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Journal of Long-Term Eff ects of Medical Implants, 14(5)341–346 (2004) Joseph K. McLaughlin, PhD
A World Leader in Implant Research
William J. Blot, PhD¹ & Joseph F. Fraumeni, Jr., MD²
¹International Epidemiology Institute, Rockville, Maryland, USA, and Vanderbilt University Medical Center, Vanderbilt-Ingram Cancer Center, Nashville, Tennessee, USA; ²Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA Address all correspondence to William Blot, International Epidemiology Institute, 1455 Research Blvd, Suite 550, Rockville, MD 20850; blotw@iei.ws 1050-6934/04 $20.00 2004 by Begell House, Inc. 341
342
W. J. BLOT & J. F. FRAUMENI, JR.
ABSTRACT: Objective. To describe the key contributions of Dr. Joseph K. McLaughlin,
Outstanding Scientist of 2004. Methods. We review the scientifi c literature and indicate how
epidemiologic research conducted by Dr. McLaughlin has clarifi ed long-term health eff ects
among persons with breast and other medical implants. Results. Dr. Joseph K. McLaughlin has
conducted and directed more research into the long-term eff ects of human implants than any
other scientist worldwide. His insights greatly elucidated the long-term health consequences
associated with a variety of implanted devices, including silicone and saline breast implants,
hip and knee replacements, temporomandibular and fi nger joint devices, and pacemakers. By
initiating and bringing to fruition a series of innovative epidemiologic investigations, Dr.
McLaughlin and his colleagues have provided the scientifi c basis for making judgments about
alleged adverse health eff ects following cosmetic, reconstructive, and reparative implant surgery.
Conclusions. Dr. McLaughlin’s seminal investigations have provided reassurance that breast and
other implants have not demonstrably increased the risk of cancer or other systemic diseases.
Th e comprehensive and rigorous nature of this research merits his selection as Outstanding
Scientist of 2004.
KEY WORDS: breast implants, medical devices, epidemiology, surveillance, cancer, connective
tissue disease, neurologic disease, birth defects, confounding
Dr. joseph k. mclaughlin is President of of renal cell carcinoma, and that the risk of kidney the International Epidemiology Institute cancer rose progressively with increasing body mass (IEI), headquartered in Rockville, Mary- and with use of the analgesic phenacetin.¹-² Th e latter land, and Professor in the Department of Medicine fi nding led to follow-on studies by Dr. McLaughlin of the Vanderbilt University Medical School and and by others assessing acetaminophen, the primary Vanderbilt-Ingram Cancer Center in Nashville, metabolite of phenacetin, as a potential risk factor. Tennessee. He also holds an appointment as adjunct While these studies revealed no substantial adverse Professor of Epidemiology at the Johns Hopkins eff ect, the jury is still out on whether acetaminophen, Bloomberg School of Public Health in Baltimore, aspirin, or other non-narcotic analgesics may impart Maryland. Prior to cofounding IEI in 1994, he a small increase in the risk of renal cancer or chronic served as Epidemiologist and then Deputy Chief in renal failure.³-⁴the Epidemiology and Biostatistics Program of the Dr. McLaughlin also conducted research into National Cancer Institute. He spent two years as As- the causes of oral, esophageal, stomach, colorectal, sistant Professor at Johns Hopkins after receiving his lung, bladder, and other cancers. He showed, for in-doctoral degree in epidemiology from the University stance, that smoking and drinking account for about of Minnesota in 1981. three-fourths of all oral cancers, while low intake Dr. McLaughlin has had an exceptionally pro- of fruits and vegetables also contribute to elevated ductive career in epidemiologic research. His initial risk.⁵-⁶ He has also helped track the epidemic rise studies focused on the etiology of cancer, including in esophageal adenocarcinoma in the United States research on renal cancer that clarifi ed the roles of and showed a causal relation to obesity and to gas-tobacco smoking, diet, obesity, medical conditions, troesophageal refl ux disease rather than (as previously pharmaceutical agents, and occupational exposures. reported) acid-inhibiting drugs used as treatment.⁷ He was one of the fi rst to show, for example, that Furthermore, in a series of exploratory studies using cigarette smoking increased the risk of cancer of the linked employment–cancer registries in Sweden, Dr. renal pelvis up to 10-fold while doubling the risk McLaughlin uncovered and confi rmed a number of Journal of Long-Term Effects of Medical Implants
