Biological Hazard of Electromagnetic Field Exposure: A Review

전자기파의 생체 위해성에 관한 소고

  • Jung, Kyung-Ah (Department of Practical Arts Education, Chuncheon National University of Education) ;
  • Gye, Myung-Chan (Department of Life Science and Institute for Natural Sciences, Hanyang University)
  • 정경아 (춘천교육대학교 실과교육과) ;
  • 계명찬 (한양대학교 생명과학과)
  • Received : 2011.10.26
  • Accepted : 2011.11.14
  • Published : 2011.11.30

Abstract

The safety of human exposure to an ever-increasing number and diversity of electromagnetic field (EMF) sources both at work and at home has clearly become a public health issue. To date many $in$ $vivo$ and $in$ $vitro$ studies revealed that EMF exposure can alter cellular metabolism, endocrine function, immune activity, reproductive function, and fetal development in animal system. The major parameters found to be altered in cells or individuals following EMF exposure include an increase of free radicals, DNA damage, cancer risk, developmental defect, and reproductive dysfunctions. Epidemiological studies reported EMF can increase life-threatening illnesses such as leukemia, brain cancer, amyotrophic lateral sclerosis, clinical depression, suicide, and Alzheimer's disease has been identified. These effects of EMF exposure differ according to duration of exposure, frequency of waves, and strength (energy) of EMF. In the present review, we briefly introduced the physical properties of EMF and summarized the effect of EMF on human and wildlife animals according to types of EMF, duration of exposure at cellular and organism levels.

현대인들은 가정생활과 직업환경 속에서 다양한 종류의 전자기파에 노출되며 전자기파 노출에 따른 생체위해성은 공중보건학적으로 중요한 이슈로 대두되었다. 현재까지 많은 체외 및 체내실험 결과에서 전자기파 노출이 세포대사, 내분비, 면역, 신경, 생식, 태아발달에 영향을 미치는 것으로 보고되었다. 세포나 개체 수준에서 시행된 실험연구에서는 전자기파 노출에 의해 세포내부 자유기의 증가, DNA 손상과 암발생, 발생기형, 생식기능 저하가 나타난다. 역학조사결과 전자기파 노출은 생명을 위협하는 질병인 백혈병, 뇌암, 근위축성 측삭경화증, 우울증, 자살, 알츠하이머와 상관성이 보고되었다. 이러한 생체기능 변화는 전자기파의 주파수, 노출기간, 강도 (에너지)에 따라 다르게 나타난다. 전자기파 노출은 곤충, 어류, 양서류, 파충류, 조류 등 야생동물에서도 동물행동, 번식, 생리기능의 변화를 초래한다. 본 소고에서는 인간보건학적 측면과 생태계에서 나타난 전자기파의 위해성을 전자기파의 종류, 노출시간에 따라 세포 및 개체 수준에서 보고된 위해성 자료를 정리하였다.

Keywords

References

  1. Atli E and H Unlu. 2006. The effects of microwave frequency electromagnetic fields on the development of Drosophila melanogaster. Int. J. Radiat. Biol. 82:435-441. https://doi.org/10.1080/09553000600798849
  2. Bastuji-Garin SR and R Zittoun. 1990. Acute leukemia in workers exposed to electromagnetic fields. Eur. J. Cancer 26: 1119-1120. https://doi.org/10.1016/0277-5379(90)90266-V
  3. Bergqvist UO. 1984. Video display terminals and health: A technical and medical appraisal of the state of the art. Scand. J. Work Environ. Health 10:1-87. https://doi.org/10.5271/sjweh.2367
  4. Bernabo N, E Tettamanti, V Russo, A Martelli, M Turriani, M Mattoli and B Barboni. 2010. Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model. Theriogenology 73:1293-1305. https://doi.org/10.1016/j.theriogenology.2009.12.010
  5. BioInitiative report: a rationale for a biologically-based public exposure standard for electromagnetic fields (ELF and RF). http://www.bioinitiative.org [Updated April 26, 2011].
  6. Black DR and LN Heynick. 2003. Radiofrequency (RF) effects on blood cells, cardiac, endocrine, and immunological functions. Bioelectromagnetics Suppl. 6:S187-195.
