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Abstract

The objective of this meta-analysis was to assess whether laparoscopic-assisted vaginal hysterectomy achieves better clinical results compared with abdominal hysterectomy. Medline (PubMed), EMBASE, Web of Science, ProQuest, Cochrane Library and China Biological Medicine Database were searched to identify randomized controlled trials that compared laparoscopic-assisted vaginal hysterectomy with abdominal hysterectomy. Twenty-three trials were studied and the analysis was performed using Review Manager Version 5 and R Version 2.11.1. The results showed that laparoscopic-assisted vaginal hysterectomy was associated with a longer operation time, less blood loss, shorter hospital stay, smaller haemoglobin drop, less postoperative pain, quicker return to normal activities and fewer peri-operative complications. Quality of life is likely to be the key outcome to evaluate the approach for hysterectomy, but further research is needed. For suitable patients and surgeons, laparoscopic-assisted vaginal hysterectomy is a better choice than abdominal hysterectomy.

Keywords: Meta-analysis, Laparoscopic-assisted vaginal hysterectomy, Abdominal hysterectomy, Approach.

 

1. Introduction
Hysterectomy is one of the most common operations for benign disease [1]. In 2003, 538,722 patients underwent hysterectomy for benign disease [2]. Currently, although many other methods are available to treat benign disease, hysterectomy remains the preferred technique and its ratio also remained stable [2].

There are several types of hysterectomy: abdominal hysterectomy (AH), supracervical hysterectomy, vaginal hysterectomy, laparoscopic-assisted vaginal hysterectomy (LAVH), total laparoscopic hysterectomy and robotic hysterectomy. Since LAVH was first reported in 1989, it has gained worldwide acceptance [3]. Johnson et al. [4] found that LAVH decreased pain, surgical site infections and hospital stay, and led to a quicker return to normal activities and fewer postoperative adhesions. However, Sculpher et al. [5] found that the efficiency of the laparoscopic route was less than that of the vaginal route, but equal to the abdominal route. Kluivers et al. [6] reported that the quality of life following LAVH was better than that following AH at 6 weeks after surgery, but the difference was not significant after 1 year.

Although previous systematic reviews [4] and [7] have referred to comparisons of LAVH and AH, new research may support or refute the findings. Moreover, to date, no systematic reviews have evaluated these two methods directly. As LAVH and AH are common procedures, further evaluation and comparison is needed. As such, this study aimed to assess which method resulted in the best clinical results, and to provide evidence for decision making regarding the surgical treatment of benign disease.

2. Methods
2.1. Data sources and searches
Electronic databases and hand searching were performed from 20 February 2010 to 2 July 2010 to identify all relevant studies. The electronic databases searched were Medline (PubMed), EMBASE, Web of Science, ProQuest, Cochrane Library and China Biological Medicine Database. The keywords were ‘laparoscopic’, ‘laparoscopically’, ‘vaginal’, ‘assisted’, ‘hysterectomy’, ‘randomized’, ‘randomised’ and ‘randomly’. The ‘related’ function was used to broaden the search. No language restrictions were made. The search strings used in Medline (PubMed) and EMBASE are presented in Table 1. Other electronic databases were searched similarly.

 

The manual search was performed by screening the references cited in the acquired articles. Published systematic reviews and meta-analyses on the topic [4], [7], [8], and [9] were also searched to identify eligible studies.

2.2. Study selection
Two reviewers independently reviewed the titles and abstracts of all identified potential studies to exclude duplicates. The titles, abstracts and full texts were then scrutinized to assess whether the studies met the eligibility criteria, and to exclude the unqualified studies. The studies were assessed using qualitative synthesis. Reviewers were not blinded to the authors or outcomes. Discussions were held in the case of disagreement between the two reviewers.

2.3. Eligibility criteria
Published randomized controlled trials that compared LAVH with AH for benign disease, clearly documented the case selection criteria for LAVH and AH, and reported on at least one of the outcomes mentioned below were included in the study. Studies were excluded if the laparoscopic technique was not LAVH, the outcomes were not clearly reported, it was impossible to extract data, there was considerable overlap between studies, the study was not a randomized controlled trial, review and retrospective articles and abstracts were not documented, and the case selection criteria were not unified.

