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Open surgical biopsy for nonpalpable mammographic abnormalities: Still an option compared with core needle biopsy
Open surgical biopsy for nonpalpable mammographic abnormalities: Still an option compared with core needle biopsy James A. Hall, MD, Duffy C. Murphy, MD, Bernard R. Hall, MD, and Kyle A. Hall, RN, MSN Logansport, Indiana OBJECTIVE: Our purpose was to present information about open surgical biopsy. It is hoped that this will be helpful when reviewing information about core needle biopsy STUDY DESIGN: Review of 461 open surgical biopsies for nonpalpable mammographic abnormalities was performed. All patients were managed by the Women’s Health Center of Logansport. Core needle biopsy data came from the literature. RESULTS: Open surgical biopsy compared favorably to core needle biopsy with regard to accuracy, cost, patient convenience, recovery, adequacy of specimen, identification of primary site, and cosmetics. CONCLUSION: Despite core needle biopsy marketing, open surgical biopsy has its advantages and should not be relegated to the museum. (Am J Obstet Gynecol 1998;178:1245-50.)
Key words: Open surgical biopsy, core needle biopsy
Approximately 500,000 breast biopsies are done per year in the United States. Biopsies for nonpalpable mammographic abnormalities have become an increasingly significant proportion of this number. We will address only nonpalpable mammographic abnormalities leading to breast biopsy. Approximately 20% to 30% of these biopsies result in the discovery of a breast malignancy. The standard of care has been an open surgical biopsy with preoperative lesion localization by wire placement under mammographic guidance. A move is under way to obtain tissue through “less invasive” procedures such as core needle biopsies, usually under stereotaxic mammographic guidance. This process generally removes the surgeon from his or her dominant role in the care and the management of the breast lesion. Proponents of core needle biopsy cite several advantages over open surgical biopsies. These include lower cost, patient convenience, and satisfaction. Core needle biopsy is marketed to the public as a nonsurgical option for the patient with a nonpalpable mammographic abnormality. The purpose of this article is to compare open surgical biopsy as performed in a community hospital with core needle biopsy. Most of the articles contrasting core needle biopsy with open surgical biopsy paint a very unfavorable picture of open biopsy with regard to cost, patient convenience, and recovery.
From The Women’s Health Center of Logansport. Community Hospital Award paper, presented at the Sixty-fifth Annual Meeting of The Central Association of Obstetricians and Gynecologists, Scottsdale, Arizona, October 29–November 1, 1997. Reprint requests: James A. Hall, MD, Women’s Health Center of Logansport, Suite 170, 1201 Michigan Ave., Logansport, IN 46947. Copyright © 1998 by Mosby, Inc. 0002-9378/98 $5.00 + 0 6/6/90428
It is our contention that open surgical biopsy compares favorably to core needle biopsy with regard to cost, patient convenience, and recovery. Open biopsy also has advantages regarding accuracy and specimen adequacy. It may also eliminate the further need for cancer surgery in a significant percentage of patients. Material and methods Patients cared for at the Women’s Health Center of Logansport who had an abnormal mammogram for which the radiologist recommended tissue biopsy were subjected to open surgical biopsy with preoperative wire localization technique. The wire is placed mammographically by radiology immediately preoperatively. The biopsies are done with the patient under local anesthesia in an outpatient treatment room. Patients receive no sedation and require no anesthesia other than local. Patients are released to full activities. Specimen radiography is obtained to ensure an adequate specimen if the original abnormality contained microcalcifications. Adequate removal of the mammographic abnormality is confirmed by either specimen radiography or postbiopsy mammogram at 4 to 6 months. Frozen-section diagnosis was not performed. The specimen was taken fresh to the pathology laboratory and the margins were inked to evaluate later in case of malignancy. All the biopsies were done by the physician authors obstetrician-gynecologists at the Women’s Health Center of Logansport. A total of 461 open surgical biopsies were carried out for abnormal mammographic lesions from 1980 through 1996 (Table I); 164 of the 461 biopsies were from 1993 through 1996 (Table II). All biopsies were done at Memorial Hospital, Logansport, Indiana. A stereotaxic core needle biopsy service is not available at our hospital. We have no per1245
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Table I. Open surgical biopsy for nonpalpable mammographic abnormalities at Women’s Health Center of Logansport, 1980 through 1996 Year
No. of biopsies
No. of malignancies
1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996
1 2 4 3 18 24 8 15 16 13 69 87 37 30 33 40 61 461
0 0 0 0 0 3 1 2 3 4 6 9 5 7 8 7 12 67 (15%)
TOTAL
Table II. Open surgical biopsy for nonpalpable mammographic abnormalities at Women’s Health Center of Logansport, 1993 through 1996 Year 1993 1994 1995 1996 TOTAL
No. of biopsies
No. of malignancies
30 33 40 61 164
7 8 7 12 34 (21%)
sonal experience with this technique. Information regarding core needle biopsy has been obtained either from the literature or personal communication. Results Results will be discussed in several areas. Accuracy. Since 1980, 461 open breast biopsies have been performed by the gynecologists at the Women’s Health Center of Logansport. This resulted in the discovery of 67 cancers (15%) (Table I). The percentage of discovered malignancies increased in the period from 1993 through 1996 to 21% of biopsies (34 cancers from 164 biopsies) (Table II). We have had three surgical misses (0.6%) in 461 biopsies (Table III). A surgical miss is defined as the persistence of the abnormal mammographic area after biopsy. All three failures underwent a successful biopsy with a second attempt and were benign. The cause of the failure involved localization problems of the original target lesion. Two patients had the wrong microcalcified area localized and the third experienced migration of the wire preoperatively. Core needle biopsy surgical miss statistics are unclear in the literature. Because the core biopsies do not always remove the entire lesion, some
Table III. Surgical misses (failures to remove target lesion) at open biopsy for nonpalpable mammographic abnormalities at Women’s Health Center of Logansport, 1980 through 1996 Failure No. of biopsies
No.
