© 2006 Foundation for Promotion of Cancer Research
Evidence-Based Risk Factors for Seroma Formation in Breast Surgery
1 Division of Surgery and Breast Oncology, Nyuwakai Oikawa Hospital, Fukuoka, 2 Department of Healthcare and Social Services, University of Marketing and Distribution Sciences, Kobe, 3 Department of Surgical Oncology, Osaka University Graduate School of Medicine, Suita, Osaka, 4 Department of Epidemiology, National Institute of Public Health, Wako, Saitama, 5 Department of Gastroenterological Surgery, Kyoto University Graduate School of Medicine, Kyoto, 6 Department of Surgery, National Hospital Organization Shikoku Cancer Center, Matsuyama and 7 Department of Health Science, Kochi Women's University, Kochi, Japan
For reprints and all correspondence: Katsumasa Kuroi, Division of Surgery and Breast Oncology, Nyuwakai Oikawa Hospital, 2-21-16 Hirao, Chuo-ku, Fukuoka 810-0014, Japan. E-mail: kurochan{at}dd.iij4u.or.jp
Received November 1, 2005; accepted December 27, 2005
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Abstract |
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Background: Seroma is a common problem in breast surgery. The aim of this systematic review was to identify risk factors for seroma formation.
Methods: Articles published in English were obtained from searches of Medline and additional references were found in the bibliographies of these articles. Risk factors were graded according to the quality and strength of evidence and to the direction of association.
Results: One meta-analysis, 51 randomized controlled trials, 7 prospective studies and 7 retrospective studies were identified. There was no risk factor supported by strong evidence, but there was moderate evidence to support a risk for seroma formation in individuals with heavier body weight, extended radical mastectomy as compared with simple mastectomy, and greater drainage volume in the initial 3 days. On the other hand, the following factors did not have a significant influence on seroma formation: duration of drainage; hormone receptor status; immobilization of the shoulder; intensity of negative suction pressure; lymph node status or lymph node positivity; number of drains; number of removed lymph nodes; previous biopsy; removal of drains on the fifth postoperative day versus when daily drainage volume fell to minimal; stage; type of drainage (closed suction versus static drainage); and use of fibrinolysis inhibitor. In contrast, sentinel lymph node biopsy reduced seroma formation. Evidence was weak, or unproven, for other factors that were commonly cited in the literature.
Conclusions: Although a number of factors have been correlated with seroma formation, strong evidence is still scarce. However, there is evidence showing that sentinel lymph node biopsy reduces seroma formation.
Key Words: seroma • risk factor • breast cancer • mastectomy
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INTRODUCTION |
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Ever since mastectomy was first carried out by Halsted in 1882, surgeons have faced several problems such as necrosis of the skin flaps, breakdown of the wound, hematoma, seroma, and infection (1). Among them, seroma, a subcutaneous collection of serous fluid, is a common problem in breast surgery. As it usually resolves within a few weeks, many surgeons view this problem as an unavoidable nuisance rather than a serious complication (1,2). However, excessive accumulation will stretch the skin and cause it to sag, resulting in patient discomfort and sometimes prolongation of hospital stay (3). To prevent seroma formation, it is important to estimate individual risk of seroma formation. In this study, we carried out a systematic review of risk factors for seroma formation.
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METHODS |
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The primary outcome of interest was the incidence of seroma formation after breast surgery in patients with primary breast cancer. To identify published articles on seroma, a computer-assisted MEDLINE search was conducted from 1966 up to July 2005. We also searched the Cochrane Library database for relevant systematic reviews, and additional references were found in the bibliographies of these articles. The reference terms ‘breast cancer’, ‘mastectomy’, ‘breast-conserving surgery’, ‘seroma’, ‘lymphocele’ and ‘lymphocyst’ were used as both keyword and subject terms. We included meta-analysis, randomized controlled trials (RCTs), prospective studies, systematic review of RCTs or prospective studies, and retrospective studies if they included at least 200 patients. The search was limited to studies published in English, and unpublished data were not located.
Data were extracted by one reviewer and checked independently by a second. Attempts were made to contact study authors if additional information was required to adequately complete the data extraction form. The direction of association was defined as follows: increase, significant association between a factor and increase of seroma formation; decrease, significant association between a factor and decrease of seroma formation; no association, no significant association between a factor and seroma formation. When multiple studies were available on a factor, consistency, predominance and bidirectionality were considered when all showed the same direction, when there was a mixture of no association and either an increase or a decrease, and when there was a mixture of an increase and a decrease, respectively.
