Acta chir belg, 2003, 103, 212-216

Arm Morbidity after Complete Axillary Lymph Node Dissection for Breast
Cancer
P. H. A. F. Nagel*, E. D. M. Bruggink*, Th. Wobbes**, L. J. A. Strobbe*
Departments of Surgery Canisius Wilhelmina Hospital Nijmegen*, University Hospital Nijmegen**, The Netherlands.

Key words. Axillary dissection ; breast cancer ; arm morbidity ; sentinel node biopsy.
Abstract. The aim of the study was to clarify the factors causing and/or influence morbidity following axillary dissection in patients treated for breast cancer by either lumpectomy or mastectomy.
The records of 106 women with invasive breast cancer treated between 1996 and 1997 were retrospectively reviewed.
Objective assessment included measurement of lymphoedema, shoulder mobility and axillary sensation. A questionnaire was used for subjective assessment of arm morbidity and pain. Lymphoedema was present in 13% of patients, a
restriction in shoulder function in 24%, while 93% of patients had an impaired sensation in the axillary region.
Lymphoedema and restriction in shoulder function were common in patients after adjuvant axillary radiation. Morbidity
following axillary lymph node dissection is high and confirms the potentially severe effects of a staging procedure on a
relatively young population. Adjuvant radiotherapy increases morbidity significantly and therefore indications for adjuvant axillary radiotherapy should be revised with scrutiny for each patient individually, bearing in mind the disastrous
consequences of the combination of radiotherapy and surgery on the axilla.

Introduction

Patients and Methods

Breast cancer is the most common type of cancer frequently occurring in relatively young women with a
peak incidence between 50-60 years. The incidence of
breast cancer in the Netherlands is 120 in 100.000
women, resulting in 9.500 new cases of breast cancer
yearly, with a 70-80% 5-year survival (1). Treatment by
mastectomy or lumpectomy with irradiation of the
breast combined with axillary lymph node dissection
(ALND) is still the golden standard for invasive breast
cancer, although the use of ALND is questioned in
recent years (2-6). Controversy arises because of inherent morbidity following ALND without directly contributing to survival.
Seroma, abscess formation, loss of axillary sensation,
pain, disturbance of shoulder function and lymphoedema, all add to a delayed recovery, patient discomfort and
increased health costs. Because of this morbidity following routine ALND, methods are being developed to
predict the behaviour of the primary tumour, without
performing complete ALND. The use of axillary sampling (7), a limited level I dissection (8-9), and recently
the sentinel node biopsy (10) have been advocated as
alternatives.
The aims of this study are to measure the morbidity
of ALND and implement methods for quantifying this
disability and its influence on daily activity.

From January 1995 to December 1996, 256 patients

with breast cancer were treated at our department by
either mastectomy or breast conserving therapy with
complete axillary dissection. After excluding the
patients with carcinoma in situ, malignancies elsewhere,
relapse or proven distant metastatic process, a random
selection was made and 126 patients were invited to participate. One hundred and six patients responded and
were evaluated by one of the authors (PN) on shoulder
function, arm volume, arm circumference and axillary
sensation. All patients undergoing breast-conserving
therapy received irradiation of the breast. Patients were
operated on by surgical residents under supervision of
experienced surgeons or by the experienced surgeons
themselves.
The questionnaire included the simple shoulder
test (11), a tool for subjective arm function assessment
and the brief pain inventory (12), a pain measurement
tool using a visual analogue scale (VAS) and a questionnaire on influence of pain in daily activity. Patients were
asked to rate the pain intensity experienced in recent
weeks, prior to the measuring moment.
Questions on lymphoedema, impaired shoulder function and loss of axillary sensation influencing daily
activities were added to assess subjective morbidity.
Lymphoedema was assessed by volume measurement

