- Email: [email protected]
Arm morbidity after breast conservation and axillary therapy
The Brrarr c I993 4.273-276 0 Pearson Professionul Ltd 1995
Arm morbidity A. M. Thompson,**t
after breast conservation
and axillary
therapy
M. Air,? W. J. L. Jack,* G. R. Kerr,* A. Rodgers and U. Chettyt
*Universiry Department of Surgery, Royal Infirmary, fBreast Unit, #Department of Clinical General Hospital, BDeparhnent of Radiation Oncology, Alfred Hospital, Prahran, Australia
Oncology,
Western
S U MM A R Y. Pre-operative and postoperative upper limb volume, limb circumference and shoulder girdle mobility were measured in 121 consecutive patients who bad a conservation approach for breast cancer. Axillary management comprised (i) axillary node sampling (n = 28), or (ii) axillary node sampling plus regional radiotherapy (n = 61), or (iii) axillary node clearance (levels I, II and III) (n = 19) or (iv) axillary node dissection (levels I and II) plus regional radiotherapy (n = 13). Upper limb volume on the treated side increased significantly (P < 0.01) for both groups (i) and (ii). Upper limb circumference was significantly greater after more extensive axillary surgery ((iii) and (iv)) than for node sampling ((i) or (ii)) (P = 0.006). Upper limb volume increased by over 200 ml in 39 patients (32%). Axillary radiotherapy (groups (ii) and (iv)) significantly reduced shoulder girdle mobility (P < 0.05). The combination of axillary node dissection and radiotherapy carried the highest morbidity. This study demonstrates that upper limb morbidity at 1 year following breast conservation reflects the extent of axillary surgery and the use of axillary irradiation. Axillary node sampling, with axillary irradiation if node positive, or a level ID axillary clearance are associatedwith similar levels of upper limb morbidity and are both appropriate options for staging and/or treating the axilla during breast conserving surgery.
INTRODUCTION Breast conservation has lead to a re-appraisal of the extent of axillary surgery and radiotherapy in breast cancer.‘.?Controversy exists as to the most appropriate axillary managementwhich gives both diseasecontrol and prognostic information.3-9The morbidity of these axillary proceduresin breast conservation has received little attention. While operations on the breast alone rarely cause upper limb oedema,‘Oupper limb morbidity is a recognized complication of axillary surgery as part of breast conservation therapy; ‘i-i4 however, upper limb morbidity has rarely been accurately documented. By contrast, following mastectomy, increasedupper limb morbidity follows more radical surgery,is.‘6although the incidence and severity of arm swelling following axillary clearance wascomparableto that of samplingin one recent study.” In addition, upper limb morbidity is a recognized complication of adding axillary radiotherapy to axillary surgery after mastectomy,‘* but may confer no survival advantage.i9 The aims of the present study were to prospectively document upper limb morbidity in patients undergoing Address correspondence to: A. M. Thompson, University Department of Surgery, Royal Infvmary of Edinburgh, Edinburgh EH3 9YW, UK 273
breast conservation; to objectively quantify the relationship between upper limb morbidity and the method of managementof the axilla and to determine whether such morbidity was related to particular combinations of therapy.