  7. Brainard GC, R Kavet and LI Kheifets. 1999. The relationship between electromagnetic field and light exposures to melatonin and breast cancer risk: A review of the relevant literature. J. Pineal Res. 26:65-100. https://doi.org/10.1111/j.1600-079X.1999.tb00568.x
  8. Bryant HE and EJ Love. 1989. Video display terminal use and spontaneous abortion risk. Int. J. Epidemiol. 18:132-138. https://doi.org/10.1093/ije/18.1.132
  9. Burchard JF, DH Nguyen and E Block. 1998. Progesterone concentrations during estrous cycle of dairy cows exposed to electric and magnetic fields. Bioelectromagnetics 19:438-443. https://doi.org/10.1002/(SICI)1521-186X(1998)19:7<438::AID-BEM6>3.0.CO;2-2
  10. Cecconi S, G Gualtieri, A Di Bartolomeo, G Troian, MG Cifone and R Canipari. 2000. Evaluation of the effects of extremely low frequency electromagnetic fields on mammalian follicle development. Hum. Reprod. 15:2319-2325. https://doi.org/10.1093/humrep/15.11.2319
  11. Chemeris NK, AB Gapeyev, NP Sirota, OY Gudkova, NV Kornienko, AV Tankanag, IV Konovalov, ME Buzoverya, VG Suvorov and VA Logunov. 2004. DNA damage in frog erythrocytes after in vitro exposure to a high peak-power pulsed electromagnetic field. Mut. Res. 558:27-34. https://doi.org/10.1016/j.mrgentox.2003.10.017
  12. Chung MK, SJ Lee, YB Kim, SC Park, DH Shin, SH Kim and Kim JC. 2005. Evaluation of spermatogenesis and fertility in F1 male rats after in utero and neonatal exposure to extremely low frequency electromagnetic fields. Asian J. Androl. 7:189-194. https://doi.org/10.1111/j.1745-7262.2005.00007.x
  13. Dawson BV, IG Robertson, WR Wilson, LJ Zwi, JT Boys and AW Green. 1998. Evaluation of potential health effects of 10 kHz magnetic fields: A rodent reproductive study. Bioelectromagnetics 19:162-171. https://doi.org/10.1002/(SICI)1521-186X(1998)19:3<162::AID-BEM4>3.0.CO;2-#
  14. Dufty AM and JR Belthoff. 1997. Corticosterone and the stress response in young western screech-owls: effects of captivity, gender, and activity period. Physiol. Zool. 70:143-149.
  15. Falzone N, C Huyser, P Becker, D Leszczynski and DR Franken. 2011. The effect of pulsed 900-MHz GSM mobile phone radiation on the acrosome reaction, head morphometry and zona binding of human spermatozoa. Int. J. Androl. 34:20-26. https://doi.org/10.1111/j.1365-2605.2010.01054.x
  16. Fernie KJ, DM Bird and RD Dawson. 2000. Effects of electromagnetic fields on the reproductive success of American kestrels. Physiol. Biochem. Zool. 73:60-65. https://doi.org/10.1086/316726
  17. Fernie KJ and SJ Reynolds. 2005. The effects of electromagnetic fields from power lines on avian reproductive biology and physiology: a review. J. Toxicol. Environ. Health B. Crit. Rev. 8:127-140. https://doi.org/10.1080/10937400590909022
  18. Flipo D, M Fournier, C Benquet, P Roux, C Le Boulaire, C Pinsky, FS LaBella and K Krzystyniak. 1998. Increased apoptosis, changes in intracellular $Ca^{2+}$, and functional alterations in lymphocytes and macrophages after in vitro exposure to static magnetic field. J Toxicol Environ, Health 54:63-76. https://doi.org/10.1080/009841098159033
  19. Furubayashi T, A Ushiyama, Y Terao, Y Mizuno, K Shirasawa, P Pongpaibool, AY Simba, K Wake, M Nishikawa and K Miyawaki. 2009. Effects of short-term W-CDMA mobile phone base station exposure on women with or without mobile phone related symptoms. Bioelectromagnetics 30: 100-113. https://doi.org/10.1002/bem.20446
  20. Ghione S, C Del Seppia, L Mezzasalma, M Emdin and P Luschi. 2004. Human head exposure to a 37 Hz electromagnetic field: effects on blood pressure, somatosensory perception, and related parameters. Bioelectromagnetics 25:167-175. https://doi.org/10.1002/bem.10180
  21. Goldhaber MK, MR Polen and RA Hiatt. 1988. The risk of miscarriage and birth defects among women who use video display terminals during pregnancy. Am. J. Ind. Med. 13: 695-706. https://doi.org/10.1002/ajim.4700130608
  22. Goodman EM, B Greenebaum and MT Marron. 1995. Effects of electromagnetic fields on molecules and cells. Int. Rev. Cytol. 158:279-338.
