Minimally Invasive Therapy. 2013; Early Online, 1–9
ORIGINAL ARTICLE
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Impact of surgical approach on blood loss during intracapsular myomectomy
ANDREA TINELLI1, LISELOTTE METTLER2, ANTONIO MALVASI3, BRAD HURST4, WILLIAM CATHERINO5, OSPAN A MYNBAEV6, MARCELLO GUIDO7, IBRAHIM ALKATOUT2 & THORALF SCHOLLMEYER2 1
Department of Obstetrics and Gynecology, Vito Fazzi Hospital, Lecce, Italy, 2Kiel School of Gynaecological Endoscopy, Department of Obstetrics and Gynaecology, University, Hospitals Schleswig-Holstein, Campus Kiel, Germany, 3 Department of Obstetrics and Gynecology, Santa Maria Hospital, Bari, Italy, 4Assisted Reproduction Center, Carolinas Medical Center, Charlotte, NC, USA, 5Department of Obstetrics and Gynecology, USUHS, Associate Program Director, Division of REI, PRAE, NICHD, NIH, Bethesda, USA, 6Experimental Researches & Modelling Division, Moscow State University of Medicine and Dentistry, Moscow, Russian Federation, and 7Laboratory of Hygiene, Department of Biological and Environmental Sciences and Technologies, Faculty of Sciences, University of Salento, Lecce, Italy
Abstract Background: Myomectomy is one of the most common surgical procedures in gynecology and has implications on fertility and subsequent pregnancies. We compared the impact of surgical approach on blood loss during laparoscopic and abdominal intracapsular myomectomy. Material and methods: The evaluation comprised 124 fertile women with subserous or intramural myomas: 66 patients treated by laparoscopy and 58 patients treated by laparotomy. The intracapsular myoma enucleation technique was similar for both approaches. All procedures were analyzed for the evaluation of intra- and postsurgical blood loss and intra- and short-term post-operative surgical outcomes. Results: The operating time for laparoscopic intracapsular myomectomy was longer (95 ± 7.2 min vs. 63 ± 5.6, p < 0.0001), but was associated with reduced intra- (65 ± ml vs. 105 ± 5, p < 0.0001) and post-surgical blood loss (30 ± 5 vs. 60 ± 5 ml, p < 0.0001), as well as diminished application of pain relief medication (8 patients vs. 17, p < 0.05), compared to open intracapsular myomectomy. Conclusions: The surgical approach did not substantially affect the technique of intracapsular myomectomy; however, laparoscopy significantly reduced intra- and postoperative blood loss and resulted in better short-term outcomes than after open surgery. Our results underscore the advantages of trying to reduce the rate of laparotomic myomectomy, one of the leading surgical interventions associated with infertility and sterility.
Key words: Uterine myomas, fibroids, myomectomy, laparoscopy, fertility, complications, carbon dioxide pneumoperitoneum, peritoneal trauma
Introduction Uterine myomas are the most common benign solid tumors of the female genital tract, manifested in 25–30% of women during the reproductive years. Symptomatic myomas are an indication for myomectomy which is the treatment of choice even when there is no further desire for pregnancy (1).
Since Kurt Semm introduced laparoscopy as an approach for myomectomy in 1979 (2), the advantages of this approach over open surgery have been shown in several studies (3). Laparoscopic myomectomy has been progressively implemented by major surgical schools worldwide since this approach appears to minimize postoperative morbidity. Hence, the proportion of laparoscopic myomectomies is gradually increasing.
Correspondence: L. Mettler, Kiel School of Gynaecological Endoscopy, Department of Obstetrics and Gynaecology, University, Hospitals Schleswig-Holstein, Campus Kiel, Arnold-Heller-Str. 3, House 24, D-24105 Kiel, Germany. Fax: +49 431 5972149. E-mail:
[email protected]; ;
[email protected] ISSN 1364-5706 print/ISSN 1365-2931 online 2013 Informa Healthcare DOI: 10.3109/13645706.2013.839951
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B
C
D
Figure 1. Intracapsular myomectomy procedure: (A) uterine transvaginal ultrasound section showing the myoma pseudocapsule as a “ring of fire” around the fibroid by EcoColorDoppler; (B) incision of the uterine serosa to the myometrium by a hook low wattage electrode (£30 watts) revealing the pseudocapsule and uterine myoma; (C) myoma pseudocapsule fibrovascular network covering myoma during laparoscopy; (D) abdominal removal of the myoma by progressive detachment of the surrounding pseudocapsule, with its careful preservation (B, C): color enhancement done with PICASA software).
