Lymphocelespostradicalj.1442 2042.2011.02797.x

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Original Article: Clinical Investigationiju_2797 638..645

Risk factors for pelvic lymphoceles post-radicalprostatectomyWael Y Khoder, Matthias Trottmann, Alexander Buchner, Andrea Stuber, Sabine Hoffmann,

Christian G Stief and Armin J Becker

Department of Urology, University Hospital Munich–Grosshadern, Ludwig-Maximilians-University Munich, Munich, Germany

Background: Lymphoceles (LC) represent a well-described rare complication post-radical prostatectomy (RP). Our aim

was to determine risk factors and to develop possible prevention strategies for LC in a community-based study.

Methods: Data from 1163 RP-patients from 67 clinics between January 2002 and December 2004 were retrospectively

evaluated. Patients underwent pelvic imaging procedures/LC-management during 3 weeks of rehabilitation post-RP.

Results: LC were identified in 304 patients (26%). Lymphadenectomy was carried out in 92% of patients (1001/1086

patients), from which 28% had LC (n = 277) versus 14% without lymphadenectomy (12/85, P = 0.007). Complications (lower

limb edema, pain, thrombosis, infection and bladder compression) were observed in 9% of patients (28/304; 2.4% of totalpatients); necessitating therapy. LC therapy was carried out in 59 patients (5.9%) with pelvic lymph node dissection (PLND)

and in no patients (0%) without PLND (P = 0.021). Risk factors included were patients’ age, body mass index, prostate

volume, TNM-classification, number of removed lymph nodes, previous surgery/therapy, heparin prophylaxis, surgical

instruments and pelvic lymphadenectomy. Univariate analysis showed lymphadenectomy as the only significant risk factor

for the development of LC post-RP (P = 0.007). When applying multivariate analyses using stepwise logistic regression,

only lymphadenectomy was associated with a significant risk for lymphoceles (odds ratio= 2.6, 95% CI = 1.3–4.9,

P = 0.004). Adjusting for other factors, no other factor came close to being significant (P < 0.05). All symptomatic LC were

successfully treated without further sequelae.

Conclusions: Subclinical LC post-RP are more common than thought, and rarely necessitate intervention. Pelvic lym-

phadenectomy represents the only significant factor contributing to LC-development. Because of this, prevention remains

difficult.

Key words: complications of lymphocele, pelvic lymphoceles, radical prostatectomy.

Introduction

A lymphocele (LC) is a collection of lymphatic fluid as a

consequence of surgical dissection of afferent lymphatic

vessels. It is a well-documented complication after pelvic

surgery, with an incidence up to 27%.1 Nowadays, it is the

most frequent non-functional complication of radical pros-

tatectomy and pelvic lymph node dissection (PLND).

LC-development is a problem for patients, because of its

health-related sequelae, such as secondary infection and

thromboembolic events as a result of compression of pelvic

vessels. A correlation between LC and deep venous throm-

bosis (DVT)/pulmonary embolism was shown.2 Further-

more, approximately 50% of all re-interventions carried out

in patients post-radical prostatectomy (RP) were for

LC-management.3

A positive association between the number of removed

lymph nodes (LN) and age at RP with the risk of LC devel-

opment was reported. The most informative predictive

thresholds were 65 years-of-age and 20 LN.4

The exact mechanism (s) of LC-formation and risk

factors have not been completely studied. In the present

retrospective community representative study, tried to obtain

more answers about the risk factors, development and pos-

sible prevention strategies for this problem.

Methods

Between January 2002 and December 2004, data from 1163

patients after RP were retrospectively examined for postop-

erative LC incidence, risk factors and therapeutic manage-

ment. RP were carried out by various surgeons from 67

urological departments (35% of patients were from five

high-volume centers with 250 RP annually). There were

no selection criteria except extravasations in cystography.