PATIENTS AND METHCJDS A prospective study of upper limb morbidity was conducted on 121 consecutive women who underwent breastconservation surgery for breastcancer at the Edinburgh Breast Unit. All 121 patients had Stage I or Stage II disease:palpable unilateral breast cancer measuringless than 4 cm in diameter on caliper measurement(UICC T, or T,), without clinical evidence of distant metastases.The patients selectedbreastconservation in preference to mastectomy after full discussion with a nurse counsellor. The managementof the axilla was decided after discussion between the surgeon, radiation oncologist, medical oncologist and patient. Each patient had wide local excision of the tumour and breast irradiation (45 Gy in 20 fractions over 4 weeks). The selection of axillary surgical procedure and/or radiotherapy followed discussion amongstthe clinicians and was basedon Unit protocols in operation at the time. The patients were entered into
274
The Breast Table
1
Patient treatment
groups
Patients groups
No. patients
Wide local excision
Breast irradiation
Axillary node *sampling
i ii. . . 111 iv
28 61 19 13
Yes Yes Yes Yes
Yes Yes Yes Yes
Yes Yes
four groups (Table 1). Axillary node sampling was selected for all patients with upper outer quadrant breast cancers to ensure that if radiotherapy fields had to extend towards the axilla to cover the scar, a cleared axilla would not be irradiated. For patients who received axillary radiotherapy, megavoltage therapy was delivered directly to an anterior field covering the axilla (but blocking the humeral head) and comprised 45 Gy maximum in 20 fractions over 4 weeks, with a single posterior field applied to bring the mid-axillary dose to 45 Gy. Upper limb volume, upper limb circumference and combined gleno-humeral/scapular movement were measured by one individual (MA). Both the treated and the untreated upper limbs were examined pre-operatively and at least 12 months after completion of postoperative radiotherapy. As a measure of upper limb swelling, the arm volume and arm circumference were assessed. Arm volume was measured by water displacement; each upper limb was inserted into a water bath (at room temperature) and the patient gripped a handle in the bath at a known depth to ensure reproducibility.rs The change in arm volume on the treated side was calculated from the formula: change in arm volume on the treated side (postoperative volume - pre-operative volume) minus change in arm volume on the untreated side. Upper limb circumferences were measured at 10 cm distal to and 15 cm proximal to the olecranon12 and the median of three measurements at each site was used. Shoulder mobility was assessed by asking the patient to put her hand behind her back from above (abduction with external rotation) then below (adduction with internal rotation) and the distance of the middle fingertip from the spinous process of the 7th cervical vertebra measured in centimetres. Flexion and pure glenohumeral abduction were measured as previously described.‘* All patients received a physiotherapy advice sheet preoperatively and all received postoperative physiotherapy. NO subjective record of upper limb morbidity was made and upper limb power, hand grip or intercostobrachial nerve damage were not assessed.
Statistical methods Differences in measurements within and between treatment groups comparing treated to untreated limbs and pre-treatment to post-treatment measurements were compared using paired t-tests and Mann-Whitney U tests when comparing two groups, and by analysis of variance when comparing four.
Axillary clearance (level 1, Il. Ill)
Axillary irradiation
Axillary dissection (level I, II)
Yes Yes Yes
Yes
RESULTS The four groups of patients were comparable in terms of mean patient age, length of follow-up TNM stage, pathological nodal involvement with tumour, and postoperative wound infection rates. There was no significant difference for any of the groups in arm volume or circumference or impairment of shoulder movement in the upper limb of the untreated side.
Upper limb volume In all four groups the mean volume of the upper limb on the treated side increased following therapy (Table 2 & Fig. 1A). There was a significant increase in both patient groups who had axillary node sampling (t-test; P = 0.004 sampling alone, P = 0.003 sampling and radiotherapy) but the mean increase in volume did not achieve statistical significance in patients who had axillary node dissection to level II plus radiotherapy (t-test; P = 0.064) and was not significant (t-test; P = 0.39) in the patients who had axillary clearance (levels I, II and III). However, there was a wide range of change in arm volume and 44 of the 121 patients actually had a reduction in volume on the treated side. Conversely, a substantial increase in upper limb volume (greater than 200 ml) was noted in 39 patients (32%).
Table 2 Changes in arm volume conservation
and arm circumference
in breast
Group
i ,I = 28
ii n = 61
III n=
iv n=
Sample
Sample
Clearance
Dissection
Nil
45 Gy
Nil
45 Gy
F2l%)
:380%)
;29%)
7 (54%)
+108
+81
+75
+216
(-250 +500)
(-380 +520)
(-534 +880
;32%)
&W)
3/6* (50%)
:69%)
+0.32 (-I - +5)
+0.25 (-I - +2)
+0.67* (0 - +2)
+I.15 (0 - +3)
Axillary surgery Radiotherapy Number of patients with increase in arm volume >2OOml Mean change in ipsilateral volume for all patients
in cm3;(range) Number of patients with increase in arm circumference Mean change in circumference (cm: ranne) *measured
in only 6 of the 19 patients. /
19
-
13
(-370 +850)
(iv) L -8 Arm
Before
Affer
Belore 1.2 -
250 -
lo-
Meon C@change in circumlerence 0,6(cm)
Mean change in volume (cm’)
morbidity
Before
Alter
after
breast
conservation
and
axillary Before
Affer
275
therapy After
1 cm
0 -1
‘C”““” ---,
-/ii!) ‘--(ii)
h
(iv)
-2J
(B)
(iii1
,’
Before
0
, (il
-9
(A)
After
1
cm
-1
"'"."".. h
‘*.