2.4. Definitions of interventions and outcomes of interest
2.4.1. Definitions of interventions
In LAVH(a), the uterine vessels were ligated laparoscopically but part of the operation was performed vaginally. In LAVH(b), the laparoscopic component did not involve division of the uterine vessels [10]. AH was defined as removal of the uterus through an incision in the lower abdomen [7].

2.4.2. Outcomes of interest and definitions
The operative outcomes were: (1) operation time (min), calculated from the first incision to the closure of all wounds; (2) blood loss (ml), estimated by calculating the blood volume of the suction machine during surgery excluding liquid used for intraperitoneal washing, and by weighing swabs; (3) hospital stay (days), defined as the number of days in hospital after surgery excluding the day of surgery; (4) postoperative pain, assessed using a 0–10-point visual analogue scale; (5) haemoglobin drop (g/100 ml), defined as the decrease in haemoglobin from pre-operative level to postoperative level; and (6) return to normal activities (days), defined as the number of days after discharge from hospital until full recovery.

Peri-operative complications were subdivided into major and minor complications [11], and were defined as one or more of the following criteria adapted from a previous publication [9]—major complications: visceral damage (bladder, ureter or bowel), vaginal vault dehiscence and other life-threatening complications, such as thromboembolic disease; minor complications: pelvic haematoma, febrile morbidity (not specified), need for blood transfusion and other miscellaneous complications, including anaesthetic problems and vault granulation. Overall complications were defined as major plus minor complications.

2.5. Data extraction and quality assessment
Two reviewers extracted the data independently using Microsoft Excel (USA). The data were summarized beyond the analysis if the following attempts failed: (1) contacted corresponding authors via e-mail to access the original data or suitable results, and sought the relevant data in previous published systemic review and meta-analysis articles [4], [7], [8], and [9] when the continuous data were not expressed as means and standard deviations; and (2) the units of outcomes were impossible to convert in a mathematical way when they were not expressed in the predefined form. If conversions from LAVH to AH were reported without specifically reporting that the data were analysed in the AH group, the data were considered to have remained in the LAVH group. A discussion was held if the data of the two reviewers differed, and the final data were agreed by both reviewers.

The quality of individual studies was assessed using the Cochrane methods for assessing the risk of bias [12]. Specifically, study quality was assessed by evaluating the methods of randomization, allocation concealment, blinding, whether incomplete outcome data were addressed, and if the study was free of selective reporting and other bias.

2.6. Statistical analysis
Analysis was performed using Review Manager Version 5 and R Version 2.11.1 [13] in accordance with the recommendations of Cochrane Handbook Version 5.0.2 [12] and the Preferred Reporting Items for Systemic Reviews and Meta-analysis (PRISMA) guidelines [14] and [15]. p ≤ 0.05 was taken to indicate statistical significance.

Heterogeneity was evaluated using χ2-test and I2[12]. The random effect model was used when heterogeneity was significant; otherwise, the fixed effect model was used. If I2 > 50%, meta-regression analyses with random effects [16], [17], and [18] were performed (R, package meta) to detect the possible sources of heterogeneity according to the prespecified potential effect modifiers, including LAVH categorization, setting (single centre or multicentre), year of publication, power calculation (reported or not) and adequate sequence generation (reported or not). In addition, sensitivity analyses were conducted by alternating analytical models. To further assess the effect of individual studies on the summary estimate of effect, influence analyses were performed to recalculate the pooled estimate by omitting one study at a time (R, package meta). If the results indicated a factor to be the possible source of heterogeneity, subgroup analyses were conducted on the factor.

Continuous and dichotomous variables were analysed using mean difference (MD) with 95% confidence intervals (CI) and the inverse variance method, and odds ratio (OR) with 95% CI and the Mantel–Haenszel method, respectively. When there were no events in one group, this was solved by adding 0.5 to each cell of the 2 × 2 table [19] and [20]. If there were no events for both groups, the study was excluded.

Publication bias was evaluated by funnel plot, and the funnel plot's asymmetry was assessed using Egger's test [21] (R, package meta). p < 0.1 was considered to represent significant asymmetry.

