Diana Zuckerman, Journal of the American Medical Women’s Association: February 2008
Abstract
Many of the more than 182,000 women who will be newly diagnosed with breast cancer this year will not have access to all the information they need to make the surgical and treatment choices that are most appropriate for them. Research clearly shows that lumpectomy and other breast-conserving surgeries are just as safe as mastectomy for most women with early stage disease, and yet approximately half will undergo the more disfiguring procedures. Choices about breast implants and autologous tissue reconstruction are based, at best, on a few published studies that provide limited information about the long-term safety of these procedures. Many healthy women who have strong family histories of breast cancer consider prophylactic mastectomies, and their decisions are also based on very limited information, because there are few studies showing the effectiveness of that procedure. This paper delineates how limited information and biased recommendations can undermine breast cancer patients’ ability to make informed choices.
Introduction
Breast cancer is the most common malignancy in women in the United States; more than 182,000 women will be newly diagnosed this year.1 Unlike previous generations, most of these women will have several choices to make, including the type of surgery, whether to have radiation, the type of adjuvant therapy (chemotherapy or hormonal therapy), and the type of reconstruction, if any. However, many of these women will not have access to all the information they need to make the choices that are most appropriate for them.
There is considerable research evidence that where a woman lives, her income level and health insurance, the type of medical facility, when her doctor was trained, and the doctor’s enthusiasm for breast-conserving-surgery may have more impact on her surgical treatment than her specific diagnosis. For example, research has clearly shown that most women who are diagnosed with noninvasive or early-stage breast cancer can be very safely and effectively treated with breast-conserving surgery. And yet, so few women have this surgery that it raises questions about whether they are objectively informed about the advantages and disadvantages of their surgical options.2,3,4,5 In addition, the lack of research on some prevention and treatment options makes it impossible for many women to obtain the information they need to make fully informed choices. The purpose of this paper is to delineate how these and other choices made by many breast cancer patients may be based on limited information and sometimes biased recommendations, rather than the objective information needed for informed consent.
The historical context is essential to understanding why information may be inadequate. Many of today’s breast surgeons were trained at a time when there were few choices in breast cancer treatment, and tradition may still influence some doctors against breast-conserving surgery.6 Halsted developed the radical mastectomy in the 1890s; this procedure removed the breast, skin, nipple, areola, pectoral muscles, and all the axillary lymph nodes on the same side. Even more radical procedures were sometimes used, removing part of the breastbone and ribs to get the internal mammary nodes. In the 1940s, doctors in England developed the modified radical mastectomy, which removed the breast and axillary lymph nodes, but left the chest muscles intact. Although the reoccurrence rates seemed comparable to those for the Halsted, the modified radical mastectomy did not become more common than the Halsted procedure in most US hospitals until the mid-1970s.7
When researchers determined that many breast cancers grow slowly, treatment decisions became less urgent, and clinical trials were conducted to evaluate less radical procedures. In a study started in 1971, Fisher compared the survival of women who were randomized into three treatment groups: radical mastectomy, simple mastectomy (which removes only the breast and areola), and simple mastectomy with radiation.8 After 15 years, the survival rate was the same for all three groups. This study, published in 1985, was a turning point, resulting in surgical choices for more women diagnosed with breast cancer. Choices about radiation, chemotherapy, hormonal therapy, and reconstruction also influence surgical decisions. Now that women have so many choices to make, informed consent has become an important issue for breast cancer patients.
Informed consent relies on a patient receiving accurate information and freely making a decision based on that information. If objective information is not available on some aspects of breast cancer treatment because of lack of research, then the patient should be told that there is no research, or that existing research is inconclusive. If physicians describe their own experiences to patients, they should also explain the limitations of that information compared to data from long-term, objective empirical research.9
Breast-Conserving Surgery
In a landmark study comparing women with early-stage breast cancer who received breast-conserving surgery followed by radiation with those who had mastectomy, Fisher and his colleagues reported that eight years after surgery, approximately 91% of the women in both groups remained free of cancer.10 A consensus conference convened by the National Institutes of Health (NIH) in 1991 concluded that breast-conserving surgery with radiation was as effective as mastectomy for the treatment of early-stage breast cancer.11 The participants understood that breast-conserving surgery would not be the choice of every woman who was eligible, and that the expense, inconvenience, and fear of radiation would deter some women; nevertheless, the consensus was that lumpectomy and other breast-conserving surgery would be preferable for most patients.