In a systematic review and meta-analysis of intraoperative parameters and outcomes of laparoscopic versus open myomectomy in 576 patients from six randomized controlled trials it could be shown that despite prolonged surgery, laparoscopic myomectomy is associated with a lower hemoglobin drop, reduced operative blood loss, full patient recovery at day 15, diminished postoperative pain and fewer overall complications. The authors concluded that laparoscopic myomectomy is a better choice than open surgery if performed by suitably specialized surgeons in selected patients (4). For some years, we have been involved in the design and standardization of a method for the removal of myomas by preserving their pseudocapsule, i.e. a fibro- and neurovascular entity with angiogenic
activity and a specific gene expression profile distinguishable from myomas (5). On the ultrasound screen the pseudocapsule can be traced as an echogenic line (a few millimeters in diameter) surrounding the myoma (6). The recognition of this anatomic entity (7) has permitted the development of laparoscopic myomectomy by an intracapsular technique, a new surgical approach that involves enucleating a myoma from its pseudocapsule (Figure 1) (8,9). A large prospective study with long term followup is required to find out whether women who undergo laparoscopic intracapsular myomectomy have better long-term outcomes and fewer complications due to preservation of the uterine neural integrity and its functionality.
Blood loss during intracapsular myomectomy
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15 mmHg CO2 intra-abdominal pressure
Venous blood return
Intrathoracic pressure
End-diastolic volume
CVP
Stroke volume
Brain venous drainage
Cardiac output
Intra-cranial pressure
Plasma CO2 Compression of arterioles/intraabdominal aorta pH
Sympathetic nervous system
Vascular resistance
Uterine bleeding Figure 2. Effects of the increased intra-abdominal pressure on systemic/local (uterine) hemodynamics during laparoscopic myomectomy (CVP, Central Venous Pressure).
According to our mathematical model and theoretical calculation bleeding can be even more pronounced during intracapsular myomectomy, since the pseudocapsule is surrounded by a rich vascular network that feeds the myoma (10). The main principle of myomectomy is to perform all manipulations as precisely and bloodlessly as possible, and the new surgical technique of intracapsular myomectomy meets this requirement. However, it is not known whether the surgical approach has an impact on blood loss during intracapsular myomectomy aimed at preserving the pseudocapsule. CO2 insufflation can influence blood loss during intracapsular myomectomy as increased intra-peritoneal pressure can lead to the occlusion of the small blood vessels and capillaries of the pseudocapsule. This effect, combined with less traumatic manipulations, could result in beneficial outcomes of surgery. Based on these considerations, the aim of the present investigation was to compare the effects of laparoscopic and abdominal intracapsular myomectomy on blood loss, operating time and short-term outcomes (Figure 2). Material and methods At four university-affiliated hospitals, between January 2008 and December 2011, 137 patients of
reproductive age with uterine myomas were selected for this prospective cohort trial (level of evidence II-2). The indications for surgical treatment were symptomatic myomas, including unexplained infertility (11). All procedures used in the present study were in accordance with the guidelines of the Helsinki Declaration on Human Experimentation. The study protocol, which had been approved by the local ethics committee, was explained to the patients before they entered the trial. All patients signed the informed consent form. Exclusion criteria included major medical conditions or endocrine disorders, current or past use of GnRH analogues (12) (with a washout period of at least six months before enrollment), hypoechoic or calcified leiomyomas diagnosed at ultrasound (13), hyperplasia with cytological atypia in the endometrial biopsy performed for abnormal uterine bleeding, an abnormal Pap test and a positive urine pregnancy test. Patients who had been recruited but were then found to have suspected adenomyosis or an adenomyoma, pedunculated fibroids, small myomas (37 C), post-operative antibiotic administration, duration of hospital stay and post-operative myometrial hematoma (>3 cm) detected by ultrasound during the patient’s hospital stay. As the main intraoperative blood loss was from the myometrial incision, the intraoperative blood loss was assessed by cannula aspirators for both groups by measuring the blood aspirated from the time of the myometrial incision to the hysterorraphy. All results collected during the trial were analyzed by two independent researchers who were not involved in surgery or the follow-up. The long-term postoperative recurrence of myomas, pregnancy rates, long-term adverse events, or costs were not evaluated as these measures were beyond the scope of the present study.