  23. Greenberg B, VP Bindokas and JR Gaujer. 1981. Biological effects of a 760 kV transmission line: Exposures and thresholds in honeybee colonies. Bioelectromagnetics 2:315. https://doi.org/10.1002/bem.2250020404
  24. Grigor'ev IuG. 2003. Biological effects of mobile phone electromagnetic field on chick embryo (risk assessment using the mortality rate). Radiats. Biol. Radioecol. 43:541-543.
  25. Grigor'ev IuG. 2005. The electromagnetic fields of cellular phones and the health of children and of teenagers (the situation requiring to take an urgent measure). Radiats. Biol. Radioecol. 45:442-450.
  26. Grigor'ev IuG, AV Shafirkin and AL Vasin. 2003. Bioeffects of chronic exposure to radiofrequency electromagnetic fields of low intensity (standardization strategy). Radiats. Biol. Radioecol. 43:501-511.
  27. Grigor'ev OA, EP Bicheldei and AV Merkulov. 2003. Anthropogenic EMF effects on the condition and function of natural ecosystems. Radiats. Biol. Radioecol. 43:544-551.
  28. Harkins TT and CB Grissom. 1994. Magnetic field effects on B12 ethanolamine ammonia lyase: Evidence for a radical mechanism. Science 263:958-960. https://doi.org/10.1126/science.8310292
  29. Harrington JM, DI McBride, T Sorahan, GM Paddle and M van Tongeren. 1997. Occupational exposure to magnetic fields in relation to mortality from brain cancer among electricity generation and transmission workers. Occup. Environ. Med. 54:7-13. https://doi.org/10.1136/oem.54.1.7
  30. Hydro-Quebec. 1989. Electricity in the air. Montreal, PQ: Hydro-Quebec.
  31. Iorio R, R Scrimaglio, E Rantucci, S Delle Monache, A Di Gaetano, N Finetti, F Francavilla, R Santucci, E Tettamanti and R Colonna. 2007. A preliminary study of oscillating electromagnetic field effects on human spermatozoon motility. Bioelectromagnetics 28:72-75. https://doi.org/10.1002/bem.20278
  32. Ivancsits S, A Pilger, E Diem, O Jahn and HW Rudiger. 2005. Cell type-specific genotoxic effects of intermittent extremely low-frequency electromagnetic fields. Mutat. Res. 583:184-188. https://doi.org/10.1016/j.mrgentox.2005.03.011
  33. Ivancsits S, E Diem, A Pilger, HW Rudiger and O Jahn. 2002. Induction of DNA strand breaks by intermittent exposure to extremely-low-frequency electromagnetic fields in human diploid fibroblasts. Mutat. Res. 519:1-13. https://doi.org/10.1016/S1383-5718(02)00109-2
  34. Johansen C and J Olsen. 1998. Mortality from amyotrophic lateral sclerosis, other chronic disorders and electric shocks among utility workers. Am. J. Epidemiol. 148:362-368. https://doi.org/10.1093/oxfordjournals.aje.a009654
  35. Johansson A, S Nordin, M Heiden and M Sandstrom. 2010. Symptoms, personality traits, and stress in people with mobile phone-related symptoms and electromagnetic hypersensitivity. J. Psychosom. Res. 68:37-45. https://doi.org/10.1016/j.jpsychores.2009.06.009
  36. Johansson O. 2009. Disturbance of the immune system by electromagnetic fields-A potentially underlying cause for cellular damage and tissue repair reduction which could lead to disease and impairment. Pathophysiology 16:157-177. https://doi.org/10.1016/j.pathophys.2009.03.004
  37. Jung KA, HS Ahn, YS Lee and MC Gye. 2007. Effect of a 20 kHz sawtooth magnetic field exposure on the estrous cycle in mice. J. Microbiol. Biotechnol. 17:398-402.