Arm Morbidity after Complete Axillary Lymph Node

(13-14) and measurement of arm circumference of both
arms using the untreated side as control (15). The volume measurement was done by immersing the arm in
90 flexed position in a reservoir of warm water with an
outlet at exactly 15 cm from the bottom. The overflow
was measured using a balance. Lymphoedema was
defined using the division proposed by KISSIN M. W. et
al. (14). Moderate lymphoedema is a difference in arm
volume within a range of 200 to 500 ml ; severe lymphoedema is a difference in arm volume more than
500 ml. The arm circumference was measured 15 cm
above and 10 cm below the olecranon using a measuring-tape. Care was taken to avoid constriction of the soft
tissues by the tape. Lymphoedema was defined as a difference in circumference of 2 cm at one of the measuring points (14-15).
Shoulder function was measured in abduction and
anteflexion using a goniometer, with the patient standing
against a wall in an upright position. Patients were asked
to make the movements within pain limits. A restriction
in shoulder function was defined as 20 or more difference in range of motion between the treated side and
unaffected side (16). Postoperative therapy for shoulder
function was not given on a routine basis and mobilization was started the first postoperative day.
Impairment of axillary sensation was measured using
a pinprick test. For lymphoedema and shoulder function
the unaffected side was used as internal control. Eight
patients were excluded in the objective measurement of
shoulder function because of a pre-existing shoulder
problem (n = 5) or a previous ALND at the contralateral
side (n = 3). The latter three patients were also excluded
for lymphoedema measurement
Data were analysed using Epi Info Version 6b,
(Centres for Disease Control & Prevention, USA, World
Health Organisation, Geneva, Switzerland).
For relations between metric variables, the Pearson
correlation coefficient was used. We compared mean
using the t-test and percentages using the l2 test. The
extent to which the variables were independently associated was examined using a logistic or linear regression
analysis. A p-value < 0.05 was defined as statistically
significant.
Results
General data
The mean age of the respondents was 56 years (SD
13.3), with a median follow-up of 14.3 months (range 425 months). Sixty-two percent of the patients were postmenopausal. According to the UICC tumour staging
(International Union Against Cancer), 36 patients had
stage I, 65 patients stage II, and 5 patients stage III
disease. Twenty-nine patients were treated by breast

213
Table I
Morbidity found in this study compared to literature.
Present study

Seroma
Infection
Lymphoedema
Shoulder dysfunction
Pain

(%)

56
6
13
26
51

(53)
(5)
(13)
(25)
(48)

Literature (%)
15, 17, 18, 19, 20, 21
(10-52)
(1-14)
(7-20)
(16-36)
(16-36)

conserving therapy (27%) and 77 patients by modified

radical mastectomy (73%).
Eleven patients received adjuvant radiotherapy on the
axilla and supraclavicular region in combination with
chemo- or hormonal therapy, 24 patients received only
hormonal therapy (tamoxifen) and 14 patients
chemotherapy alone. Fifty-six patients (53%) had postoperative seroma, complicated in 7 patients by
wound/seroma infection (Table I). Eight patients had a
re-intervention, 5 patients for wound infection and 3
patients for haematoma.
Ninety-three percent of the patients had operationrelated morbidity varying from lymphoedema to loss of
sensation in the axilla.
Lymphoedema
Thirteen patients (12.6%) were identified having lymphoedema by volumetric measurement with an average
volume difference of 280 ml (range 225 ml-442 ml).
None of the patients had severe lymphoedema
(> 500 ml). When using circumference measurement, in
10 patients moderate lymphoedema was found.
Although the measurement using circumference was
significantly related to the volumetric method (p-value
0.001), it proved to be less accurate in identifying
patients with lymphoedema ; 3 patients were not identified having lymphoedema using the circumference measurement. Two patients experienced important limitations in daily activity due to lymphoedema.
Eleven patients received adjuvant radiotherapy on the
axilla and peri-clavicular region, of which 6 patients
(55%) had lymphoedema identified with the volumetric
measurement. After correction for the lymph node stage
with logistic regression, we found a significant relation
between adjuvant radiotherapy and lymphoedema (pvalue = 0.001, odds ratio 37.2) (Table II).
Shoulder function
A restriction in shoulder function was observed in 39 out
of 106 patients (37%). Anteflexion was restricted in
6 patients (median 27, range 25-45), abduction in
7 patients (median 35, range 30-70). A combined