461
3
% 0.6
residual of the target lesion may be expected to remain after biopsy. It is a leap of faith to assume that what remains in the breast matches pathologically with the tissue that was removed. Brenner et al.1 reported a combined series of core needle biopsies from 10 breast centers with a 97% overall accuracy (3% false negative) compared with immediate excisional biopsy after the core needle biopsy with five tissue core samples. Reynolds et al.2 reported up to a 6.6% false-negative rate. It is generally agreed that the learning curve with core needle biopsy is steep and that over time the false-negative rate reduces. When surgical accuracy was compared, open surgical biopsy has an advantage over core needle biopsy. Proponents of core needle biopsy rely on the fact that most of the biopsy results are going to be benign and therefore a slightly lessened accuracy rate is acceptable. One wonders how acceptable this decreased ability to remove the target lesion is if the patient is or is not a member of one’s own family. The advantage to open biopsy is that the entire target lesion can be removed for adequate histologic sampling. Core needle biopsy also is limited by interpretation of samples when either atypical hyperplasia or in situ changes are encountered. Differentiation between in situ carcinoma and invasive carcinoma with core needle biopsy is not possible unless definite invasive changes are noted. Patients with atypical ductal hyperplasia or in situ carcinoma on core needle biopsy will need open biopsy to rule out invasive malignancy, whereas patients with open biopsy will not need further surgery because of removal of the entire target lesion. Cost. Cross et al.3 stated that the core needle biopsy average cost is $1200. Personal communication with an Indianapolis-based breast center confirms this figure. The $1200 charge includes the facility, biopsy, and radiology charges. It does not include pathologic examination. Costs of open surgical biopsy performed by the Women’s Health Center of Logansport have been reviewed from 1993 to 1996. The average total expense for surgeon’s fee, hospital charges, and radiology was $1400. Fees for pathologic studies were excluded. This contrasts with many literature reports that open biopsy costs range in the several thousand dollar area. Thus the cost differential appears to be approximately $200 per procedure, or approximately 16%. Liberman et al.4 reported that
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Table IV. Relationship of margin to residual disease after open surgical biopsy nonpalpable mammographic abnormality at Women’s Health Center of Logansport, 1993 through 1996 Biopsy margin and No. of cases Tumor transected (n = 6) Tumor at inked margin (n = 8) Margins clear (n = 20)(7 patients had subsequent lumpectomy)
Residual tumor 5 0 1
No residual tumor 1 8 6
Total cancers biopsied: 34.
core needle biopsy costs are 50% lower than open biopsy. We do not find Liberman’s4 cost estimates to be accurate. Literature review of cost estimates favoring core needle biopsy also do not take total costs into account. Management of some patients with abnormal areas with core needle biopsy will ultimately have increased costs not required of those who have open surgical biopsy. These extra costs are not included in literature reviews and relate to serial postbiopsy mammograms and further surgery required of some core needle biopsy patients. Patients having core needle biopsy may be required to have serial mammograms after biopsy, secondary to the need to follow the residual target lesion remaining in the breast. There are extra costs secondary to the need for open biopsy for areas showing atypical changes. The patients with open surgical biopsies also do not need further cancer surgery if the biopsy produced clear margins. All patients with core needle biopsy discovered malignancies will need further surgery. Liberman4 quoted costs relating to open biopsy to include preoperative testing, inpatient days, and days lost from work. None of these factors are relative to open biopsy in our series. There was no preoperative testing, inpatient days, or days lost from work. Therefore any cost comparison with these factors should be the same as core needle biopsy. When all of these factors are taken into account, especially the need for open surgical biopsy or lumpectomy in some patients who have had core needle biopsy, it appears that the $200 differential in the original procedure may be lost in later charges. Specimen adequacy if malignant. Invasive or in situ breast carcinoma will not be totally excised by core needle biopsy. The patients with diagnosis made in this manner will need further excision (lumpectomy). From 1993 through 1996, 34 breast cancers were discovered in our series (Table II). All these nonpalpable mammographic abnormalities were diagnosed by open breast biopsy technique. There were six cases in which tumor was obviously transected at the margin. There were eight cases in which tumor cells approached the inked margin, but there was no definite transection (Table IV). There were 20 cases in which the margins were clear. The 20 patients with clear margins would not need further surgery at the malig-
nancy site. Depending on the histologic findings, they may or may not need axillary lymphadenectomy. Thus the open breast biopsy might be the entire cancer operation required by the patient. Even if axillary node dissection was required, for these 20 patients reexcision of the primary site (lumpectomy) would not be necessary. Evaluation of the lumpectomy specimens of the six patients who had tumor transection at the margin revealed that five had residual carcinoma. None of the eight patients who had tumors at the inked margin but without obvious transection had residual disease in the lumpectomy specimen. Seven of the patients with clear margins had lumpectomy procedures. Six of these seven did not have any residual tumor, whereas one had residual ductal carcinoma in situ. This residual finding was not unexpected because the original biopsy specimen revealed extensive multifocal ductal carcinoma in situ changes. A core needle biopsy–diagnosed breast cancer will require reexcision in all patients. Open breast biopsy in our series resulted in nearly 60% of the patients having clear surgical margins. It can logically be argued that none of these patients would need reexcision (except possibly in the case of multifocal disease). It is also interesting to note that none of the patients with tumor at the inked margin but without obvious transection had residual tumor. Although our series is small, it appears that unless tumor is obviously transected at the margin, it can be assumed that little chance of residual disease exists. Therefore in our series, 28 of the 34 patients could be managed without reexcision. This is a significant difference from core needle biopsy. Identification of primary site. One of the difficulties of core needle biopsy is identification of the primary surgical site. It may not be possible to tell where the primary site was in the breast after core needle biopsy. Open biopsy leads to a precise knowledge of where reexcision, if required, needs to be directed. It may also prove difficult for radiation oncologists to identify the primary site in a patient diagnosed by core needle biopsy. Reynolds et al.2 reported a case of carcinoma diagnosed by core needle biopsy that later lumpectomy found no residual tumor. Reexcision was done, and residual carcinoma was noted at a different site than expected. Cosmetics. No one has addressed in core needle