3. Results
The search strategy identified 23 studies [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43], and [44] (Fig. 1). Analysis was conducted on 2051 patients (1023 LAVH, 1028 AH). The characteristics of the included studies, and descriptions of study quality and assessment are shown in Table 2, Table 3, and Table 4 and Fig. 2.

 

3.1. Assessment of study quality
3.1.1. Adequate sequence generation
Six studies [22], [30], [35], [38], [39], and [44] stated that they were randomized but did not report the randomization method. Seventeen studies [23], [24], [25], [26], [27], [28], [29], [31], [32], [33], [34], [36], [37], [40], [41], [42], and [43] reported an adequate randomization method, of which 14 studies [24], [25], [26], [27], [28], [29], [31], [32], [33], [34], [36], [37], [42], and [43] used a computer-generated sequence, one study [23] used a randomized number table, and two studies [40] and [41] used sealed opaque envelopes by opening individually.

3.1.2. Allocation concealment
Eleven studies [23], [24], [27], [28], [29], [31], [32], [36], [37], [40], and [41] reported allocation concealment, of which nine studies [23], [24], [27], [29], [31], [36], [37], [40], and [41] used sealed opaque envelopes, one study [28] was conducted by a third party, and one study [32] used telephone inquiry. Eleven studies [22], [25], [26], [30], [33], [34], [35], [38], [39], [42], and [44] did not report allocation concealment and one study [43] just stated ‘unknown to surgeons’.

3.1.3. Blinding
Twenty studies [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [35], [36], [39], [40], [41], [42], [43], and [44] did not report blinding, and two studies [34] and [38] indicated that blinding was used but did not report the method. Only one study [37] reported an adequate blinding method.

3.1.4. Incomplete outcome data addressed
•• Dropouts. Eighteen studies [22], [23], [26], [27], [29], [30], [31], [32], [33], [35], [36], [37], [38], [39], [40], [41], [43], and [44] reported no dropouts, and five studies [24], [25], [28], [34], and [42] reported dropouts. Dropouts were excluded from the analysis in four studies [24], [28], [34], and [42], while one study [25] included the data in the analysis where possible.
•• Intention to treat. Five studies reported dropouts, of which two studies [25] and [28] specifically reported intention to treat, and three studies [24], [34], and [42] did not. One study [33] did not report dropouts, but its analysis was undertaken according to the treatments received rather than intention to treat (two patients converted from LAVH to AH, and were analysed in the AH group).

3.1.5. Free of selective reporting
Twelve studies [22], [23], [24], [27], [30], [33], [34], [35], [38], [39], [42], and [43] did not report their primary outcome or power calculations, so it was unclear whether the outcomes were reported in the predefined way. Eleven studies [25], [26], [28], [29], [31], [32], [36], [37], [40], [41], and [44] reported their sample size calculation and predefined their primary outcome.

Operation time and hospital stay were assessed in all of the studies. Blood loss was assessed in 16 studies [24], [25], [26], [29], [30], [31], [32], [33], [34], [35], [37], [38], [39], [41], [42], and [43]. Postoperative pain was assessed in nine studies [23], [25], [26], [30], [32], [36], [37], [39], and [44], with three studies [23], [25], and [37] presenting graphs. Haemoglobin drop was assessed in nine studies [23], [26], [27], [30], [32], [36], [41], [42], and [43]. Return to normal activities was assessed in nine studies [23], [24], [25], [29], [31], [32], [40], [41], and [43], with one study [25] presenting a graph. Eighteen studies [22], [23], [24], [25], [26], [27], [28], [29], [31], [32], [33], [36], [37], [40], [41], [42], [43], and [44] assessed complications, and one study [28] categorized the complications into major and minor. Twelve studies [24], [25], [27], [28], [29], [33], [34], [36], [40], [41], [42], and [43] reported conversions in surgery.

