IJG-07949; No of Pages 5 International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Hysterectomy trends over a 9-year period in an endoscopic teaching center Thoralf Schollmeyer a,1, Mohamed Elessawy a,⁎,1, Babis Chastamouratidhs a, Ibrahim Alkatout a, Ivo Meinhold-Heerlein b, Liselotte Mettler a, Walter Jonat a, Marion T. Weigel a a b
Department of Obstetrics and Gynecology, Kiel School of Gynecological Endoscopy, University Hospitals Schleswig-Holstein, Kiel, Germany Department of Obstetrics and Gynecology, RWTH Aachen University, Aachen, Germany
a r t i c l e
i n f o
Article history: Received 23 August 2013 Received in revised form 17 December 2013 Accepted 4 April 2014 Keywords: Benign indications Complications Hysterectomy Laparoscopy Teaching
a b s t r a c t Objective: To investigate trends in the performance of hysterectomy at a single certified endoscopic teaching center. Methods: Data were collected retrospectively from 953 patients who underwent hysterectomy between 2002 and 2010 for benign indications at UKSH, Germany. Preoperative risk scores were assigned to patients. Results: The most frequent indications for hysterectomy were uterine myoma, adenomyosis, prolapse, endometrial hyperplasia, menstrual disorders, and endometriosis. The shortest operating time was recorded for vaginal hysterectomy (VH) and the longest for laparoscopically assisted VH (LAVH). The average uterine weight was highest for abdominal hysterectomy (AH) and lowest for VH. The major postoperative complication rate was 11.8% for laparoscopic supracervical hysterectomy (LSH) and 23.5% for AH. The highest intraoperative complication rate occurred with AH (46.4%) and the lowest with total laparoscopic hysterectomy (TLH; 3.6%). The minor postoperative complication rate was 5.9%. The mean preoperative score was 1.09 ± 1.51 for AH, 0.75 ± 0.96 for VH, 1.04 ± 1.30 for LSH, 1.0 ± 1.40 for LAVH, and 1.38 ± 1.52 for TLH. Conclusion: Laparoscopic hysterectomies have become more common and were associated with decreased complication rates, despite the higher preoperative risk score of these patients. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Hysterectomy is the most frequently performed major gynecologic surgical procedure [1,2]. The overall rate of hysterectomy in Germany in 2005–2006 was 362.9 (295.0 for benign diseases of the genital tract and 44.0 for primary malignant tumors of the genital tract) per 100 000 women per year [3]. The Centers for Disease Control and Prevention reported that the US hysterectomy rate in 2000–2004 was 5.4 per 1000 women per year [4]. The art of surgery has developed and changed with the advancement of technology so that hysterectomy is now performed primarily as a minimally invasive operation. Benign indications for hysterectomy are symptomatic or growing uterine myomas, adenomyosis, abnormal uterine bleeding, endometriosis, and prolapse of the uterus [5]. The choice of route for hysterectomy is dependent on many factors: size and mobility of uterus; body mass index (BMI, calculated as weight in kilograms divided by the square of height in meters); preoperative history; anatomic variation; level of experience of surgeon; and patient preference. Laparoscopic hysterectomy (LH) is the method of choice whenever vaginal hysterectomy (VH) is not possible [6,7]. A well-trained ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Kiel School of Gynecological Endoscopy, UKSH, Arnold-Heller-Strasse 3, House 24, 24105 Kiel, Germany. Tel.: +49 431 5972086; fax: +49 431 5972149. E-mail addresses: [email protected], [email protected] (M. Elessawy). 1 Authors contributed equally.
operative team is needed to achieve safe surgery with a lower complication rate and a shorter operation time [8,9]. When choosing the laparoscopic technique, the advantages and disadvantages of laparoscopic supracervical hysterectomy (LSH) and total laparoscopic hysterectomy (TLH) have to be considered for each patient. The aim of the present study was to describe trends in the performance of hysterectomy between 2002 and 2010 in a single university hospital (a certified teaching center) in Germany. 2. Materials and methods The present study was a retrospective analysis of hysterectomy performed for benign disease at the Department of Obstetrics and Gynecology, University Hospital Schleswig-Holstein, Campus Kiel, Germany. Data were retrospectively collected from patient records and analyzed. The operation information lists were collected from the operation recording archive data backup for the period January 1, 2002, to October 31, 2010. Before treatment at the study center, patients sign an informed consent form allowing the use of their specimen and clinical data for research purposes. Institutional review board or ethics committee approval is not required in such cases. Patient data—including age, BMI, parity, previous operations, indications for operation, duration of hospital stay, operation time, weight of uterus, histopathologic report for removed specimen, hemoglobin decrease, and intra- and postoperative complications—were organized in
http://dx.doi.org/10.1016/j.ijgo.2013.12.017 0020-7292/© 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
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T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