OUTSTANDING SCIENTIST OF 2003
343
occupation–cancer associations. While certain occu- from impaired survival after breast cancer diagnosis. pational exposures appeared causally linked to cancer, For example, in a review by the International Agency he found that many reported associations were more for Research on Cancer (IARC), it was concluded that likely to be false-positives resulting from random fl uc- there was suffi cient evidence that silicone implants tuations from multilayered and multi-subset analyses. are not carcinogenic to the breast.¹⁷Th is experience prompted Dr. McLaughlin to publish However, concerns were also voiced that women several methodologic papers on the conduct and in- with silicone gel-fi lled breast implants may be at terpretation of epidemiologic studies and how bias increased risk of developing other cancers, such as and confounding can aff ect study fi ndings.⁸-¹¹ leukemia and multiple myeloma. Th e subsequent Perhaps the specifi c area of research for which Dr. work of Dr. McLaughlin was central to the conclu- McLaughlin has devoted most attention is the eff ect sion reached by scientifi c review bodies that there is of implanted devices on human health. Dr. McLaugh- no demonstrable excess of any form of cancer among lin has launched a series of epidemiologic studies to women with silicone breast implants.¹⁷-²² evaluate whether implants increase the risk of cancer, In recent years, concerns began to center on a pos- connective tissue diseases, and various other condi- sible link between connective tissue disease (CTD) tions. In a bibliography of more than 360 publications, and silicone breast implants. In the 1980s and early over 50 original papers in the peer-reviewed scientifi c 1990s, anecdotal case reports suggesting a possible literature have described risks of disease among indi- excess of autoimmune disorders among women viduals receiving surgical implants. Th e most extensive with breast implants came to the attention of the series of publications involved breast implants.
US Food and Drug Administration (FDA). While Th e initial concerns about the adverse eff ects of the initial publications focused on systemic sclerosis breast implants involved cancer, especially breast (scleroderma), clinical reports also appeared on the cancer. It was suggested that foreign materials such occurrence of other autoimmune diseases, including as silicone might lead to scarring, infl ammation, or Graves’ disease, Hashimoto’s thyroiditis, systemic other changes with malignant potential, and that and discoid lupus erythematosus, mixed connective the ability to detect early breast cancer would be tissue disease, morphea, polymyositis, dermatomyo-limited in women with breast implants, because the sitis, Raynaud’s syndrome, rheumatoid arthritis, and opaque implants might interfere with physical breast Sjogren’s syndrome. In large-scale, long-term cohort examination or mammographic visualization of breast studies by Dr. McLaughlin, no evidence was found tumors, leading to delays in breast cancer diagnosis linking silicone breast implants to any individual and thus to higher fatality rates. In cohort studies CTD or all CTDs combined.²³-²⁵ Th ese results were in Denmark, Sweden, and Fınland involving a total confi rmed by other investigators, leading to an In-of about 12,000 women with breast implants, Dr. stitute of Medicine consensus report indicating “no McLaughlin and his colleagues found that the risks elevated relative risk or odds ratio for an association were actually decreased rather than increased among of implants with disease.”¹⁸women with breast implants.¹²-¹⁵ In addition, they More diffi cult to evaluate has been the concern showed that women with breast implants were on that breast implants may lead to subtle or atypical average diagnosed with breast cancer at the same manifestations of CTD. However, in nationwide stage as controls, with no statistically signifi cant dif- cohort studies with virtually 100% follow-up in ference in overall survival between the two groups.¹⁶ Sweden and Denmark, Dr. McLaughlin and his Th is research was instrumental to consensus reports colleagues found no excess of fi bromyalgia among indicating that women with cosmetic breast implants women with implants.²⁶-²⁸ Furthermore, validation of are not at increased risk for breast cancer or for de- the diagnosis “unspecifi ed rheumatism” did not reveal layed detection of breast cancer, nor do they suff er a pattern of symptoms suggestive of atypical CTD Volume 14, Number 5, 2004
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W. J. BLOT & J. F. FRAUMENI, JR.