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Table I. Baseline characteristics of patients with number, size and localization of myomas (overall mean ± SD or median range with p values). Parameters
Group 1 Laparoscopic myomectomy 66 patients
Group 2 Open myomectomy 58 patients
p
Age, years
35.7 ± 5.4 (range 30–41)
36.4 ± 6.1 (range 30–42)
0.4991 (NS)^
BMI
23.4 ± 2.1
24.5 ± 2.0
0.0035 (< 0.01)^
Parity
1.3 ± 0.2
1.2 ± 0.5
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Previous abdominal surgery
3 (appendicitis, cholecystectomy ovarian cyst removal)
2 (extrauterine pregnancy appendicitis)
0.1375 (NS)^ > 0.9999 (NS)**
Single fibroid
37 (56 %)
28 (48.2 %)
0.3864 (NS)*
Multiple fibroid
29 (44 %)
30 (51.8 %)
0.3864 (NS)*
2 fibroids
14 (48.2 %)
10 (33 %)
0.5766 (NS)*
3 fibroids
10 (34.4 %)
13 (43 %)
0.5766 (NS)*
4 fibroids
5 (17.4 %)
7 (24 %)
0.5450 (NS)**
7.6 ± 1.6
6.5 ± 1.8
0.0005 (< 0.01)^
Dominant myoma diameter (cm) Dominant myoma (localization) Intramural
30 (45.4%)
36 (62%)
0.0643 (NS)*
Subserosal
36 (54.6%)
22 (38%)
0.0643 (NS)*
Posterior
39 (59 %)
24 (41 %)
0.0490 (< 0.05)*
Anterior
22 (41 %)
34 (59 %)
0.0490 (< 0.05)*
Dominant myoma (site)
^by unpaired t test; *by c2 test; **by Fisher’s exact test.
Results were presented as mean ± standard deviation or median range. p-values < 0.05 were considered statistically significant.
Two statistical software programs, the STATVIEW 5.1 system for Macintosh (Abacus Concepts, Inc., Berkeley, CA, 1992) and GrapPadPrism5 for Windows (GraphPad Software, Inc., La Jolla, CA USA), were used to record all statistical tests.
Statistical analysis Results Sample Power 2.0 was used for power analysis to determine the number of procedures necessary in each of the two groups. A power analysis was designed with a prerequisite of a 95% confidence interval (CI) around an estimated fraction of error of no more than ± 13% for each procedure to be clinically significant. A power calculation verified that 57 patients in each group would be necessary to detect a difference with an alpha error level of 5% and a beta error of 80%. Comparisons between the two groups with normality and homogeneity of variances were performed by 2-tailed unpaired Student t test and paired t-test. Alternatively, comparisons between groups with abnormality and heterogeneity of variances were performed by Welch t test. The Chi square and Fisher exact tests were used for categorical variables. Table statistics two-way ANOVA was also used when it was appropriate to compare intra- and post-surgical blood loss and other parameters as repeated measured values.
Complications, such as blood transfusions, conversion to hysterectomy or laparotomy, bowel injury, endometriosis, deep venous thrombosis, infections or re-exploration for postoperative hemoperitoneum or pelvic hematomas were not observed in either group. The mean age of patients and their parity rate were not significantly different between the two groups (Table I), whereas body mass index was significantly higher in women subjected to open surgery (p = 0.0035). Only a few patients in each group had undergone previous surgical procedures in the abdominal cavity; there were no statistically significant differences (p = 0.99). There were 56.1 ± 5.0 versus 48.9 ± 5.0 patients with single fibroids and 51.8 ± 5.0 versus 48.2 ± 5.0 patients with multiple fibroids in Groups 1 and 2, respectively (Table I). The number of single fibroids was not significantly different (p = 0.38) between the laparoscopy and the open surgery group. The number of double, triple and quadruple fibroids was also not
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Table II. Intra- and post-surgical clinical outcomes and duration of hospital stay (overall mean ± SD or median range with p values). Parameters Total operative surgical time (min)
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Uterine cavity opening
Group 1 Laparoscopic myomectomy 66 patients
Group 2 Open myomectomy 58 patients
p
95 ± 7.2 {102-87)
63 ± 5.6 {68-57)
0.0001 (< 0.01)^
3
2
> 0.9999 (NS)**
Intra-surgical blood loss (ml)
65 ± 5
105 ± 5
0.0001 (< 0.01)^^ #
Post-surgical blood loss measured by catheter inside pelvis for 24 h (ml)
30 ± 5
60 ± 5
0.0001 (< 0.01)^^ # 0.0173 (< 0.05)*
Need for pain medication (no. of patients)
8
17
Fever (no. of patients with fever >37 C on first days after surgery)
3
9
0.0647 (NS)**
Postoperative ileus (no. of patients)
2
6
0.1449 (NS)**
Therapeutic post-operative antibiotic treatment (no. of patients)
2
7
0.0812 (NS)**
US haematoma (>3 cm) detected in myometrium after 24 h (no. of patients)
3
6
0.3025 (NS)**
Postoperative bladder pain after Foley removal (no. of patients)
1
7
0.0250 (< 0.05)**
Duration of hospital stay (days)
1.5 ± 0.5
3.5 ± 0.5
0.0001 (< 0.01)^^
^by unpaired t test; ^^by Welch t test modified; *by c2 test; **by Fisher’s exact test; #by Bonforreni post test two-way ANOVA.