Excel version 12.2 (Microsoft, Redmond, WA, USA). Operating time was calculated from the first incision to the final stitches. Hemoglobin level was measured 1 day preoperatively and 1 day postoperatively, with the difference recorded. Uterus weight was recorded from pathology reports. Of the 953 patients who underwent hysterectomy for benign disease during the study period, 766 met the inclusion criteria. Thirty women were excluded from the comparison criteria because of malignant histopathologic reports, 97 were excluded because of improper or incomplete recording of their data, and 60 patients did not sign an informed consent form allowing the use of their clinical data for research. Indications for surgery included fibroids, abnormal uterine bleeding, adenomyotic formations, endometriosis, and precancerous lesions of the uterus or the cervix. In the majority of cases, the operations were performed by consultants; LH procedures were performed by doctors holding the MIC I, II, or III qualification, which is awarded by the Arbeitsgruppe Gynaekologische Endoskopie (task force for gynecologic endoscopy). The department has established the Kiel School of Gynecological Endoscopy, where laparoscopic techniques are taught and have been highly standardized to reduce complications [10]. The operative techniques compared were VH, abdominal hysterectomy (AH), TLH, LSH, and laparoscopically assisted VH (LAVH). In order to have clear comparison parameters, it was decided that a preoperative risk score should be assigned to patients and that postoperative complications should be classified as major or minor. For the preoperative score, patients who had undergone a previous laparoscopy were assigned 1 point; those who had undergone a previous laparotomy were assigned 2 points; those who had undergone 1 cesarean delivery were assigned 3 points; those who had undergone 2 cesarean deliveries were assigned 4 points; those who had undergone 3 cesarean deliveries were assigned 5 points; and those with no previous operations were assigned 0 points. The preoperative score was recorded for 785 patients. Injury to blood vessels requiring a blood transfusion and injury to the intestines, rectum, and urinary tract (including ureter and urinary bladder) were classified as intraoperative complications. Major postoperative complications included postoperative bleeding and reoperations; minor postoperative complications included hematomas, vaginal bleeding, wound infections, dysuria, urinary tract infections, and fever. SPSS version 20 (IBM, Armonk, NY, USA) was used to log and analyze the data. The χ2 test was used to analyze the difference between 2 proportions; the t test was used to determine the significance of the difference between 2 proportions or percentages; the Mann–Whitney U test was used to compare a quantitative value between 2 groups of patients. Demographic and surgical data were analyzed via analysis of variance, Kruskal–Wallis test, χ2 test, or Fisher exact test. For age, BMI, hospital stay, operating time, uterus weight, and hemoglobin decrease, a mean ± SD value was calculated. P b 0.05 was considered to be statistically significant. 3. Results In total, 766 patients fulfilled the inclusion criteria of the study. The most frequently performed operative technique was VH (291 patients
[38.0%]), followed by AH (203 patients [26.5%]), LSH (163 patients [21.3%]), TLH (66 patients [8.6%]), and LAVH (43 patients [5.6%]) (Table 1). The majority of patients in the AH cohort had delivered 0 or 1–2 children (42.6% and 46.5%, respectively). By contrast, 59.1% of patients who underwent VH had 1–2 previous deliveries, 35.4% had delivered 3 or more children, and 5.5% were nulliparous. The percentage of nulliparous women who underwent LAVH was slightly higher (16.3%). The majority of patients who underwent LSH or TLH had delivered 1–2 children (46.6% and 57.6%, respectively). In these patient cohorts, 11.7% and 16.7%, respectively, had delivered 3 or more children. Mean BMI was 25.85 ± 5.40 in the different treatment cohorts. The mean preoperative score was 1.09 ± 1.51 for AH, 0.75 ± 0.96 for VH, 1.04 ± 1.30 for LSH, 1.0 ± 1.40 for LAVH, and 1.38 ± 1.52 for TLH. Most patients had a preoperative score of 0 or 1 (332 and 344, respectively) (Table 2). A preoperative score of 0 or 1 was most common among patients who underwent VH. Preoperative scores of 3 or higher were more common among patients who underwent AH. The predominant indication for hysterectomy was uterine myoma (58.6%), followed by uterine prolapse (17.9%) and abnormal bleeding (11.7%) (Table 3). Vaginal hysterectomy was the technique most frequently performed in cases of uterine prolapse; for abnormal bleeding, LSH was the most common operative technique. Most patients with endometriosis underwent a laparoscopic operation. The preferred techniques for treating adenomyosis were TLH and LAVH. Mean operation time was shortest for VH (76.03 ± 34.63 minutes). The longest operation times were associated with TLH (130.24 ± 38.27 minutes) and LAVH (137 ± 53.80 minutes) (Table 4). Mean uterine weight varied among the different operative techniques. The lightest uteri were extracted via VH (127.77 ± 78.35 g), whereas the average uterine weight in cases of AH was 518.58 ± 425.0 g (Fig. 1). Although the cervix is left in situ during LSH, the average uterine weight for this technique was higher (244.92 ± 185.82 g) than for TLH and LAVH (205.11 ± 149.33 and 159.24 ± 91.05 g, respectively). The mean decrease in hemoglobin was largest during LAVH (1.83 ± 1.08 g/dL) and AH (1.63 ± 1.08 g/dL). By contrast, LSH and TLH were associated with the smallest hemoglobin decrease (0.7 ± 0.84 and 0.82 ± 0.94 g/dL, respectively). During the study period, there were no mortalities recorded in association with hysterectomy for benign indications. From a total of 953 hysterectomies, complications were recorded in 52 (5.5%) cases (Table 4). The 2 entirely laparoscopic techniques (LSH and TLH) had a lower rate of complications than the other techniques. Intraoperative complications were recorded in 28 of 953 (2.9%) cases: 10 (35.7%) cases of VH; 13 (46.4%) cases of AH; 3 (10.7%) cases of LSH; 1 (3.6%) case of LAVH; and 1 (3.6%) case of TLH. The most common intraoperative complications were urinary bladder lesions (8 cases). They occurred in 3 cases of VH, 2 cases of AH, and 3 cases of LSH. Major postoperative complications occurred in 17 of 953 (1.8%) cases. The largest number was seen among patients who underwent VH (n = 7 [41.2%]) but a high percentage was among women who underwent LAVH (n = 3