214

P. H. A. F. Nagel et al.
Table II
Lymphoedema in relation to adjuvant radiotherapy

Volume

Adjuvant
radiotherapy
(n)

No adjuvant
radiotherapy
(n)

Total
(n)

< 200 ml
200 ml

5
6

85
7

90
13

11

92

103

Total

Fig. 1
Axillary nodes removed

Table III
Restriction in shoulder movement in relation to adjuvant
radiotherapy
Restriction in
abduction/anteflexion

Adjuvant
radiotherapy
n (%)

No adjuvant
radiotherapy
n (%)

< 20
20

2 (18)
9 (82)

73 (72)
17 (28)

Total

11

90

Restriction is shown as a difference between treated and unaffected

side.

Axillary sensation
A decrease in sensation of the axillary region in the
enervation area of the intercostobrachial nerve was seen
in 99 patients (93%). A significant relation between
adjuvant radiotherapy, time after operation, lymph node
status and number of removed lymph nodes was absent.
Lymph node status

restriction in anteflexion and abduction was observed in

26 patients (median 45, range 27-120).
Eleven patients received adjuvant radiotherapy on the
axilla and peri-clavicular region, of which 9 (82%) had
a restriction in anteflexion and abduction ; the remaining
2 patients had no restriction in shoulder function. After
correcting for lymph node stage with logistic regression,
a significant relation between restriction in shoulder
function and adjuvant radiotherapy was found (p-value =
0.001, odds ratio 16.7) (Table III).
The shoulder function measured with a goniometer
has a good correlation with the simple shoulder test (correlation coefficient r = 0.65, p-value = 0.001). Therefore
both methods can be used to measure an impaired
shoulder function.
Pain
Fifty-five patients had no pain at time of follow-up related to the operation ; the remaining 51 patients (48%)
had a median pain score of 2, (range 1-10). Measurement of the influence of pain on daily activity gave a
median score of 2, (range 0-10).
There is a relation between pain and impaired shoulder function. Patients with an impairment of shoulder
function have a median pain score of 3.0 compared
to 0.7 in absence of impairment of shoulder function
(p-value < 0.0001).

In the axillary fat a mean of 11 lymph nodes (SD 4.6)

was found by the pathologist (Fig. 1). Thirty four percent of the patients had less than 10 nodes removed. The
number of nodes removed had no influence on shoulder
function, lymphoedema, pain or axillary sensation.
However, we did find a significant relation between
an increased number of removed nodes and a higher
possibility of finding a tumour positive node (p-value
0.015) (Table IV).
Discussion
In the present study, we found a substantial morbidity of
ALND as part of the treatment of invasive breast cancer.
The influence on daily life is high, especially due to
restriction in shoulder function and pain. Almost every
patient has some sort of complaint that can be ascribed
to ALND varying from lymphoedema 13%, restriction
in shoulder function 37%, pain 48% and numbness in
the axillary region 93%. These figures can be compared
to those described in literature : lymphoedema : 7-16%,
shoulder function impairment : 16-30%, pain : 16-36%
and numbness 30-90% (15, 17-21).
This high overall morbidity can at least partly be
ascribed to the short median period of follow-up
(14.3 months - range 5-25), since morbidity resulting
from pain, shoulder stiffness and loss of axillary sensation tends to improve with longer follow-up. In contrast,
lymphoedema rates and grade tend to increase with
longer follow-up (14, 16, 20)

Arm Morbidity after Complete Axillary Lymph Node

Table IV
Number of patients with positive nodes compared to the
number of dissected nodes
Number of lymph nodes
dissected

Patients
(n)

Patients with positive

lymph nodes
n (%)

0-9
10-19
20-30

42
75
6

10 (24)
33 (44)
3 (50)