All patients underwent 3 weeks of rehabilitation in a spe-

cialized hospital where they were recruited and where all

examinations were either carried out or organized. Every

Correspondence: Wael Y Khoder, M.Sc., M.D., F.E.B.U., Urolo-

gische Klinik und Poliklinik, Klinikum Grosshadern, Marchion-

inistr. 15, 81377, Munich, Germany. Email: wael.khoder@

med.uni-muenchen.de

Received 10 December 2010; accepted 17 May 2011.

Online publication 20 June 2011

International Journal of Urology (2011) 18, 638–643 doi: 10.1111/j.1442-2042.2011.02797.x

638 © 2011 The Japanese Urological Association



patient underwent at least one pelvic ultrasound (US) at the

beginning of hospitalization to diagnose/exclude any com-

plications. LC were diagnosed clinically, during regular US

carried out by a urology team and then by an experienced radiologist, as well as postoperative abdominal computed

tomography (CT). Patients who had LC were controlled

before discharge from hospital. The LC volume was mea-

sured by 3-D volume measurement during US.

If the patient had LC-related symptoms (e.g. pain, edema

etc.), it was considered clinically symptomatic/complicated

LC, otherwise it was considered as subclinical LC (inciden-

tal diagnosis).

LC were defined as any clear fluid collection anatomically

associated with the pelvic sidewall without suspected anas-

tomotic insufficiency (after cystograms) or resolving

hematomas. In case of suspicion, CT was carried out. Aspi-ration or tube drainage in symptomatic cases confirmed the

diagnosis. PLND was defined as excision of all fibro-fatty

tissue along the external iliac vein, including the bifurcation

of the common iliac artery together with fibro-fatty tissue

within the obturator fossa. Sentinel PLND was carried out

under radioguided surgery (with 250 MBq 99 m technetium

nanocolloid). These were found in internal iliac LN (37.7%),

together with the external iliac vein (19%) or with the obtu-

rator fossa (9.2%) as well as presacral, pararectal and

paravesical (16%).5 All demographic, surgical and follow-up

parameters were included in a univariate, as well as

multivariate analysis seeking any significance of LC-development. All variables were considered as continu-

ous variables without any cut-off values or size limits.

Furthermore, risk factors were considered without subclas-

sifications (e.g. PLND, if extended or not, which technique

etc.), selection or exclusion (whether it seems logically

applicable or not). The present study was intended to be

community-based without adjustment for surgeon or depart-

ment. Statistical analysis was only directed to find answers

about the possible risk factors in general.

RP was carried out in 89.7% of patients (1024/1141),

laparoscopic extraperitoneal prostatectomy (EERPE) was

carried out in 6.5% of patients (74/1141) and perineal pros-

tatectomy in 3.8% of patients (43/1141). PLND was carried

out in 95.8% (931/972) of the RP patients, 78.9% (56/71) of

EERPE patients and 22.9% (8/35) of perineal prostatectomy

patients (carried out perineally with the same yield of LN[median 10]; P < 0.001). Information about operation tech-

nique and PLND was missing in 22 and 77 patients, respec-

tively. All patients had one 24-Fr closed drainage system

crossing the extraperitoneal space and fixed in the right

lateral lower abdomen, postoperatively. This was removed

when the amount of fluid was 30 mL/24 h. Prophylactic

subcutaneous abdominal or upper arm low molecular weight

heparin (LMWH) was given starting 1 day before surgery

for the whole hospital stay.

Furthermore, extensive search of the PUBMED database

was carried out and all previous experiences were used to

explain and optimize the developed concepts.

Statistical analysis

For comparison of continuous variables (e.g. age, body mass

index) between different patient groups (e.g. with/without

lymphocele) the Mann–Whitney U -test was used. Catego-

rized data (e.g. tumor classification, operation technique)

was analyzed with the c2-test. Logistic regression models

were used to analyse potential factors for LC-occurrence.