The quality of evidence was ranked as follows according to the ‘levels of evidence and grades recommendation’ of the Oxford Center for Evidence-based Medicine (4): level 1, systematic review of RCTs, and individual RCT; level 2, systematic review of cohort studies, and individual cohort study including low-quality RCT; level 3, systematic review of case–control studies, and individual case–control study; level 4, case series, and poor quality cohort and case–control studies; level 5, expert opinion without explicit critical appraisal, or based on physiology, bench research or first principles. The strength of evidence was categorized as grade A (strong), consistent level 1 studies; grade B (moderate), consistent level 2 or 3 studies, or extrapolations from level 1 studies; grade C (weak), level 4 studies or extrapolations from level 2 or 3 studies; grade D (unproven), level 5 evidence or troublingly inconsistent or inconclusive studies of any level. When there was no consistency, extrapolations were made either if there was predominance in the direction with at least two study differences or if evidence was based on a study, and troublingly inconsistent was considered if there was bidirectionality. Otherwise, the evidence was regarded as ‘inconclusive’.
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MAIN FEATURES |
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One meta-analysis (5), 51 RCTs (6–56), 7 prospective studies (57–63) and 7 retrospective studies (64–70) were eligible for formal appraisal and inclusion in this review (Table 1). Considering the quality of the RCTs, all of them except one were graded as level 2, as these were usually underpowered, and the method of random allocation and concealment and sample size justification were not described in detail. If provided, methods of random allocation and concealment were inappropriate, or quality was dubious due to multiplicity of comparison. The meta-analysis was also graded as level 2, as this was based on low-quality RCTs. Moreover, studies included were heterogeneous, and parameter estimates were not provided in several. Therefore, we did not use formal meta-analytic techniques, but provided summarized evidence by detailed systematic review of the best evidence available on seroma formation. For this, risk factors for seroma formation were subdivided into four categories: patients and tumor characteristics, surgical factors, postoperative management and nonsurgical modalities.
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PATIENTS AND TUMOR CHARACTERISTICS
In this category, age, anemia, body mass or obesity index, body weight, breast size, diabetes mellitus, grade, histological type, hormone receptor status, hypertension, nodal status or positivity of lymph nodes (LNs), number of positive LNs, pathological tumor size, side, smoking, specimen size, specimen weight, stage, tumor location and tumor size were assessed.
Among them, two studies had found a positive association between body weight and seroma formation (31,58), and one of them had also found that hypertension is associated with an increase of seroma formation (58). In contrast, as for hormone receptor status (17,51), nodal status or positivity of LNs (17,27,58,59), and stage (17,57), studies consistently showed no association with seroma formation. Similarly, no individual study found a significant association with other factors such as presence of anemia (64) or diabetes mellitus (64), smoking (64), breast size (64), grade (51), histological type (68), pathological tumor size (51), side (51), specimen weight or size (69) and tumor location (58). On the other hand, existing evidence was inconclusive for age (17,27,31,32,51,57,58), body mass index or obesity index (30,31), number of positive LNs (13,16,51,61) and tumor size (51,58).
SURGICAL FACTORS
This category was further subdivided into extent of mastectomy, wound drainage, surgical devices, suture flap fixation and miscellaneous.
EXTENT OF MASTECTOMY
With respect to the extent of mastectomy, two studies have demonstrated that extended radical mastectomy increases seroma formation as compared with simple mastectomy (64,65). In contrast, one study has indicated that immediate reconstruction following MRM decreases seroma formation (69). However, no association was found between preservation or removal of the pectoral fascia and seroma formation (49), and association was inconclusive when radical mastectomy was compared with modified radical mastectomy (MRM) (64,65) and was bidirectional among six studies comparing MRM and breast-conserving surgery (16,31,33,51,57,59).
With respect to axillary dissection, four studies have consistently indicated that the number of removed LNs does not influence seroma formation (17,31,51,59). Similarly, one study has demonstrated that the extent of axillary dissection does not affect seroma formation (68). On the other hand, an RCT of Purushotham et al. (55) has demonstrated that sentinel LN biopsy (SLNB) is associated with significantly less seroma formation than conventional axillary dissection.