significantly different between patients operated via laparoscopy and those operated by open surgery (p = 0.57). Significantly larger dominant fibroids were found during laparoscopic intracapsular myomectomy compared to open surgery. The mean diameter of dominant myomas was 7.6 ± 1.6 in Group 1 and 6.5 ± 1.8 cm in Group 2 (p = 0.0005). There was a larger proportion of subserosal fibroids in the laparoscopy group (p = 0.06) and a larger proportion of intramural fibroids in the open surgery group (p = 0.06). We found a significantly increased localization of dominant myomas in the posterior wall of the uterus in the laparoscopy group, compared to an increased localization of dominant myomas in the anterior wall in the open surgery group (p = 0.049). The total operating time was significantly longer in patients operated via laparoscopy than by open surgery (97 ± 7.2 vs. 63.0 ± 5.6 min) (Table II, p = 0.0001). The uterine cavity was perforated three times during laparoscopy and twice during open surgery (p = 0.99). The average intraoperative blood loss was 65.0 ± 5.1 versus 105.0 ± 5.1 ml and post-operative blood loss 30.0 ± 5.1 versus 60.0 ± 5.1 ml for Groups 1 and 2, respectively (Table II). Intra- and postoperative blood loss was significantly reduced in patients operated via laparoscopy compared to those who underwent open surgery (p = 0.0001). A significantly lower number of patients required pain relief medication after laparoscopy compared to open surgery (8/66 vs. 17/58, p = 0.017).
Hematomas (>3 cm) were detected in the myometrium 24 hours after surgery in 3/66 patients in Group 1 and in 6/58 patients in Group 2 (p = 0.302). Postoperative ileus was observed in 2/66 in Group 1 and in 6/58 patients in Group 2 (p = 0.144). Postoperative bladder pain after Foley removal occurred in 1/66 patients after laparoscopy and in 7/58 patients after open surgery (p = 0.025). Fever (>37 C) during the first days after surgery was manifested in 3/66 patients after laparoscopy and in 9/58 patients after open surgery (p = 0.064). Antibiotic treatment was prescribed for 2/66 patients in Group 1 and for 7/58 patients in Group 2 (p = 0.081). Postoperative parameters, including fever, therapeutic antibiotic treatment, postoperative ileus and hematoma (>3 cm, detected in the myometrium 24 hours after surgery) were not significantly different between the two groups, despite a tendency for a better recovery profile in patients operated via laparoscopy. The hospital stay was shorter for patients operated via laparoscopy (1.5 ± 0.5 days) compared to patients who underwent open surgery (3.5 ± 0.5 days) (Table II, p = 0.0001). A statistician evaluated pre- and postsurgical laboratory assays. Women had a higher preoperative hemoglobin in Group 2 (13.2 g/dl in Group 1 ± 1.4 and 12.3 ± 1.3 in Group 2), while the postoperative hemoglobin levels were similar (11.4 ± 1.1 g/dl in Group 1 and 11.5 ± 1.2 in Group 2). The
Blood loss during intracapsular myomectomy
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preoperative hematocrit values were similar in both groups (36.7 ± 2.6 in Group 1 and 37.3 ± 3.4 in Group 2), while the postoperative hematocrit values were significantly different (32.9 ± 3.7 in Group 1 and 34.5 ± 4.2 in Group 2). The preoperative values of red cells were different, 4150 ± 245 million/mm3 in Group 1 and 4330 ± 265 in Group 2, and postoperative values were 3650 ± 185 and 3750 ± 190, respectively.
