Lymphoedema: estimating the size of the problem

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Lymphoedema: estimating the size of the problem

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Lymphoedema: estimating the size of the problem

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Lymphoedema: estimating the size of the problem

Anne F Williams Centre for Research and Implementation of Clinical Practice, Thames Valley University,
London and University of Glasgow, Glasgow, Peter J Franks Professor of Health Sciences, Centre for Research
and Implementation of Clinical Practice, Thames Valley University, London and Christine J Moffatt Professor of
Nursing, Centre for Research and Implementation of Clinical Practice, Thames Valley University, London

Lymphoedema is a problem frequently encountered by professionals working in palliative care. This article reviews the evidence on the magnitude of the problem of lymphoedema in the general population and provides evidence on specific high risk groups within it.

Prevalence is a good indicator of the burden of disease for chronic problems such as lymphoedema, as it indicates the numbers of patients who require care. Incidence is indicative of changes in the causes of lymphoedema and the success of any prevention programmes. Both are important means of assessing the current level of need and the
potential for the changing needs in managing this condition. Problems exist in all studies in relation to precise definitions of lymphoedema, inconsistent measures to assess differential diagnosis and poorly defined populations. While there is some evidence of high rates in
relation to breast cancer therapy, the total burden of lymphoedema in the general population is largely unknown. Palliative Medicine 2005; 19: 300 /313

Key words: chronic oedema; epidemiology; prevalence; Lymphoedema; incidence

Introduction

Lymphoedema is a chronic swelling arising from the
accumulation of fluid and other tissue elements that would
otherwise drain via the lymphatic system. It can be a
grossly disfiguring condition, usually affecting a limb,
which causes discomfort and may cause pain, and can be
complicated by recurrent infections often requiring hospital
admission. Untreated, limbs can become huge and the
term elephantiasis illuminates their appearance. Sufferers
report the psychological impact of the condition to be
considerable. Causes include cancer treatment, parasitic
infection and congenital problems in the development of
the lymphatic system.

In addition, lymphoedema frequently
occurs in patients with other chronic diseases
e.g., spina bifida, rheumatoid arthritis and stroke.
While not exclusive to palliative care services, the
association between cancer therapy and lymphoedema
has led to many services being located within the palliative
care system. The emphasis of treatment is on helping the
patient to achieve as much self-sufficiency and independence
as possible, given the chronic nature of their
condition and to reduce the incidence of co-morbidity
and the need for intensive therapy and hospitalisation.

This article will review the epidemiology of lymphoedema,
with particular reference to the prevalence and
incidence of the condition.

Epidemiology definitions

Epidemiology is defined as the study of disease in relation to populations.1 Within this there are a number of key measures that are important in defining the disease burden (prevalence) and the number of new cases that develop over a specified time period (incidence). Both measures are important to services providing care to patients since they will indicate the potential care requirements of a population and examine how the disease profile is likely to change over time as new cases add to this burden. The task of obtaining accurate figures for lymphoedema incidence and prevalence is, however, complex and the literature is limited. This paper will discuss some of the difficulties associated with exploring lymphoedema incidence and prevalence and review relevant literature related to specific types of lymphoedema and lymphoedema-associated conditions.

Defining cases of lymphoedema

In evaluating the prevalence and incidence of a condition
it is essential to describe precisely how the disease is
defined. A repeatable, valid and accepted definition will
allow for comparisons between and within ‘at risk’
populations to evaluate temporal and geographical
differences and give some indication of the nature of
the disease. Whilst definitions are essential to determine
the consistency of measurement, lymphoedema is rarely
defined in precise terms. In a previous review, Logan
highlighted some of the problems inherent in ascertaining
rates in lymphoedema.2 Amongst various studies there
are inconsistencies in methods used to determine the
Address for correspondence: Peter J Franks, CRICP, Thames Valley University, 32 /38 Uxbridge Road, London W5 2BS, UK.

E-mail: peter.franks@tvu.ac.uk

Palliative Medicine 2005; 19: 300 /313

# 2005 Edward Arnold (Publishers) Ltd 10.1191/0269216305pm1020oa presence of swelling, quantify the degree of swelling and assess skin and tissue changes.

In a recent publication we have used a general
definition of chronic oedema/lymphoedema to describe
the overall presence of swelling to health professionals.
Population studies of this nature frequently rely on
clinical classification of a condition, which may be
confirmed at a later date using more objective invasive
and non-invasive tests.