Table 1 Patient characteristics.a Parameter
AH
VH
LAVH
LSH
TLH
Total
No. of operations Age, y Parity 0 1–2 ≥3 BMIb
203 (26.5) 44.8 ± 6.73
291 (38.0) 52.9 ± 13.77
43 (5.6) 44.5 ± 7.67
163 (21.3) 44.4 ± 6.32
66 (8.6) 44.1 ± 5.40
766 (100.0) 47.9 ± 10.87
86 (42.6) 95 (46.5) 22 (10.9) 26.5 ± 5.52
16 (5.5) 172 (59.1) 103 (35.4) 26.2 ± 5.61
7 (16.3) 19 (44.2) 17 (39.5) 25.7 ± 6.35
68 (41.7) 76 (46.6) 19 (11.7) 24.3 ± 4.18
17 (25.8) 38 (57.6) 11 (16.7) 25.4 ± 4.83
194 400 172 25.8 ± 5.40
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as number (percentage) or mean ± SD. b Calculated as weight in kilograms divided by the square of height in meters.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
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Table 2 Preoperative scores.a Preoperative score
AH
VH
LSH
LAVH
TLH
Total
0 1 3 4 5 6 8
98 (29.5) 66 (19.2) 15 (40.5) 20 (36.4) 5 (35.7) 0 (0.0) 1 (100.0)
130 (39.2) 151 (43.9) 6 (16.2) 10 (18.2) 3 (21.4) 0 (0.0) 0 (0.0)
64 (19.3) 78 (22.7) 11 (29.7) 12 (21.8) 3 (21.4) 1 (50.0) 0 (0.0)
18 (5.4) 20 (5.8) 0 (0.0) 3 (5.5) 1 (7.1) 1 (50.0) 0 (0.0)
22 (6.6) 29 (8.4) 5 (13.5) 10 (18.2) 2 (14.3) 0 (0.0) 0 (0.0)
332 (100.0) 344 (100.0) 37 (100.0) 55 (100.0) 14 (100.0) 2 (100.0) 1 (100.0)
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as number (percentage).
Table 3 Indications for operations.a Indication
AH
VH
LAVH
LSH
TLH
Total
Uterine myoma Adenomyosis Abnormal bleeding Hyperplasia of uterus and cervix Prolapse Endometriosis Total
238 (74.8) 22 (6.9) 37 (11.6) 6 (1.9) 3 (0.9) 12 (3.8) 318
158 (40.8) 41 (10.6) 40 (10.3) 11 (2.8) 131 (33.9) 6 (1.6) 387
31 (58.5) 7 (13.2) 5 (9.4) 1 (1.9) 3 (5.7) 6 (11.3) 53
145 (63.0) 25 (10.9) 39 (17.0) 0 (0.0) 4 (1.7) 17 (7.4) 230
50 (68.5) 12 (16.4) 3 (4.1) 1 (1.4) 0 (0.0) 7 (9.6) 73
622 (58.6) 107 (10.1) 124 (11.7) 19 (1.9) 141 (17.9) 48 (4.5) 1061
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as number (percentage).
[17.6%]). Laparoscopic supracervical hysterectomy and TLH had similar complication rates: 11.8% (n = 2) and 5.9% (n = 1), respectively. Reoperation occurred 6 times in cases of VH, representing the highest incidence of major complications: 3 times for LAVH, twice for LSH, and once for TLH. Minor postoperative complications were recorded in 56 of 953 (5.9%) hysterectomies: 23 (41.1%) cases of VH; 24 (42.9%) cases of AH; 3 (5.4%) cases of LSH; 3 (5.4%) cases of LAVH; and 3 (5.4%) cases of TLH. Hematoma was recorded in 15 cases of AH and 13 cases of VH. As a consequence, wound infection rates were also higher after either of these treatments. Intraoperative complications occurred more frequently with increased uterine weight (P = 0.029). Hemoglobin decrease was larger in the event of intraoperative complications (P = 0.019). Hospital stay and operation time were prolonged in cases involving intraoperative complications (P b 0.001 and P = 0.027, respectively), showing a direct correlation. Increased BMI and uterine weight showed no correlation with postoperative complications (P = 0.748 and P = 0.743, respectively). In the study department, the number of laparoscopic operations increased during the study period, whereas the numbers of VH and AH procedures decreased steadily. Between 2007 and 2010, the numbers of AH and VH operations decreased owing to the increased numbers of LSH and TLH procedures. In 2010, LSH (37.9%) and TLH (15.3%) represented 53.2% of the total number of hysterectomies, while VH and AH represented 25% and 21.7%, respectively (Fig. 2).
4. Discussion The present results confirm the major benign indications for hysterectomy among all operative techniques used at the study center. For certain indications (e.g. uterine prolapse), VH was performed in the majority of patients. The number of previous births was also highest in the group that underwent VH. Operating time was shortest for VH and longest for TLH. Many factors could be responsible for this variation; for example, VH has been practiced for many years, which makes surgeons more familiar with the technique. A large uterus or the presence of adhesions could also result in prolonged operating times for TLH and AH, and time required for morcellation is one of the reasons for longer operation times for LSH and TLH [11]. The change in route of operation with LAVH (from abdominal to vaginal) could be another reason for extended operating time [12]. The 2 laparoscopic techniques for hysterectomy (LSH and TLH) were associated with lower complication rates than were VH and AH. The availability of manipulators has made the performance of LH easier [13,14]. The low complication rates are particularly interesting because the mean preoperative score was highest for patients who underwent TLH (1.38 vs 1.09 for patients who underwent AH), indicating that these patients had undergone the most previous abdominal operations. In the present study, the most common intraoperative complications were urinary bladder lesions (0.7%), which occurred in cases of VH,
Table 4 Operation criteria and complications. Parameter
AH
VH
LAVH
LSH
TLH
Total
Operation time, min Weight of uterus, g Decrease in hemoglobin, g/dL Intraoperative complications Major complications
107.71 ± 47.09 518.58 ± 424.34 1.63 ± 1.08 13 (46.4) 4 (23.5)
76.03 ± 34.63 127.77 ± 78.35 1.29 ± 0.96 10 (35.7) 7 (41.2)
137.00 ± 53.80 159.24 ± 91.05 1.83 ± 1.07 1 (3.6) 3 (17.6)
106.59 ± 44.53 244.92 ± 187.78 0.70 ± 0.83 3 (10.7) 2 (11.8)
130.24 ± 38.27 205.11 ± 149.32 0.82 ± 0.942 1 (3.6) 1 (5.9)
28/953 (2.9) 17/953 (1.8)
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as mean ± SD or number (percentage).