Because of the retrospective character of the study, there

were some missing data in several variables, resulting in

different total case numbers for the various statistical

reports. P-values below 0.05 were regarded as significant.

All calculations were carried out using software STATIS-

TICA (release 8, StatSoft, Tulsa, OK, USA).

Results

Patients and tumor characteristics

Table 1 shows the relationship of age, body mass index,

pathology obtained prostate volume and preoperative

prostate-specific antigen level and the risk of LC

development.

Table 1 Correlation of continuous variables with lymphocele formation in 1163 patients

LC No LC P-value

Median Range Median Range

Age 64 47–78 63 46–78 0.025

BMI 26.0 16.3–38.7 26.1 18.5–40.4 0.502

Prostate volume 50 15–180 42 10–180 0.070

PSA 8.7 0.1–300 7.6 0.1–106 0.185

Number of removed LN 10 1–31 9 1–36 0.589

BMI, body mass index; LC, pelvic lymphoceles; LN, lymph nodes.

Risk factors for pelvic lymphoceles

© 2011 The Japanese Urological Association 639



LC occurred in 27% of patients (201/741) who had pT2

tumors, in 25% (85/346) with pT3 and in 19% (6/31) with

pT4 tumors ( P = 0.459). Furthermore, 27% of patients

(12/45) with missing tumor stage data had LC.

LC was found in 22% of patients with Gleason score

5 (38/176), in 26% (84/321) with Gleason score 6, in30% (97/323) with Gleason score 7, in 23% (17/74) with

Gleason score 8 and 17% (10/60) with Gleason score 9

( P = 0.107). 28% of patients (58/209) with missing Gleason

score data had LC.

In addition, LC occurred in 22% of grade 1 (G1) tumors

(13/60), in 26% of G2 (181/700), in 27 of G3 tumors

(71/265; P = 0.715) and in 28% of patients (39/138) with

missing G data.

LC developed in 29% of patients (19/65) with LN

involvement (N+) versus 27% of patients (264/964) with

free nodes ( P = 0.747). Of the patients with missing LN

status, 16% (21/132) developed LC.Similarly, LC occurred in 25% of patients (61/240) with

positive surgical margins (R +) versus 25% (151/611)

( P = 0.831) with free margins (R0) and in 29% of patients

(92/312) with missing surgical margin status.

There was no significant difference in LC-incidence

between the patients with and without preoperative anti-

androgen therapy, 29% (31/107) versus 26% (273/1056)

( P = 0.484). No significant difference in incidence was

found between patients with versus without postoperative

radiotherapy, (22% [17 from 79] vs 26% [287 from 1084];

P = 0.333).

There was no significant difference between university,teaching, tertiary and private hospitals (31 vs 25 vs 29 vs

31%, respectively).

Surgical factors

As shown in Table 2, LC were found in 27% of patients

(275/1024 patients) after RP, in 30% (22/74) after EERPE

and in 16% (7/43) after perineal prostatectomy, showing no

significant difference in incidence ( P = 0.253). Many

cutting and/or coagulation devices were used during the

operations, such as bipolar coagulation or ultrasonic shears.

LC developed in 28% of patients (53/192) using a nerve-sparing technique versus 22% (28/128) using a wide exci-

sion ( P = 0.248). The information about nerve-sparing

technique was missing for 843 patients. Of these patients,

26% (223/843) developed a LC. Lymphadenectomy was

carried out in 92% of patients (1001/1086 patients with

available data about PLND status), from which 28% had LC

(n = 277) versus 14% without PLND (12/85; P = 0.007). Of

the patients with missing data about PLND, 19% (15/77)

showed a LC. Logistic regression analysis (Table 3) showed

PLND as the only significant risk factor for LC (odds

ratio = 2.6; 95% confidence interval 1.3–4.9; P = 0.004).