-
161.1
‘.
-2 -3
(iv)
-10
(A)
(‘2)
Fig. l-Changes in upper limb volume and arm circumference in breast conservation therapy. Mean change in upper limb volume (A) and mean change in arm circumference (B) on the treated side in patients after: (i) wide local excision, breast irradiation, axilhuy node sample (ii) wide local excision, breast irradiation, axillary node sample and axillary irradiation (iii) wide local excision, breast irradiation, axillary clearance (iv) wide local excision, breast irradiation. axillary dissection and axillary irradiation.
Fig. 2-Changes in upper limb morbidity following breast conservation therapy. Mean change in elevation (A), abduction plus external rotation (B) and abduction plus internal rotation (C) at the shoulder on the treated side on patients after: (i) wide local excision, breast irradiation, axillary node sample (ii) wide local excision, breast irradiation, axillary node sample and axillary irradiation (iii) wide local excision, breast irradiation, axillary clearance (iv) wide local excision, breast irradiation. axillary dissection and axillary irradiation.
Arm circumference
morbidity after 1 yedo or the morbidity may become less severe with time.17 At 12 months, disease recurrence is unlikely to contribute to upper limb morbidity in patients suitable for breast conservation: the effects demonstrated by this study were therefore attributable to the surgery and/or radiotherapy.
The arm circumference increased in the majority of patients who had axillary dissection or axillary clearance to level III (groups (iii) and (iv)). Moreover, the mean increase in arm circumference following surgery (Table 2 & Fig. 1B) was significantly greater in patients who had extensive axillary surgery compared with those who had ax&try node sampling (ANOVA, F = 7.94, df = 1,
P = 0.006). Upper limb mobility Patients who had radiotherapy after axillary node sample had significantly reduced upper limb elevation when compared with those who had no radiotherapy (t = 2.88, P = O.OOS), (Fig. 2). There was no significant difference, however, between those who had level III axillary clearance and those who had level II node dissection plus radiotherapy. Rotatory movements at the shoulder (abduction with external rotation and adduction with internal rotation) were significantly reduced by the addition of radiotherapy to either axillary surgical procedure (ANOVA F = 7.88, df = 1, P = 0.006 for abduction ANOVA F = 4.83, df = 1, P = 0.03 for adduction).
DISCUSSION This study has objectively demonstrated that upper limb swelling and impaired upper limb mobility may complicate the conservation approach to breast cancer and that such morbidity is common 12 months after treatment. However, patients may continue to develop upper limb
Upper limb swelling A significant increase in upper limb volume was noted for the two groups of patients who had axillary sampling whereas arm circumference was significantly increased for the two groups of patients who had more extensive surgery. This suggests that the two methods of measurement do not correlate closely. Although limb volume may be a more accurate measure of lymphoedema,i7 arm circumference is easier to measure’*J’ and should also be recorded. An increase in upper limb volume of 200 ml is considered by many as clinically significant and potentially disabling.‘“.i7.” It is of concern that 39 patients (32%) achieved this level and 8 (5 of whom had level II axillary dissection and radiotherapy) exceeded 500 ml, a greater increase than that reported after mastectomy and axillary node clearance.‘7 Our data suggest that published series in which less than 10% of patients had upper limb lymphoedema after breast conservation and axillary clearance may greatly underestimate the problem.‘.‘4.23 More extensive surgery, particularly when combined with radiotherapy, was associated with at least as substantial upper limb swelling as with mastectomy and axillary therapy, and our data indicate it may be even more common after breast conservation than after mastectomy.‘0~‘s~16J8
Upper linii~ mobility Upper limb mobility was adversely affected in all 4 . g&ups of patients beated by conservation, as noted post-mastectomy.” The addition of radiotherapy further impaired upper limb mobility, regardless of the axillary surgery performed. Radiotherapy was associatedwith reduced upper limb mobility even though the humeral head and the glenohumeral joint were protected; this may reflect damage to the rotator cuff muscles rather than the joint capsule. The debate on the management of the axilla in breast
conservation is often basedon data relating to disease control and the quality of prognostic information”,‘** without sufficient attention to upper limb morbidity. We have demonstrated that level II axillary dissection and subsequent radiotherapy causes substantial upper limb and shoulder girdle morbidity and should no longer be
performed. However, even axillary sampling alone or axillary clearancealone result in detectable upper limb morbidity. Evidence of axillary node metastases is important for prognosis7.8 and can be accurately determined by axillary node sampling.24 From the objective measure-
ments used in this study, axillary node sampling, with the addition
of axillary
radiotherapy
only
if there is
evidenceof tumour in the lymph nodes,may be the treatment of choice.