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biopsy reports the cosmetic issue. Core needle biopsy places three to five, 14-gauge core needles through the breast. This may require small skin incisions. Depending on where they are placed and the patient’s scarring tendencies, this may be less acceptable than a single surgical scar well placed. Most open biopsies can be done with a circumareolar incision. This is cosmetically very acceptable. Often the scar is difficult to see. Most open biopsy scars are small and 4 to 5 cm long. Patient satisfaction and complications. Reports in the literature contrast patient opinions of core needle biopsy versus open biopsy. Our patients expressed no significant complaints. We had no significant complications. No hematomas requiring drainage were present. No infections or abscess occurred. Patient opinion about having five 14-gauge needles placed through the breast is needed. Literature reports core needle biopsy as a complication-free procedure. Given the large blood vessels often encountered during open biopsy, we wonder how core needle biopsy avoids an occasional hematoma, infection, or abscess. Physician responsible for decision making. Management of the patient with an abnormal mammogram does not proceed in a vacuum. Patients with this problem have other issues such as hormonal management, contraception, and pregnancy concerns. The patients need to be able to integrate all of their health concerns, not just those relating to mammographic abnormalities. Although we admit and applaud the radiologist’s expertise in reading mammograms and placing localization wires, it is our belief that the management of the breast disease is done best by clinician with a primary care or surgical background (preferably both). Most core needle biopsies will be done in mammographic centers managed by radiologists. Open surgical biopsy of abnormal mammographic areas can be done by the gynecologist. It is our belief that it is the gynecologist who is best suited to manage this aspect of women’s health care. Comment Although this is not a scientific double-blinded study comparing core needle biopsies with open surgical biopsy, it is our belief that we have made a case that open surgical biopsy with preoperative wire localization technique is the preferred method for management of abnormal mammographic areas. Certainly many of the disadvantages proposed to open biopsy are exaggerated. For the patient who desires the best attempt at surgical accuracy, as well as the possibility of eliminating the need for further surgery beyond the open biopsy, open surgical biopsy is the preferred method. The differences in cost are minimal and may be negated in the total patent population when serial mammograms, follow-up open biopsies, and lumpectomies that may be needed in patients having core needle biopsy are contrasted with those who had open biopsies that do not need such procedures.
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It is our hope that gynecologists and other primary care physicians will properly advise patients that the open surgical biopsy should not be relegated to the historical museum but is an excellent option for the patient with a mammographic abnormality. REFERENCES
1. Brenner RJ, Farardo L, Fisher PR, et al. Percutaneous core biopsy of the breast: effect of operator experience number of samples on diagnostic accuracy. AJR Am J Roentgenol 1996;166:341-6. 2. Reynolds HE, Jackson VP, Gin FM, et al. Large gauge core needle biopsy of the breast. Breast J 1996;2:370-3. 3. Cross MJ, Evans WP, Peters GN, et al. Sterotactic breast biopsy as an alternative to open excisional biopsy. Ann Surg Oncol 1995;2:195-200. 4. Liberman L, Fahs MC, Denshaw DD, et al. Impact of stereotaxic core breast biopsy on cost of diagnosis. Radiology 1995;195: 633-7.
Editors’ note: This manuscript was revised after these discussions were presented. Discussion DR. JAMES R. DOLAN, Park Ridge, Illinois. Hall et al. report a retrospective review of their experience with 461 open needle-localized breast biopsies over a 16-year period. The range of positivity (malignancy) in the literature for nonpalpable mammographically suspicious lesions is 20% to 30%. Stereotactic core needle biopsies have been advocated for the diagnosis of “benign-appearing” lesions and also lesions that are “highly suggestive of malignancy.” Reported advantages of stereotactic core needle biopsies are numerous and include lower cost of the procedure, less patient inconvenience, minimal recovery, minimal patient discomfort, and overall greater patient satisfaction. Disadvantages of stereotactic core needle are listed by Hall et al. and include the appropriate role of stereotactic core needle biopsy is not yet clearly determined, abnormal lesions are not removed, the surgeon is removed from the dominant decision-making role, all patients with a positive result still need excisional biopsy, and a steep learning curve for the performing radiologists exists. Other disadvantages are a reported 2.3% to 6.6% false-negative rate, difficulty with differentiation between in situ and invasive lesions, minimum of five passes with a 14-gauge needle lead to patient dissatisfaction, and patients’ anxiety over the requirement for a follow-up interval mammogram. Hall et al. discuss the advantages of needle-localized open biopsy as increased accuracy, increased specimen adequacy, the excision may serve as the definitive lumpectomy for most patients if cancer is detected, and the entire lesion is removed and examined histologically. Stereotactic core needle biopsy suite/service was not available at the author’s institution; therefore no randomized comparisons can be obtained. Sixty-seven cancers (67/461, 15%) were detected in their series. They reported three surgical misses, and all three patients were subsequently found to have benign disease. All
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biopsies were performed as an outpatient and with local anesthesia. No complications and excellent cosmesis were reported. These results compare similarly to our experience; however, we prefer to perform our biopsies, especially for deep lesions, with local anesthesia and intravenous sedation. Stolier recently reported his experience with 244 stereotactic core needle biopsies from 1993 to 1996. He analyzed his data regarding the mammographic indication for biopsy. Those patients with suspicious microcalcifications had a positive stereotactic core needle biopsy rate of 18.4%. Of those with a mammographically “probably benign mass” the cancer positivity rate by stereotactic core needle biopsy was only 1.8%. The interpreting radiologist’s threshold for abnormality is variable and is an important determinant as to which diagnostic modality is preferable. The American College of Radiology has developed and endorsed the Breast Imaging Reporting and Data System to standardize terminology regarding mammographic assessment categories. In my opinion it is important to remember that stereotactic core needle biopsy is a diagnostic and not a therapeutic procedure. A recent report entitled Stereotactic Core Needle Biopsy of the Breast: A Report of the Joint Task Force published in CA, A Cancer Journal For Clinicians (1997;47:171-90) further defines the role of stereotactic core needle biopsy, needle-localized open biopsy, and their indications and contraindications. Other recommendations include appropriate follow-up guidelines and recommendations for interval mammogram and specimen handling. Management algorithms that use both biopsy techniques are endorsed and are equally useful. None of the papers I reviewed in preparation of this discussion suggested or advocated that either stereotactic core needle biopsy or needle-localized excisional open biopsies should be relegated to the historical museum at the exclusion of the other technique contrary to Dr. Hall’s claim. Both procedures have usefulness in the clinical armamentarium for the management of mammographically detected abnormalities and have specific usefulness on the basis of proper patient selection and after complete and thorough counseling of the patient. Dr. Hall and his coauthors report very succinctly their experience, and I congratulate them on their efforts. My questions for Dr. Hall are as follows: 1. Is there any role for stereotactic needle core biopsy in his opinion? 2. In a patient with a highly suspicious mammographic lesion, could stereotactic core needle biopsy before definitive therapy possibly be helpful when the patient undergoes counseling regarding her various acceptable treatment options? SUGGESTED READINGS
Bassett L, Winchester DP, et al. Stereotactic core-needle biopsy of the breast: a report of the Joint Task Force of the American College of Radiology, American College of Surgeons, and College of American Pathologists. CA Cancer J Clin 1997;47: 171-90. Fajardo LL, DeAngelis GA. The role of stereotactic biopsy in ab-
Hall et al. 1249
normal mammograms. Surg Oncol Clin North Am 1997;6:28599. Frazee RC, Roberts JW, et al. Open versus stereotactic breast biopsy. Am J Surg 1996;172:491-5. Morrow M, Schmidt R, et al. Preoperative evaluation of abnormal mammographic findings to avoid unnecessary breast biopsies. Arch Surg 1994;129:1091-6. Stolier AJ. Stereotactic breast biopsy: a surgical series. J Am Coll Surg 1997;185:224-8. Wallace JE, Sayler C, et al. The role of stereotactic biopsy in assessment of nonpalpable breast lesions. Am J Surg 1996;171:471-3.
