Annals of Surgical Oncology 9:654-662 (2002)
© 2002 Society of Surgical Oncology
Sensory Morbidity After Sentinel Lymph Node Biopsy and Axillary Dissection: A Prospective Study of 233 Women
Larissa K. F. Temple, MD, MSc,
Roberta Baron, MSN, AOCN©,
Hiram S. Cody, III, MD,
Jane V. Fey, MPH,
Howard T. Thaler, PhD,
Patrick I. Borgen, MD,
Alexander S. Heerdt, MD,
Leslie L. Montgomery, MD,
Jeanne A. Petrek, MD and
Kimberly J. Van Zee, MS, MD
From the Department of Surgery (LKFT), Breast Service (RB, HSC, JVF, PIB, AH, LM, JAP, KJVZ), and the Department of Biostatistics (HTT), Memorial Sloan-Kettering Cancer Center, New York, New York.
Correspondence: Address correspondence and reprint requests to: Kimberly J. Van Zee, MS, MD, FACS, 1275 York Ave., MRI 1026, New York, NY 10021; Fax: 212-794-5812; E-mail: vanzeek{at}mskcc.org
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ABSTRACT
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Background: We prospectively compared the sensory morbidity and lymphedema experienced after sentinel node biopsy (SLNB) and axillary dissection (ALND) over a 12-month period by using a validated instrument.
Methods: Patients undergoing breast-conserving therapy completed the Breast Sensation Assessment Scale (BSAS) at baseline and 3, 6, and 12 months after surgery. Repeated-measures analysis of variance was used to compare ALND and SLNB over the 12-month period. Upper- and lower-arm circumference measurements at baseline and 12 months were used to assess lymphedema.
Results: SLNB was associated with substantial sensory morbidity, although significantly less than ALND, over time on all four subscales and the summary score. A statistically significant improvement in sensory morbidity occurred for both groups in the first 3 months, with no further change thereafter. For both types of axillary surgery, younger patients had significantly higher BSAS scores than older patients. There was no significant difference in arm circumference between patients with SLNB and ALND at 12 months.
Conclusions: Among women undergoing breast-conserving therapy, SLNB has significant sensory morbidity, although approximately half that of ALND. Sensory morbidity improves in the first 3 months after surgery, but patients continue to report sensory morbidity at 1 year. Longitudinal follow-up is required to further assess lymphedema.
Key Words: Sentinel lymph node biopsy • Axillary dissection • Morbidity • Breast cancer
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INTRODUCTION
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Axillary lymph node dissection (ALND) has traditionally been the gold standard for staging the axilla in breast cancer patients. The morbidity of ALND has been well documented, with two recent studies reporting 55%1 to 72%2 of women reporting long-term sensory changes and 11%1 to 73%2 reporting mobility changes. Lymphedema was also demonstrated to be a significant long-term sequela of ALND in a recently published 20-year study of consecutively treated patients, which found that 49% of patients have the sensation of arm swelling and two thirds have documented changes in arm circumference.3 In addition to the presence of these morbidities, validated measures have demonstrated that patients with lymphedema4 or decreased range of motion5 have a lower quality of life.
Sentinel lymph node biopsy (SLNB) has been adopted as an alternative method of staging the axilla in women with breast cancer. A recent survey of the Fellows of the American College of Surgeons showed that 77% of responding surgeons reported use of SLNB.6 Although the morbidity of SLNB is believed to be less than that of ALND, it has not been well studied. The morbidity has been described in a series of 90 patients with SLNB who reported discomfort, shoulder dysfunction, and sensory changes.7 The morbidity of SLNB and ALND have been compared in two studies, with lower levels of numbness,8,9 pain, 8 delay in return to work,9 and impaired mobility8 reported in patients who underwent SLNB. These studies, however, were retrospective, small (ALND = 35, SLNB = 358; ALND = 48, SLNB = 489), used no validated measure, and surveyed patients at variable points of time after surgery. The incidence and severity of lymphedema after SLNB have recently been reported.8–11 These preliminary data suggest that lymphedema occurs after SLNB, although less often than after ALND.9–11
Although SLNB is generally assumed to be less morbid, it was our clinical impression that patients reported more symptoms than anticipated after this procedure. Although the morbidity of SLNB is likely less than that seen after ALND, an understanding of the quality, quantity, and time course of the sensory morbidity is important for patient education. We undertook a prospective study to evaluate the sensory morbidity and incidence of lymphedema resulting from SLNB and compared it with that associated with conventional ALND after SLNB.