Lymphoedema was identified using the volumetric

measurement in 13 patients all having mild lymphoedema. No patients were identified having severe lymphoedema. However, 3 patients had severe impairment
of daily activities due to lymphoedema. These patients
might in fact be considered to have functionally severe
lymphoedema. Consequently, a subjective scoring system should be developed in order to quantify the influence of lymphoedema on daily life. Currently, all
patients at our hospital with measured lymphoedema as
well as those patients with complaints suggestive of
lymphoedema are referred to a dedicated manual therapist.
Although the volumetric method is more accurate in
measuring lymphoedema, circumference measurement
is easier to perform and therefore more practical in an
out-patient setting (14).
Restriction in shoulder function, anteflexion or
abduction, was present in 39 patients (37%). Combining
anteflexion and abduction to define a restriction in
shoulder function, results in 26 patients with a more
severe restriction (median 45). The latter definition correlates well with the subjective impairment (simple
shoulder test). The simple shoulder test could therefore
be used for follow-up avoiding time consuming measurements in an out-patient setting. This subjective evaluation is satisfactory for daily practice to identify an
impaired shoulder function and the possible effect of
physiotherapy on shoulder function.
The morbidity of ALND is especially severe in those
women undergoing adjuvant radiotherapy in the axillary
region. The incidence of lymphoedema and impairment
of shoulder function is higher among patients receiving
adjuvant radiotherapy (20-21). At the time of this
research, patients in our clinic received adjuvant radiotherapy on the axilla based on extra-nodal growth, > 4
nodes positive or a positive apical node.
Almost half of patients have pain as a result of the
operation, however the median VAS score is low. Pain
can be caused by infection, seroma, injury to the intercostobrachial nerve, radiotherapy and postural changes
(22-23). Since psychosocial factors heavily affect pain

215
experience, evaluation of pain influence on daily activities is more important than measurement of pain intensity alone and a pain measurement tool should therefore
include both measurements.
The relationship between pain and impairment of
shoulder function is not yet described in literature and
might be explained by a restriction in shoulder function
caused by pain or vice versa. This relationship needs further study as to the cause and possible treatment of two
of the most serious and invalidating sequellae of ALND.
Numbness in the axillary region occurred in almost
every patient (93%), probably due to the transsection of
the intercostobrachial nerve which is not preserved during operation in our hospital. Five percent of these
patients said to experience severe impairment in daily
activities. Although preservation of the intercostobrachial nerve reduces sensory impairment, no influence
on restriction of shoulder function, lymphoedema, pain
or seroma formation has been described (2-3).
We were not able to show any influence of the number of lymph nodes removed on the development of lymphoedema probably because of the low variance in number of removed nodes. However dissection of level III
nodes has been related to increased risk of lymphoedema (2). Poor sampling of the pathologist most likely
causes the low number of nodes removed. There was no
gross difference in removed nodes between different
surgeons. Recently, we described a good assessment tool
(2) by use of X-ray for lymph node determination in the
axillary dissection specimen. This might be used to see
if the low number of nodes removed is indeed caused by
inadequate sampling.
Due to screening programmes, early detection of
breast cancer has led to increasing numbers of ALND
with disease-free axillary nodes (3, 5). Therefore sentinel node biopsy has recently been promoted in order to
replace unnecessary ALND by removing only the first
draining lymph node. Many studies confirm that a disease-free sentinel node reliably predicts a disease-free
axilla (10, 26). However, when the sentinel node biopsy
concept proves successful, patients presenting with a
tumour positive sentinel node currently still need a complete ALND. Depending on the extent of nodal involvement, adjuvant radiotherapy is often still indicated to
optimize local control. Patients with tumour positive
nodes and especially those needing adjuvant radiotherapy remain at high risk for morbidity following ALND.
In conclusion, these results confirm the potentially
severe effects of a staging procedure on a relatively
young population. It is a plea for implementing the sentinel node biopsy leading to a selective ALND policy.
Indications for adjuvant axillary radiotherapy should be
revised with scrutiny for each individual patient, bearing
in mind the disastrous consequences of the combination
of radiotherapy and surgery on the axilla.

216
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P. H. A. F. Nagel
Departments of Surgery
Canisius Wilhelmina Hospital Nijmegen
The Netherlands