‘Chronic oedema is a broad term used to describe
oedema which has been present for more than 3
months and involves one or more of the following
areas: limb/s, hands/feet, upper body (breast/chest,
shoulder, back), lower body (buttocks, abdomen),
genital (scrotum, penis, vulva), head, neck or face.
Oedema which develops as a result of a failure in the
lymphatic system is referred to as lymphoedema but
chronic oedema may have a more complex underlying
aetiology. At this stage we do not expect to make a
differential diagnosis but need to record the actual
numbers of people with oedema suggestive of chronic
oedema/lymphoedema, even if a medical diagnosis has
not been confirmed.’3

This recent prevalence study used a case ascertainment
method in an urban health authority and identified a
prevalence figure of 1.33 per 1000.3 However, the authors
suggest this may underestimate the actual number as the
ascertainment of patients through health professionals is
limited where not all patients are likely to be receiving
treatment for their condition. Nevertheless, it is similar to
the 1.44 per 1000 prevalence of chronic oedema in
Norway reported by Petlund.4

Differential diagnoses

There are a number of problems in establishing a
differential diagnosis in lymphoedema, particularly in
relation to primary lymphoedema.5 Although lymphoscintigraphy
is an invaluable tool in assisting in the
diagnostic process, investigative methods are not universally
standardized and can be inadequate. In some
instances, several contributory factors, such as obesity
and venous insufficiency, may confuse the clinical picture
and make accurate diagnosis difficult.5

Despite these difficulties, attempts have been made
over several decades to provide a classification for
lymphoedema.6 9 Browse and Stewart suggested that
only those with obvious abnormality of the large vessels
or aplasia/dysplasia of the peripheral channels should be
considered as having primary lymphoedema and describe
these as genetically determined or acquired later in life.8,9

It is clear that identification of primary lymphatic
abnormalities can be problematic due to the varying
presentations and difficulties with investigation and
differential diagnosis.

The classification of secondary lymphoedema is also
highly problematic. These may be post-traumatic, postinflammation/
infection, secondary to lymph node dissection
and irradiation or result from a range of other
factors.8

The development of swelling, particularly in
those with advanced cancer, may sometimes be due to
failure of more than one system. Lymphatic damage or
insufficiency may be compounded by venous obstruction,
cardiac, renal or hepatic failure. Swelling associated with
chronic venous disease is often not recognised as a
lymphoedema-type problem, despite the knowledge that
ulceration and infection are likely to damage the
lymphatic system.

The term ‘chronic oedema’ has become widely used in describing a range of oedemas, some with a considerable lymphatic component and
many of which have complicated aetiologies. Consideration
of these other types of oedema clearly influences the
data on incidence and prevalence.

While this paper concentrates on lymphatic problems
associated with westernized countries, tropical lymphoedema
is acknowledged as a significant problem in other
parts of the world. Lymphatic filariasis and infestation by
Wuchereria bancrofti is a major cause of lymphoedema in
some areas of Africa and India and has significant
implications for health services in these countries.10

Measuring lymphoedema

Various methods exist for the measurement and calculation
of the degree of swelling.11 Measurement using water
displacement, electric volumetry and skin circumferences
are the most common techniques but are open to
variations in their use. For example, skin circumferences
may be taken at a wide range of sites on the limb. In the
UK the most common technique consists of 4 cm
circumferences extending distally to proximally, which
are used to calculate the total volume of the limb as the
sum of a series of cylinders. A number of studies have
explored the validity and reliability of arm volume
measured by these different methods and most conclude
that while these methods are highly correlated and
reliable, they are not interchangeable and cannot be
mixed or substituted.12 14

In their review Stanton et al . highlight a volume of
/200 ml as measured by water displacement as a
sensitive indicator of arm lymphoedema and this definition
is used in many studies.11 Clearly, reducing this
cut-off figure to /100 ml may appear to increase the
prevalence of lymphoedema,15 but it may also be argued that this also enables identification of mild oedema.

Stanton et al. , however, suggest that percentage differences
are more universally applicable, allowing for
easier comparison and, as such, a difference of 10% in
volume may be an appropriate cut-off point.11 The
potential accuracy of the volumes also requires standar-
Lymphoedema: estimating the size of the problem 301
dization and accuracy in protocols for measurement and
calculations.16

More recently, Bland et al . have suggested the value of
a 5% or /1 cm increase in arm circumference is a reliable detector of probable lymphoedema in the clinical setting.
17

However, although circumferential measurements
are widely used in the literature, many people with
lymphoedema do not have uniform swelling throughout
the limb and it is common for swelling to be localized to
hand or upper arm.18,19 This indicates that reliance on
the use of one or two circumferential measurements of
the swollen limb is inadequate and also does not take in
account any changes in limb circumference due to
increased fat or muscle mass. Asymmetry in limb circumferences
and volumes, due to arm dominance, should also
be a consideration.20

Ideally, circumferences should be taken along the length of the limb and the total limb volume with possible proximal and distal limb segment
volumes should be calculated. Many studies have used
subjective reporting of swelling alone, though the correlation
with objective measures is often poor.18,21

Time to lymphoedema development

The length of time to lymphoedema development is also
an important consideration. Most patients experience an
acute post-operative oedema and this leads to temporary
limb swelling. Persistent oedema for greater than three
months duration is more likely to be lymphoedema and
oedema prior to this point should be excluded. Additionally,
studies need to be undertaken over an adequate
time period as lymphoedema may develop at any stage
post-treatment. Edwards et al. showed the onset of
lymphoedema to occur in the first 18 months postsurgery,
21 while others report a thirty-nine month median
time interval to lymphoedema development.22 This
suggests that a longer follow up is required to ensure
that a late lymphoedema is recognized.19,23

Literature search methodology

A search was undertaken of PubMed, Medline (from
1966), CINAHL (from 1982), the Cochrane Database of Systematic Reviews up to December 2003 and The International Society of Lymphology Congress Proceedings.