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
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T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
Fig. 1. Comparison of different operative techniques. Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy.
AH, and LSH. The rate of urinary bladder lesions in Finland was reported to be 6.9% for LH and 7.1% for VH [15]. Some studies have reported that urinary tract lesions occur more frequently during LH [6,8,16]. An association was found in the present study between intraoperative complications and increased uterine weight, consistent with the literature [17]. The major postoperative complication rate was 1.8% and the minor postoperative complication rate was 5.9%. Hemoglobin decrease in
cases of VH was 1.29 g/dL, which was higher than for LSH or TLH. Hwang et al. [18] reported increased blood loss for VH compared with AH. Candiani et al. [19] reported a lower hemoglobin decrease for LH compared with VH. Donnez et al. [20] reported that the percentage of AH procedures decreased from 23% in 1990 to 4% in 2006 after the introduction of LH at a university hospital in Brussels, Belgium. With the development of
Fig. 2. Development of operative techniques between 2002 and 2010. Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
laparoscopic techniques, the distribution of methods varies in different countries. In 2010, VH represented 59.9% and AH 19.3% of all hysterectomy methods in Germany, while VH represented 22%, AH 64%, and LAVH 14% in the USA [21]. At the study department, the number of laparoscopic operations is increasing steadily owing to the establishment of TLH and LSH in 2003 and 2004, respectively. The standardization of the techniques has resulted in a decrease in the incidence of complications. This, in turn, has led to an increase in the number of laparoscopic hysterectomies. In conclusion, the decision regarding the route of hysterectomy is dependent on surgeon experience and operative indication. Shared decision making and consent between the surgeon and the patient are highly recommended. This decision should be individualized for each patient to find the best route for hysterectomy. Conflict of interest The authors have no conflicts of interest. References [1] Altgassen C, Michels W, Schneider A. Learning laparoscopic-assisted hysterectomy. Obstet Gynecol 2004;104(2):308–13. [2] Briese V, Ulfig N, Mylonas I. Vaginal hysterectomy. Gynakologe 2002;35:116–24. [3] Stang A, Merrill RM, Kuss O. Prevalence-corrected hysterectomy rates by age and indication in Germany 2005-2006. Arch Gynecol Obstet 2012;286(5):1193–200. [4] Whiteman MK, Hillis SD, Jamieson DJ, Morrow B, Podgornik MN, Brett KM, et al. Inpatient hysterectomy surveillance in the United States, 2000-2004. Am J Obstet Gynecol 2008;198(1):34.e1–7. [5] Hornemann A, Thill M, Bohlmann MK, Fischer D, Diedrich K, Altgassen C. Hysterectomy - vaginal, abdominal or laparoscopically assisted? Gynakologe 2008;5: 337–42. [6] Müller A, Thiel FC, Renner SP, Winkler M, Häberle L, Beckmann MW. Hysterectomy-a comparison of approaches. Dtsch Arztebl Int 2010;107(20):353–9. [7] Kovac SR, Barhan S, Lister M, Tucker L, Bishop M, Das A. Guidelines for the selection of the route of hysterectomy: application in a resident clinic population. Am J Obstet Gynecol 2002;187(6):1521–7.
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[8] Schindlbeck C, Klauser K, Dian D, Janni W, Friese K. Comparison of total laparoscopic, vaginal and abdominal hysterectomy. Arch Gynecol Obstet 2008;277(4):331–7. [9] Lyons TL. Laparoscopic supracervical hysterectomy. Obstet Gynecol Clin North Am 2000;27(2):441–50. [10] Schollmeyer T, Elessawy M. Total Laparoscopic Hysterectomy. In: Schollmeyer T, Mettler L, Rüther D, Alkatout I, editors. Practical Manual for Laparoscopic & Hysteroscopic Gynecological Surgery. New Delhi: Jaypee Brothers Medical Pub; 2013. p. 301–10. [11] Condous G, Bignardi T, Alhamdan D, Van Calster B, Van Huffel S, Timmerman D, et al. What determines the need to morcellate the uterus during total laparoscopic hysterectomy? J Minim Invasive Gynecol 2009;16(1):52–5. [12] Chen SY, Chang DY, Sheu BC, Torng PL, Huang SC, Hsu WC, et al. Laparoscopicassisted vaginal hysterectomy with in situ morcellation for large uteri. J Minim Invasive Gynecol 2008;15(5):559–65. [13] Mueller A, Boosz A, Koch M, Jud S, Faschingbauer F, Schrauder M, et al. The Hohl instrument for optimizing total laparoscopic hysterectomy: results of more than 500 procedures in a university training center. Arch Gynecol Obstet 2012;285(1): 123–7. [14] Ou CS, Joki J, Wells K, Zabriske V, Hamilton K, Tsuang M, et al. Total laparoscopic hysterectomy using multifunction grasping, coagulating, and cutting forceps. J Laparoendosc Adv Surg Tech A 2004;14(2):67–71. [15] Brummer TH, Jalkanen J, Fraser J, Heikkinen AM, Kauko M, Mäkinen J, et al. FINHYST, a prospective study of 5279 hysterectomies: complications and their risk factors. Hum Reprod 2011;26(7):1741–51. [16] Nieboer TE, Johnson N, Lethaby A, Tavender E, Curr E, Garry R, et al. Surgical approach to hysterectomy for benign gynaecological disease. Cochrane Database Syst Rev 2009;3:CD003677. [17] Hillis SD, Marchbanks PA, Peterson HB. Uterine size and risk of complications among women undergoing abdominal hysterectomy for leiomyomas. Obstet Gynecol 1996;87(4):539–43. [18] Hwang JL, Seow KM, Tsai YL, Huang LW, Hsieh BC, Lee C. 