The NIH holds consensus conferences to help experts come to a consensus about medical issues; the conferences also serve a public education function because the NIH publicizes the conclusions to physicians and patients across the country. The NIH consensus conference on breast cancer surgery was intended to help breast-conserving surgery gain wider acceptance by informing physicians and the public that these procedures are as safe as more radical surgery. In the decade since then, however, most of the women who have been eligible for lumpectomies have undergone mastectomies instead.
Women who are poor and who live in certain parts of the country are especially unlikely to have breast-conserving surgery. For example, in a 1995-1996 study of patients at a large, urban, university-affiliated Texas hospital serving primarily medically indigent patients, only 16% of those eligible received breast-conserving surgery.5 Although fear of breast cancer or radiation may make some women reluctant to choose breast-conserving surgery, one would expect that information clearly explaining that they would live just as long with lumpectomies as with mastectomies would reassure more than 16% of any group of women. Since breast-conserving surgery was believed to be safest for women with early-stage breast cancer, one would expect well-informed women with stage I breast cancer to be significantly more likely to undergo breast-conserving surgery than those with stage II breast cancer. Instead, the vast majority of women in this study underwent mastectomies regardless of stage, and the authors expressed concern that the surgeons’ opinions and recommendations were the likely reason for the high rate of mastectomy.
Several studies indicate that physicians’ knowledge or attitudes can deter women from choosing breast-conserving surgery. In a study of 157 hospitals in North Carolina, Kotwall et al found that patients were more likely to undergo breast-conserving surgery if their surgeons were trained after 1981 (by which time lumpectomies were becoming more widely accepted).3 Attitudes may be more important than knowledge; Tarbox et al reported that a substantial proportion of surgeons who knew that lumpectomy was as safe as mastectomy unknowingly influenced patients in favor of mastectomy with subtly biased presentations.4Similarly, Cady and Stone reported that the surgeon’s “interest and enthusiasm” for breast-conserving surgery increased the likelihood of patients choosing that treatment.12 Physician attitudes were also found to be influential in earlier studies of breast-conserving surgery.13,14
Lumpectomy with radiation is often more expensive than mastectomy,12 so financial incentives may also contribute to unnecessary mastectomies. Studies of low-income women indirectly support concerns that breast cancer patients are making surgical decisions that may not be based on informed choice. For example, the study of Texas indigent patients mentioned above5 found that mastectomy was more common among women with limited financial resources. A study of 20,000 breast cancer patients in North Carolina also reported lower lumpectomy rates among patients who did not have private insurance.3 Economic incentives may be influential even among Medicare patients, whose breast surgery is paid for by the federal government. A study of Virginia Medicare patients treated in 1992 and 1993 found that only 26% of the women who would be considered good candidates for breast-conserving surgery had such surgery, and this choice was most likely if the hospital had radiation oncology facilities on the grounds.15 Convenience was apparently not the only reason; patients who underwent surgery in hospitals without on-site radiation facilities were less likely to have breast-conserving surgery whether radiation facilities were nearby or far away. These findings suggest that economic incentives may influence surgeons’ discussion of treatment options or recommendations.
Researchers believe that physician knowledge and attitudes are a likely explanation for the dramatic regional differences they have documented in breast-conserving surgery: in 1986, breast-conserving surgery was more than twice as common in the Middle Atlantic states and New England than in the South Central states.16 There were also dramatic regional differences in a national study of ductal carcinoma in situ; 58% of women in New Mexico received mastectomies for this noninvasive breast cancer compared to only 29% in Connecticut.17 In a study of18 randomly selected hospitals in Massachusetts and 30 in Minnesota, 75% of Massachusetts women who were eligible for breast-conserving surgery made that choice, compared to only half in Minnesota.2 Convenience of radiation facilities could have been a factor, because Minnesota is more rural; however, informed consent seemed to play an important role as well. More mastectomy patients in Minnesota reported that their physicians did not discuss breast-conserving surgery, and even when their physicians did discuss the option, more Minnesota women reported choosing mastectomy because their physicians recommended it.2 Patient compliance with physicians’ recommendations is a related issue; Kotwall et al found that mastectomy patients were more likely to rely on the recommendations of their physicians, whereas patients who had breast-conserving surgery were more likely to obtain second opinions or to say they made the decision themselves.18
Differences in physician knowledge and attitudes could also contribute to widely varying breast-conserving surgery rates within states. For example, economic influences and hospital size or location did not fully explain breast-conserving surgery rates that ranged from 0 to 44% among Virginia hospitals caring for more than 12 Medicare breast cancer cases per year.15 Sometimes the difference in physician or clinic attitudes is very explicit. For example, the Mayo Clinic, which is the best-known medical facility in Minnesota, reported that its eligibility criteria for lumpectomy was different from other facilities, resulting in fewer women having breast-conserving surgery.19
Several states have laws aimed at improving informed consent by requiring the disclosure of options for the treatment of breast cancer.20 Research has shown the benefits and limitations of these efforts: after passage of the state laws, breast-conserving surgery rates increased by 9% in Michigan and 13% in Hawaii. The increases were not maintained over time, however, and the authors speculated that requiring physicians to provide objective information does not necessarily change their recommendations.