The terms lymphoedema, chronic oedema, prevalence,
incidence and epidemiology were used. Filarial
lymphoedema was omitted from the search as it was felt to be beyond the scope of this review.

Primary lymphoedema

At present there are no published figures to confirm
prevalence and incidence of primary lymphoedema.
However, a small number of audits and reviews in the
UK have provided some evidence on the numbers of
patients with primary lymphoedema of those attending
lymphoedema clinics. A national study by the British
Lymphology Society reported that 8% of 603 patients
newly referred to 27 UK lymphoedema clinics over a
three-month period suffered from primary lymphoedema.
24

Williams et al. estimated that 12% of the 714
patients attending a lymphoedema clinic over the previous
five years suffered from primary lymphoedema.25
Furthermore, an audit of the 908 patients attending a
clinic over a four-year period, reported 218 (24%) having
non-cancer lymphoedema.26 Of these 218, 62 (28%) were
diagnosed with primary lymphoedema, although only
14 had unequivocal evidence of a primary lymphatic
disorder, the remainder having a history suggestive of a
primary lymphatic cause. However, those already attending
clinics are likely to represent ‘the tip of the iceberg’
and it is likely that patients with primary disease will be
under-represented due to poor diagnosis and services
that often concentrate on patients with cancer related
disease. This is illustrated by the long lead time from
disease onset to referral for treatment.24

Other studies outside the UK have adopted a more
epidemiological approach to investigations of primary
lymphoedema. A retrospective evaluation of primary
lymphoedema in Minnesota (USA) between 1955 and
1974 estimated an annual incidence rate of 1.15/100 000
in the population aged under 20.27

More recently, a national epidemiological study in Spain surveyed 308
centres such as surgical and vascular units.28 From
2743 people with lymphoedema identified by these units, 1009 (36.8%) were reported as having primary lymphoedema.

Of these, 2% were recognised as having congenital
lymphoedema (present from birth), 30% were estimated
to have lymphoedema praecox (swelling developing
around puberty) and 68% were reported as having
lymphoedema tarda (lymphoedema developing in later
life). The apparently high number with lymphoedema
tarda indicates that many of these may in fact have
secondary lymphoedema.

Lipoedema

Rudkin and Miller reviewed 250 cases of lower limb
lymphoedema and showed that around 4% exhibited
unique characteristics representative of lipoedema, a
condition distinct from lymphoedema but often diagnosed
as primary lymphoedema.29 Again, there are no
clear figures indicating the numbers affected by this
condition that is frequently associated with, but often
mistaken for, lymphatic insufficiency.
302 AF Williams et al.

Secondary non-cancer-related swelling
There may be a range of factors contributing to the
development of lymphoedema, including chronic venous
disease, trauma, inflammation, infection and conditions
such as arthritis. However, prevalence and incidence data
on these secondary causes are limited. One small study in
the UK explored the prevalence of oedema in leg ulcer
patients in hospital and the community.30 It suggested
that oedema was present in 55% of the 56 patients,
although the prevalence in the community-based patients
was much greater at 77%. Another study of 689 chronic
leg ulcers identified 17 cases of ulceration due to
lymphoedema.31

Blankfield et al. investigated the causes of bilateral
leg oedema in 45 primary care patients in the USA.32
Investigation with ECG and duplex scan of the legs
identified 33% with cardiac cause, 42% with pulmonary hypertension and 22% with venous insufficiency.

Other causes of leg swelling included medication,
nephrotic syndrome and hypoalbuminemia. The researchers
concluded that leg swelling, particularly in
those over 45-years-old, requires investigation as problems
such as congestive cardiac failure and pulmonary
hypertension are poorly recognised, particularly in
their early stages.

Cancer-related lymphoedema

Lymphoedema related to cancer and/or cancer treatment
may be readily identified as patients usually have an
obvious clinical history and have regular follow up after
their cancer treatment. In the audit by Sitzia et al. ,24 80%
of the 603 newly assessed patients were estimated to have
cancer-related lymphoedema, this group suffering from
swelling for a much shorter period than those with
primary lymphoedema.

Lymphoedema is most commonly associated with
surgery and/or irradiation to the lymph nodes. Shaw
and Rumball reviewed the case notes of 208 patients
who underwent cervical, axillary or inguinal lymphadenectomy in order to study the incidence of complications.33

Their classification distinguished between early
(less than one month) and late (more than one month)
onset. They reported an overall incidence of late
lymphoedema as 14.9% and identified lymphoedema as
the most common long-term complication, particularly
in patients who underwent groin dissection. The study
did not identify how lymphoedema was defined or
measured.