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(12):1132–8. [19] Candiani M, Izzo S, Bulfoni A, Riparini J, Ronzoni S, Marconi A. Laparoscopic vs vaginal hysterectomy for benign pathology. Am J Obstet Gynecol 2009;200(4):368.e1–7. [20] Donnez O, Jadoul P, Squifflet J, Donnez J. A series of 3190 laparoscopic hysterectomies for benign disease from 1990 to 2006: evaluation of complications compared with vaginal and abdominal procedures. BJOG 2009;116(4):492–500. [21] Jacobson TZ, Duffy JM, Barlow D, Koninckx PR, Garry R. Laparoscopic surgery for pelvic pain associated with endometriosis. Cochrane Database Syst Rev 2009;4: CD001300.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Hysterectomy trends over a 9-year period in an endoscopic teaching center Thoralf Schollmeyer a,1, Mohamed Elessawy a,⁎,1, Babis Chastamouratidhs a, Ibrahim Alkatout a, Ivo Meinhold-Heerlein b, Liselotte Mettler a, Walter Jonat a, Marion T. Weigel a a b
Department of Obstetrics and Gynecology, Kiel School of Gynecological Endoscopy, University Hospitals Schleswig-Holstein, Kiel, Germany Department of Obstetrics and Gynecology, RWTH Aachen University, Aachen, Germany
a r t i c l e
i n f o
Article history: Received 23 August 2013 Received in revised form 17 December 2013 Accepted 4 April 2014 Keywords: Benign indications Complications Hysterectomy Laparoscopy Teaching
a b s t r a c t Objective: To investigate trends in the performance of hysterectomy at a single certified endoscopic teaching center. Methods: Data were collected retrospectively from 953 patients who underwent hysterectomy between 2002 and 2010 for benign indications at UKSH, Germany. Preoperative risk scores were assigned to patients. Results: The most frequent indications for hysterectomy were uterine myoma, adenomyosis, prolapse, endometrial hyperplasia, menstrual disorders, and endometriosis. The shortest operating time was recorded for vaginal hysterectomy (VH) and the longest for laparoscopically assisted VH (LAVH). The average uterine weight was highest for abdominal hysterectomy (AH) and lowest for VH. The major postoperative complication rate was 11.8% for laparoscopic supracervical hysterectomy (LSH) and 23.5% for AH. The highest intraoperative complication rate occurred with AH (46.4%) and the lowest with total laparoscopic hysterectomy (TLH; 3.6%). The minor postoperative complication rate was 5.9%. The mean preoperative score was 1.09 ± 1.51 for AH, 0.75 ± 0.96 for VH, 1.04 ± 1.30 for LSH, 1.0 ± 1.40 for LAVH, and 1.38 ± 1.52 for TLH. Conclusion: Laparoscopic hysterectomies have become more common and were associated with decreased complication rates, despite the higher preoperative risk score of these patients. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Hysterectomy is the most frequently performed major gynecologic surgical procedure [1,2]. The overall rate of hysterectomy in Germany in 2005–2006 was 362.9 (295.0 for benign diseases of the genital tract and 44.0 for primary malignant tumors of the genital tract) per 100 000 women per year [3]. The Centers for Disease Control and Prevention reported that the US hysterectomy rate in 2000–2004 was 5.4 per 1000 women per year [4]. The art of surgery has developed and changed with the advancement of technology so that hysterectomy is now performed primarily as a minimally invasive operation. Benign indications for hysterectomy are symptomatic or growing uterine myomas, adenomyosis, abnormal uterine bleeding, endometriosis, and prolapse of the uterus [5]. The choice of route for hysterectomy is dependent on many factors: size and mobility of uterus; body mass index (BMI, calculated as weight in kilograms divided by the square of height in meters); preoperative history; anatomic variation; level of experience of surgeon; and patient preference. Laparoscopic hysterectomy (LH) is the method of choice whenever vaginal hysterectomy (VH) is not possible [6,7]. A well-trained ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Kiel School of Gynecological Endoscopy, UKSH, Arnold-Heller-Strasse 3, House 24, 24105 Kiel, Germany. Tel.: +49 431 5972086; fax: +49 431 5972149. E-mail addresses: [email protected], [email protected] (M. Elessawy). 1 Authors contributed equally.