DR. JOHN KNAUS, Skokie, Illinois. Compared with open breast biopsy, stereotactic needle biopsy has been proposed as a less invasive and more cost-effective method of delineating the pathologic nature of nonpalpable, suspicious mammographic lesions. This is reasonable considering 500,000 to 1 million excisional breast biopsies are done each year, with 300,000 to 900,000 being benign. The authors present their experience with 461 needlelocalized open breast biopsies performed over 17 years to validate the continued clinical importance of this procedure. The authors make four main points in comparing open breast biopsies with stereotactic core breast biopsies: 1. Stereotactic biopsies may create the possibility of “multiphysician” care for the patient. 2. Stereotactic biopsies may provide less than optimal results when the abnormal lesion is small, when there are multiple lesions, or when an insufficient specimen may be recovered for pathologic examination. 3. The patient may have a negative experience. 4. The cost difference reported in this review is less than quoted elsewhere in the literature. The management of breast disease always requires individualized clinical decisions. The ideal choice for diagnosing the nature of suspicious, nonpalpable mammographically detected breast lesions has yet to be defined. Open biopsy has obvious advantages but significant cost and many benign diagnoses. Stereotactic breast biopsies and the newer large core/excisional biopsy have advantages in many circumstances. Questions for the authors: 1. Is complete excision of highly suspicious lesions compromised by all biopsies being performed with local anesthesia? 2. What are the authors’ current criteria for stereotactic biopsy referral in their practice? 3. With the report of this large community hospital breast surgical experience, do these authors believe these procedures are safely applicable to university obstetrics-gynecology teaching programs? DR. ROBERT K. ZURAWIN, Houston, Texas. I am struck by the emotionality of these arguments, and I have several questions for Dr. Hall. The biopsy techniques discussed here are reminiscent for gynecologists of the early discussions of laparoscopy versus laparotomy. Nobody argues that laparotomy is the “gold standard” for gynecologic surgery, but anybody older
1250 Hall et al.
than 50 who has ever performed laparoscopy and was not trained in it in their residency probably can appreciate the steep learning curve and that that should not be a deterrent for using a viable technique or a cone biopsy versus colposcopy and more conservative techniques. I think that insufficient attention has been paid to the fact that many of these women require multiple biopsies. Almost all of them result in scarring and distortion of the breast tissue, which makes detection of future lesions more difficult, and although it is not indicated for everybody, for example, women with small breasts or lesions near the chest wall, I would like the authors to please comment on those aspects. In other words, patient experience. For example, with multiple biopsies, the woman never sees the needle going in. She is lying flat on the table. Can you address those issues of an analogy between a possibly very useful technique and the emotionality of the argument? DR. HALL (Closing). I thank the discussants for their comments and support. Two of the questions were the same: What is the role of stereotaxis in our practice? In our hospital, our radiologists—and it is a small community hospital—do not have a stereotactic unit. They are in the beginning of this steep learning curve, and they have elected not to become involved in it. So in our practice, we do not have any role for that right now, but I guess the one place where a stereotactic biopsy perhaps would play a role is in the patient who for one reason or another you have already decided or the patient has already decided she would rather have a mastectomy rather than lumpectomy, and the stereotactic biopsy could go ahead and make the diagnosis in a highly suspicious lesion. Other than that, I guess in my naive way, I just do not really know at this point where stereotaxis fits, although I am sure over time maybe it will have a role that even I will figure out; however, at this time, the open biopsies have just not proven to be that morbid of a procedure and the cosmetics—and yes, some of these patients will have multiple biopsies. It is a very emotionally charged issue and it is extremely important that we do not relegate our patients to our friends, the radiologists, because these pa-
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tients are scared to death and they have lots of questions regarding could this be my estrogen and should I ever get pregnant again. Before you know it, they are getting their answers from other places than from us. So at this point the stereotactic role in my practice is extremely limited. I do not believe that we compromise the later reoperations, if I understood the one question, as far as going back later. We try not to take too big a piece of tissue, but we also try to take enough tissue so that if it is malignant, we can perhaps save the patient a return trip to the operating room. So we do evaluate margins very close. We get specimens radiographically. We work very hard to make sure that we have got the lesion in question out and we try to get margins or at least evaluate margins because many of these lesions are extremely small, and the biopsy itself may be the only surgery that the patient does need. I agree with Dr. Knaus that the way it looks in breast management, the axillary left node dissection is rapidly going to be in a museum or at least a sentinel node or something. So the surgery for breast disease is becoming less and less. Therefore it becomes more and more doable for current obstetrician-gynecologists, and yes, I would encourage university teaching programs to make it part of their program. I think that is more of a turf battle at a teaching center than it is a reality battle. I think this is a part of practice that blends into what we should be doing. It is certainly something we are surgically able to do, and it should start at the university teaching level by teaching residents to do these procedures. That learning curve will then fall over to the rest of us in private practice. It has not been a difficult thing as far as getting patients to accept this, and we have had very few patients who have come back and said this was just a horrible experience. We have had a few patients who have gone down the road to the big breast center at the next nearby town and have come back and said, “I’ll never do that again because I felt like a shish kebab laying there on the table and being skewered.” So it is just a question of which way do you want to go for your patients; and I think we need to take a more active role in advising our patients of the options.