In this way prognostic
information
is
obtained, morbidity is minimized but regional control of the diseaseis achieved. Level III axillary clearance alone may be an alternative meansof establishingprognostic information and disease control for high upper outer quadrant
breast cancers or when
radiotherapy
is
not considered appropriate. Because of the need for prognostic staging and the risk of upper limb morbidity we do not support the use of axillary radiotherapy
without an axillary node stagingprocedure. This study has quantified upper limb morbidity
in breast conservation, and suggests that more extensive surgery leads to greater upper limb swelling and that
radiotherapy can compound the problem by reducing shouldergirdle mobility. A randomizedstudy of axillary sample (with the addition of radiotherapy if node positive) versuslevel III axillary node clearance is being performed at present to further consider the effects of treatment on locoregional diseasecontrol, survival, and upper limb morbidity, both objective and subjective.
2. Fisher B, Bauer M, Wickerham L, Redmond C. Fisher E R. Relationship of the number of positive axillary nodes 10 the prognosis of patients with primary breast cancer. Cancer 1983; 52: 1551-1557. 3. Leslie M D, Maher E J. Node negative breast cancer. BMJ 1990; 300: 346-348. 4. Recht A. Connolly S. Schmitt J el al. Conservative surgery and radiation therapy for early breast cancer: results controversies and unsolved problems. Sernin Oncol 1986: 13: 434-449. 5. Sacks N P M, Barr L C, Allan S M, Baum M. The role of axillary dissection in operable breast cancer. The Breast 1992; 1: 4149. 6. Mazeron J J. Otmezguine Y. Huart J, Pierquin B. Conservative treatment of breast cancer: results of management of axillary lymph node area in 3353 patients. Lancet 1985; 1387 (Letter). 7. Nixon S J. Steele R J C, Hawkins J R. McGregor J. Forrest A P M. Prediction of recurrence after mastectlmy for operable breast cancer. Br J Surg 1985; 72: 7-9.
8. Carter C L, Allen C. Henson D E. Relation of tumour size, lymph node status and survival in 24 740 breast cancer cases. Cancer 1989; 63: 181-187. 9. Dewar J A. S-in D. Benhamou E et al. Management of the
axilla in conservatively treated breast cancer: 592 patients treated a[ institut Rustave-Roussy.Int J Radiat Oncol Biol Phys 1987; 13: 475-481. IO. Browse N L. Lymphoedema of the arm. BMJ 1987; 295: 4-5. I I. Romsdahl M M, Montague E D, Ames F C et al. Conservation surgery and irradiation as treatment for early breast cancer. Arch Surg 1983; 1 IS: 521-528. 12. Hayward J L, Winter P J, Tong D. A new approach 10 the conservative treatment of early breast cancer. Surgery 1984; 95: 270-274. 13. Benson E T, Thorogood J. The effect of surgical technique on the local recurrence rates following mastectomy. Eur J Surg Oncol 1986; 12: 267-27 I. 14. Lawson D. Weinstein M. Goldberg I et al. Oedema of the arm as
a function of the extent of axillary surgery in patients with Sraee 1 & ll cancer of the breast treated by $&uy iadiotherapy. IntJ Radial Oncol Biol Phvs 1986: 12: 1575-1582. 15. Swedborg I, Wallgren A. The effect of pre- and postmastectomy
radiotherapy on the degree of edema shoulder-joint mobility, and gripping force. Cancer I98 1; 47: 877-88 I. 16. Kissin M W, Querci della Rovere G, Easton D, Westbury G. Risk of lymphoedema following the treatment of breast cancer. Br J Surg 1986; 73: 580-584. 17. Hoe A L. Iven D, Royle G T, Taylor 1. Incidence of arm swelling following axillary clear&e for breast cancer. Br J Surg 1992: 79: 261-262. 18. Aitken R J, Gaze M N. Rodger A, Chetty U, Forrest A P M. Arm morbidity within a trial of mastectomy and either nodal sample with selective radiotherapy or axillary clearance. Br J Surg 1989; 76: 568-571. 19. Henderson C. Canellos G P. Cancer of the breast. The past decade. N Engl J Med 1980; 302: 17-30. 20. Yeoh E K, Denham J W, Davies S A, Spittle M F. Primary breast cancer, complications of axillary management. Acta Radiologica Oniology 1986; 25: 105-l 08. 21. Ryttor N, Holin N V, Quist N, Blichert-Toff M. Influence of adjuvent irradiation on the development of late arm oedema and impaired shoulder mobility after mastectomy for cancer of the 22.