There was no significant difference in regard to the number

of resected LN between the two groups: median 10 (range

1–31) LN in patients with LC. Median 9 (range 1–36) LN in

patients without LC ( P = 0.589). Furthermore, 25% (13/51)

of the patients with sentinel LN dissection and 26% (291/

Table 2 Correlation of categorical variables with lympho-

cele formation in 1163 patients

% LC n LC/n total P-value

pT2 27 201/741 0.529

pT3a 23 48/207pT3b 27 37/139

pT4 19 6/31

Gleason6 25 122/497 0.059

Gleason 7 30 97/323

Gleason 8–10 20 27/134

N0 27 264/964 0.747

N+ 29 19/65

R0 25 151/611 0.831

R+ 25 61/240

Anti-androgen therapy 29 31/107 0.484

No anti-androgen therapy 26 273/1056

Radiotherapy 22 17/79 0.333No radiotherapy 26 287/1084

Type of hospital

0.132Academic 31 80/258

Community 26 197/753

Operation technique

0.253Retropubic 27 275/1024

EERPE 30 22/74

Perineal 16 7/43

Nerve-sparing 28 53/192 0.248

Wide excision 22 28/182

LAE 28 277/1001 0.007

No LAE 14 12/85

SLN 25 13/51 0.914

No SLN 26 291/1112

EERPE, extraperitoneal endoscopic radical prostatectomy;

N+, lymph node metastasis; N0, tumor free lymph nodes;

perineal RP, perineal radical prostatectomy; PLND, pelvic

lymph node dissection; pT, pathological stage; R+, positive

surgical margins; R0, free surgical margins; RRP, retropubic

radical prostatectomy; SLN, sentinel lymph node dissection.

Table 3 Multivariate analysis (logistic regression model) offactors that were significantly correlated with lymphocele

formation in univariate analysis

Odds ratio 95% CI P-value

Age 1.7 0.9–3.1 0.085

Lymphadenectomy 2.6 1.3–4.9 0.004

WY KHODER ET AL.




1112) of the patients without sentinel LN dissection had LC

( P = 0.914). Therapeutic intervention was carried out in 59

LC-patients. There were 5.9% (59/1001) LC requiring inter-

vention in patients after PLND compared with no therapy in

patients without PLND ( P = 0.021). There was no correla-

tion between the number of removed LN and the need for intervention therapies: median 9 (range 1–36) LN in patients

without therapy versus median 10 (range 2–27) LN in

patients with therapy, respectively ( P = 0.476). There was no

correlation between other parameters and LC requiring

therapy.

Lymphocele characteristics

LC were diagnosed in 304 patients (26%) through postop-

erative abdominal US with a median volume of 83 mL

(range 20–1800 mL). There was no correlation between the

localization of the LC (26% left side, 57% right side, 11% bilateral, 6% paravesical) and the operation technique

( P = 0.404). A total of 83% of the LC were unilateral.

Complications were observed in 9% (28/304) of

LC-patients: lower limb edema occurred in 4.3% (13

patients), pain in 3.0% (9 patients) thrombosis in 1.3% (4

patients), infection in 1.3% (4 patients) and compression of

the bladder (progressively increasing incontinence) in 0.3%

(1 patient). There was no correlation between the incidence

of complications and the surgical approach ( P = 0.393).

Data about the complete progress of LC-volume over the

whole follow-up period were complete in 48 cases. The

median LC-volume was higher in patients with complica-tions than in patients without (median volume 120 mL

[range 20–1800 mL] vs 83 mL [range 20–500 mL], respec-

tively; P = 0.258). Patients with <100 mL LC-volume had

23% incidence of complications versus 27% in patients with

100 mL LC-volume ( P = 0.738). Patients with LC therapy

had a significantly higher LC volume than patients without

therapy (median 110 mL vs 48 mL, P = 0.049). LC therapy

was carried out prophylactically in some patients with large

LC to prevent complications.