The statistical associations between mastectomy rates and financial incentives and physician characteristics do not prove that women are not receiving accurate information. However, five studies explicitly examined how physicians’ attitudes influenced their patients’ decisions and found that they either directly or indirectly influenced informed consent.2,4,12,13,14 A sixth study found that doctors trained in the era before lumpectomies were proven equally safe were less likely to perform them.3A seventh study found that women who had mastectomies were more likely to have relied on their physicians for advice, and women with breast-conserving surgery were more likely to have sought second opinions or relied on themselves for the decision.18 When considered together, these studies and those documenting different rates associated with geographic, insurance, socioeconomic, and other factors strongly suggest that physician attitudes and recommendations, most likely influenced by knowledge, training, and financial incentives, affected the information that patients received or the way they interpreted that information. In addition, the steady increase in lumpectomy rates during the last eight years, despite no new research regarding its safety, suggests substantial changes in the information that women are receiving, from their physicians or elsewhere.
Prophylactic Mastectomy
As women have become more aware of the risk factors for breast cancer, including family history and gene mutations, healthy women who are concerned about their risk of cancer are deciding whether to undergo prophylactic mastectomies. This raises informed consent issues in two ways: Are women receiving accurate and understandable information about their risk of breast cancer? And are they appropriately informed about the risks and benefits of prophylactic mastectomy?
The fact that women were willing to undergo prophylactic mastectomies even before research indicated that the surgery significantly reduces the risk of cancer indicates the level of fear associated with the disease. Statistics warning that one of every eight women will get breast cancer are often quoted in the media, but it is less widely understood that the lifetime risk is much higher than the risk for women under age 50 and exponentially higher than the risk that a woman of any age will get cancer in the next five years. The first step in informed consent for women considering prophylactic mastectomies should be to clarify the differences between lifetime risk and short-term risk, and to emphasize that estimates about the risks associated with genetic factors are very preliminary.
Informed consent for prophylactic mastectomy is limited by the paucity of research. One study indicated that prophylactic mastectomy reduced the rate of breast cancer in women with strong family histories of the disease.21 Those results were described on television and radio and published in major newspapers across the country, including The New York Times, The Washington Post, USA Today, and the Chicago Tribune. Two letters to the editor of the medical journal that published the study, however, pointed out that the risk of undergoing a mastectomy unnecessarily is also high. Hamm et al estimated that 13 women at moderate risk would lose their breasts unnecessarily for every prophylactic mastectomy that actually prevented one woman at moderate risk from getting breast cancer, and that 42 women at moderate risk of breast cancer or 25 women at high risk would have to have prophylactic mastectomies in order to prevent one death from breast cancer.22 Ernster estimated that 98% of women at moderate risk of breast cancer would not benefit from prophylactic mastectomy in terms of reduced mortality.23 According to a Lexis-Nexis search, the information from the letters was not widely published in the mass media and is therefore probably less available to women considering prophylactic mastectomy.
Reconstruction Options
If a woman has a mastectomy, she must also decide whether to undergo reconstruction and what kind of reconstruction, and her decision about mastectomy may be influenced by her views on the safety of reconstruction. Therefore, accurate, unbiased information regarding reconstruction is essential even before a woman decides to have a mastectomy.
