries: Implications for honey bee health. PLoS One, 5, e9754 (2010). 
  13. Stoner, K.A., Eitzer, B.D., Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut. PLoS One, 8, e77550 (2013). 
  14. Drummond, F.A., Ballman, E.S., Eitzer, B.D., Du Clos, B., Dill, J., James, D., Exposure of honey bee (Apis mellifera L.) colonies to pesticides in pollen. Environ. Entomol., 47, 378-387 (2018).  https://doi.org/10.1093/ee/nvy023
  15. Nai, Y.S., Chen, T.Y., Chen, Y.C., Chen, C.T., Chen, B.Y., Chen, Y.W., Revealing pesticide residues under high pesticide stressin Taiwan's agricultural environment probed by fresh honey Bee (Hymenoptera: Apidae) pollen. J. Econ. Entomol., 110, 1947-1958 (2017).  https://doi.org/10.1093/jee/tox195
  16. Chaimanee, V., Chantawannakul, P., Khongphinitbunjong, K., Kamyo, T,. Pettis, J.S., Comparative pesticide exposure to Apis mellifera via honey bee-collected pollen in agricultural and non-agricultural areas of Northern Thailand. J. Apic. Res., 58, 720-729 (2019).  https://doi.org/10.1080/00218839.2019.1637224
  17. Tong, Z., Duan, J., Wu, Y., Liu, Q., He, Q., Shi, Y., Yu, L., Cao, H., A survey of multiple pesticide residues in pollen and beebread collected in China. Sci. Total Environ., 640-641, 1578-1586 (2018).  https://doi.org/10.1016/j.scitotenv.2018.04.424
  18. Lambert, O., Piroux, M., Puyo, S., Thorin, C., L'Hostis, M., Wiest, L., Bulete, A., Delbac, F., Pouliquen, H., Widespread occurrence of chemical residues in beehive matrices from apiaries located in different landscapes of western France. PLoS One., 8, e67007 (2013). 
  19. Calatayud-Vernich, P., Calatayud, F., Simo, E., Pico, Y., Pesticide residues in honey bees, pollen and beeswax: Assessing beehive exposure. Environ. Pollut., 241, 106-114 (2018).  https://doi.org/10.1016/j.envpol.2018.05.062
  20. Tosi, S., Costa, C., Vesco, U., Quaglia, G., Guido, G., A 3-year survey of Italian honey bee-collected pollen reveals widespread contamination by agricultural pesticides. Sci. Total Environ., 615, 208-218 (2018).  https://doi.org/10.1016/j.scitotenv.2017.09.226
  21. Beyer, M., Lenouvel, A., Guignard, C., Eickermann, M., Clermont, A., Kraus, F., Hoffmann, L., Pesticide residue profiles in bee bread and pollen samples and the survival of honeybee colonies-a case study from Luxembourg. Environ. Sci. Pollut. Res. Int., 25, 32163-32177 (2018).  https://doi.org/10.1007/s11356-018-3187-4
  22. Friedle, C., Wallner, K., Rosenkranz, P., Martens, D., Vetter, W., Pesticide residues in daily bee pollen samples (April-July) from an intensive agricultural region in Southern Germany. Environ. Sci. Pollut. Res. Int., 28, 22789-22803 (2021).  https://doi.org/10.1007/s11356-020-12318-2
  23. Pohorecka, K., Skubida, P., Miszczak, A., Semkiw, P., Sikorski, P., Zagibajlo, K., Teper, D., Koltowski, Z., Skubida, M., Zdanska, D., Bober, A., Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J. Apic. Sci., 56, 115-134 (2013). 