operative team is needed to achieve safe surgery with a lower complication rate and a shorter operation time [8,9]. When choosing the laparoscopic technique, the advantages and disadvantages of laparoscopic supracervical hysterectomy (LSH) and total laparoscopic hysterectomy (TLH) have to be considered for each patient. The aim of the present study was to describe trends in the performance of hysterectomy between 2002 and 2010 in a single university hospital (a certified teaching center) in Germany. 2. Materials and methods The present study was a retrospective analysis of hysterectomy performed for benign disease at the Department of Obstetrics and Gynecology, University Hospital Schleswig-Holstein, Campus Kiel, Germany. Data were retrospectively collected from patient records and analyzed. The operation information lists were collected from the operation recording archive data backup for the period January 1, 2002, to October 31, 2010. Before treatment at the study center, patients sign an informed consent form allowing the use of their specimen and clinical data for research purposes. Institutional review board or ethics committee approval is not required in such cases. Patient data—including age, BMI, parity, previous operations, indications for operation, duration of hospital stay, operation time, weight of uterus, histopathologic report for removed specimen, hemoglobin decrease, and intra- and postoperative complications—were organized in
http://dx.doi.org/10.1016/j.ijgo.2013.12.017 0020-7292/© 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
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T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
Excel version 12.2 (Microsoft, Redmond, WA, USA). Operating time was calculated from the first incision to the final stitches. Hemoglobin level was measured 1 day preoperatively and 1 day postoperatively, with the difference recorded. Uterus weight was recorded from pathology reports. Of the 953 patients who underwent hysterectomy for benign disease during the study period, 766 met the inclusion criteria. Thirty women were excluded from the comparison criteria because of malignant histopathologic reports, 97 were excluded because of improper or incomplete recording of their data, and 60 patients did not sign an informed consent form allowing the use of their clinical data for research. Indications for surgery included fibroids, abnormal uterine bleeding, adenomyotic formations, endometriosis, and precancerous lesions of the uterus or the cervix. In the majority of cases, the operations were performed by consultants; LH procedures were performed by doctors holding the MIC I, II, or III qualification, which is awarded by the Arbeitsgruppe Gynaekologische Endoskopie (task force for gynecologic endoscopy). The department has established the Kiel School of Gynecological Endoscopy, where laparoscopic techniques are taught and have been highly standardized to reduce complications [10]. The operative techniques compared were VH, abdominal hysterectomy (AH), TLH, LSH, and laparoscopically assisted VH (LAVH). In order to have clear comparison parameters, it was decided that a preoperative risk score should be assigned to patients and that postoperative complications should be classified as major or minor. For the preoperative score, patients who had undergone a previous laparoscopy were assigned 1 point; those who had undergone a previous laparotomy were assigned 2 points; those who had undergone 1 cesarean delivery were assigned 3 points; those who had undergone 2 cesarean deliveries were assigned 4 points; those who had undergone 3 cesarean deliveries were assigned 5 points; and those with no previous operations were assigned 0 points. The preoperative score was recorded for 785 patients. Injury to blood vessels requiring a blood transfusion and injury to the intestines, rectum, and urinary tract (including ureter and urinary bladder) were classified as intraoperative complications. Major postoperative complications included postoperative bleeding and reoperations; minor postoperative complications included hematomas, vaginal bleeding, wound infections, dysuria, urinary tract infections, and fever. SPSS version 20 (IBM, Armonk, NY, USA) was used to log and analyze the data. The χ2 test was used to analyze the difference between 2 proportions; the t test was used to determine the significance of the difference between 2 proportions or percentages; the Mann–Whitney U test was used to compare a quantitative value between 2 groups of patients. Demographic and surgical data were analyzed via analysis of variance, Kruskal–Wallis test, χ2 test, or Fisher exact test. For age, BMI, hospital stay, operating time, uterus weight, and hemoglobin decrease, a mean ± SD value was calculated. P b 0.05 was considered to be statistically significant. 3. Results In total, 766 patients fulfilled the inclusion criteria of the study. The most frequently performed operative technique was VH (291 patients
[38.0%]), followed by AH (203 patients [26.5%]), LSH (163 patients [21.3%]), TLH (66 patients [8.6%]), and LAVH (43 patients [5.6%]) (Table 1). The majority of patients in the AH cohort had delivered 0 or 1–2 children (42.6% and 46.5%, respectively). By contrast, 59.1% of patients who underwent VH had 1–2 previous deliveries, 35.4% had delivered 3 or more children, and 5.5% were nulliparous. The percentage of nulliparous women who underwent LAVH was slightly higher (16.3%). The majority of patients who underwent LSH or TLH had delivered 1–2 children (46.6% and 57.6%, respectively). In these patient cohorts, 11.7% and 16.7%, respectively, had delivered 3 or more children. Mean BMI was 25.85 ± 5.40 in the different treatment cohorts. The mean preoperative score was 1.09 ± 1.51 for AH, 0.75 ± 0.96 for VH, 1.04 ± 1.30 for LSH, 1.0 ± 1.40 for LAVH, and 1.38 ± 1.52 for TLH. Most patients