3.1.6. Free of other bias
Sixteen studies [22], [26], [27], [29], [30], [31], [34], [35], [36], [37], [38], [39], [42], [43], and [44] appeared to be free of other sources of bias, whereas seven studies [23], [24], [25], [32], [33], [40], and [41] had other potential sources of bias. Two studies [23] and [40] reported different surgeons for different procedures, and one study [32] reported more residents in training as first surgeons in AH. Three studies [24], [25], and [41] reported the receipt of funding; for one study [24], this was not according to intention to treat, and one study [41] only reported tissue trauma in uncomplicated operations. One study [33] reported no funding, but its analysis was not according to intention to treat.

3.2. Meta-analysis results of operative outcomes and complications
Fig. 3 shows the forest plots for operative outcomes and complications. A random effect model was used for operation time, blood loss, hospital stay and return to normal activities because heterogeneity was significant (p < 0.05).

4. Discussion
This study performed a meta-analysis to evaluate all randomized controlled trials that compared LAVH with AH for benign disease, according to eligibility criteria. The search strategy was broad and had no language limitation to reduce any potential bias. According to the quality assessment, most studies had a high risk of bias due to blinding and a low risk of other forms of bias.

Meta-regression and subgroup analyses indicated that power calculation, adequate sequence generation and LAVH categorization may be possible sources of heterogeneity, but these three factors were not the main sources of heterogeneity as high or moderate heterogeneity still existed. Sensitivity analysis indicated sufficient stability of analyses results. As such, this meta-analysis was potentially limited by clinical rather than statistical heterogeneity, due to various factors in the treatment of benign disease by hysterectomy, such as different types of disease (myoma, menorrhagia, adenomyosis, etc.), and variations in surgical procedures and skill level of surgeons.

Although vaginal hysterectomy offers fewer postoperative complications, less blood loss, shorter hospital stay and convalescence, and lower costs compared with AH [45] and [46], many surgeons do not feel comfortable when confronted with traditional contra-indications of the vaginal route [36]. LAVH, which combines the advantages of laparoscopy and the vaginal route, has many advantages compared with AH, although it also has some disadvantages, such as longer operation time and more operative bleeding, compared with vaginal hysterectomy [47].

The results show that LAVH has a significantly longer operation time than AH. As most time was spent in the laparoscopic phase of the operation, this may be due to the learning curve for laparoscopy. Laparoscopy is a complex technique requiring a high level of skill and good hand–eye co-ordination as the surgeon receives limited tactile feedback. However, comprehensive training of surgeons and the development of surgical instruments may lead to a decrease in the operation time for LAVH in the future. Another contributing factor was the volume of the myoma or uterus; if the target volume was too large, more procedures were required, and this was time consuming. Even experienced surgeons would reduce their speed to guarantee safety in these circumstances. Nevertheless, with more research into methods of volume reduction, LAVH will become easier and faster.

The study found that blood loss was significantly lower for LAVH than AH. This may be due to more precise and accurate anatomical location of bleeding points, better sight of deep vascular structures and less tissue trauma. In the laparoscopic phase of LAVH, clear visualization and the zoom function makes it easier to locate the bleeding points. The vaginal phase of LAVH offers familiar sights and senses to control bleeding, as for AH [48]. Furthermore, as LAVH is performed through three trocar ports and AH involves abdominal incision, LAVH leads to less tissue trauma. However, it should be noted that the experience of surgeons will affect the control of bleeding.

This study found that hospital stay was significantly shorter following LAVH compared with AH. As LAVH leads to less tissue and visceral trauma, and less inflammation [49] and [50], faster recovery is possible, thus decreasing the length of hospital stay.

Postoperative pain and haemoglobin drop were reduced significantly, and return to normal activities was significantly quicker following LAVH compared with AH. However, this meta-analysis was not sufficiently powerful to draw conclusions as few studies reported these outcomes; more data are needed for evaluation. Nevertheless, the results might provide evidence for less blood loss and shorter hospital stay following LAVH, although the conclusions need further review.

This study found that LAVH led to significantly more major complications, and fewer minor and overall complications than AH. Most major complications were bladder and urinary tract injuries, probably caused by the resident surgeons. These complications would be less common among more experienced surgeons [24]. The feasibility and safety of LAVH have been accepted worldwide, and the finding of fewer minor and overall complications following LAVH compared with AH confirms this concept. Since LAVH leads to fewer tissue and visceral injuries, there is less need for blood transfusions, and fewer cases of urinary and vaginal cuff infection, haematomas, etc. Surgery with a low complication rate implies a shorter hospital stay [24], so these results may explain the shorter hospital stay following LAVH. However, the greatest benefit from LAVH is achieved with appropriate selection of patients and surgeons.