Key words: Open surgical biopsy, core needle biopsy
Approximately 500,000 breast biopsies are done per year in the United States. Biopsies for nonpalpable mammographic abnormalities have become an increasingly significant proportion of this number. We will address only nonpalpable mammographic abnormalities leading to breast biopsy. Approximately 20% to 30% of these biopsies result in the discovery of a breast malignancy. The standard of care has been an open surgical biopsy with preoperative lesion localization by wire placement under mammographic guidance. A move is under way to obtain tissue through “less invasive” procedures such as core needle biopsies, usually under stereotaxic mammographic guidance. This process generally removes the surgeon from his or her dominant role in the care and the management of the breast lesion. Proponents of core needle biopsy cite several advantages over open surgical biopsies. These include lower cost, patient convenience, and satisfaction. Core needle biopsy is marketed to the public as a nonsurgical option for the patient with a nonpalpable mammographic abnormality. The purpose of this article is to compare open surgical biopsy as performed in a community hospital with core needle biopsy. Most of the articles contrasting core needle biopsy with open surgical biopsy paint a very unfavorable picture of open biopsy with regard to cost, patient convenience, and recovery.
From The Women’s Health Center of Logansport. Community Hospital Award paper, presented at the Sixty-fifth Annual Meeting of The Central Association of Obstetricians and Gynecologists, Scottsdale, Arizona, October 29–November 1, 1997. Reprint requests: James A. Hall, MD, Women’s Health Center of Logansport, Suite 170, 1201 Michigan Ave., Logansport, IN 46947. Copyright © 1998 by Mosby, Inc. 0002-9378/98 $5.00 + 0 6/6/90428
It is our contention that open surgical biopsy compares favorably to core needle biopsy with regard to cost, patient convenience, and recovery. Open biopsy also has advantages regarding accuracy and specimen adequacy. It may also eliminate the further need for cancer surgery in a significant percentage of patients. Material and methods Patients cared for at the Women’s Health Center of Logansport who had an abnormal mammogram for which the radiologist recommended tissue biopsy were subjected to open surgical biopsy with preoperative wire localization technique. The wire is placed mammographically by radiology immediately preoperatively. The biopsies are done with the patient under local anesthesia in an outpatient treatment room. Patients receive no sedation and require no anesthesia other than local. Patients are released to full activities. Specimen radiography is obtained to ensure an adequate specimen if the original abnormality contained microcalcifications. Adequate removal of the mammographic abnormality is confirmed by either specimen radiography or postbiopsy mammogram at 4 to 6 months. Frozen-section diagnosis was not performed. The specimen was taken fresh to the pathology laboratory and the margins were inked to evaluate later in case of malignancy. All the biopsies were done by the physician authors obstetrician-gynecologists at the Women’s Health Center of Logansport. A total of 461 open surgical biopsies were carried out for abnormal mammographic lesions from 1980 through 1996 (Table I); 164 of the 461 biopsies were from 1993 through 1996 (Table II). All biopsies were done at Memorial Hospital, Logansport, Indiana. A stereotaxic core needle biopsy service is not available at our hospital. We have no per1245
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Table I. Open surgical biopsy for nonpalpable mammographic abnormalities at Women’s Health Center of Logansport, 1980 through 1996 Year
No. of biopsies
No. of malignancies
1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996
1 2 4 3 18 24 8 15 16 13 69 87 37 30 33 40 61 461
0 0 0 0 0 3 1 2 3 4 6 9 5 7 8 7 12 67 (15%)
TOTAL
Table II. Open surgical biopsy for nonpalpable mammographic abnormalities at Women’s Health Center of Logansport, 1993 through 1996 Year 1993 1994 1995 1996 TOTAL
No. of biopsies
No. of malignancies
30 33 40 61 164
7 8 7 12 34 (21%)
sonal experience with this technique. Information regarding core needle biopsy has been obtained either from the literature or personal communication. Results Results will be discussed in several areas. Accuracy. Since 1980, 461 open breast biopsies have been performed by the gynecologists at the Women’s Health Center of Logansport. This resulted in the discovery of 67 cancers (15%) (Table I). The percentage of discovered malignancies increased in the period from 1993 through 1996 to 21% of biopsies (34 cancers from 164 biopsies) (Table II). We have had three surgical misses (0.6%) in 461 biopsies (Table III). A surgical miss is defined as the persistence of the abnormal mammographic area after biopsy. All three failures underwent a successful biopsy with a second attempt and were benign. The cause of the failure involved localization problems of the original target lesion. Two patients had the wrong microcalcified area localized and the third experienced migration of the wire preoperatively. Core needle biopsy surgical miss statistics are unclear in the literature. Because the core biopsies do not always remove the entire lesion, some
Table III. Surgical misses (failures to remove target lesion) at open biopsy for nonpalpable mammographic abnormalities at Women’s Health Center of Logansport, 1980 through 1996 Failure No. of biopsies
No.