had a preoperative score of 0 or 1 (332 and 344, respectively) (Table 2). A preoperative score of 0 or 1 was most common among patients who underwent VH. Preoperative scores of 3 or higher were more common among patients who underwent AH. The predominant indication for hysterectomy was uterine myoma (58.6%), followed by uterine prolapse (17.9%) and abnormal bleeding (11.7%) (Table 3). Vaginal hysterectomy was the technique most frequently performed in cases of uterine prolapse; for abnormal bleeding, LSH was the most common operative technique. Most patients with endometriosis underwent a laparoscopic operation. The preferred techniques for treating adenomyosis were TLH and LAVH. Mean operation time was shortest for VH (76.03 ± 34.63 minutes). The longest operation times were associated with TLH (130.24 ± 38.27 minutes) and LAVH (137 ± 53.80 minutes) (Table 4). Mean uterine weight varied among the different operative techniques. The lightest uteri were extracted via VH (127.77 ± 78.35 g), whereas the average uterine weight in cases of AH was 518.58 ± 425.0 g (Fig. 1). Although the cervix is left in situ during LSH, the average uterine weight for this technique was higher (244.92 ± 185.82 g) than for TLH and LAVH (205.11 ± 149.33 and 159.24 ± 91.05 g, respectively). The mean decrease in hemoglobin was largest during LAVH (1.83 ± 1.08 g/dL) and AH (1.63 ± 1.08 g/dL). By contrast, LSH and TLH were associated with the smallest hemoglobin decrease (0.7 ± 0.84 and 0.82 ± 0.94 g/dL, respectively). During the study period, there were no mortalities recorded in association with hysterectomy for benign indications. From a total of 953 hysterectomies, complications were recorded in 52 (5.5%) cases (Table 4). The 2 entirely laparoscopic techniques (LSH and TLH) had a lower rate of complications than the other techniques. Intraoperative complications were recorded in 28 of 953 (2.9%) cases: 10 (35.7%) cases of VH; 13 (46.4%) cases of AH; 3 (10.7%) cases of LSH; 1 (3.6%) case of LAVH; and 1 (3.6%) case of TLH. The most common intraoperative complications were urinary bladder lesions (8 cases). They occurred in 3 cases of VH, 2 cases of AH, and 3 cases of LSH. Major postoperative complications occurred in 17 of 953 (1.8%) cases. The largest number was seen among patients who underwent VH (n = 7 [41.2%]) but a high percentage was among women who underwent LAVH (n = 3
Table 1 Patient characteristics.a Parameter
AH
VH
LAVH
LSH
TLH
Total
No. of operations Age, y Parity 0 1–2 ≥3 BMIb
203 (26.5) 44.8 ± 6.73
291 (38.0) 52.9 ± 13.77
43 (5.6) 44.5 ± 7.67
163 (21.3) 44.4 ± 6.32
66 (8.6) 44.1 ± 5.40
766 (100.0) 47.9 ± 10.87
86 (42.6) 95 (46.5) 22 (10.9) 26.5 ± 5.52
16 (5.5) 172 (59.1) 103 (35.4) 26.2 ± 5.61
7 (16.3) 19 (44.2) 17 (39.5) 25.7 ± 6.35
68 (41.7) 76 (46.6) 19 (11.7) 24.3 ± 4.18
17 (25.8) 38 (57.6) 11 (16.7) 25.4 ± 4.83
194 400 172 25.8 ± 5.40
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as number (percentage) or mean ± SD. b Calculated as weight in kilograms divided by the square of height in meters.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
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Table 2 Preoperative scores.a Preoperative score
AH
VH
LSH
LAVH
TLH
Total
0 1 3 4 5 6 8
98 (29.5) 66 (19.2) 15 (40.5) 20 (36.4) 5 (35.7) 0 (0.0) 1 (100.0)
130 (39.2) 151 (43.9) 6 (16.2) 10 (18.2) 3 (21.4) 0 (0.0) 0 (0.0)
64 (19.3) 78 (22.7) 11 (29.7) 12 (21.8) 3 (21.4) 1 (50.0) 0 (0.0)
18 (5.4) 20 (5.8) 0 (0.0) 3 (5.5) 1 (7.1) 1 (50.0) 0 (0.0)
22 (6.6) 29 (8.4) 5 (13.5) 10 (18.2) 2 (14.3) 0 (0.0) 0 (0.0)
332 (100.0) 344 (100.0) 37 (100.0) 55 (100.0) 14 (100.0) 2 (100.0) 1 (100.0)
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as number (percentage).
Table 3 Indications for operations.a Indication
AH
VH
LAVH
LSH
TLH
Total
Uterine myoma Adenomyosis Abnormal bleeding Hyperplasia of uterus and cervix Prolapse Endometriosis Total
238 (74.8) 22 (6.9) 37 (11.6) 6 (1.9) 3 (0.9) 12 (3.8) 318
158 (40.8) 41 (10.6) 40 (10.3) 11 (2.8) 131 (33.9) 6 (1.6) 387
31 (58.5) 7 (13.2) 5 (9.4) 1 (1.9) 3 (5.7) 6 (11.3) 53
145 (63.0) 25 (10.9) 39 (17.0) 0 (0.0) 4 (1.7) 17 (7.4) 230
50 (68.5) 12 (16.4) 3 (4.1) 1 (1.4) 0 (0.0) 7 (9.6) 73
622 (58.6) 107 (10.1) 124 (11.7) 19 (1.9) 141 (17.9) 48 (4.5) 1061
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as number (percentage).
[17.6%]). Laparoscopic supracervical hysterectomy and TLH had similar complication rates: 11.8% (n = 2) and 5.9% (n = 1), respectively. Reoperation occurred 6 times in cases of VH, representing the highest incidence of major complications: 3 times for LAVH, twice for LSH, and once for TLH. Minor postoperative complications were recorded in 56 of 953 (5.9%) hysterectomies: 23 (41.1%) cases of VH; 24 (42.9%) cases of AH; 3 (5.4%) cases of LSH; 3 (5.4%) cases of LAVH; and 3 (5.4%) cases of TLH. Hematoma was recorded in 15 cases of AH and 13 cases of VH. As a consequence, wound infection rates were also higher after either of these treatments. Intraoperative complications occurred more frequently with increased uterine weight (P = 0.029). Hemoglobin decrease was larger in the event of intraoperative complications (P = 0.019). Hospital stay and operation time were prolonged in cases involving intraoperative complications (P b 0.001 and P = 0.027, respectively), showing a direct correlation. Increased BMI and uterine weight showed no correlation with postoperative complications (P = 0.748 and P = 0.743, respectively). In the study department, the number of laparoscopic operations increased during the study period, whereas the numbers of VH and AH procedures decreased steadily. Between 2007 and 2010, the numbers of AH and VH operations decreased owing to the increased numbers of LSH and TLH procedures. In 2010, LSH (37.9%) and TLH (15.3%) represented 53.2% of the total number of hysterectomies, while VH and AH represented 25% and 21.7%, respectively (Fig. 2).