  24. Roszko, M.L., Kaminska, M., Szymczyk, K., Jedrzejczak, R., Levels of selected persistent organic pollutants (PCB, PBDE) and pesticides in honey bee pollen sample in poland. PLoS One, 11, e0167487 (2016), 
  25. Greenpeace, (2023, June 19). The bee's burden: an analysis of pesticide residues in comb pollen (beebread) and trapped pollen from honey bees (Apis mellifera) in 12 uropean countries. Retrieved from https://www.greenpeace.org/static/planet4-international-stateless/2014/04/8318d052-469-thebees-burden-2.pdf 
  26. Shahali, Y., Allergy after ingestion of bee-gathered pollen: influence of botanical origins. Ann. Allergy Asthma Immunol., 114, 250-251 (2015).  https://doi.org/10.1016/j.anai.2014.11.009
  27. Thakur, M., Nanda, V., Composition and functionality of bee pollen: A review. Trends Food Sci. Technol., 98, 82-106 (2020).  https://doi.org/10.1016/j.tifs.2020.02.001
  28. Ministry of Food and Drug Safety (MFDS), (2023, June 19). Regulations for Inspection of Imported Food. Retrieved from https://www.mfds.go.kr/brd/m_211/view.do?seq=14609&srchFr=&srchTo=&srchWord=&srchTp=&itm_seq_1=0&itm_seq_2=0&multi_itm_seq=0&company_cd=&company_nm=&page=6 
  29. Powles, S.B., Yu, Q., Evolution in Action: Plants Resistant to Herbicides. Annu. Rev. Plant Biol., 61, 317-347 (2010).  https://doi.org/10.1146/annurev-arplant-042809-112119
  30. Nc State University College of Agriculture and Life Sciences, (2023, June 19). Pesticide Toxicity to Bees "Traffic Light". Retrieved from https://www.ncagr.gov/pollinators/documents/Bee%20Pesticide%20Risk%20Traffic%20Light%203-2-17.pdf 
  31. Bernal, J., Garrido-Bailon, E., Del, M.J., Gonzalez, A.V., Martin, R., Diego, J.C., Jimenez, J.J., Bernal, J.L., Higes, M., Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J. Econ. Entomol., 103, 1964-1971 (2010).  https://doi.org/10.1603/EC10235
  32. Rickwood, C.J., Galloway, T.S., Acetylcholinesterase inhibition as a biomarker of adverse effect: A study of Mytilus edulis exposed to the priority pollutant chlorfenvinphos. Aquat. Toxicol., 67, 45-56 (2004).  https://doi.org/10.1016/j.aquatox.2003.11.004
  33. Wexler, P., 2014. Encyclopedia of Toxicology, 3rd edition, Elsvier Inc., Alpharetta, GA, USA, pp. 851-854. 
  34. Ministry of Food and Drug Safety (MFDS), Food code, MFDS, Cheongju, Korea (2022). 
  35. Sparks, T.C., Crossthwaite, A.J., Nauen, R., Banba, S., Cordova, D., Earley, F., Ebbinghaus-Kintscher, U., Fujioka, S., Hirao, A., Karmon, D., Kennedy, R., Nakao, T., Popham, H.J.R., Salgado, V., Watson, G.B., Wedel, B.J., Wessels, F.J., Insecticides, biologics and nematicides: Updates to IRAC's mode of action classification - a tool for resistance management. Pestic. Biochem. Physiol., 167, 104587 (2020). 
  36. WHO, 2019, The WHO recommended classification of pesticides by hazard and guidelines to classification 2019, 2019 edition, WHO, Geneva, Switzerland, pp. 29 
  37. Eurofins Scientific, (2022, August 1). Ban of Chlorpyrifos and Chlorpyrifos-methyl in the EU and the USA. Retrieved from https://www.eurofins.de/food-analysis/food-news/food-testing-news/ban-of-chlorpyrifos-and-chlorpyrifos-methyl/
  38. Guo, Z.J., Miyoshi, H., Komyoji, T., Haga, T., Fujita, T., Uncoupling activity of a newly developed fungicide, fluazinam [3-chloro-N-(3-chloro-2,6-dinitro-4-trifluoromethylphenyl)-5-trifluoromethyl-2-pyridinamine]. BBA Bioenerg., 1056, 89-92 (1991).  https://doi.org/10.1016/S0005-2728(05)80077-5
  39. Ministry of Food and Drug Safety (MFDS), Guidelines on standard procedures for preparing analysis method, MFDS, Cheongju, Korea, 15-16 (2016). 
  40. Ministry of Food and Drug Safety (MFDS), (2022, January 27). Analytical practices manual for pesticide residues in foods(5th ed). Retrieved from https://www.foodsafetykorea.go.kr/residue/article/view.do?articleKey=18&searchTitleFlag=1&boardKey=0&menuKey=4&subMenuKey=5¤tPageNo=1 
  41. Taiwan Food and Drug Administration, "Standards for pesticide limits in foods", (2019, November 6). Retrieved from https://www.kati.net/file/down.do?path=/board/2019/11/&fileName=%5BKATI%5D+%EB%B9%84%EA%B4%80%EC%84%B8%EC%9E%A5%EB%B2%BD%EC%9D%B4%EC%8A%88_%EB%8C%80%EB%A7%8C%2C%EB%86%8D%EC%95%BD+%EC%9E%94%EB%A5%98+%ED%97%88%EC%9A%A9%EC%B9%98+%EC%88%98%EC%A0%95%EC%95%88+%EB%B0%9C%ED%91%9C.pdf.pdf