DiscussionThe present patient cohort from 67 clinics represents a non-

selected group of men who underwent pelvic imaging pro-

cedures during standard 3-week rehabilitation post-RP. The

present cross-sectional study represents the community in

Bavaria Governorate, because it corresponds to a randomly

selected group of patients from all patients who underwent

radical prostatectomy in the given period (3 years). Further-

more, the patients included represent small and high-volume

clinics, which is a further aspect of a community represen-

tative study.

The present results confirm the published data that

subclinical-LC occur with higher frequency.1,6 These resolve

spontaneously and rarely become symptomatic requiring

treatment. Diagnosis is mostly with US, although small LC

can be obscured necessitating abdominal-CT in unclear/

complicated cases. Meanwhile, clinically relevant LC might

reach large sizes and/or cause many complications.

The strict extraperitoneal access seems responsiblefor the absence of lymph drainage causing 2.4%

symptomatic-LC (28/1163 patients). Interestingly, the

reported total complication rate after EERPE is 9.68%,

which renders the symptomatic-LC as the most frequent

post-RP-complication.7

There is a wide range of differences in LC-incidence

between studies, suggesting differences in the thoroughness

of operation techniques, different identification methods or

diagnostic imaging, but the actual etiological and preventive

mechanism(s) of this phenomenon remain speculative.

Several surgical devices have been investigated, hoping to

achieve better hemostasis and reduce seroma formation.Some of our surgeons speculated an increase in LC-

incidence after excessive electrocauterization of lymph

vessels (LV), rather than ligation. This is consistent with the

findings of Porter et al .8 Furthermore, no significant effect

of ultrasonic scalpel was reported,9 which suggests ligation

of lymphatics as an important aspect of PLND-technique.

Meanwhile, 14% of patients had LC without PLND, which

could suggest rough surgical manipulation, abnormal lymph

pathways or pelvic collections (e.g. because of pelvic drain).

These were all asymptomatic and necessitated no treatment.

Interestingly, we observed that only PLND, as such, sig-

nificantly affected the rate of LC-formation regardless of thenumber of LN, which opposes Naselli et al .10 The definition

of an extended LN-dissection is controversial. LN-count has

been suggested by some authors to differentiate an extended

from limited dissection.11 However, as LN-count is not avail-

able to the surgeon during surgery, it is wise to define this

solely on the template excision.12 The current study showed

no increased LC-incidence with increasing number of LNs,

supporting our theory that LC-formation depends solely on

the technique with adequate ligation of lymphatics. Further-

more, there was no correlation between the number of LN

and the need for intervention therapies for LC ( P = 0.476).

Capitanio et al .4 reported, in a patient collection from anacademic center, an informative threshold of 20 LN to

increased LC risk, which was not found in the present

community-based study.

We believe that every surgeon dealing with pelvic-LV will

produce his own rate of LC. Sansalone et al .13 reported a

similar observation that the injury of the lymphatic network

close to the external iliac arteries is the main route for lymph

collection after kidney transplantation and that this can be

greatly decreased by using the common iliac axis as the site

for vascular anastomoses away from this lymphatic injury.

Positive-LN were suspected to increase LC-formation

after gynecological operations.14 This was not found in the





current study and could be explained by lymphatic obstruc-

tion. Similarly, the reason that radioguided surgery often

fails to detect all positive nodes was suggested to be its high

false-positive rate, explained by the fact that tumor cells

obstruct the LV, preventing tracer transport to all “sentinel

nodes”.15

Surgeons should be more aware of this postoperative

complication, particularly with high molecular weight

heparin (HMWH) prophylaxis.16 Prophylactic heparin has

been implicated as a possible risk factor of LC.17–19 In the

current study, LMWH injection in the abdominal wall or

arm was used as a perioperative standard prophylaxis for all

patients. There was no observed increased incidence of

LC-formation compared with the literature. The same

results were stated by Koch and Smith,20 encouraging the

use of prophylactic LMWH injections in the arm rather than

the lower limbs. Furthermore, studies evaluating prophy-

laxis starting postoperatively showed little apparent compro-mise in efficacy compared with when prophylaxis was

initiated before surgery.20 Thus, our concept of starting

LMWH preoperatively and continuing throughout the hos-

pital stay could be recommended.