4. Discussion The present results confirm the major benign indications for hysterectomy among all operative techniques used at the study center. For certain indications (e.g. uterine prolapse), VH was performed in the majority of patients. The number of previous births was also highest in the group that underwent VH. Operating time was shortest for VH and longest for TLH. Many factors could be responsible for this variation; for example, VH has been practiced for many years, which makes surgeons more familiar with the technique. A large uterus or the presence of adhesions could also result in prolonged operating times for TLH and AH, and time required for morcellation is one of the reasons for longer operation times for LSH and TLH [11]. The change in route of operation with LAVH (from abdominal to vaginal) could be another reason for extended operating time [12]. The 2 laparoscopic techniques for hysterectomy (LSH and TLH) were associated with lower complication rates than were VH and AH. The availability of manipulators has made the performance of LH easier [13,14]. The low complication rates are particularly interesting because the mean preoperative score was highest for patients who underwent TLH (1.38 vs 1.09 for patients who underwent AH), indicating that these patients had undergone the most previous abdominal operations. In the present study, the most common intraoperative complications were urinary bladder lesions (0.7%), which occurred in cases of VH,
Table 4 Operation criteria and complications. Parameter
AH
VH
LAVH
LSH
TLH
Total
Operation time, min Weight of uterus, g Decrease in hemoglobin, g/dL Intraoperative complications Major complications
107.71 ± 47.09 518.58 ± 424.34 1.63 ± 1.08 13 (46.4) 4 (23.5)
76.03 ± 34.63 127.77 ± 78.35 1.29 ± 0.96 10 (35.7) 7 (41.2)
137.00 ± 53.80 159.24 ± 91.05 1.83 ± 1.07 1 (3.6) 3 (17.6)
106.59 ± 44.53 244.92 ± 187.78 0.70 ± 0.83 3 (10.7) 2 (11.8)
130.24 ± 38.27 205.11 ± 149.32 0.82 ± 0.942 1 (3.6) 1 (5.9)
28/953 (2.9) 17/953 (1.8)
Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy. a Values are given as mean ± SD or number (percentage).
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
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T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
Fig. 1. Comparison of different operative techniques. Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy.
AH, and LSH. The rate of urinary bladder lesions in Finland was reported to be 6.9% for LH and 7.1% for VH [15]. Some studies have reported that urinary tract lesions occur more frequently during LH [6,8,16]. An association was found in the present study between intraoperative complications and increased uterine weight, consistent with the literature [17]. The major postoperative complication rate was 1.8% and the minor postoperative complication rate was 5.9%. Hemoglobin decrease in
cases of VH was 1.29 g/dL, which was higher than for LSH or TLH. Hwang et al. [18] reported increased blood loss for VH compared with AH. Candiani et al. [19] reported a lower hemoglobin decrease for LH compared with VH. Donnez et al. [20] reported that the percentage of AH procedures decreased from 23% in 1990 to 4% in 2006 after the introduction of LH at a university hospital in Brussels, Belgium. With the development of
Fig. 2. Development of operative techniques between 2002 and 2010. Abbreviations: AH, abdominal hysterectomy; LAVH, laparoscopically assisted vaginal hysterectomy; LSH, laparoscopic supracervical hysterectomy; TLH, total laparoscopic hysterectomy; VH, vaginal hysterectomy.
Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
T. Schollmeyer et al. / International Journal of Gynecology and Obstetrics xxx (2014) xxx–xxx
laparoscopic techniques, the distribution of methods varies in different countries. In 2010, VH represented 59.9% and AH 19.3% of all hysterectomy methods in Germany, while VH represented 22%, AH 64%, and LAVH 14% in the USA [21]. At the study department, the number of laparoscopic operations is increasing steadily owing to the establishment of TLH and LSH in 2003 and 2004, respectively. The standardization of the techniques has resulted in a decrease in the incidence of complications. This, in turn, has led to an increase in the number of laparoscopic hysterectomies. In conclusion, the decision regarding the route of hysterectomy is dependent on surgeon experience and operative indication. Shared decision making and consent between the surgeon and the patient are highly recommended. This decision should be individualized for each patient to find the best route for hysterectomy. Conflict of interest The authors have no conflicts of interest. References [1] Altgassen C, Michels W, Schneider A. Learning laparoscopic-assisted hysterectomy. Obstet Gynecol 2004;104(2):308–13. [2] Briese V, Ulfig N, Mylonas I. Vaginal hysterectomy. Gynakologe 2002;35:116–24. [3] Stang A, Merrill RM, Kuss O. Prevalence-corrected hysterectomy rates by age and indication in Germany 2005-2006. Arch Gynecol Obstet 2012;286(5):1193–200. [4] Whiteman MK, Hillis SD, Jamieson DJ, Morrow B, Podgornik MN, Brett KM, et al. Inpatient hysterectomy surveillance in the United States, 2000-2004. Am J Obstet Gynecol 2008;198(1):34.e1–7. [5] Hornemann A, Thill M, Bohlmann MK, Fischer D, Diedrich K, Altgassen C. Hysterectomy - vaginal, abdominal or laparoscopically assisted? Gynakologe 2008;5: 337–42. [6] Müller A, Thiel FC, Renner SP, Winkler M, Häberle L, Beckmann MW. Hysterectomy-a comparison of approaches. Dtsch Arztebl Int 2010;107(20):353–9. [7] Kovac SR, Barhan S, Lister M, Tucker L, Bishop M, Das A. Guidelines for the selection of the route of hysterectomy: application in a resident clinic population. Am J Obstet Gynecol 2002;187(6):1521–7.
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Please cite this article as: Schollmeyer T, et al, Hysterectomy trends over a 9-year period in an endoscopic teaching center, Int J Gynecol Obstet (2014), http://dx.doi.org/10.1016/j.ijgo.2013.12.017