Breast cancer-related lymphoedema

In 1921, Halstead recognised the problems of arm
swelling following breast surgery and assumed this
‘surgical elephantiasis’ was due to streptococcal infection. 34 A summary of the literature on breast cancer related lymphoedema is given in Table 1.15,18,21 23,42 66 It is clear from Table 1 that there have been a large number of investigations of breast cancer related lymphoedema.

The majority of these studies have attempted
to identify factors in the treatment of the breast cancer
that predispose patients to develop lymphoedema. The
studies indicate that there is a wide range of incidences,
much of which may be explained by differences in case
definition and sampling procedures. There appear to be a
number of themes around the risk factors associated
with lymphoedema development, particularly, the use of
irradiation,15,36,37,39,45,47,49,54 56 the extent of axillary
node dissection,35,36,40,54,56,59 61,63,65,66 combined axillary
surgery and irradiation,22,41,43,46,48,50,51,60,62, obesity,
21,35,36,45,57,61 surgical wound infection,37,40,45,57
tumour stage and extent of surgery.21,48,49,51,56 Despite
improvements in surgical technique it is difficult to see
reductions in the incidence of lymphoedema, with
more recent studies still exhibiting high rates of development
in excess of 30% of women treated.18,63,64
However, this may be a consequence of detecting more
mild cases in isolated parts of the arm, such as the hand
or forearm.18

Lymphoedema secondary to groin dissection
The study by Shaw and Rumball reported a 40%
incidence of lymphoedema following groin dissection
confirming a previous study of 55% of 90 patients who
underwent ilio-inguinal dissection.33,67 When 33 of the
previous 90 patients were followed up at a review clinic,
26 (79%) reported some experience of swelling, often
worse in the first six months after surgery. Twenty-two
(67%) of the 33 patients had persistent lymphoedema at
the time of review, a follow up period ranging from one
to eight years post-treatment.

Lymphoedema secondary to malignant
melanoma

Commonly the management of malignant melanoma
involves ilio-inguinal lymph node dissection and a study
from 1977 reported a lymphoedema incidence of up to
80% in these patients.68 Other studies have identified
lymphoedema in 23 and 26% of patients, respectively and
Lymphoedema: estimating the size of the problem 303

Table 1 Summary of papers/studies of breast cancer-related lymphoedema and reported risk factors
Author/s and dates Details Reported incidence Measurement method Definition of oedema Risk factors described
Fitts et al. (1954)53 Review of papers and study of
130 women following radical mastectomy 8 /95% (reviewed papers).

49% (study group)
Clinical examination Not defined Obesity; number of axillary nodes
removed; wound margin necrosis
Treves (1957)36 Study of 768 women following
mastectomy