461
3
% 0.6
residual of the target lesion may be expected to remain after biopsy. It is a leap of faith to assume that what remains in the breast matches pathologically with the tissue that was removed. Brenner et al.1 reported a combined series of core needle biopsies from 10 breast centers with a 97% overall accuracy (3% false negative) compared with immediate excisional biopsy after the core needle biopsy with five tissue core samples. Reynolds et al.2 reported up to a 6.6% false-negative rate. It is generally agreed that the learning curve with core needle biopsy is steep and that over time the false-negative rate reduces. When surgical accuracy was compared, open surgical biopsy has an advantage over core needle biopsy. Proponents of core needle biopsy rely on the fact that most of the biopsy results are going to be benign and therefore a slightly lessened accuracy rate is acceptable. One wonders how acceptable this decreased ability to remove the target lesion is if the patient is or is not a member of one’s own family. The advantage to open biopsy is that the entire target lesion can be removed for adequate histologic sampling. Core needle biopsy also is limited by interpretation of samples when either atypical hyperplasia or in situ changes are encountered. Differentiation between in situ carcinoma and invasive carcinoma with core needle biopsy is not possible unless definite invasive changes are noted. Patients with atypical ductal hyperplasia or in situ carcinoma on core needle biopsy will need open biopsy to rule out invasive malignancy, whereas patients with open biopsy will not need further surgery because of removal of the entire target lesion. Cost. Cross et al.3 stated that the core needle biopsy average cost is $1200. Personal communication with an Indianapolis-based breast center confirms this figure. The $1200 charge includes the facility, biopsy, and radiology charges. It does not include pathologic examination. Costs of open surgical biopsy performed by the Women’s Health Center of Logansport have been reviewed from 1993 to 1996. The average total expense for surgeon’s fee, hospital charges, and radiology was $1400. Fees for pathologic studies were excluded. This contrasts with many literature reports that open biopsy costs range in the several thousand dollar area. Thus the cost differential appears to be approximately $200 per procedure, or approximately 16%. Liberman et al.4 reported that
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Table IV. Relationship of margin to residual disease after open surgical biopsy nonpalpable mammographic abnormality at Women’s Health Center of Logansport, 1993 through 1996 Biopsy margin and No. of cases Tumor transected (n = 6) Tumor at inked margin (n = 8) Margins clear (n = 20)(7 patients had subsequent lumpectomy)
Residual tumor 5 0 1
No residual tumor 1 8 6
Total cancers biopsied: 34.
core needle biopsy costs are 50% lower than open biopsy. We do not find Liberman’s4 cost estimates to be accurate. Literature review of cost estimates favoring core needle biopsy also do not take total costs into account. Management of some patients with abnormal areas with core needle biopsy will ultimately have increased costs not required of those who have open surgical biopsy. These extra costs are not included in literature reviews and relate to serial postbiopsy mammograms and further surgery required of some core needle biopsy patients. Patients having core needle biopsy may be required to have serial mammograms after biopsy, secondary to the need to follow the residual target lesion remaining in the breast. There are extra costs secondary to the need for open biopsy for areas showing atypical changes. The patients with open surgical biopsies also do not need further cancer surgery if the biopsy produced clear margins. All patients with core needle biopsy discovered malignancies will need further surgery. Liberman4 quoted costs relating to open biopsy to include preoperative testing, inpatient days, and days lost from work. None of these factors are relative to open biopsy in our series. There was no preoperative testing, inpatient days, or days lost from work. Therefore any cost comparison with these factors should be the same as core needle biopsy. When all of these factors are taken into account, especially the need for open surgical biopsy or lumpectomy in some patients who have had core needle biopsy, it appears that the $200 differential in the original procedure may be lost in later charges. Specimen adequacy if malignant. Invasive or in situ breast carcinoma will not be totally excised by core needle biopsy. The patients with diagnosis made in this manner will need further excision (lumpectomy). From 1993 through 1996, 34 breast cancers were discovered in our series (Table II). All these nonpalpable mammographic abnormalities were diagnosed by open breast biopsy technique. There were six cases in which tumor was obviously transected at the margin. There were eight cases in which tumor cells approached the inked margin, but there was no definite transection (Table IV). There were 20 cases in which the margins were clear. The 20 patients with clear margins would not need further surgery at the malig-
nancy site. Depending on the histologic findings, they may or may not need axillary lymphadenectomy. Thus the open breast biopsy might be the entire cancer operation required by the patient. Even if axillary node dissection was required, for these 20 patients reexcision of the primary site (lumpectomy) would not be necessary. Evaluation of the lumpectomy specimens of the six patients who had tumor transection at the margin revealed that five had residual carcinoma. None of the eight patients who had tumors at the inked margin but without obvious transection had residual disease in the lumpectomy specimen. Seven of the patients with clear margins had lumpectomy procedures. Six of these seven did not have any residual tumor, whereas one had residual ductal carcinoma in situ. This residual finding was not unexpected because the original biopsy specimen revealed extensive multifocal ductal carcinoma in situ changes. A core needle biopsy–diagnosed breast cancer will require reexcision in all patients. Open breast biopsy in our series resulted in nearly 60% of the patients having clear surgical margins. It can logically be argued that none of these patients would need reexcision (except possibly in the case of multifocal disease). It is also interesting to note that none of the patients with tumor at the inked margin but without obvious transection had residual tumor. Although our series is small, it appears that unless tumor is obviously transected at the margin, it can be assumed that little chance of residual disease exists. Therefore in our series, 28 of the 34 patients could be managed without reexcision. This is a significant difference from core needle biopsy. Identification of primary site. One of the difficulties of core needle biopsy is identification of the primary surgical site. It may not be possible to tell where the primary site was in the breast after core needle biopsy. Open biopsy leads to a precise knowledge of where reexcision, if required, needs to be directed. It may also prove difficult for radiation oncologists to identify the primary site in a patient diagnosed by core needle biopsy. Reynolds et al.2 reported a case of carcinoma diagnosed by core needle biopsy that later lumpectomy found no residual tumor. Reexcision was done, and residual carcinoma was noted at a different site than expected. Cosmetics. No one has addressed in core needle
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biopsy reports the cosmetic issue. Core needle biopsy places three to five, 14-gauge core needles through the breast. This may require small skin incisions. Depending on where they are placed and the patient’s scarring tendencies, this may be less acceptable than a single surgical scar well placed. Most open biopsies can be done with a circumareolar incision. This is cosmetically very acceptable. Often the scar is difficult to see. Most open biopsy scars are small and 4 to 5 cm long. Patient satisfaction and complications. Reports in the literature contrast patient opinions of core needle biopsy versus open biopsy. Our patients expressed no significant complaints. We had no significant complications. No hematomas requiring drainage were present. No infections or abscess occurred. Patient opinion about having five 14-gauge needles placed through the breast is needed. Literature reports core needle biopsy as a complication-free procedure. Given the large blood vessels often encountered during open biopsy, we wonder how core needle biopsy avoids an occasional hematoma, infection, or abscess. Physician responsible for decision making. Management of the patient with an abnormal mammogram does not proceed in a vacuum. Patients with this problem have other issues such as hormonal management, contraception, and pregnancy concerns. The patients need to be able to integrate all of their health concerns, not just those relating to mammographic abnormalities. Although we admit and applaud the radiologist’s expertise in reading mammograms and placing localization wires, it is our belief that the management of the breast disease is done best by clinician with a primary care or surgical background (preferably both). Most core needle biopsies will be done in mammographic centers managed by radiologists. Open surgical biopsy of abnormal mammographic areas can be done by the gynecologist. It is our belief that it is the gynecologist who is best suited to manage this aspect of women’s health care. Comment Although this is not a scientific double-blinded study comparing core needle biopsies with open surgical biopsy, it is our belief that we have made a case that open surgical biopsy with preoperative wire localization technique is the preferred method for management of abnormal mammographic areas. Certainly many of the disadvantages proposed to open biopsy are exaggerated. For the patient who desires the best attempt at surgical accuracy, as well as the possibility of eliminating the need for further surgery beyond the open biopsy, open surgical biopsy is the preferred method. The differences in cost are minimal and may be negated in the total patent population when serial mammograms, follow-up open biopsies, and lumpectomies that may be needed in patients having core needle biopsy are contrasted with those who had open biopsies that do not need such procedures.