Although various outcomes of hysterectomy have been reported worldwide, there has been no discussion regarding which outcomes are of key importance [7]. Quality of life is likely to be the most key outcome because it reflects patients’ experiences of treatment and takes into account the effects of complications [6] and [51]. Questionnaires such as Short Form-36/Short Form-12 or a quality-of-life scale, such as quality-adjusted life years, could be used to assess quality of life. However, few studies have reported this outcome and further evaluation is needed.

There is no doubt that individual surgeons have their own indications when choosing the approach for hysterectomy. However, the advantages and disadvantages of each approach should be taken into account when making a decision.

5. Conclusion
This study showed that LAVH had a longer operation time, less blood loss, shorter hospital stay, smaller haemoglobin drop, less postoperative pain, quicker return to normal activities and fewer peri-operative complications compared with AH. For suitable patients and surgeons, LAVH is a better choice than AH. However, more studies and more data, particularly regarding quality of life, are needed for further evaluation.

References
[1] L.S. Wilcox, L.M. Koonin, R. Pokras, L.T. Strauss, Z. Xia, H.B. Peterson. Hysterectomy in the United States 1988–1990. Obstet Gynecol. 1994;83:555-594
[2] T. Falcone, M. Walters. Hysterectomy for benign disease. Obstet Gynecol. 2008;111:753-767 Crossref.
[3] H. Reich, J. DeCaprio, F. McGlynn. Laparoscopic hysterectomy. J Gynecol Surg. 1989;5:213-216 Crossref.
[4] N. Johnson, D. Barlow, A. Lethaby, E. Tavender, L. Curr, R. Garry. Methods of hysterectomy: systematic review and meta-analysis of randomised controlled trials. BMJ. 2005;330:1478 Crossref.
[5] M. Sculpher, A. Manca, J. Abbott, J. Fountain, S. Mason, R. Garry. Cost effectiveness analysis of laparoscopic hysterectomy compared with standard hysterectomy. BMJ. 2004;328:134-137
[6] K. Kluivers, N. Johnson, P. Chien, M. Vierhout, M. Bongers, B. Mol. Comparison of laparoscopic and abdominal hysterectomy in terms of quality of life: a systematic review. Eur J Obstet Gynecol Reprod Biol. 2008;136:3-8 Crossref.
[7] T.E. Nieboer, N. Johnson, A. Lethaby, et al. Surgical approach to hysterectomy for benign gynaecological disease. Cochrane Database Syst Rev. 2009;3:CD003677
[8] Z.H. Huang, R.Q. Tu, L.J. Wu. Comparison among minor invasive surgical approaches to hysterectomy for benign gynecological diseases: a systematic review and meta-analysis. Chin J Evid Based Med. 2009;10:323-338
[9] C. Walsh, S. Walsh, T. Tang, M. Slack. Total abdominal hysterectomy versus total laparoscopic hysterectomy for benign disease: a meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2009;144:1-2
[10] H. Reich, L. Roberts. Laparoscopic hysterectomy in current gynecological practice. Rev Gynaecol Pract. 2003;3:32-40 Crossref.
[11] C. Chapron, A. Fauconnier, F. Goffinet, G. Bréart, J. Dubuisson. Laparoscopic surgery is not inherently dangerous for patients presenting with benign gynaecologic pathology. Hum Reprod. 2000;17:1334-1342
[12] J.P.T. Higgins, S. Green. Cochrane handbook for systematic reviews of interventions. Version 5.0.2. (The Cochrane Collaboration, 2009)
[13] R Development Core Team. R: a language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, 2010) http://www.R-project.org Available at:
[14] D. Moher, A. Liberati, J. Tetzlaff, D.G. Altman, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535 Crossref.