breast. Acta Oncol 1988; 27: 667-670. Tracy G D, Reeve T S, Fritzsimmons E, Rundle F F. Observations
Acknowledgements The authors wish to thank Lord Hartwell for his generous support of this study and Mr R. J. Aitken
for conshuctive
comments.
of the swollen
arm after radical mastectomy.
Oncol Biol Phys 1986; 12: 2079-2083. 24. Steele R J C. Forrest A P M, Gibson T, Stewart
References 1. Veronesi U, Saccozzi R, Del VeUhio M. Comparing radical mastectomywith quadrantectomy axillary dissection and radiotherapy in patients with small cancers of the breast. N Engl J Med 1981; 305: 6-l I.
Aust
NZ J Surg 1961; 30: 204-207. 23 Pezner R D, Patterson M P, Hill R L et al. Arm oedema in patients treated conservatively for breast cancer: relationship to patients age and axillary node dissection techniques. Int J Radiat H J, Chetty
U.
The efficacy of lower axillary sampling in obtaining lymph node stams in breast cancer: a controlled randomized trial. Br J Surg 1985; 72: 368-369.
Date submitted 5 May 1994 Date accepted I9 October 1994
Arm morbidity A. M. Thompson,**t
after breast conservation
and axillary
therapy
M. Air,? W. J. L. Jack,* G. R. Kerr,* A. Rodgers and U. Chettyt
*Universiry Department of Surgery, Royal Infirmary, fBreast Unit, #Department of Clinical General Hospital, BDeparhnent of Radiation Oncology, Alfred Hospital, Prahran, Australia
Oncology,
Western
S U MM A R Y. Pre-operative and postoperative upper limb volume, limb circumference and shoulder girdle mobility were measured in 121 consecutive patients who bad a conservation approach for breast cancer. Axillary management comprised (i) axillary node sampling (n = 28), or (ii) axillary node sampling plus regional radiotherapy (n = 61), or (iii) axillary node clearance (levels I, II and III) (n = 19) or (iv) axillary node dissection (levels I and II) plus regional radiotherapy (n = 13). Upper limb volume on the treated side increased significantly (P < 0.01) for both groups (i) and (ii). Upper limb circumference was significantly greater after more extensive axillary surgery ((iii) and (iv)) than for node sampling ((i) or (ii)) (P = 0.006). Upper limb volume increased by over 200 ml in 39 patients (32%). Axillary radiotherapy (groups (ii) and (iv)) significantly reduced shoulder girdle mobility (P < 0.05). The combination of axillary node dissection and radiotherapy carried the highest morbidity. This study demonstrates that upper limb morbidity at 1 year following breast conservation reflects the extent of axillary surgery and the use of axillary irradiation. Axillary node sampling, with axillary irradiation if node positive, or a level ID axillary clearance are associatedwith similar levels of upper limb morbidity and are both appropriate options for staging and/or treating the axilla during breast conserving surgery.