Discussion Blood loss during surgery is a common cause of postsurgical inflammation and subsequent adhesion formation, which in turn reduces the ultimate effectiveness of surgery and represents a major cause of morbidity (14). In this study laparoscopic intracapsular myomectomy resulted in significantly less intra- and postsurgical blood loss despite the longer operating time and the larger size of myomas in the open surgery group. An explanation is needed to shed light on the mechanisms which lead to less blood loss during laparoscopic myomectomy compared to open surgery, as has been shown in many studies (3,4,16–22). A plausible hypothesis to explain the lower intraoperative blood loss with laparoscopy is that myometrial hemostasis is helped by increased intraperitoneal pressure counterweighing the parenchymal pressure of the uterus. However, other mechanical and neuro-humoral factors may account for reduced bleeding from excised pseudocapsule micro vessels after establishing the carbon dioxide pneumoperitoneum. Regional/systemic hemodynamic changes that limit surgical blood loss are expected to occur as soon as intra-abdominal pressure reaches the threshold of 10 to 12 mmHg (23). In addition, a CO2 insufflation pressure, maintained at 15 mmHg during laparoscopy, stimulates a sympathetically mediated vasoconstriction through the activation of arterial stretch receptors and chemoregulation. The high intra-peritoneal pressure also has a direct compressive effect on abdominal vessels, leading to a further reduction in tissue perfusion pressure and blood flow. However, the compression of intra-abdominal blood vessels including aorta and vena cava inferior (24) increases systemic vascular resistance and contributes to uterine and splanchnic hypoperfusion (25) (Figure 2). The mechanical impact of a carbon dioxide pneumoperitoneum on capacitance vessels contributes to the pelvic vasoconstriction by activating a cascade of events culminating in a central nervous system
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response. The increased intra-peritoneal pressure has adverse effects on the venous blood return, and therefore on cardiac output through a direct compressive action on the inferior vena cava and venous capacitance vessels (26–28). The depressed cardiac output results in a reflex sympathetic response (e.g. release of catecholamines, vasopressin), leading to peripheral vasoconstriction (29). Increased intracranial pressure enhances the sympathetic outflow by distension of the cerebral arteries. In fact, the upward compression of the diaphragm causes an increased intra-thoracic pressure and elevated central venous pressure, ultimately leading to intra-cranial hypertension (30). Carbon dioxide absorption across the peritoneal membrane is responsible for hypercapnia and subsequent acidosis, sustaining a sympathetic output and visceral vasoconstriction (chemoreceptor-activated response) (31). However, these hypercapnia-derived hemodynamic changes are presumably less important than those mechanically induced since the blood bicarbonate buffer system and respiratory elimination by respiratory-volume controlled mechanical lung ventilation effectively prevent the accumulation of carbon dioxide. The increased utilization of laparoscopic myomectomy inevitably introduces economic considerations. A cost analysis was recently conducted by Behera et al. (32) who found that abdominal myomectomy is the least expensive approach when compared with laparoscopic or roboticassisted laparoscopy. However, the authors did not evaluate the impact of each surgical route on the quality of life, so they did not consider the important social benefits of laparoscopic surgery. Furthermore, costs associated with lost wages and loss of productivity due to the prolonged hospitalization and longer recovery period following open abdominal surgery were not assessed. Even if most myomectomies are still performed by laparotomy because of the complexity of the procedure and the technical difficulty, with extensive suturing for a multi-layered uterine closure, the overall benefits of laparoscopic myomectomy are well recognized by the scientific community. One of the advantages is the significant reduction of bleeding, the focus of the current study. The main biases in this paper relate to the nonrandomized cohort trial, the unequal number of patients in the two groups and the ambiguity of the intraoperative blood loss measurements. Firstly, our study was designed as a cohort trial (level of evidence II-2); therefore, the choice of surgical
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approach was based on the surgeons’ preference. The surgeons maintained a laparoscopy/laparotomy ratio of 1:1 in each hospital and among themselves. Secondly, after exclusion of those patients who did not meet the inclusion criteria there were no attempts to keep an equal number of surgical procedures in the laparoscopy and laparotomy groups. The study involved many surgeons from different hospitals, which led to ambiguity in the intraoperative blood loss measurements. The mean diameter of the dominant fibroid was approximately 1 cm larger in the laparoscopy group. Consequently, the fibrovascular network in the pseudocapsule was larger and presumably required greater coagulation and dissection. Surprisingly, the surgical outcome was better than in the open surgery group. Conclusions In spite of the similarities of the intracapsular myomectomy technique itself (8,12,14,33) performed via laparoscopy or laparotomy and the prolonged operating time of the laparoscopy procedure, the laparoscopic access route proved to be the most beneficial. The advantages of the laparoscopic approach are the significantly reduced parameters of both intra- and post-surgical blood loss, decreased bladder pain after Foley removal, the lower number of patients requiring pain relief medication and the shorter hospital stay. In addition, laparoscopic intracapsular myomectomy resulted in slightly improved short-term outcomes in relation to postoperative fever, myometrium scar hematomas, ileus and antibiotic treatment compared to open surgery.
Acknowledgements We thank Dawn Rüther for editing the manuscript. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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