WOUND DRAINAGE
In this category, intensity of negative suction pressure, no drainage, number of drains, type of drainage (closed suction versus passive drainage), type of drainage unit (evacuated bottle type versus bellow type) and type of drainage tube (multiple hole type versus multiple channel type) were assessed.
As for no drainage, 5 out of 8 studies had reported that this policy increases seroma formation (10,17,37,50,54,56,61,62). However, seroma formation was not influenced by the intensity of negative suction pressure (8,25,30,53,57), by the number of drains (16,18,47), or by the choice of closed suction drainage or passive drainage (6,7,23). These findings were consistent among studies. Similarly, in an RCT by Britton et al. (8), choice of evacuated bottle type or bellow type did not affect the number of aspirations required. In contrast, in a study of Porter et al. (36), a flat-type drain with multiple channels running the length of the drain reduced seroma formation as compared with a flat-type drain with multiple holes. It was speculated that the holes might clog more easily than the channels, which could lead to premature removal of drains. However, this study was not primarily planned to assess drain type, and the drain was selected according to the attending surgeon's preference.
SURGICAL DEVICES
Several surgical devices including electrocautery, laser scalpel, argon diathermy, ultrasonic scalpel and ultrasonic scissors have been investigated in an effort to achieve better hemostasis and to reduce seroma formation. However, no individual study has shown a significant effect on seroma formation with or without use of argon diathermy (28), a laser scalpel (21) or an ultrasonic scalpel (63). In contrast, according to the author's reply, the use of ultrasonic scissors has reduced seroma formation in an RCT by Lumachi et al. (51). In this study, level I and II axillary dissection was performed using either ultrasound scissors, or scissors and ligation, and electrocautery was used only for skin flap dissection. On the other hand, the use of electrocautery was significantly associated with increased seroma formation in an RCT by Porter et al. (36). In this study, the flap and fascia were dissected either by electrocautery or by scalpel, while control of small bleeding vessels with electrocautery and sharp dissection of the axillary nodes was performed in both groups.
SUTURE FLAP FIXATION
Suture flap fixation is a surgical technique for securing flaps to underlying tissues to close the dead space with sutures. Although this technique is not commonly performed, it is interesting to note that an RCT by Coveney et al. (19) has demonstrated that this technique reduces seroma formation in patients undergoing mastectomy. In association with this, an RCT by Purushotham et al. (45) has demonstrated that mastectomy without drainage does not increase seroma formation when this technique is applied. Also, a prospective study by Schuijtvlot et al. (61) has demonstrated that seroma formation is reduced by the use of this technique in patients undergoing BCT without axillary drainage.
MISCELLANEOUS
Moreover, several factors such as previous biopsy, blood loss, blood transfusion, operation time, skin incision, skin graft, surgeon and type of anesthesia have been assessed, and individual study has demonstrated that a longer operation time and diagonal skin incision as compared to vertical skin incision increase seroma formation (32,64). On the other hand, no association was found for previous biopsy (16,57), type of anesthesia (local or general) (17) or blood transfusion (58). Available evidence was inconclusive for whether or not skill or experience of the surgeon influences seroma formation (20,32,57), for quantity of blood loss (17,36), and for use or non-use of a skin graft (64,68).
POSTOPERATIVE MANAGEMENT
This category was subdivided into drainage volume, timing of drain removal, timing of shoulder movement, immobilization of the shoulder and use of an external pressure garment or compression dressing.
DRAINAGE VOLUME
Drainage volume during the initial 3 or 5 postoperative days (POD), total drainage volume and drainage volume in the 24 h before drain removal were assessed in terms of seroma formation. Among them, a positive association between drainage volume during the initial 3 POD and seroma formation was consistent between two RCTs (31,39). In contrast, evidence was inconclusive for drainage volume in the 24 h before drain removal (29,57,60), total drainage volume during the initial 5 POD (29,30) or total drainage volume (14,29,51,57,58). In this respect, the effect of total drainage volume might be confounded by duration of drainage and vice versa. However, interaction between total drainage volume and duration of drainage was not always documented in detail.
TIMING OF DRAIN REMOVAL
Several RCTs comparing timing of drain removal have provided complicated results. For example, in an RCT comparing removal of the drain on the fifth POD with removal on the eighth POD, the incidence of seroma formation was significantly high in the former (43). However, in that study, the drain was also removed when drainage volume fell to 30 ml or less per day for 2 consecutive days, and the actual day of drain removal between two groups was not provided. In contrast, in two RCTs comparing drain removal on the fifth POD and removal when daily drainage volume became minimal (14,29), the timing of drain removal did not affect seroma formation. In the study by Inwang et al. (14) drains were usually removed at the 10th to 14th POD in the latter group, while the actual day of drain removal was not reported in the study by Ackroyd et al. (29).