41% Circumferential measurements ]/3 cm Circumference
increase compared with
contralateral limb
Axillary surgery; obesity;
irradiation
Britton and Nelson
(1962)37
Review of 19 papers 1908 /1960
and study of 114 lymphoedema
patients
6.7 /62.5% (reviewed papers) Circumferential measurements ]/2 cm Circumference
increase compared with
contralateral limb
Post-op wound complications:
delayed healing; cellulitis,
irradiation damage to skin
Howell-Hughes and
Patel (1966)38
Review of 11 papers 1944 /1960 41 /80% Not discussed Not defined Lymphatic and venous
obstruction due to fibrous tissue
Markowski
et
al.
(1981)39
Study of 58 women following
mastectomy; 39% had irradiation
31% Circumferential measurements
at five sites
]/1.5 cm Circumference
increase at two or more sites
compared with contralateral
limb
Irradiation; inadequate nutrition
leading to delayed wound healing
Penzer
et
al.
(1986)40
Study of 74 women following
breast conserving surgery and
breast irradiation; 86% had axillary
node dissection (AND) and 24%
had axillary irradiation
14% overall; 7% (those B/60
years) 25% (those /60)
Circumferential measurements
at two sites (forearm and upper
arm)
]/2.5 cm Circumference
increase compared with
contralateral limb or pitting
oedema in dorsum of hand
Age /60 years; axillary node
dissection; wound infection;
surgical splitting of pectoralis
minor muscle in /60 years
Ryttov
et
al. (1988)41 Study of 57 patients following
mastectomy; 23% had irradiation
11% (surgery alone); 46%
(surgery and irradiation)
Circumference 10 cm above
epicondyle
]/2.5 cm Circumference
increase compared with
contralateral limb
Adjuvant irradiation in those with
metastatic axillary nodes
Badr El Din
et
al.
(1989)42
Review of files of 100 patients
with stage 3 breast cancer treated
1974 /1988; all had neo-adjuvant
irradiation and 74% had neoadjuvant
chemotherapy; 92% had
mastectomy
22% Not discussed / case study
review
Not defined Not defined
Aitken
et
al. (1989)43 Study of 94 patients; 42% had
mastectomy and axillary
clearance; 58% had mastectomy
and axillary sampling and 52% of
these had irradiation
8 /32% Circumference at 15 cm above
and 10 cm below olecranon
Not defined Combined axillary surgery and
irradiation
Hoe
et
al. (1992)44 Study of 118 patients; 51% had
mastectomy and axillary
clearance; 49% had wide local
excision and axillary clearance
then breast irradiation
7.6% Water displacement ]/200 ml Increase compared
with contralateral limb
Similar risk with axillary sampling
and clearance
Segerstro¨m
et
al.
(1992)45
Study of 136 women following
mastectomy and AND; 63% had
irradiation
21 /89% (depending on factors
studied)
Water displacement ]/150 ml Increase compared
with contralateral limb
Obesity; oblique skin incision;
infection; irradiation
Thompson
et
al.
(1995)46
Study of 121 patients following
wide local excision and axillary
surgery; 61% had irradiation
21% (axillary sampling); 30%
(axillary sampling and
irradiation); 29% (axillary
clearance); 54% (axillary
clearance and irradiation)
Water displacement.
Circumferences at 10 cm distal
and 15 cm proximal to
olecranon
]/200 ml Increase compared
with contralateral arm
Combined axillary surgery and
irradiation
304 AF Williams et al.
Table 1 ( Continued)
Author/s and dates Details Reported incidence Measurement method Definition of oedema Risk factors described
Ferrandez
et
al.
(1996)47
Study of 683 women following
mastectomy, axillary node
sampling and irradiation
41% Circumference at eight sites on
arm
]/1.5 cm Circumference
increase at two or more
adjacent sites compared with
contralateral limb
Axillary irradiation; delayed
wound healing; thoracic fibrosis
Kissin
et
al. (1996)48 Study of 200 patients following
mastectomy (35%) or wide local
excision (WLE) (65%); 44% had
irradiation
8.3% (axillary irradiation);
9.1% (axillary sampling and
irradiation); 7.4% (axillary
clearance); 38.3% (axillary
radiotherapy and irradiation)
Circumference at 15 cm above
lateral epicondyle and water
displacement
]/200 ml Increase compared
with contralateral limb
Combined axillary surgery and
irradiation; breast irradiation;
nodal status; tumour stage
Mortimer
et
al.
(1996)49
Review of 1077 women following
mastectomy (93%) and WLE (7%)
for unilateral breast cancer
without recurrence; 467 (43%)
had irradiation
28 /38% Self reported questionnaire /
method validated
Self reported Irradiation; mastectomy has
greater risk than WLE
Suneson
et
al.
(1996)50
Study of 362 women with breast
cancer comparing those treated in
1983 (94% mastectomy: 6%
WLE) and those treated in 1988
(71% mastectomy: 29% WLE);
irradiation in 48% (1983) and 52%
(1988)
8 /15% Not discussed Not defined Number of /ve axillary lymph
nodes; combined axillary
dissection and irradiation
Schunemann and
Willich (1997)51
Study of 5868 women treated
1972 /1995; various combinations
of surgery and irradiation
24% (overall); 22.3 /44.4%
(depending on cancer
treatment)
Circumferential measurements
10 cm above and 10 cm below
olecranon
]/2 cm Circumference
increase compared with
contralateral limb
Combined surgery and irradiation;
radical breast surgery
Petrek and Heelan
(1998)52
Review of seven papers and study
of 272 women treated 1976 /78
6 /30% (reviewed papers);
28% (study group)
Self reported circumferential
measurements at two sites
below and above the
olecranon / method validated
Circumference increase
compared with contralateral
limb. ]/2 inches / severe.
1 /2 inches / minimal
Not identified
Kissane
et
al.
(1998)53
Study of 303 women treated for
early stage breast cancer
4.3% Self reported Not defined Not identified
Berlin
et
al. (1999)15 Study of 226 women following
mastectomy in 1979 /1983 (five
year follow up); unknown number
had irradiation
20% Water displacement ]/100 ml Increase compared
with contralateral limb
/ve axillary lymph nodes
requiring irradiation
Højris
et
al. (2000)54 Study of 84 women following
mastectomy and axillary node
dissection for stage 1 and 2 breast
cancer; high risk patients had
adjuvant irradiation and/or
chemotherapy
26% (subjective report)
3 /14%
Circumference 15 cm above
and 10 cm below the
olecranon. Also used nine
circumferential measures to
calculate volume
]/200 ml Increase compared
with contralateral limb
Axillary dissection; non-significant
increased risk in irradiated group
Tengrup
et
al.
(2000)55
Study of 110 women T1, N0
staging following mastectomy and
axillary dissection; 68% had
irradiation
19% Self reported and water
displacement
/10% Increase in arm
volume in relation to
preoperative
volume
Irradiation
Edwards (2000)21 Study of 201 women treated
1994 /6; 57% had mastectomy
(22% irradiated); 43% WLE (72%