in women with silicone implants.²⁹ With regard to confounding is addressed. Based on this experience their musculoskeletal pain profi le or the prevalence with implant studies, Dr. McLaughlin has reported of fi bromyalgia, the group exposed to silicone did not on the insidious eff ects of “confounding by indica-diff er from women with breast reduction surgery or tion” in epidemiologic research of implants.¹¹ In this from an additional comparison group with no breast situation, an association reported between a device surgery. Moreover, by examining rheumatic diagnoses or medication and disease may actually be due to the and symptoms among groups of women with breast underlying condition for which the device or medi-implants, breast reduction, or no breast surgery,³⁰ sig- cation is prescribed. Identifying and correcting for nifi cant diff erences were not seen in the occurrence such confounding is often very diffi cult, prompting of fi bromyalgia or related complaints. However, in Dr. McLaughlin to alert the epidemiologic as well as all groups the frequency of symptoms was strongly clinical communities to its distorting eff ects.
associated with preimplant rheumatic conditions, In addition, Dr. McLaughlin has evaluated the underscoring the importance of taking antecedent long-term eff ects of other implanted devices, includ-conditions into account when evaluating the risk of ing artifi cial hips, knees, fi nger joints, temporoman-CTDs among women with breast implants. In ad- dibular joints, and pacemakers.³⁶-⁴¹ He has used the dition, Dr. McLaughlin and colleagues performed a same scientifi c model—namely, population cohort series of studies of neurologic disease among women studies that take advantage of the unique data systems with breast implants and found no excess of these in Scandinavian countries. Th ese investigations have conditions when compared with controls.³¹-³³ Finally, been reassuring in fi nding no evidence of increased Dr. McLaughlin has taken the lead in evaluating the risk of cancer or other systemic illness among indi-association between breast implants and suicide risk, viduals with other implant types. which was previously reported in epidemiologic stud-ies.³⁴ In a recent review, he set forth the methodologic framework necessary for research to evaluate whether CONCLUSIONthis association is causal or a result of preimplant patient characteristics.³⁵ In summary, Dr. McLaughlin has been a pioneer Th e studies of women with breast implants in and leader in the initiation and conduct of a sys- Scandinavian populations illustrate the rigorous, tematic series of epidemiologic investigations that methodologic approach taken by Dr. McLaughlin in have comprehensively evaluated the health eff ects evaluating potential disease risks. He has taken care of medical implants. His seminal contributions to to ensure that followup is complete, that appropriate the fi eld clearly merit his selection as Outstanding control or comparison groups are employed, and that Scientist of 2004.
Jr. Renal Cancer. In: Schottenfeld D, Fraumeni JF Jr (Eds): Cancer Epidemiology and Prevention. New 1. McLaughlin JK, Blot WJ, Mandel JS, Schuman LM, York: Oxford University Press, 1996.
Mehl ES, Fraumeni JF Jr. Etiology of cancer of the 4. Fored CM, Ejerblad E, Lindblad P, Fryzek JP, Dick-renal pelvis. J Natl Cancer Inst 1983; 71:287–291.
man PW, Signorello LB, Lipworth L, Elinder C- 2. McLaughlin JK, Mandel JS, Blot WJ, Schuman LM, G, Blot WJ, McLaughlin JK, Zack MM, Nyrén O. Mehl ES, Fraumeni JF Jr. A population-based case- Acetaminophen, aspirin, and chronic renal failure. control study of renal cell carcinoma. J Natl Cancer 5. McLaughlin JK, Gridley G, Block G, Winn DM, 3. McLaughlin JK, Blot WJ, Devesa SS, Fraumeni JF Preston-Martin S, Schoenberg JB, Greenberg RS, Journal of Long-Term Effects of Medical Implants
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Stemhagen A, Ershow AG, Blot WJ, Fraumeni JF cancer at diagnosis among women with cosmetic Jr. Dietary factors in oral and pharyngeal cancer. J breast implants. Br J Cancer 2003; 88:832–838. Natl Cancer Inst 1988; 80:1237–1243.