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METHODS
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Patient Population
Patients were prospectively accrued between November 1, 1999, and November 1, 2000, at Memorial Sloan-Kettering Cancer Center (MSKCC). To study the specific sensory morbidity of axillary surgery as distinct from sensations resulting from breast surgery, only patients who had undergone breast-conserving therapy (BCT) were included in this study. Therefore, patients were eligible to participate if they had BCT with SLNB or BCT with SLNB followed by immediate or delayed ALND. Patients were excluded if they were <18 years old or had had surgery for a prior breast cancer, bilateral breast surgery, or preoperative chemotherapy.
After approval of the study by the Institutional Review Board at MSKCC, a full-time research study assistant identified eligible patients and recruited them at their initial postoperative visit (3–15 days after surgery). Basic demographic data, including age, stage, adjuvant therapy, type and side of surgery, and the side of the dominant hand, were obtained for patients who consented.
Of the 417 eligible patients, 314 were approached and 279 agreed to participate. Of these 279 patients, 271 women began the study by completing the baseline questionnaire. Patients completed additional Breast Sensation Assessment Scale (BSAS) (This instrument has been copyrighted by Memorial Sloan-Kettering Cancer Center, 2002) questionnaires at 3 months (n = 251), 6 months (n = 239), and 12 months (n = 233). Only patients who completed the BSAS at all time points (baseline and 3, 6, and 12 months) were included in the formal analyses (n = 233).
Breast Sensation Assessment Scale
Patients were asked to complete the BSAS during their initial postoperative visit. The BSAS questionnaire is an instrument that measures the prevalence, severity, and distress of 18 symptoms.12 The BSAS has four subscales—discomfort (including symptoms of throbbing, soreness, aching, tenderness, pain, and numbness), mobility (including symptoms of pulling, tightness, stiffness, and hardness), paresthesias (including symptoms of pricking, burning, tingling, and twinging), and piercing (including symptoms of shooting, penetrating or nagging pain, and sharpness)—and a summary score. The score of each subscale was calculated by taking the mean of the sum of severity and distress for each sensation within the subscale. The summary score is the average of the scores on the four subscales. The BSAS has been demonstrated to have good internal consistency, test-retest reliability, and validity.12,13
Although the majority of patients who required an ALND were identified and underwent ALND during the initial surgery, some patients underwent an ALND after their initial postoperative visit and therefore after completing their initial questionnaire. These patients completed a second baseline questionnaire 3 to 15 days after the second surgical procedure (delayed ALND). For all analyses, data (demographic, arm measurement, and BSAS survey) from the time of definitive ALND were used and served as the new baseline date for completion of future questionnaires.
After completing the baseline questionnaire, patients were observed over time. Subsequent BSAS questionnaires were mailed to patients at 2, 5, and 10 months after their surgery. In addition, patients were asked about adjuvant therapy. If the questionnaire was not returned within 1 month from the time it was mailed, a reminder phone call was made. Only questionnaires returned within 1 month of the follow-up phone call were accepted; if not accepted within 1 month, the data for this time period became ineligible. Patients who did not return their questionnaire were asked at their next appointment whether they wished to continue in the study. Returned questionnaires were reviewed and patients contacted by telephone up to five times to obtain outstanding data. Overall, <1% of items were left unanswered.
Lymphedema
Patients had arm measurements at the time of surgery and 12 months after surgery. The ipsilateral and contralateral arms were measured at 10 cm above the olecranon process and 5 cm below the olecranon process. To control for weight gain or loss, changes in arm circumference between baseline and 12 months were calculated and compared with similar measurements for the contralateral arm. The differences in arm measurements were calculated for both the upper arm and forearm:
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Changes in the upper- and lower-arm measurements between patients with SLNB and ALND were compared by using Student’s t-test for independent groups.