  38. Juutilainen J and K Saali. 1986. Development of chick embryos in 1 Hz to 100 kHz magnetic fields. Radiat. Environ. Biophys. 25:135-140. https://doi.org/10.1007/BF01211737
  39. Kato M, K Honma, T Shigemitsu and Y Shiga. 1994. Circularly polarized 50-Hz magnetic field exposure reduces pineal gland and blood melatonin concentrations of Long-Evans rats. Neurosci. Lett. 166: 59-62. https://doi.org/10.1016/0304-3940(94)90840-0
  40. Kim JY, SY Hong, YM Lee, SA Yu, WS Koh, JR Hong, T Son, SK Chang and M Lee. 2008. In vitro assessment of clastogenicity of mobile-phone radiation (835 MHz) using the alkaline comet assay and chromosomal aberration test. Environ. Toxicol. 23:319-327. https://doi.org/10.1002/tox.20347
  41. Kim SH, JE Song, SR Kim, H Oh, YM Gimm, D Yoo, JK Pack and YS Lee. 2004. Teratological studies of prenatal exposure of mice to a 20 kHz sawtooth magnetic field. Bioelectromagnetics 25:114-117. https://doi.org/10.1002/bem.10164
  42. Komazaki S and K Takano. 2007. Induction of increase in intracellular calcium concentration of embryonic cells and acceleration of morphogenetic cell movements during amphibian gastrulation by a 50-Hz magnetic field. J. Exp. Zool. A. Ecol. Genet. Physiol. 307:156-162.
  43. Kowalczuk CL, L Robins, BK Butland, JM Thomas and RD Saunders. 1994. Effects of prenatal exposure to 50 Hz magnetic fields on development in mice: 1. Implantation rate and fetal development. Bioelectromagnetics 15:349-361. https://doi.org/10.1002/bem.2250150409
  44. Lantow M, J Schuderer, C Hartwig and M Simko. 2006. Free radical release and HSP70 expression in two human immune-relevant cell lines after exposure to 1800 MHz radiofrequency radiation. Radiat. Res. 165:88-94. https://doi.org/10.1667/RR3476.1
  45. Lee JS, SS Ahn, KC Jung, YW Kim and SK Lee. 2004. Effects of 60 Hz electromagnetic field exposure on testicular germ cell apoptosis in mice. Asian J. Androl. 6:29-34.
  46. Lee KS, JS Choi, SY Hong, TH Son and K Yu. 2008. Mobile phone electromagnetic radiation activates MAPK signaling and regulates viability in Drosophila. Bioelectromagnetics 29:371-379. https://doi.org/10.1002/bem.20395
  47. Lei Y, T Liu, FA Wilson, D Zhou, Y Ma and X Hu. 2005. Effects of extremely low-frequency electromagnetic fields on morphine-induced conditioned place preferences in rats. Neurosci. Lett. 390:72-75. https://doi.org/10.1016/j.neulet.2005.08.001
  48. Lincoln GA and KI Maeda. 1992. Reproductive effects of placing microimplants of melatonin in the mediobasal hypothalamus and preoptic area in rams. J. Endocrinol. 132:201-215. https://doi.org/10.1677/joe.0.1320201
  49. London SJ, DC Thomas, JD Bowman, E Sobel and JM Peters. 1991. Exposure to residential electric and magnetic fields and risk of childhood leukemia. Am. J. Epidemiol. 134:923-937.
  50. Malpaux B, A Daveau, F Maurice, V Gayrard and JC Thiery. 1993. Short days effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol. Reprod. 48:752-760. https://doi.org/10.1095/biolreprod48.4.752
  51. Mancinelli F, M Caraglia, A Abbruzzese, G d'Ambrosio, R Massa and E Bismuto. 2004. Non-thermal effects of electromagnetic fields at mobile phone frequency on the refolding of an intracellular protein: myoglobin. J. Cell Biochem. 93:188-196. https://doi.org/10.1002/jcb.20164
  52. McCarty DE, S Carrubba, AL Chesson, C Frilot, E Gonzalez-Toledo and AA Marino. 2011. Electromagnetic hypersensitivity: evidence for a novel neurological syndrome. Int. J. Neurosci. 121:670-676. https://doi.org/10.3109/00207454.2011.608139
  53. McDonald AC, JC McDonald, B Armstrong, N Cherry, AD Nolin and D Robert. 1988. Work with visual display units during pregnancy. Br. J. Ind. Med. 45:509-515.