INTRODUCTION Breast conservation has lead to a re-appraisal of the extent of axillary surgery and radiotherapy in breast cancer.‘.?Controversy exists as to the most appropriate axillary managementwhich gives both diseasecontrol and prognostic information.3-9The morbidity of these axillary proceduresin breast conservation has received little attention. While operations on the breast alone rarely cause upper limb oedema,‘Oupper limb morbidity is a recognized complication of axillary surgery as part of breast conservation therapy; ‘i-i4 however, upper limb morbidity has rarely been accurately documented. By contrast, following mastectomy, increasedupper limb morbidity follows more radical surgery,is.‘6although the incidence and severity of arm swelling following axillary clearance wascomparableto that of samplingin one recent study.” In addition, upper limb morbidity is a recognized complication of adding axillary radiotherapy to axillary surgery after mastectomy,‘* but may confer no survival advantage.i9 The aims of the present study were to prospectively document upper limb morbidity in patients undergoing Address correspondence to: A. M. Thompson, University Department of Surgery, Royal Infvmary of Edinburgh, Edinburgh EH3 9YW, UK 273
breast conservation; to objectively quantify the relationship between upper limb morbidity and the method of managementof the axilla and to determine whether such morbidity was related to particular combinations of therapy.
PATIENTS AND METHCJDS A prospective study of upper limb morbidity was conducted on 121 consecutive women who underwent breastconservation surgery for breastcancer at the Edinburgh Breast Unit. All 121 patients had Stage I or Stage II disease:palpable unilateral breast cancer measuringless than 4 cm in diameter on caliper measurement(UICC T, or T,), without clinical evidence of distant metastases.The patients selectedbreastconservation in preference to mastectomy after full discussion with a nurse counsellor. The managementof the axilla was decided after discussion between the surgeon, radiation oncologist, medical oncologist and patient. Each patient had wide local excision of the tumour and breast irradiation (45 Gy in 20 fractions over 4 weeks). The selection of axillary surgical procedure and/or radiotherapy followed discussion amongstthe clinicians and was basedon Unit protocols in operation at the time. The patients were entered into
274
The Breast Table
1
Patient treatment
groups
Patients groups
No. patients
Wide local excision
Breast irradiation
Axillary node *sampling
i ii. . . 111 iv
28 61 19 13
Yes Yes Yes Yes
Yes Yes Yes Yes
Yes Yes
four groups (Table 1). Axillary node sampling was selected for all patients with upper outer quadrant breast cancers to ensure that if radiotherapy fields had to extend towards the axilla to cover the scar, a cleared axilla would not be irradiated. For patients who received axillary radiotherapy, megavoltage therapy was delivered directly to an anterior field covering the axilla (but blocking the humeral head) and comprised 45 Gy maximum in 20 fractions over 4 weeks, with a single posterior field applied to bring the mid-axillary dose to 45 Gy. Upper limb volume, upper limb circumference and combined gleno-humeral/scapular movement were measured by one individual (MA). Both the treated and the untreated upper limbs were examined pre-operatively and at least 12 months after completion of postoperative radiotherapy. As a measure of upper limb swelling, the arm volume and arm circumference were assessed. Arm volume was measured by water displacement; each upper limb was inserted into a water bath (at room temperature) and the patient gripped a handle in the bath at a known depth to ensure reproducibility.rs The change in arm volume on the treated side was calculated from the formula: change in arm volume on the treated side (postoperative volume - pre-operative volume) minus change in arm volume on the untreated side. Upper limb circumferences were measured at 10 cm distal to and 15 cm proximal to the olecranon12 and the median of three measurements at each site was used. Shoulder mobility was assessed by asking the patient to put her hand behind her back from above (abduction with external rotation) then below (adduction with internal rotation) and the distance of the middle fingertip from the spinous process of the 7th cervical vertebra measured in centimetres. Flexion and pure glenohumeral abduction were measured as previously described.‘* All patients received a physiotherapy advice sheet preoperatively and all received postoperative physiotherapy. NO subjective record of upper limb morbidity was made and upper limb power, hand grip or intercostobrachial nerve damage were not assessed.
Statistical methods Differences in measurements within and between treatment groups comparing treated to untreated limbs and pre-treatment to post-treatment measurements were compared using paired t-tests and Mann-Whitney U tests when comparing two groups, and by analysis of variance when comparing four.