On the other hand, evidence was inconclusive when seroma formation was compared between drain removal on the first or third POD, and when drainage volume fell to a minimal level (39,49,60,62). In two RCTs (39,49), early removal of drains increased seroma formation, whereas two other prospective studies did not find a significant association (60,62). In addition, in a study by Parikh et al. (15), there was no significant difference in the incidence of seroma formation between removal on the third POD and on the sixth POD.
TIMING OF SHOULDER MOVEMENT, IMMOBILIZATION, AND USE OF AN EXTERNAL PRESSURE GARMENT OR COMPRESSION DRESSING
With respect to the timing of shoulder movement, five RCTs have found no significant influence when compared between shoulder movement from the first or third POD and that from the 5th to 10th POD (9,12,13,27,38), whereas a meta-analysis of five RCTs (11,32,33,71,72) found that early shoulder movement increased seroma formation (5). In contrast, three RCTs investigating the effect of shoulder immobilization using a bandage, collar and cuff or a sling, on seroma formation (9,11,27), consistently found that temporary shoulder immobilization did not have a significant effect on seroma formation. Evidence was inconclusive for the use of an external pressure garment or compression dressing (34,40), although the concept is to obliterate dead space by applying external pressure to the flaps and to encourage adhesion of the flaps to the underlying muscles.
NONSURGICAL MODALITIES
This category includes radiation, neoadjuvant chemotherapy, use of adhesive glue and antifibrinolytic agents. With respect to radiation, a retrospective study of Say et al. (64) has demonstrated that pre- or postoperative radiation therapy does not affect seroma formation in patients who have undergone radical mastectomy. Similarly, neoadjuvant chemotherapy did not influence seroma formation in an RCT comparing neoadjuvant chemotherapy with immediate surgery (24).
With regard to the use of adhesive glue such as fibrin glue or bovine thrombin, nine RCTs found no significant effect on seroma formation (20,31,35,42,44,46,48,52,59), and an RCT by Vaxman et al. (26) even revealed that the use of fibrin glue increased seroma formation. Similarly, in an RCT by Jain et al. (50), patients were randomized to receive suction drainage or to receive no drain, and those allocated to no drainage were further randomized for application of fibrin sealant to the dissected area or to no intervention. Overall, this RCT failed to show any significant effect of the use of fibrin sealant on seroma formation. In addition, an RCT by Johnson et al. (54) failed to show any advantage to using fibrin glue without drainage over a drain. Similarly, the use of fibrin glue and fibrinolysis inhibitor or perioperative and postoperative administration of fibrinolysis inhibitor did not reduce seroma formation (22,52). The concept of the use of fibrinolysis inhibitor was based on the hypothesis that fibrinolytic activity of the plasmin system in serum and lymph might contribute to fluid accumulation.
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SUMMARY OF EVIDENCE ON RISK FACTORS FOR SEROMA FORMATION |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURESSUMMARY OF EVIDENCE ON...References |
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Each factor for seroma formation is categorized as shown in Table 2 according to the direction of the association and strength of evidence. Although there was no risk factor supported by strong evidence, there was moderate evidence to support the risk of seroma formation in individuals with heavier body weight, extended radical mastectomy as compared with simple mastectomy, and a greater initial three-day drainage volume. On the other hand, the following factors did not have a significant influence on seroma formation: the duration of drainage; hormone receptor status; immobilization of the shoulder; intensity of negative suction pressure; LN status or positivity of LNs; number of drains; number of removed LNs; previous biopsy; removal of drains on the fifth POD versus when the daily drainage volume fell to a minimal; stage; type of drainage (closed suction versus static drainage); and use of fibrinolysis inhibitor. In contrast, as might have been expected, SLNB reduced seroma formation. For the other factors that were commonly sited in the literature, evidence was weak or unproven.
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Thus, although a number of factors have been correlated with seroma formation, strong data on factors associated with seroma formation are still rare, and it seems to be difficult to identify patients who will ultimately suffer from seroma. However, this study has provided findings that are useful for identifying commonly cited risk factors that have no evidence to support them.
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