irradiated)
11%; (23.4% subjective) Water displacement and self
reported. Volume adjusted to
address natural asymmetry of
arms
]/10% Increase in arm
volume compared with
contralateral arm
High BMI; axillary surgery;
mastectomy /risk than WLE;
tumour size and grade
Lymphoedema: estimating the size of the problem 305
Table 1 ( Continued)
Author/s and dates Details Reported incidence Measurement method Definition of oedema Risk factors described
Herd-Smith
et
al.
(2001)56
Study of 1278 women;
mastectomy (24%); 19% had
WLE and axillary node dissection
without irradiation; 57% had WLE,
axillary node dissection and breast
irradiation
15.9% Arm circumference six 6 sites
to calculate% difference
/5% Increase in sum of the
differences between the two
arms
Post-operative breast irradiation;
T2 tumour classification; ( /30
lymph nodes removed /
borderline risk)
Petrek
et
al. (2001)57 Study of 263 women treated
1976 /8 and followed up over
twenty years
13%; (49% self-reported) Circumferences at four
sites / self measurement
Circumference increase any
one site compared with
contralateral limb; ]/2 inches
defined as severe but noted
50% had mild swelling defined
as increase of B/0.5 inches
Infection; injury; weight gain
Duff
et
al. (2001)23 Study of 100 women with
unilateral breast cancer; 64% had
mastectomy; 36% had WLE and
axillary node clearance
10% Optoelectronic volometer /200 ml Increase compared
with contralateral limb
No association between lymphoedema
and type of surgery or
number of lymph nodes removed
Sener
et
al. (2001)58 Study of 420 women treated with
mastectomy or WLE; 72% had
sentinel lymphadenectomy (SL);
28% had level 1 /2 axillary
clearance due to metastatic
disease in sentinel nodes
3% (SL); 17% (SL and axillary
dissection)
‘Arm measurements’ taken
pre- and post-operatively but
no detail given
/20% Volume increase
compared to contralateral arm
Extent of axillary staging; tumour
in upper outer quadrant of breast;
post-operative trauma and/or
infection to arm
Albrecht
et
al.
(2002)59
Study of 655 women following
WLE and axillary dissection or
irradiation; compared to others
treated elsewhere with combined
axillary surgery and irradiation
1% (axillary irradiation); 26%
(axillary dissection)
Circumferential
measurements / not detailed
/1 cm Increase in
circumference compared with
contralateral arm ( /2 cm if
dominant arm)
Axillary dissection in postmenopausal
women
Kwan
et
al. (2002)60 Study of 112 patients treated
1993 /7 with WLE and breast
irradiation or mastectomy; most
had level 1 or 2 axillary dissection;
high risk patients had irradiation to
supraclavicular and axillary nodes
12.5%; 5% (axillary surgery);
30% (axillary surgery and
irradiation)
Self report questionnaire.
Water displacement.
Circumferences at four sites
/200 ml Increase compared
with contralateral limb. Self
reported
Axillary dissection and irradiation
Meric
et
al. (2002)61 Study of 294 patients treated
1990 /92 with WLE; all had breast
irradiation; 88% had axillary
dissection; 44% had irradiation to
axillary and supraclavicular nodes
13.6%; 18% (surgery with
breast and axillary irradiation);
10% (following surgery alone)
Circumferential measurements
10 cm above and 10 cm below
lateral epicondyle. Subjective
reporting
Any increase in circumference
compared to contralateral arm.
Self report
Axillary node dissection; high
body weight
Nagel
et
al. (2003)62 Study of 106 women treated
1995 /6; 73% had mastectomy;
27% had WLE; 10% had
irradiation
13% Water displacement.
Circumference 15 cm above
and 10 cm below olecranon.
Questionnaire
/200 ml Increase in volume
compared to contralateral arm.
]/2 cm Increase in
circumference at any one
point (identified as less
sensitive than water
displacement)
Axillary lymph node dissection;
adjuvant axillary irradiation
Querci della Rovere
et
al. (2003)18
Study of 198 women following
level 1 and 2 axillary dissection;
with oedema for /6 months;
20% had mastectomy and axillary
dissection; 71% had WLE and AD;
10% had only AD
32.8%; (27.8% were mild to
moderate); (5% were severe).
Oedema seen in single sites
but not affecting whole of arm
in most cases e.g., hand,
forearm
Circumferences at 15 cm
above and 10 cm below elbow.
Subjective assessment by
patient, nurse and doctor
/5% Increase in
circumference compared to
contralateral arm (mild);
moderate /B/10%; severe /
/10%
Nodal status; affected dominant
arm; right sided cancer increases
risk of forearm oedema;
non-consultant surgeon
306 AF Williams et al.
Table 1 ( Continued)
Author/s and dates Details Reported incidence Measurement method Definition of oedema Risk factors described
Geller
et
al. (2003)63 Study of 145 women; 62% had
WLE; 38% had mastectomy; 86%
had AND; 67% had irradiation
38% Self-reported (telephone
interviews)
Age B/50 years; axillary node
dissection; cytotoxic
chemotherapy; work outside
home; lower risk if treated for
hypertension
Kornblith
et
al.
(2003)64
Study of 153 women followed up
at 20 years post adjuvant
chemotherapy; 65% had
mastectomy; unknown number
had irradiation
39% Self-reported (telephone
interviews)
None described
Powell
et
al.
(2003)22
Study of 714 women (727 arms)
women with stage 1 and 2 breast
cancer and treated with breast
conservation surgery and breast
irradiation; 32% had irradiation to
axilla and supraclavicular nodes;
15% had level 1 /3 axillary
dissection
4.1%; 10.7% (axillary surgery
and irradiation)
Circumference of forearm at
10 cm below olecranon
/2 cm Increase in forearm
circumference compared with
contralateral limb. /4 cm /
severe
Combined axillary node surgery
and irradiation
Rampaul
et
al.
(2003)65
Study of patients with primary
breast cancer diagnosed between
1973 and 2000; excluding those
with uncontrolled axillary
ecurrence. Part 1: 1242 patients.
Part 2: 677 patients
Part 1: 0.4% reporting
problematic symptoms
affecting quality of life (not
numbers with swelling). Part
2: 6.2% reported ‘a lot of’
swelling
Part 1: patient self report and
clinical examination by
clinician. Part 2: patient
questionnaires
Suggest circumferential
measurements are of limited
value
Not specific but identify
unnecessary axillary interventions
as increasing the risk
Golshan
et
al.
(2003)66
Study of 125 women (node
negative at time of surgery); 62%
had sentinel lymph node biopsy
and 91% of these had irradiation;
38% had AND; 77% of these had
irradiation
2.6% (sentinel node biopsy
and axillary sampling); 27%
(axillary node dissection)
Circumferences at 10 cm
above and 10 cm below
olecranon
]/3 cm Increase in
circumference compared
with contralateral arm
Axillary node dissection has
greater risk than sentinel node
biopsy