Statistical Analysis
Given the multiple comparisons, analyses were considered to be significant only if the P value was <.01. The statistical software SPSSTM 9 for Windows (SPSS Inc., Chicago, IL) was used for statistical analyses. Repeated-measures analyses of variance were used to assess the effect of SLNB and ALND over time on the subscales and the summary score. Where appropriate, exploratory analyses used Pearson’s correlation to compare two continuous variables, Student’s t-test to compare between two groups, and repeated measures to compare the effect of various clinical variables on the SLNB and ALND patients over time.
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RESULTS
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Patient Population
The overall study completion rate was 83.5% (233 of 279) among those who agreed to participate and 86% (233 of 271) among those who started the study. The baseline subscale and summary scores of patients who did and did not complete all four BSAS surveys were not significantly different (Table 1). The excellent completion rate and absence of differences between patients who did or did not complete all four surveys suggests that the study sample is representative of the eligible patients at MSKCC.
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TABLE 1. Patient population: a comparison of baseline summary scores between women completing all questionnaires (study patients) and patients excluded for not completing one or more BSAS surveys (excluded patients)
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Among the 233 women who participated in this study, 171 underwent SLNB alone, and 62 had SLNB followed by ALND. Demographic data, listed in Table 2, demonstrate no significant differences between the two groups of patients. In addition, the number of sentinel nodes removed did not differ between patients with SLNB and ALND. However, by the very definition of the treatment groups, those patients who underwent ALND had more axillary nodes removed, a more advanced cancer stage, and more systemic treatment than those in the SLNB group.
Breast Sensation Assessment Scale
The majority of patients undergoing either type of axillary procedure experienced sensory changes. The prevalence of sensations in both the SLNB and ALND groups is shown at baseline (Fig. 1a) and 12 months (Fig. 1b). The frequency of very severe or distressing (3 or 4 on a 1–4 Likert scale) sensory changes for both groups at baseline and 12 months is shown in Fig. 2. Patients who underwent SLNB experienced symptoms that were less prevalent and also less frequently severe and distressing than those who underwent ALND. Overall, patients were more likely to report symptoms as severe rather than distressing. The prevalence of all symptoms, as well as the frequency of very severe or distressing symptoms, decreased over time in both groups. Thus, patients experienced sensory changes very often, but the majority were not severe or distressing.
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FIG. 1. Prevalence of sensations at baseline (A) and 12 months (B) in patients undergoing axillary lymph node dissection (ALND) and sentinel lymph node biopsy (SLNB).
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FIG. 2. (A) Prevalence of severe or very severe symptoms in axillary lymph node dissection (ALND) and sentinel lymph node biopsy (SLNB) patients at baseline and 12 months. (B) Prevalence of severe or very severe symptoms in ALND and SLNB patients at 12 months. (C) Prevalence of quite or very distressing symptoms in ALND and SLNB patients at baseline. (D) Prevalence of quite or very distressing symptoms in ALND and SLNB patients at 12 months.
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With use of repeated measures over the four time points, patients who underwent SLNB had significantly lower scores on the discomfort (F = 20.9, P < .001), mobility (F = 67.5, P < .001), paresthesias (F = 15.4, P < .001), and piercing (F = 5.9, P = .015) subscales (Fig. 3A–D) and the summary score (F = 22.5, P < .001; Fig. 4) when compared with patients who had undergone ALND. For both ALND and SLNB, there was significant improvement over time in the BSAS discomfort (F = 79.4, P < .001), mobility (F = 40.3, P < .001), paresthesias (F = 58.6, P < .001), and piercing (F = 13.6, P < .001) subscale scores and in the BSAS summary score (F = 74.8, P < .001). Although patients with SLNB continued to demonstrate some improvement over time, the only statistically significant improvement over time occurred in the first 3 months for all four subscales (P < .001) and the summary score (P < .001; Figs. 3 and 4).
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FIG. 3. Mean scores on the Breast Sensation Assessment Scale subscales in axillary lymph node dissection (ALND) and sentinel lymph node biopsy (SLNB) over 12 months of follow-up: (A) discomfort, (B) mobility, (C) paresthesias, and (D) piercing.
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FIG. 4. Mean summary scores on the Breast Sensation Assessment Scale in axillary lymph node dissection (ALND) and sentinel lymph node biopsy (SLNB) over 12 months of follow-up.