17. International Agency for Research on Cancer 6. Gridley G, McLaughlin JK, Block G, Gluch M, Blot (IARC). Surgical implants and other foreign bod- WJ. Vitamin supplement use and reduced risk of ies. IARC Monograph on the Evaluation of Carci- oral and pharyngeal cancer. Am J Epidemiol 1992; nogenic Risks to Humans, Volume 74. Lyon: IARC 7. Chow WH, Finkle WD, McLaughlin JK, Frankl 18. Institute of Medicine (IOM). Safety of Silicone H, Ziel HK, Fraumeni JF Jr. Th e relation of gastro- Breast Implants. Bondurant S, Ernster V, Herdman esophageal refl ux diseases and its treatment to ad- R, editors. Washington, DC: National Academy enocarcinomas of the esophagus and gastric cardia. 19. European Committee on Quality Assurance and 8. Wacholder S, McLaughlin JK, Silverman DT, Medical Devices in Plastic Surgery. Consensus Mandel JS. Selection of controls in case-control declaration on breast implants, 23-6-2000. Israel, studies. I. Principles. Am J Epidemiol 1992; 135: 9. Wacholder S, Silverman DT, McLaughlin JK, 20. National Institutes of Health. Breast implants: sta- Mandel JS. Selection of controls in case-control tus of research at the National Institutes of Health. studies. II. Types of controls. Am J Epidemiol 1992; 7/16/2003. Available online at //www4.od.nih.gov/ orwh/implants.pdf. Accessed October 24, 2003. 10. Wacholder S, Silverman DT, McLaughlin JK, 21. Independent Review Group (IRG). Silicone Gel Mandel JS. Selection of controls in case-control Breast Implants: Report of the IRG (United King- studies. III. Design options. Am J Epidemiol 1992; 22. Tugwell P, Wells G, Peterson J, Welch V, Page J, 11. Signorello LB, McLaughlin JK, Lipworth L, Friis S, Davison C, McGowan J, Ramroth D, Shea B. Do Sorensen HT, Blot WJ. Confounding by indication: silicone breast implants cause rheumatologic dis- implications for implant research. J Long Term Eff orders? A systematic review for a court-appointed national science panel. Arthritis Rheum 2001; 44: 12. Friis S, McLaughlin JK, Mellemkjaer L, Kjoller KH, Blot WJ, Boice JD Jr, Fraumeni JF Jr, Olsen JH. 23. Lipworth L, Tarone RE, McLaughlin JK. Silicone Breast implants and cancer risk in Denmark. Int J breast implants and connective tissue disease: an updated review of the epidemiologic evidence. Ann 13. Mellemkjaer L, Kjoller K, Friis S, McLaughlin JK, Hogsted C, Winther JF, Breiting V, Krag C, Kjaer 24. Friis S, Mellemkjaer L, McLaughlin JK, Breiting SK, Blot WJ, Olsen JH. Cancer occurrence after cos- V, Kjaer SK, Blot W, Olsen JH. Connective tissue metic breast implantation in Denmark. Int J Cancer disease and other rheumatic conditions following breast implants in Denmark. Ann Plast Surg 1997; 14. McLaughlin JK, Nyren O, Blot WJ, Yin L, Josefsson S, Fraumeni JF Jr, Adami HO. Cancer risk among 25. Nyren O, Josefsson S, McLaughlin JK, Blot WJ, women with cosmetic breast implants: a population- Engqvist M, Hakelius L, Boice JD Jr, Adami H-O. based cohort study in Sweden. J Natl Cancer Inst Risk of connective tissue disease and related disor- ders among women with breast implants: A nation- 15. Pukkala E, Boice JD, Jr., Hovi SL, Hemminki E, wide retrospective cohort study in Sweden. Br Med Asko-Seljavaara S, Keskimaki I, McLaughlin JK, Pakkanen M, Teppo L. Incidence of breast and 26. Lipworth L, Tarone RE, McLaughlin JK. Breast other cancers among Finnish women with cosmetic implants and fi bromyalgia: a review of the epidemio- breast implants, 1970–1999. J Long Term Eff Med logic evidence. Ann Plast Surg 2004; 52:284–287. 27. Kjoller K, Friis S, Mellemkjaer L, McLaughlin JK, 16. Holmich L, Mellemkjer L, Gunnarsdottir K, Tange Winther JF, Lipworth L, Blot WJ, Fryzek J, Olsen U, Krag C, Meller S, McLaughlin J. Stage of breast JH. Connective tissue disease and other rheumatic Volume 14, Number 5, 2004
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conditions following cosmetic breast implantation in among women with cosmetic breast implants: a Denmark. Arch Intern Med 2001; 161:973–979. review of the epidemiologic evidence. J Long Term 28. Fryzek JP, McLaughlin JK, Nyren O. Response: Eff Med Implants 2003; 13:445–450.