Araki et al . showed in a large RP series that a drain might

not be necessary in all cases.21,22 This was consistent with

recent studies in other surgical specialties.23 There was no

decrease in LC-incidence alleviating the role of the drainage

in reducing the risk of LC. In contrast, there were reports

favoring drainage.14,24 Meanwhile, it is wise to use a

postoperative drain after EERPE where there are already

punctures.Furthermore, leaving pelvic drains in situ for some days

was reported to impair the reparative and absorptive capaci-

ties of peritoneum, contributing to the problem that its use

was intended to prevent.14,25 Consequently, some intend to

leave the peritoneum open23 or to use an omental J-flap26 to

avoid pelvic collections. The former concept was recently

reported to reduce the rate of post-RP-LC.7

Similar to axial seroma after axillary lymphadenec-

tomy,27,28 there was a progressive increase in the incidence

and size of LC during the first postoperative month as the

patients resumed their normal activities. These LC were

soon stable in size, requiring intervention in just 13.4% of cases. Contemporary to axial seroma, prophylactic postop-

erative pressure bandage is not applicable for pelvic-LC,

which makes this observation irrelevant for LC-prophylaxis,

but it might be relevant for the timing of treatment. Though,

following up LC during the postoperative month before

planning interventional therapy, in the absence of complica-

tions, seems appropriate.

Obesity has been identified as a LC risk factor after

kidney transplantation,29 which was not found in current

study. Similarly, adjuvant therapies, such as hormonal abla-

tion, were not a risk factor. The small, but significant, dif-

ference in age regarding LC-incidence (univariate analysis)

in the present study was probably a result of the high number

of patients and younger patients compared with the pub-

lished informative threshold (63 vs 65 years, respectively).4

The most important issue when dealing with lymphoceles

remains its prevention. This is difficult, because the actual

etiological factors are not definitely described in the litera-ture, but current multivariate analysis showed PLND as a

single independent risk factor. Injury or division of efferent

LV during PLND might cause subsequent accumulation of

lymph fluid in the retroperitoneal space. Pelvic operations

require thorough knowledge about the normal anatomy of

lymphatics and its multiple variants. Careful ligation of lym-

phatics at all margins of resection seems a logical tool to

prevent subsequent LC-formation. Another way is prophy-

lactic opening of the peritoneum at the operation end.7 As

mentioned, it is advisable to avoid the administration of

heparin in the lower limbs. Application of fibrin sealant was

recently published as a preventive measure.30

Isolation and ligation of leaking LV reported for recurrent symptomatic

inguinal LC is difficult to apply to pelvic lymphatics, which

have complex anatomy.

Last, several publications have shown that lymph, like

plasma, contains coagulation factors, and delayed coagula-

tion and wound closure in dissected LV because of specific

characteristics in their cellular structure and the composition

of clotting factors in lymph fluid could result in LC.2,31

The present study has some limitations. First, its retro-

spective character, but a prospective study will have ethical

and technical problems. The patient number is enough to

develop a generalized concept, but our intention was to provide a frame that could hopefully be compared with the

other experiences. Also, dealing with the data as

community-based without specifications/exclusion criteria,

for example, surgeon/approach related, was intended to gen-

eralize the concept. This could be seen as critical by some

authors. Last, as a rare complication, it is difficult to

describe LC-etiology and progress precisely, but hopefully

accumulating experiences could help in this matter.

PLND is the only independent significant factor contrib-

uting to the development of post-RP-LC, which makes pro-

phylaxis difficult. Complications are rare and interventions

are rarely necessary, but high suspension is advisable.

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