  54. Nam KC, JH Lee, HW Noh, EJ Cha, NH Kim and DW Kim. 2009. Hypersensitivity to RF fields emitted from CDMA cellular phones: a provocation study. Bioelectromagnetics 30:641-650. https://doi.org/10.1002/bem.20518
  55. National Institute of Environmental Health Sciences (NIEHS). 1998. Working group report: Assessment of health effects from exposure to power-line frequency electric and magnetic fields. In: Portier CJ, Wolfe MS, editors. US National Institutes of Health. NIH Publication No. 98-3981. Research Triangle Park: NIEHS .
  56. Nelson JF, L Karelus, MD Bergman and LS Felicio. 1995. Neuroendocrine involvement in aging: evidence from studies of reproductive aging and caloric restriction. Neurobiol. Aging 16:837-843. https://doi.org/10.1016/0197-4580(95)00072-M
  57. Nishimura T, H Okano, H Tada, E Nishimura, K Sugimoto, K Mohri and M Fukushima. 2010. Lizards respond to an extremely low-frequency electromagnetic field. J. Exp. Biol. 213 (Pt 12):1985-1990. https://doi.org/10.1242/jeb.031609
  58. Nishimura T, H Tada, X Guo, T Murayama, S Teramukai, H Okano, J Yamada, K Mohri and M Fukushima. 2011. 1-$\mu$T extremely low-frequency electromagnetic field vs. sham control for mild-to-moderate hypertension: a double-blind, randomized study. Hypertens. Res. 34:372-377. https://doi.org/10.1038/hr.2010.246
  59. Ohnishi Y, F Mizuno, T Sato, M Yasui, T Kikuchi and M Ogawa. 2002. Effects of power frequency alternating magnetic fields on reproduction and pre-natal development of mice. J. Toxicol. Sci. 27:131-138. https://doi.org/10.2131/jts.27.131
  60. Pourlis AF. 2009. Reproductive and developmental effects of EMF in vertebrate animal models. Pathophysiology 16:179-189. https://doi.org/10.1016/j.pathophys.2009.01.010
  61. Preece AW, JW Hand, RN Clarke and A Stewart. 2000. Power frequency electromagnetic fields and health. Where's the evidence? Phys. Med. Biol. 45:R139-154. https://doi.org/10.1088/0031-9155/45/9/201
  62. Reichmanis M, FS Perry, AA Marino and RO Becker. 1979. Relation between suicide and the electromagnetic field of verhead power lines. Physiol. Chem. Phys. 11:395-403.
  63. Reiter RJ. 1993. Static and extremely low frequency electromagnetic field exposure reported effects on the circadian production of melatonin (review). J. Cell. Biochem. 51:394-403.
  64. Rodriguez M, D Petitclerc, JF Burchard, DH Nguyen and E Block. 2004. Blood melatonin and prolactin concentrations in dairy cows exposed to 60 Hz electric and magnetic fields during 8 h photoperiods. Bioelectromagnetics 25:508-515. https://doi.org/10.1002/bem.20024
  65. Rodriguez M, D Petitclerc, JF Burchard, DH Nguyen, E Block and BR Downey. 2003. Response of the estrous cycle in dairy cows exposed to electric and magnetic fields (60 Hz) during 8-h photoperiods. Anim. Reprod. Sci. 99:11-20.