The first breast implants were developed in the early 1960s for augmentation, not reconstruction. Halsted opposed reconstruction, and radical mastectomies left little tissue for it. With the increased popularity of modified radical mastectomies and simple mastectomies, however, plastic surgeons began to recommend the use of implants, urging that breast cancer patients had the “right” to replace breasts lost to cancer.24
At the time breast implants were first sold in the 1960s, the US Food and Drug Administration (FDA) did not regulate medical devices and therefore did not evaluate implant safety. When the FDA was given that authority in 1976, breast implants and many other devices were “grandfathered” and therefore allowed to stay on the market at least temporarily. Although there were warnings on the package inserts in the box containing breast implants, including the risk of breast hardening, rupture and gel leakage, infection, hematoma, swelling, pain, and necrosis,25 the package insert is enclosed in a sealed box that is not opened until surgery in order to keep the implant sterile. Implant patients are therefore dependent on their doctors for safety information. A pamphlet developed and widely distributed by the American Society of Plastic and Reconstructive Surgeons described implants as safe and did not mention that there were no empirical studies of long-term health effects.25
In 1991, the FDA required implant manufacturers to submit data proving that silicone gel breast implants were safe and effective, but the studies submitted were deemed too poorly designed to prove safety or effectiveness.26 In an almost unprecedented decision, however, the FDA allowed continued sale of silicone implants to mastectomy patients and women who wanted implant replacements, to meet a “public health need.” In 1992, the FDA approved a large-scale “clinical trial” to be conducted by one implant manufacturer, which was open to virtually any mastectomy patient; no data from that trial have yet been published or reviewed by the FDA.
Because of the lack of research on any kind of breast implants and concern about the almost one million women who already had them, Congress passed legislation in 1992 requiring the National Institutes of Health (NIH) to study the safety of breast implants. The NIH director refused to include mastectomy patients in this study of more than 13,000 implant patients, explaining to members of Congress that it would complicate the study design.26 There are, therefore, no epidemiological safety studies of mastectomy patients with implants funded by the federal government. Very few studies have examined even the short-term health outcome for mastectomy patients.27,28 Some studies of mastectomy patients have reported substantial complications, but their results are not widely disseminated and therefore are not available to most doctors or patients. For example, a five-year prospective study of silicone gel implants conducted by one implant manufacturer indicated that 24% of the mastectomy patients underwent at least one implant-related additional surgery within the first year, and 24% underwent surgery to remove at least one implant within the first two years (McGhan Medical Corporation, unpublished data, 1998). This unpublished study is available only on request from the Institute of Medicine (IOM) Library in Washington, DC.
Saline-filled breast implants have had a similar history. The FDA reviewed safety data provided by two manufacturers in March 2000 and approved the implants despite evidence that approximately three-fourths of the mastectomy patients studied had had serious complications in the first three years, including pain, implant rupture, additional surgery, hardness, or the need to have the implant removed.9,29 The FDA required the two implant manufacturers to add new warnings to their package inserts, but these warnings are, as before, provided to the surgeons in the sealed implant box rather than to the patients.
Women considering mastectomy and reconstruction should be informed of the lack of peer-reviewed research on implants for mastectomy patients and the high rupture, resurgery, and complication rates reported in unpublished studies. They should also be advised that no studies of the health risks of a saline implant with bacteria or mold breaking inside the body have been conducted. Patients will not have the information needed to make informed decisions if neither they nor their doctors have access to objective, peer-reviewed research conducted on mastectomy patients. Representatives of the American Society of Plastic and Reconstructive Surgeons provided testimony to the FDA that breast implants are very safe and that serious complications are rare.9 In contrast, a review of research conducted by FDA scientists reported that rupture was common, and an FDA study found that more than 79% of patients had at least one broken implant within 11 to 15 years.30,31
In the last decade, alternative breast reconstruction techniques have become increasingly available, using muscle and fat from the abdomen or back. Published studies on the safety and effectiveness of these types of breast reconstruction are limited; most are small case series of plastic surgeons’ own patients, which clearly raises questions about generalizability and objectivity. Even so, the articles raise concerns about skin or fat necrosis,32 especially among smokers;33 problems with inexperienced physicians,30 high complication rates,31,34 burns on reconstructed breasts due to impaired thermoregulatory capacity of transplanted tissue;35 and death.36
These surgeries are lengthy, complicated procedures, and the researchers warn that success rates vary greatly depending on the skill of the surgeon; it is therefore unlikely that the results from one practice are generalizable to most patients. In the absence of large multicenter clinical trials or empirical studies of a doctor’s own patients it is not possible for most doctors to provide good estimates of the risks associated with these procedures to their patients, thus greatly limiting informed consent.