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Some clinical factors that were hypothesized to influence sensory morbidity were significant. First, age played an important role in the sensations reported by women. Younger women reported significantly more symptoms regardless of the type of surgery when compared with older women (F = 12.16, P = .001; Fig. 5). Second, the extent of surgery for patients undergoing SLNB influenced the degree of sensory morbidity. The number of nodes removed was positively correlated with the summary scores at baseline (r = .62, P = .001) but not in follow-up (r = .17, P = .03). In contrast, in ALND patients, the summary score was not significantly associated at baseline (r = -.05, P = .7) or at follow-up (r = .22, P = .08) with the total number of nodes removed. When patients undergoing SLNB were grouped by the level of highest dissection (level I, n = 160 vs. level II, n = 11), there was no significant difference in summary scores at baseline (F = .01, P = .92) or follow-up (F = .75, P = .38). Thus, these data confirm the clinical impressions that younger age and more extensive dissection in SLNB are associated with increased sensory morbidity.
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FIG. 5. Mean summary score and the effect of age over 12 months of follow-up. ALND, axillary lymph node dissection; SLNB, sentinel lymph node biopsy.
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Other factors hypothesized to affect sensory morbidity were not found to be significantly associated with the scores. No significant differences were found in the scores for patients who received early (<3 months after surgery) or late (>3 months after surgery) radiation in either the SLNB or ALND group (F = 2.84, P = .09). Although patients with surgery on the side of the dominant hand had slightly higher summary scores (F = 2.66, P = .10), the scores were not statistically significant.
To ensure that the morbidity experienced by patients who underwent delayed ALND in no way differed from that experienced by patients who underwent immediate ALND, two additional exploratory analyses were performed. For the small subset of patients who underwent delayed ALND, and who therefore completed the BSAS baseline questionnaire two times (after initial SLNB and again after delayed ALND), the subscale and summary scores from the first questionnaire (after SLNB) were compared with those from the second questionnaire (after delayed ALND) by using a within-subject Student’s t-test. In all cases, we found significantly more sensory changes reported on all four subscales and on the summary score after delayed ALND than were reported after initial SLNB, indicating that within a given patient, SLNB results in less sensory morbidity (Table 3). Next, we compared baseline scores for immediate and delayed ALND cases and found no significant increase in the number of symptoms reported after delayed ALND (Table 4). On the basis of this finding, it seems unlikely that the within-subject differences observed between SLNB and ALND (Table 3) are attributable to these patients reporting higher scores after delayed ALND than they would have after immediate ALND. Thus, on the basis of the results of these two additional analyses, we believe that there is no significant difference in associated morbidity between immediate and delayed ALND.
Lymphedema
Follow-up arm measurements were taken at approximately 1 year after surgery. For SLNB, the median time to follow-up measurements was 11.8 months (range, 9.8–14.2 months), and for those undergoing ALND, it was 11.4 months (range, 9.6–14.2 months). There was no significant difference in the body mass index between patients with ALND and SLNB (Table 5). There was no statistically significant change in either group for upper-arm or forearm circumference at the 12-month follow-up period.
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DISCUSSION
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Our data demonstrate that both SLNB and ALND result in sensory morbidity, with patients who undergo ALND reporting significantly more sensory morbidity than patients who undergo SLNB. The morbidity reported by patients undergoing SLNB is greater than generally assumed. This discrepancy may be due to surgeons’ misconceptions that originate in past experience with diagnosing entities such as lymphoma, in which removal of an isolated palpable axillary node is associated with only minimal morbidity. Often, however, an SLNB entails much more extensive dissection than a simple axillary biopsy and frequently necessitates identification and dissection of several different afferent lymphatics or nodes, resulting in much more tissue disruption and, therefore, significant postoperative symptoms. Rather than thinking of an SLNB as similar to a simple axillary biopsy, it may be more appropriate to consider it as having half the sensory morbidity of ALND.
Sensory morbidity improves with time in both SLNB and ALND patients. The only significant improvement, however, occurred during the first 3 months, with no additional significant improvement occurring between months 3 and 12. Although one might expect some additional improvement to occur, other authors have also documented little change over time.14,15 Thus, to the clinician, these data provide important information that can be used to counsel patients.
It is important to translate the BSAS subscales and summary scores into meaningful information for the patient. First, we can tell patients that the majority will have some sensory morbidity, with a small minority having very severe or distressing sensations. This finding reflects our clinical impression that most patients report symptoms that are bothersome rather than severe or very distressing. Second, on the basis of the differences in the summary scores, patients undergoing SLNB experienced approximately 50% less sensory morbidity than patients undergoing ALND over the 12-month period.