  66. Roy S, Y Noda, V Eckert, MG Traber, A Mori, RP Liburdy and L Packer. 1995. The phorbol 12-myristate 13-acetate (PMA)-induced oxidative burst in rat peritoneal neutrophils is increased by a 0.1mT(60 Hz) magnetic field. FEBS Lett. 376:164-166. https://doi.org/10.1016/0014-5793(95)01266-X
  67. Roychoudhury S, J Jedlicka, V Parkanyi, J Rafay, L Ondruska, P Massanyi and J Bulla. 2009. Influence of a 50 hz extra low frequency electromagnetic field on spermatozoa motility and fertilization rates in rabbits. J. Environ. Sci. Health A. Tox. Hazard Subst. Environ. Eng. 44:1041-1047. https://doi.org/10.1080/10934520902997029
  68. Santini MT, G Rainaldi and PL Indovina. 2009. Cellular effects of extremely low frequency (ELF) electromagnetic fields. Int. J. Radiat. Biol. 85:294-313. https://doi.org/10.1080/09553000902781097
  69. Schnorr T, B Grajewski, R Hornung, MJ Thun, G Egeland, W Murray, D Conover and W Halperin. 1991. Video display terminals and the risk of spontaneous abortion. N. Engl. J. Med. 324:727-733. https://doi.org/10.1056/NEJM199103143241104
  70. Simko M and MO Mattsson. 2004. Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: possible immune cell activation. J. Cell Biochem. 93:83-92. https://doi.org/10.1002/jcb.20198
  71. Skauli KS, JB Reitan and BT Walther. 2000. Hatching in zebra-fish (Danio rerio) embryos exposed to a 50 Hz magnetic field. Bioelectromagnetics 21:407-417. https://doi.org/10.1002/1521-186X(200007)21:5<407::AID-BEM10>3.0.CO;2-V
  72. Sobel E, M Dunn, Z Davanipour, Z Qian and HC Chui. 1996. Elevated risk of Alzheimer's disease among workers with likely electromagnetic field exposure. Neurology 47:1477-1481. https://doi.org/10.1212/WNL.47.6.1477
  73. Stevens RG and S Davis. 1996. The melatonin hypothesis: Electric power and breast cancer. Environ. Health Perspect. 104 (Suppl 1):135-140. https://doi.org/10.1289/ehp.96104s1135
  74. Stevens RG, S Davis, DB Thomas, LE Anderson and BW Wilson. 1992. Electric power, pineal function, and the risk of breast cancer. FASEB J. 6:853-860.
  75. Tan DX, LC Manchester, RJ Reiter, WB Qi, M Zhang, ST Weintraub, J Cabrera, RM Sainz and JC Mayo. 1999. Identification of highly elevated levels of melatonin in bone marrow: Its origin and significance. Biochim. Biophys. Acta. 1472:206-214. https://doi.org/10.1016/S0304-4165(99)00125-7
  76. Tappa B, H Amao, A Ogasa and KW Takahashi. 1989. Changes in the estrous cycle and number of ovulated and fertilized ova in aging female IVCS mice. Exp. Anim. 38:115-119.
  77. Tenorio BM, GC Jimenez, RN Morais, SM Torres, R Albuquerque Nogueira and VA Silva Junior. 2011. Testicular development evaluation in rats exposed to 60 Hz and 1 mT electromagnetic field. J. Appl. Toxicol. 31:223-230. https://doi.org/10.1002/jat.1584
  78. Tuschl H, W Novak and H Molla-Djafari. 2006. In vitro effects of GSM modulated radiofrequency fields on human immune cells. Bioelectromagnetics 27:188-196. https://doi.org/10.1002/bem.20191
  79. Verkasalo PK, J Kaprio, J Varjonen, K Romanov, K Heikkila and M Koskenvuo. 1997. Magnetic fields of transmission lines and depression. Am. J. Epidemiol. 146:1037-1045. https://doi.org/10.1093/oxfordjournals.aje.a009232
  80. Walleczek J. 1992. Electromagnetic field effects on cells of the immune system: The role of calcium signalling, FASEB J. 6:3177-3185.
  81. Walleczek J. 1994. Immune cell interactions with extremely low frequency magnetic fields: experimental verification and mechanisms. In On the nature of electromagnetic field interactions with biological systems, ed. AH Frey, pp. 167-180. Austin, TX: R. G. Landes.
  82. Yellon SM. 1994. Acute 60 Hz magnetic field exposure effects on the melatonin rhythm in the pineal gland and circulation of the adult Djungarian hamster. J. Pineal Res. 16:136-144. https://doi.org/10.1111/j.1600-079X.1994.tb00093.x
  83. Youbicier-Simo BJ, F Boudard, C Cabaner and M Bastide. 1997. Biological effects of continuous exposure of embryos and young chickens to electromagnetic fields emitted by video display units. Bioelectromagnetics 18:514-523. https://doi.org/10.1002/(SICI)1521-186X(1997)18:7<514::AID-BEM7>3.0.CO;2-5