[15] A. Liberati, D.G. Altman, J. Tetzlaff, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700 Crossref.
[16] S.E. Brian, H. Torsten. A handbook of statistical analyses using R. (CRC Press, 2006)
[17] H.C. van Houwelingen, L.R. Arends, T. Stijnen. Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med. 2002;21:589-624 Crossref.
[18] C.S. Berkey, D.C. Hoaglin, F. Mosteller, G.A. Colditz. A random-effects regression model for meta-analysis. Stat Med. 1995;14:395-411 Crossref.
[19] N. Mantel, W. Haenszel. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22:719-748
[20] S. Yusuf, R. Peto, J. Lewis, R. Collins, P. Sleight. Beta blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis. 1985;27:335-371 Crossref.
[21] M. Egger, S.G. Davey, M. Schneider, C. Minder. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629-634 Crossref.
[22] G. Kunz, T. Plath, G. Leyendecker. Comparison between laparoscopic assisted vaginal hysterectomy (LAVH) and abdominal hysterectomy. Geburtsh Frauenheilk. 1996;56:453-457 Crossref.
[23] A. Langebrekke, R. Eraker, B.I. Nesheim, A. Urnes, B. Busund, G. Sponland. Abdominal hysterectomy should not be considered as a primary method for uterine removal. A prospective randomised study of 100 patients referred to hysterectomy. Acta Obstet Gynecol Scand. 1996;75:404-407 Crossref.
[24] R.L. Summitt, T.G. Stovall, J.F. Steege, G.H. Lipscomb. A multicenter randomized comparison of laparoscopically assisted vaginal hysterectomy and abdominal hysterectomy in abdominal hysterectomy candidates. Obstet Gynecol. 1998;92:321-326
[25] T. Falcone, M.F.R. Paraiso, E. Mascha. Prospective randomized clinical trial of laparoscopically assisted vaginal hysterectomy versus total abdominal hysterectomy. Am J Obstet Gynecol. 1999;180:955-962 Crossref.
[26] R. Marana, M. Busacca, E. Zupi, N. Garcea, P. Paparella, G.F. Catalano. Laparoscopically assisted vaginal hysterectomy versus total abdominal hysterectomy: a prospective, randomized, multicenter study. Am J Obstet Gynecol. 1999;180:270-275 Crossref.
[27] M.M. Ferrari, N. Berlanda, R. Mezzopane, G. Ragusa, M. Cavallo, G. Pardi. Identifying the indications for laparoscopically assisted vaginal hysterectomy: a prospective, randomised comparison with abdominal hysterectomy in patients with symptomatic uterine fibroids. BJOG. 2000;107:620-625 Crossref.
[28] M.A. Lumsden, S. Twaddle, R. Hawthorn, et al. A randomised comparison and economic evaluation of laparoscopic-assisted hysterectomy and abdominal hysterectomy. BJOG. 2000;107:1386-1391 Crossref.
[29] C. Ottosen, G. Lingman, L. Ottosen. Three methods for hysterectomy: a randomised, prospective study of short term outcome. BJOG. 2000;107:1380-1385
[30] S.Q. Lin, J. Bai, W. Felix. Clinical study of laparoscopically assisted vaginal hysterectomy versus total abdominal hysterectomy. Clin Med J China. 2001;8:483-484
[31] J.L. Hwang, K.M. Seow, Y.L. Tsai, L.W. Huang, B.C. Hsieh, C. Lee. Comparative study of vaginal, laparoscopically assisted vaginal and abdominal hysterectomies for uterine myoma larger than 6 cm in diameter or uterus weighing at least 450 g: a prospective randomized study. Acta Obstet Gynecol Scand. 2002;81:1132-1138
[32] K. Schutz, M. Possover, A. Merker, W. Michels, A. Schneider. Prospective randomized comparison of laparoscopic-assisted vaginal hysterectomy (LAVH) with abdominal hysterectomy (AH) for the treatment of the uterus weighing >200 g. Surg Endosc. 2002;16:121-125