Axillary clearance (level 1, Il. Ill)
Axillary irradiation
Axillary dissection (level I, II)
Yes Yes Yes
Yes
RESULTS The four groups of patients were comparable in terms of mean patient age, length of follow-up TNM stage, pathological nodal involvement with tumour, and postoperative wound infection rates. There was no significant difference for any of the groups in arm volume or circumference or impairment of shoulder movement in the upper limb of the untreated side.
Upper limb volume In all four groups the mean volume of the upper limb on the treated side increased following therapy (Table 2 & Fig. 1A). There was a significant increase in both patient groups who had axillary node sampling (t-test; P = 0.004 sampling alone, P = 0.003 sampling and radiotherapy) but the mean increase in volume did not achieve statistical significance in patients who had axillary node dissection to level II plus radiotherapy (t-test; P = 0.064) and was not significant (t-test; P = 0.39) in the patients who had axillary clearance (levels I, II and III). However, there was a wide range of change in arm volume and 44 of the 121 patients actually had a reduction in volume on the treated side. Conversely, a substantial increase in upper limb volume (greater than 200 ml) was noted in 39 patients (32%).
Table 2 Changes in arm volume conservation
and arm circumference
in breast
Group
i ,I = 28
ii n = 61
III n=
iv n=
Sample
Sample
Clearance
Dissection
Nil
45 Gy
Nil
45 Gy
F2l%)
:380%)
;29%)
7 (54%)
+108
+81
+75
+216
(-250 +500)
(-380 +520)
(-534 +880
;32%)
&W)
3/6* (50%)
:69%)
+0.32 (-I - +5)
+0.25 (-I - +2)
+0.67* (0 - +2)
+I.15 (0 - +3)
Axillary surgery Radiotherapy Number of patients with increase in arm volume >2OOml Mean change in ipsilateral volume for all patients
in cm3;(range) Number of patients with increase in arm circumference Mean change in circumference (cm: ranne) *measured
in only 6 of the 19 patients. /
19
-
13
(-370 +850)
(iv) L -8 Arm
Before
Affer
Belore 1.2 -
250 -
lo-
Meon C@change in circumlerence 0,6(cm)
Mean change in volume (cm’)
morbidity
Before
Alter
after
breast
conservation
and
axillary Before
Affer
275
therapy After
1 cm
0 -1
‘C”““” ---,
-/ii!) ‘--(ii)
h
(iv)
-2J
(B)
(iii1
,’
Before
0
, (il
-9
(A)
After
1
cm
-1
"'"."".. h
‘*.
-
161.1
‘.
-2 -3
(iv)
-10
(A)
(‘2)
Fig. l-Changes in upper limb volume and arm circumference in breast conservation therapy. Mean change in upper limb volume (A) and mean change in arm circumference (B) on the treated side in patients after: (i) wide local excision, breast irradiation, axilhuy node sample (ii) wide local excision, breast irradiation, axillary node sample and axillary irradiation (iii) wide local excision, breast irradiation, axillary clearance (iv) wide local excision, breast irradiation. axillary dissection and axillary irradiation.
Fig. 2-Changes in upper limb morbidity following breast conservation therapy. Mean change in elevation (A), abduction plus external rotation (B) and abduction plus internal rotation (C) at the shoulder on the treated side on patients after: (i) wide local excision, breast irradiation, axillary node sample (ii) wide local excision, breast irradiation, axillary node sample and axillary irradiation (iii) wide local excision, breast irradiation, axillary clearance (iv) wide local excision, breast irradiation. axillary dissection and axillary irradiation.
Arm circumference
morbidity after 1 yedo or the morbidity may become less severe with time.17 At 12 months, disease recurrence is unlikely to contribute to upper limb morbidity in patients suitable for breast conservation: the effects demonstrated by this study were therefore attributable to the surgery and/or radiotherapy.