Lymphoedema: estimating the size of the problem 307
a previous review has indicated a 6 /20% incidence of
lymphoedema in patients following combined inguinal
and pelvic lymph node dissection for stage III melanoma.
69 71

Karakousis et al . studied 77 patients following groin
dissection, mainly for malignant melanoma.72 They
identified oedema in 21% of these patients and reported
those who had a primary tumour of the lower leg to be
significantly more likely to develop swelling. They also
showed that those who wore compression garments postoperatively
were less likely to develop swelling. The same
author later studied 205 patients following groin dissection
and suggested that all had some localized oedema of
the anteromedial thigh, with around 40% having swelling
of the lower leg.73 Interestingly, Urist et al. also
suggested lymphoedema to be mostly confined to the
thigh.70

Strobbe et al. studied 71 patients with positive iliac
and/or obturator fossa nodes, reporting mild/moderate
lymphoedema in 19% and severe lymphoedema in 6%
of patients.74 A study by Serpell et al. reviewed
73 lymphadenectomies in 64 patients, showing lymphoedema
to be more common after groin dissection,
occurring in 29% of patients following inguinal surgery
compared to 6% of axillary dissections.75 This study
defined lymphoedema as post-operative swelling persisting
beyond three months and highlighted the use of postoperative
prophylactic measures, such as seven days bed
rest and six months use of below knee compression
hosiery to reduce the risk of lymphoedema.To reduce the
risk of lymphoedema, Wrone et al. suggest that sentinel
node biopsy is associated with a 1.7% incidence of
lymphoedema and Lawton et al . have described the
use of a fascia-preserving technique when complete
lymphadenectomy is indicated.76,77 This study reported permanent oedema in 8% of patients following axillary dissection and 14% of those having groin dissection.

A transient oedema was also present in 48% of the groin
dissection group, resolving over a median of twelve
months. Factors including obesity, post-operative seroma
and occult metastases have been described as contributing
to the risk of lymphoedema in this group.75,76

Lymphoedema secondary to genitourinary
cancers

There is limited literature on this subject and Okeke et al.
suggest that lymphoedema is uncommon from cancers of
pelvic genitourinary organs, such as kidney and testes.78
However, in patients with advanced disease and complications,
such as recurrence or pelvic tumour mass
obstructing venous and lymphatic return, gross oedema
of the legs and genitalia will often occur. Worldwide, the
problem of genital lymphoedema is most common
secondary to filariasis and is also associated with primary
cancer-related lymphoedema and traumatic injury.79 87
Soto et al . reported lymphoedema in 100% of men
following inguinal dissection for penile carcinoma.82
Martin Martinez et al . have also shown lymphoedema
in 28.5% of these patients following inguinal lymphadenectomy
and Ornellas et al. have reported a figure of
16% in this same group.84,85 Male circumcision has also
been shown to be associated with lymphoedema.88

Henningsohn et al. have recently described the development
of swelling or heaviness in the legs or lower
abdomen in 20% of those following radical radiotherapy
compared to 10% of those who had radical cystectomy
and urostomy for carcinoma of the bladder.89 They
indicated that lymphoedema is a minor problem in this
group.