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It is our hope that gynecologists and other primary care physicians will properly advise patients that the open surgical biopsy should not be relegated to the historical museum but is an excellent option for the patient with a mammographic abnormality. REFERENCES
1. Brenner RJ, Farardo L, Fisher PR, et al. Percutaneous core biopsy of the breast: effect of operator experience number of samples on diagnostic accuracy. AJR Am J Roentgenol 1996;166:341-6. 2. Reynolds HE, Jackson VP, Gin FM, et al. Large gauge core needle biopsy of the breast. Breast J 1996;2:370-3. 3. Cross MJ, Evans WP, Peters GN, et al. Sterotactic breast biopsy as an alternative to open excisional biopsy. Ann Surg Oncol 1995;2:195-200. 4. Liberman L, Fahs MC, Denshaw DD, et al. Impact of stereotaxic core breast biopsy on cost of diagnosis. Radiology 1995;195: 633-7.
Editors’ note: This manuscript was revised after these discussions were presented. Discussion DR. JAMES R. DOLAN, Park Ridge, Illinois. Hall et al. report a retrospective review of their experience with 461 open needle-localized breast biopsies over a 16-year period. The range of positivity (malignancy) in the literature for nonpalpable mammographically suspicious lesions is 20% to 30%. Stereotactic core needle biopsies have been advocated for the diagnosis of “benign-appearing” lesions and also lesions that are “highly suggestive of malignancy.” Reported advantages of stereotactic core needle biopsies are numerous and include lower cost of the procedure, less patient inconvenience, minimal recovery, minimal patient discomfort, and overall greater patient satisfaction. Disadvantages of stereotactic core needle are listed by Hall et al. and include the appropriate role of stereotactic core needle biopsy is not yet clearly determined, abnormal lesions are not removed, the surgeon is removed from the dominant decision-making role, all patients with a positive result still need excisional biopsy, and a steep learning curve for the performing radiologists exists. Other disadvantages are a reported 2.3% to 6.6% false-negative rate, difficulty with differentiation between in situ and invasive lesions, minimum of five passes with a 14-gauge needle lead to patient dissatisfaction, and patients’ anxiety over the requirement for a follow-up interval mammogram. Hall et al. discuss the advantages of needle-localized open biopsy as increased accuracy, increased specimen adequacy, the excision may serve as the definitive lumpectomy for most patients if cancer is detected, and the entire lesion is removed and examined histologically. Stereotactic core needle biopsy suite/service was not available at the author’s institution; therefore no randomized comparisons can be obtained. Sixty-seven cancers (67/461, 15%) were detected in their series. They reported three surgical misses, and all three patients were subsequently found to have benign disease. All
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biopsies were performed as an outpatient and with local anesthesia. No complications and excellent cosmesis were reported. These results compare similarly to our experience; however, we prefer to perform our biopsies, especially for deep lesions, with local anesthesia and intravenous sedation. Stolier recently reported his experience with 244 stereotactic core needle biopsies from 1993 to 1996. He analyzed his data regarding the mammographic indication for biopsy. Those patients with suspicious microcalcifications had a positive stereotactic core needle biopsy rate of 18.4%. Of those with a mammographically “probably benign mass” the cancer positivity rate by stereotactic core needle biopsy was only 1.8%. The interpreting radiologist’s threshold for abnormality is variable and is an important determinant as to which diagnostic modality is preferable. The American College of Radiology has developed and endorsed the Breast Imaging Reporting and Data System to standardize terminology regarding mammographic assessment categories. In my opinion it is important to remember that stereotactic core needle biopsy is a diagnostic and not a therapeutic procedure. A recent report entitled Stereotactic Core Needle Biopsy of the Breast: A Report of the Joint Task Force published in CA, A Cancer Journal For Clinicians (1997;47:171-90) further defines the role of stereotactic core needle biopsy, needle-localized open biopsy, and their indications and contraindications. Other recommendations include appropriate follow-up guidelines and recommendations for interval mammogram and specimen handling. Management algorithms that use both biopsy techniques are endorsed and are equally useful. None of the papers I reviewed in preparation of this discussion suggested or advocated that either stereotactic core needle biopsy or needle-localized excisional open biopsies should be relegated to the historical museum at the exclusion of the other technique contrary to Dr. Hall’s claim. Both procedures have usefulness in the clinical armamentarium for the management of mammographically detected abnormalities and have specific usefulness on the basis of proper patient selection and after complete and thorough counseling of the patient. Dr. Hall and his coauthors report very succinctly their experience, and I congratulate them on their efforts. My questions for Dr. Hall are as follows: 1. Is there any role for stereotactic needle core biopsy in his opinion? 2. In a patient with a highly suspicious mammographic lesion, could stereotactic core needle biopsy before definitive therapy possibly be helpful when the patient undergoes counseling regarding her various acceptable treatment options? SUGGESTED READINGS
Bassett L, Winchester DP, et al. Stereotactic core-needle biopsy of the breast: a report of the Joint Task Force of the American College of Radiology, American College of Surgeons, and College of American Pathologists. CA Cancer J Clin 1997;47: 171-90. Fajardo LL, DeAngelis GA. The role of stereotactic biopsy in ab-
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normal mammograms. Surg Oncol Clin North Am 1997;6:28599. Frazee RC, Roberts JW, et al. Open versus stereotactic breast biopsy. Am J Surg 1996;172:491-5. Morrow M, Schmidt R, et al. Preoperative evaluation of abnormal mammographic findings to avoid unnecessary breast biopsies. Arch Surg 1994;129:1091-6. Stolier AJ. Stereotactic breast biopsy: a surgical series. J Am Coll Surg 1997;185:224-8. Wallace JE, Sayler C, et al. The role of stereotactic biopsy in assessment of nonpalpable breast lesions. Am J Surg 1996;171:471-3.