The arm circumference increased in the majority of patients who had axillary dissection or axillary clearance to level III (groups (iii) and (iv)). Moreover, the mean increase in arm circumference following surgery (Table 2 & Fig. 1B) was significantly greater in patients who had extensive axillary surgery compared with those who had ax&try node sampling (ANOVA, F = 7.94, df = 1,
P = 0.006). Upper limb mobility Patients who had radiotherapy after axillary node sample had significantly reduced upper limb elevation when compared with those who had no radiotherapy (t = 2.88, P = O.OOS), (Fig. 2). There was no significant difference, however, between those who had level III axillary clearance and those who had level II node dissection plus radiotherapy. Rotatory movements at the shoulder (abduction with external rotation and adduction with internal rotation) were significantly reduced by the addition of radiotherapy to either axillary surgical procedure (ANOVA F = 7.88, df = 1, P = 0.006 for abduction ANOVA F = 4.83, df = 1, P = 0.03 for adduction).
DISCUSSION This study has objectively demonstrated that upper limb swelling and impaired upper limb mobility may complicate the conservation approach to breast cancer and that such morbidity is common 12 months after treatment. However, patients may continue to develop upper limb
Upper limb swelling A significant increase in upper limb volume was noted for the two groups of patients who had axillary sampling whereas arm circumference was significantly increased for the two groups of patients who had more extensive surgery. This suggests that the two methods of measurement do not correlate closely. Although limb volume may be a more accurate measure of lymphoedema,i7 arm circumference is easier to measure’*J’ and should also be recorded. An increase in upper limb volume of 200 ml is considered by many as clinically significant and potentially disabling.‘“.i7.” It is of concern that 39 patients (32%) achieved this level and 8 (5 of whom had level II axillary dissection and radiotherapy) exceeded 500 ml, a greater increase than that reported after mastectomy and axillary node clearance.‘7 Our data suggest that published series in which less than 10% of patients had upper limb lymphoedema after breast conservation and axillary clearance may greatly underestimate the problem.‘.‘4.23 More extensive surgery, particularly when combined with radiotherapy, was associated with at least as substantial upper limb swelling as with mastectomy and axillary therapy, and our data indicate it may be even more common after breast conservation than after mastectomy.‘0~‘s~16J8
Upper linii~ mobility Upper limb mobility was adversely affected in all 4 . g&ups of patients beated by conservation, as noted post-mastectomy.” The addition of radiotherapy further impaired upper limb mobility, regardless of the axillary surgery performed. Radiotherapy was associatedwith reduced upper limb mobility even though the humeral head and the glenohumeral joint were protected; this may reflect damage to the rotator cuff muscles rather than the joint capsule. The debate on the management of the axilla in breast
conservation is often basedon data relating to disease control and the quality of prognostic information”,‘** without sufficient attention to upper limb morbidity. We have demonstrated that level II axillary dissection and subsequent radiotherapy causes substantial upper limb and shoulder girdle morbidity and should no longer be
performed. However, even axillary sampling alone or axillary clearancealone result in detectable upper limb morbidity. Evidence of axillary node metastases is important for prognosis7.8 and can be accurately determined by axillary node sampling.24 From the objective measure-
ments used in this study, axillary node sampling, with the addition
of axillary
radiotherapy
only
if there is
evidenceof tumour in the lymph nodes,may be the treatment of choice.
In this way prognostic
information
is
obtained, morbidity is minimized but regional control of the diseaseis achieved. Level III axillary clearance alone may be an alternative meansof establishingprognostic information and disease control for high upper outer quadrant
breast cancers or when
radiotherapy
is
not considered appropriate. Because of the need for prognostic staging and the risk of upper limb morbidity we do not support the use of axillary radiotherapy
without an axillary node stagingprocedure. This study has quantified upper limb morbidity
in breast conservation, and suggests that more extensive surgery leads to greater upper limb swelling and that
radiotherapy can compound the problem by reducing shouldergirdle mobility. A randomizedstudy of axillary sample (with the addition of radiotherapy if node positive) versuslevel III axillary node clearance is being performed at present to further consider the effects of treatment on locoregional diseasecontrol, survival, and upper limb morbidity, both objective and subjective.
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Acknowledgements The authors wish to thank Lord Hartwell for his generous support of this study and Mr R. J. Aitken
for conshuctive
comments.
of the swollen
arm after radical mastectomy.
Oncol Biol Phys 1986; 12: 2079-2083. 24. Steele R J C. Forrest A P M, Gibson T, Stewart
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Date submitted 5 May 1994 Date accepted I9 October 1994