Improving Informed Consent for Breast Cancer Patients
Informed consent for breast-conserving surgery, prophylactic mastectomy, and reconstructive surgery is limited partly because physicians themselves lack the information they need to appropriately inform their patients. In all these situations, informed consent should focus on what is not known about long-term risks in addition to what is known about failure rates and local complications. Physicians should provide as much objective information as possible, including long-term follow-up data from their own patients. We do not know if most doctors inform women of the lack of research, but there is clear evidence that at least one medical association is providing women with overly optimistic statements about the safety of implants. The ASPS website currently has an article stating that “Recent scientific studies have absolved silicone gel breast implants of causing health problems in women.” This statement is apparently based on studies showing no increased risks of autoimmune disease or cancer, but it ignores the IOM and FDA conclusions that implants can cause such serious health problems as pain, infection, and the need for multiple surgeries.
Signed consent forms provide liability protection and meet research requirements by giving detailed descriptions of the risks, known and unknown. In contrast, health professionals’ oral explanations of risks and benefits may be inconsistent with their own written materials. To improve informed consent for breast cancer patients, we need more information about the process of decision making. It is certainly likely that some women who are accurately and persuasively told that lumpectomies are as safe as mastectomies will choose mastectomies, and that some women who have mastectomies will choose reconstruction even if told that there are serious short-term risks and that the long-term risks are unknown. However, it is likely that better information will change the current pattern of high rates of unnecessary mastectomies followed by reconstruction.
In summary, more long-term safety data are needed on reconstruction options, better research is needed on the efficacy of prophylactic mastectomy, and many physicians need better access to the most accurate, unbiased information already available on breast cancer surgical outcomes. In addition, research is needed to better understand why the rate for breast-conserving surgery is so low, and what programs and policies would be most effective in ensuring that breast cancer patients receive objective information in ways that enable them to make the best possible medical and surgical choices. The bottom line is that many patients do not have the information they need to make informed choices, and patient advocates and policy makers need to support objective research and develop new strategies to ensure better informed consent for breast cancer patients.
All articles are reviewed and approved by Diana Zuckerman, PhD, and other senior staff.
References
1 Cancer Facts and Figures 2000. Atlanta, Ga: American Cancer Society; 2000.
2 Guadagnoli E, Weeks JC, Shapiro CL, Gurwitz JH, Borbas C, Soumerai SB. Use of breast-conserving surgery for treatment of stage I and stage II breast cancer. J Clin Oncol. 1998; 16:101-106.
3 Kotwall CA, Covington DL, Rutledge R, Churchill MP, Meyer AA. Patient, hospital, and surgeon factors associated with breast conservation surgery: A statewide analysis in North Carolina. Ann Surg 1996;224:419-426.
4 Tarbox BB, Rockwood JK, Abernathy CM. Are modified radical mastectomies done for T1 breast cancers because of surgeon’s advice or patient’s choice? Am J Surg. 1992;164:417-420.
5 Dolan JT, Granchi TS. Low rate of breast conservation surgery in a large urban hospital serving the medically indigent. Am J Surg. 1998;176:520-524.
6 Treatment of early-stage Breast Cancer. NIH Consensus Statement Online. 1990;8:1-19. http://odp.od.nih.gov/consensus/cons/081/081_statement.htm.
7 Love SM. Dr. Susan Love’s Breast Book. 2nd ed. Reading, Mass: Addison-Wesley; 1995.
8 Fisher B, Redmond CB, Fisher E, et al. Ten-year results of randomized clinical trials comparing radical mastectomy and total mastectomy with or without radiation. N Engl J Med. 1985;312:674.
9 Testimony before the Food and Drug Administration Meeting on Saline Breast Implants, March 1, 2000. http://www.fda.gov.
10 Fisher B, Anderson S, Redmond CK, Wolmark N, Wickerham DL, Cronin WM. Reanalysis and results after 12 years of follow-up in a randomized clinical trial comparing total mastectomy with lumpectomy with or without irradiation in the treatment of breast cancer. N Engl J Med. 1995;1456-1461.
11 NIH Consensus Conference. NIH Consensus Conference: Treatment of early stage breast cancer. JAMA. 1991;265:391-395.
12 Cady B, Stone, MD. Selection of breast-preservation therapy for primary invasive breast carcinoma. Surg Clin North Am. 1990;70:1047-1049.
13 Ward S, Heidrick S, Wolberg W. Factors women take into account when deciding upon type of surgery for breast cancer. Cancer Nurs. 1989;12:344-351.