Silicone breast implants and fi bromyalgia. Plast 36. Nyren O, McLaughlin JK, Gridley G, Ekbom A, Reconstr Surg 2001; 108:2166–2167. Johnell O, Fraumeni JF Jr, Adami HO. Cancer risk 29. Jensen B, Kjoller K, McLaughlin JK, Danneskiold- after hip replacement with metal implants: a popula- Samsoe B, Bliddal H, Blot WJ, Olsen JH. Muscular tion-based cohort study in Sweden. J Natl Cancer rheumatism following breast surgery in Denmark. 37. Olsen JH, McLaughlin JK, Nyren O, Mellemkjaer 30. Jensen B, Bliddal H, Kjoller K, Wittrup IH, Friis L, Lipworth L, Blot WJ, Fraumeni JF Jr. Hip and S, Hoier-Madsen M, Rogind H, McLaughlin JK, knee implantations among patients with osteoar- Lipworth L, Danneskiold-Samsoe B, Olsen JH. thritis and risk of cancer: a record-linkage study Rheumatic manifestations in Danish women with from Denmark. Int J Cancer 1999; 81:719–722. silicone breast implants. Clin Rheumatol 2001; 20: 38. Fryzek JP, Mellemkjaer L, McLaughlin JK, Blot WJ, Olsen JH. Cancer risk among patients with 31. Winther JF, Bach FW, Friis S, Blot WJ, Mellemkjaer fi nger and hand joint and temporo-mandibular L, Kjøller K, Høgsted C, McLaughlin JK, Olsen joint prostheses in Denmark. Int J Cancer 1999; JH. Neurologic disease among women with breast implants. Neurology 1998; 50:951–955.
39. Fryzek JP, Mellemkjaer L, Friis S, McLaughlin JK, 32. Winther JF, Friis S, Baach FW, Mellemkjaer L, Rosenthal AK, Blot WJ, Olsen JH. Connective tis- Kjøller K, McLaughlin JK, Lipworth L, Blot WJ, sue disease and other related rheumatic conditions Olsen JH. Neurological disease among women with among patients with fi nger and hand joints and silicone breast implants in Denmark. Acta Neurol temporomandibular joint prostheses in Denmark. 33. Nyren O, McLaughlin JK, Yin L, Josefsson S, 40. Mellemkjaer L, Friis S, McLaughlin JK, Th omsen Engqvist M, Hakelius L, Blot WJ, Adami HO. BL, Kjøller K, Høgsted C, Winther JF, Blot WJ, Breast implants and risk of neurologic disease: a Olsen JK. Connective tissue disease after hip and population-based cohort study in Sweden. Neurol- knee implant surgery. Scand J Rheumatol 2001; 30: 34. McLaughlin JK. Do cosmetic breast implants 41. Lipworth L, Johansen C, Arnsbo P, Møller M, cause suicide? Plast Reconstr Surg 2003; 112: McLaughlin JK, Olsen JH. Cancer risk among pacemaker recipients in Denmark, 1982–1996. J 35. McLaughlin JK, Lipworth L, Tarone RE. Suicide Long Term Eff Med Implants 2002; 12:263–270. Journal of Long-Term Effects of Medical Implants

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