Lymphoedema secondary to gynaecological
cancers

Nesvold et al . cited a lack of information after gynaecological
surgery causing a delay in diagnosis and treatment
of lymphoedema.90 In this study, 83 patients reported a
20% incidence of swelling following treatment for cervical
and vulval cancers, similar to findings reported in other
studies of these patients.91,92

In vulval cancer treatment, Leminen et al. established lymphoedema to be more common in women suffering a wound infection following
radical vulvectomy including groin dissection, occurring
in 48% of patients.93 Gould et al . also showed a 29.5%
incidence in patients undergoing inguinal lymphadenectomy
in the treatment of vulvar carcinoma similar to the
28% incidence reported by other authors.94,95 Preservation
of the saphenous vein during inguinal lymphadectomy
has been advocated as decreasing morbidity in
relation to chronic oedema in this patient group in one
study.96

Lymphoedema has also been shown to occur in
three of 80 patients receiving palliative radiotherapy for
ovarian cancer, although research is limited.97
More substantial literature is available in relation to
cervical cancer. One study reported lymphoedema leading
to distress in 14% of patients, regardless of whether
surgery or surgery combined with radiotherapy was
used.98 Relatively low rates (1%) of ‘severe’ lymphoedema
have also been reported, although how severity was
established is not specified.99 Martimbeau et al . studied
402 patients following treatment for Stage IB cervical
cancer showing that 23.4% developed some degree of
lymphoedema.100 A similar result was reported in a study
by Gerdin et al. (21%) following hysterectomy and
radiotherapy, where the risk of lymphoedema was also
associated with external pelvic irradiation.101 Fiorica
et al. also studied patients following treatment for Stage
IB cervical cancer, with a median follow-up time of
308 AF Williams et al.twenty-eight months.102

No indication is given as to how lymphoedema was measured and only one out of 50 patients was identified as having swelling. Similarly
low incidence figures are reported by Bo¨sze et al. who
assessed perioperative complications in 116 women
having cervical cancer treatment.103 They reported none
with lymphoedema but three with a lymphocyst, who
might be at subsequent risk of swelling. As the authors
surmise, the relatively short follow up period (not
specified) does not allow for evaluation of late sequelae, such as chronic lymphoedema.

A comprehensive study undertaken in Sweden followed
up 54 women post hysterectomy (and radiotherapy
in some cases).104 Of these 54 women, 41% had an excess
limb volume of more than 5% larger than the unaffected
limb and in interviews, eight (15%) described the problem
as serious. Lymphoedema was also observed as more
severe in those who had undergone more than two intracavity
radiotherapy implants.

Interestingly, the authors observed that only women with unilateral lymphoedema were detected using this method, those with mild
symmetrical swelling not necessarily being identified.
Similar results were obtained in a study of 179 women
undergoing radical hysterectomy and post operative
irradiation for cervical cancer in Taiwan.105 This study
showed 42% to develop lymphoedema with 16% going on to develop severe cellulitis warranting antibiotic therapy. A further paper reported lymphoedema of the foot in 49% of women ten years post-cervical cancer treatment.

106 The role of omentoplasty in preventing complications,
such as lymphoedema and lymphocoele, in these
patients has also been described.107,108
Lymphoedema secondary to sarcoma
treatment

Two studies of lymphoedema following sarcoma treatment
have been reviewed. Lampert et al. observed
40 patients who had received wide local excision and
radiotherapy, at least two years previously.109 They
measured oedema using finger pressures to identify skin
pitting and subjectively estimated that approximately
50% had some degree of oedema. Robinson et al . studied
54 patients at least two years post-treatment of soft tissue
sarcoma of the lower limb or pelvis.110 Lymphoedema
was assessed by pinch test and Stemmer’s sign and
categorized according to its extent up the limb. Lymphoedema was identified in 16 (30%) of the patients, although 21 (39%) had experienced swelling at some time. Interestingly, the authors discuss their rationale for avoiding limb circumferential measures suggesting these may be skewed by previous surgery.

Conclusion

This review highlights limitations in the current literature,
both in terms of quality of studies and lack of sound
incidence and prevalence data. Critical reviews of methods
used raises awareness and insight into how subsequent
research might be conducted and where the
possible pitfalls may lie. There are still a number of areas
to be addressed, namely the accurate identification of
lymphoedema and the diagnostic criteria for making
differential diagnoses between different types of lymphoedema
and chronic oedemas.

There is also a need to consider other problems not highlighted in previous
studies, such as breast oedema. There is clearly a need
to produce sound incidence data on particular ‘high risk’
groups, as these will contribute to the pool of new
patients.

This prevention and early detection strategy
may help to prevent patients developing morbidities
associated with the more chronic and severe conditions
of some lymphoedema types. These data will also
contribute to our understanding of the long-term impact
of this progressive condition and provide direction for
future service development.

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