14 Liberati A, Apolone G, Nicolucci A, et al. The role of attitudes, beliefs, and personal characteristics of Italian physicians in the surgical treatment of early breast cancer. Am J Public Health. 1990;81:38.
15 Elward KS, Penberthy LT, Bear H, Swartz DM , Boudreau RM, Cook SS. Variation in the use of breast-conserving therapy for Medicare beneficiaries in Virginia: Clinical, geographic, and hospital characteristics. Clin Perform Qual Health Care. 1998;6:63-69.
16 Nattinger AB, Gottlieb MS, Veum J, et al. Geographic variation in the use of breast-conserving treatment for breast cancer. N Engl J Med. 1992;3326:1102-1107.
17 Ernster VL, Barclay J, Kerlikowske K, et al. Incidence of and treatment for ductal carcinoma in situ of the breast. JAMA. 1996;275:913-918.
18 Kotwall CA, Maxwell JG, Covington DL, Churhill P, Smith SE, Covan EK. Clinicopathologic factors and patient perceptions associated with surgical breast-conserving treatment. Ann Surg Oncol. 1996;3:169-175.
19 Grant CS. Changes in the treatment of early breast cancer at the Mayo Clinic: 1988-1992.Eur J Surg. 1996;162:93-96.
20 Nattinger AB, Hoffman RG, Shapiro R, Gottlieb MS, Goodwin JS. The effect of legislative requirements on the use of breast-conserving surgery. N Engl J Med. 1996;335:1035-1040.
21 Hartmann LC, Schaid DJ, Woods JE, et al. Efficacy of bilateral prophylactic mastectomy in women with a family history of breast cancer. N Engl J Med. 1999;340:77-84.
22 Hamm RM, Lawler F, Scheid, D. Prophylactic mastectomy in women with a family history of breast cancer. N Engl J Med. 1999;340:1837-38. Letter.
23 Ernster VL. . Prophylactic mastectomy in women with a family history of breast cancer. N Engl J Med. 1999;340:1838. Letter.
24 Jacobson N. The socially constructed breast: Breast implants and the medical construction of need. Am J Public Health. 1998;88:1254-1261.
25 Is the FDA Protecting Patients From the Dangers of Silicone Breast Implants? Hearing before the Human Resources and Intergovernmental Relations Subcommittee of the Committee on Government Operations, U.S. House of Representatives. Washington, DC: US Government Printing Office; 1991: 179-185, 278-370.
26 The FDA’s Regulation of Silicone Breast Implants: Staff Report for the Human Resources and Intergovernmental Relations Subcommittee of the Committee on Government Operations, U.S. House of Representatives. Washington, DC: US Government Printing Office; 1993.
27 Safety of Silicone Breast Implants. Washington, DC: Institute of Medicine; 1999.
28 Zuckerman D. Summary of Studies of Saline Implants and Connective Tissue Diseases. http://www.cpr4womenandfamilies.org/implant.html.
29 Local Complications of Saline Breast Implants.http://www.cpr4womenandfamilies.org/implant.html.
30 Brown SL, Silverman BG, Berg W. Rupture of silicone-gel breast implants: Causes, sequelae, and diagnosis. Lancet. 1997; 350:1531-1537.
31 Brown SL, Middleton MS, Berg WA, Soo MS, Pennello G. Prevalence of rupture of silicone gel breast implants in a population of women in Birmingham, Alabama. Am J Roentgenol 2000; 175: 1057-1064.
32 Baldwin BJ, Schusterman MA, Miller MJ, et al. Bilateral breast reconstruction: Conventional versus free TRAM. Plast Reconstr Surg. 1994;93:1410-1416.
33 Schusterman MA, Kroll SS, Miller MJ, et al. The free transverse rectus abdominis musculocutaneous flap for breast reconstruction: One center’s experience with 211 consecutive cases. Ann Plast Surg. 1994;32:234-241.
34 Delay E, Gounot N, Bouillot A, et al. Autologous latissimus breast reconstruction: A 3-year clinical experience with 100 patients. Plast Reconstr Surg. 1998;102:1461-1478.
35 Nahabedian MY, McGibbon BM. Thermal injuries in autogenous tissue breast reconstruction. Br J Plast Surg. 1998; 51:599-602.
36 Hamdi M, Weiler-Mithoff EM, Webster MH. Deep inferior epigastric perforator flap in breast reconstruction: Experience with the first 50 flaps. Plast Reconstr Surg. 1999;103:86-95.