Age seemed to be an important factor in sensory morbidity. Regardless of the type of axillary surgery, younger patients reported more symptoms when compared with older patients. Younger patients seem to be more sensitive to the discomfort caused by axillary surgery. Although this may be physiologic, it might also be due to age-related differences in expectations and previous life experiences. Although the etiology of differences in sensory perceptions between younger and older women is not completely understood, other researchers have found similar results among women who have undergone ALND.1,2
It is not surprising that we were unable to demonstrate differences in arm measurements between patients undergoing SLNB and ALND at 12 months. It is likely too early to see any differences; ongoing prospective follow-up will be necessary to assess the incidence of lymphedema in the two groups.
Other authors using validated instruments have reported the quality of life of patients undergoing axillary surgery.5,16 In fact, one group developed additional items for the Functional Assessment of Cancer Therapy-Breast that specifically addressed the effect of arm morbidity.16 This instrument has undergone preliminary validation and demonstrates psychometric properties. The instrument asks patients about the presence of only four additional symptoms, however, and does not capture the whole spectrum of sensory changes that occur. In addition, it makes no attempt to understand the effect of these symptoms on the patient. Thus, we believe the BSAS to be a more clinically relevant and meaningful instrument to assess postoperative sensory morbidity.
Given that the majority of patients with nodal metastases had a complete ALND, our SLNB group was mostly node negative and our ALND group mostly node positive. This results in a potential confounding between stage and procedure. For example, patients with more advanced disease may have a heightened awareness of sensations because they may be more concerned about recurrence. However, patients with more advanced disease may minimize their sensory morbidity, whereas women with earlier-stage disease may be more attuned to sensory changes. We believe, however, that the difference in sensory morbidity between the SLNB and ALND groups is real and unlikely to be due to stage. Among patients who had SLNB followed by a delayed ALND, significantly more sensations were reported after ALND, and this suggests that the difference was procedure related and not stage related. Also, before surgery, patients are generally asymptomatic regardless of whether they are stage I or II; symptoms occur only after the operative procedure.
The population studied here does not match the demographics of women with breast cancer in North America. The women treated at MSKCC were younger, were more frequently Caucasian, were educated, and presented with an earlier-stage cancer than is generally the case in the population of women with breast cancer in the nation. However, the study completion rate (86%) was well above the accepted minimum of 70%.17 When comparing patients who did and did not complete all four surveys, there was no difference in the scores, suggesting that the excluded patients experienced no more or less prevalent, severe, or distressing sensations than did our study population. These findings indicate that our results are representative of the population treated at our institution.
Several aspects of morbidity and quality of life were not measured in this study. First, although we asked patients about their sensory morbidity, we did not ask them about their overall or disease-specific quality of life. The sensory and mobility deficits were not objectively measured by neurological examination. In addition, the integrity of the intercostal brachial nerve was not recorded. Rather than simply being an instrument to document symptoms, however, the BSAS incorporates the severity and distress of symptoms. Patients present with significant sensory complaints. Therefore, we believe that it is important to assess the morbidity of axillary surgery from a patient’s point of view.
To the best of our knowledge, this is the first large prospective study to systematically evaluate the sensory morbidity over time with a validated instrument in women undergoing ALND and SLNB. The BSAS effectively synthesizes important information about sensory morbidity in a clinically sensible way that can be understood by both the clinician and patient. The data support the use of SLNB as a less morbid method of staging the axilla. In addition, these data can be used to educate patients that even SLNB can result in significant sensory changes.
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Acknowledgments
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The authors thank S. Raboy, BA, for her meticulous data collection and follow-up for this study. Supported in part by the Kristen Ann Carr Memorial Fellowship (LKFT).
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Footnotes
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In a prospective longitudinal study using the Breast Sensation Assessment Scale, a psychometrically validated instrument, the sensory morbidity of sentinel lymph node biopsy was found to be significant and persistent over a 1-year period. However, it was significantly less than the morbidity associated with axillary lymph node dissection.
Received for publication February 8, 2002.
Accepted for publication May 6, 2002.
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ABSTRACT
INTRODUCTION