DR. JOHN KNAUS, Skokie, Illinois. Compared with open breast biopsy, stereotactic needle biopsy has been proposed as a less invasive and more cost-effective method of delineating the pathologic nature of nonpalpable, suspicious mammographic lesions. This is reasonable considering 500,000 to 1 million excisional breast biopsies are done each year, with 300,000 to 900,000 being benign. The authors present their experience with 461 needlelocalized open breast biopsies performed over 17 years to validate the continued clinical importance of this procedure. The authors make four main points in comparing open breast biopsies with stereotactic core breast biopsies: 1. Stereotactic biopsies may create the possibility of “multiphysician” care for the patient. 2. Stereotactic biopsies may provide less than optimal results when the abnormal lesion is small, when there are multiple lesions, or when an insufficient specimen may be recovered for pathologic examination. 3. The patient may have a negative experience. 4. The cost difference reported in this review is less than quoted elsewhere in the literature. The management of breast disease always requires individualized clinical decisions. The ideal choice for diagnosing the nature of suspicious, nonpalpable mammographically detected breast lesions has yet to be defined. Open biopsy has obvious advantages but significant cost and many benign diagnoses. Stereotactic breast biopsies and the newer large core/excisional biopsy have advantages in many circumstances. Questions for the authors: 1. Is complete excision of highly suspicious lesions compromised by all biopsies being performed with local anesthesia? 2. What are the authors’ current criteria for stereotactic biopsy referral in their practice? 3. With the report of this large community hospital breast surgical experience, do these authors believe these procedures are safely applicable to university obstetrics-gynecology teaching programs? DR. ROBERT K. ZURAWIN, Houston, Texas. I am struck by the emotionality of these arguments, and I have several questions for Dr. Hall. The biopsy techniques discussed here are reminiscent for gynecologists of the early discussions of laparoscopy versus laparotomy. Nobody argues that laparotomy is the “gold standard” for gynecologic surgery, but anybody older
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than 50 who has ever performed laparoscopy and was not trained in it in their residency probably can appreciate the steep learning curve and that that should not be a deterrent for using a viable technique or a cone biopsy versus colposcopy and more conservative techniques. I think that insufficient attention has been paid to the fact that many of these women require multiple biopsies. Almost all of them result in scarring and distortion of the breast tissue, which makes detection of future lesions more difficult, and although it is not indicated for everybody, for example, women with small breasts or lesions near the chest wall, I would like the authors to please comment on those aspects. In other words, patient experience. For example, with multiple biopsies, the woman never sees the needle going in. She is lying flat on the table. Can you address those issues of an analogy between a possibly very useful technique and the emotionality of the argument? DR. HALL (Closing). I thank the discussants for their comments and support. Two of the questions were the same: What is the role of stereotaxis in our practice? In our hospital, our radiologists—and it is a small community hospital—do not have a stereotactic unit. They are in the beginning of this steep learning curve, and they have elected not to become involved in it. So in our practice, we do not have any role for that right now, but I guess the one place where a stereotactic biopsy perhaps would play a role is in the patient who for one reason or another you have already decided or the patient has already decided she would rather have a mastectomy rather than lumpectomy, and the stereotactic biopsy could go ahead and make the diagnosis in a highly suspicious lesion. Other than that, I guess in my naive way, I just do not really know at this point where stereotaxis fits, although I am sure over time maybe it will have a role that even I will figure out; however, at this time, the open biopsies have just not proven to be that morbid of a procedure and the cosmetics—and yes, some of these patients will have multiple biopsies. It is a very emotionally charged issue and it is extremely important that we do not relegate our patients to our friends, the radiologists, because these pa-
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tients are scared to death and they have lots of questions regarding could this be my estrogen and should I ever get pregnant again. Before you know it, they are getting their answers from other places than from us. So at this point the stereotactic role in my practice is extremely limited. I do not believe that we compromise the later reoperations, if I understood the one question, as far as going back later. We try not to take too big a piece of tissue, but we also try to take enough tissue so that if it is malignant, we can perhaps save the patient a return trip to the operating room. So we do evaluate margins very close. We get specimens radiographically. We work very hard to make sure that we have got the lesion in question out and we try to get margins or at least evaluate margins because many of these lesions are extremely small, and the biopsy itself may be the only surgery that the patient does need. I agree with Dr. Knaus that the way it looks in breast management, the axillary left node dissection is rapidly going to be in a museum or at least a sentinel node or something. So the surgery for breast disease is becoming less and less. Therefore it becomes more and more doable for current obstetrician-gynecologists, and yes, I would encourage university teaching programs to make it part of their program. I think that is more of a turf battle at a teaching center than it is a reality battle. I think this is a part of practice that blends into what we should be doing. It is certainly something we are surgically able to do, and it should start at the university teaching level by teaching residents to do these procedures. That learning curve will then fall over to the rest of us in private practice. It has not been a difficult thing as far as getting patients to accept this, and we have had very few patients who have come back and said this was just a horrible experience. We have had a few patients who have gone down the road to the big breast center at the next nearby town and have come back and said, “I’ll never do that again because I felt like a shish kebab laying there on the table and being skewered.” So it is just a question of which way do you want to go for your patients; and I think we need to take a more active role in advising our patients of the options.