[33] E.M. Tsai, H.S. Chen, C.Y. Long, et al. Laparoscopically assisted vaginal hysterectomy versus total abdominal hysterectomy: a study of 100 cases on light-endorsed transvaginal section. Gynecol Obstet Invest. 2003;55:105-109 Crossref.
[34] C. Atabekoglu, M. Sonmezer, M. Gungor, R. Aytac, F. Ortac, C. Unlu. Tissue trauma in abdominal and laparoscopic-assisted vaginal hysterectomy. J Am Assoc Gynecol Laparosc. 2004;11:467-472 Crossref.
[35] P. Zhang, F. Ling, Y. Zeng. A prospective randomized study of laparoscopic assisted vaginal hysterectomy versus abdominal hysterectomy. ShangHai Med J. 2004;27:736-738
[36] L. Muzii, S. Basile, E. Zupi, et al. Laparoscopic-assisted vaginal hysterectomy versus minilaparotomy hysterectomy: a prospective, randomized, multicenter study. J Minim Invasive Gynecol. 2007;14:610-615 Crossref.
[37] F. Sesti, F. Calonzi, V. Ruggeri, A. Pietropolli, E. Piccione. A comparison of vaginal, laparoscopic-assisted vaginal, and minilaparotomy hysterectomies for enlarged myomatous uteri. Int J Gynecol Obstet. 2008;103:227-231 Crossref.
[38] Q. Yue, R. Ma, D.W. Mao, et al. Effects of laparoscopically-assisted vaginal hysterectomy compared with abdominal hysterectomy on immune function. J Int Med Res. 2009;37:855-861 Crossref.
[39] L. Zhu, J.H. Lang, C.Y. Liu, H.H. Shi, Z.J. Sun, R. Fan. Clinical assessment for three routes of hysterectomy. Chin Med J (Engl). 2009;122:377-380
[40] J.H. Olsson, M. Ellstrom, M. Hahlin. A randomised prospective trial comparing laparoscopic and abdominal hysterectomy. BJOG. 1996;103:345-350 Crossref.
[41] P. Härkki-Sirén, J. Sjöberg, J. Toivonen, A. Tiitinen. Clinical outcome and tissue trauma after laparoscopic and abdominal hysterectomy: a randomized controlled study. Acta Obstet Gynecol Scand. 2000;79:866-871
[42] P.M. Yuen, T.W. Mak, S.F. Yim, et al. Metabolic and inflammatory responses after laparoscopic and abdominal hysterectomy. Am J Obstet Gynecol. 1998;179:1-5 Crossref.
[43] R. Seracchioli, S. Venturoli, F. Vianello, et al. Total laparoscopic hysterectomy compared with abdominal hysterectomy in the presence of a large uterus. J Am Assoc Gynecol Laparosc. 2002;9:333-338 Crossref.
[44] M. Ellström, M.F. Olsén, J.H. Olsson, G. Nordberg, A. Bengtsson, M. Hahlin. Pain and pulmonary function following laparoscopic and abdominal hysterectomy: a randomized study. Acta Obstet Gynecol Scand. 1998;77:923-928
[45] R.C. Dicker, J.R. Greenspan, L.T. Strauss, et al. Complications of abdominal and vaginal hysterectomy among women of reproductive age in the United States. The Collaborative Review of Sterilization. Am J Obstet Gynecol. 1982;144:841-848
[46] J.H. Dorsey, P.M. Holtz, R.I. Griffiths, M.M. McGrath, E.P. Steinberg. Costs and charges associated with three alternative techniques of hysterectomy. N Engl J Med. 1996;335:476-482 Crossref.
[47] J. Drahonovsky, L. Haakova, M. Otcenasek, L. Krofta, E. Kucera, J. Feyereisl. A prospective randomized comparison of vaginal hysterectomy, laparoscopically assisted vaginal hysterectomy, and total laparoscopic hysterectomy in women with benign uterine disease. Eur J Obstet Gynecol Reprod Biol. 2010;148:172-176 Crossref.
[48] A.R. Twijnstra, R.N.A. Kianmanesh, M.J. Smeets, J.F. Admiraal, F.W. Jansen. Twenty-first century laparoscopic hysterectomy: should we not leave the vaginal step out?. Gynecol Surg. 2009;6:311-316 Crossref.
[49] C.S. Ou, E. Beadle, J. Presthus, M. Smith. A multicenter review of 839 laparoscopic-assisted v