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Uterine sarcomas and parasitic myomas after laparoscopic hysterectomy with power morcellation

Published:December 11, 2014DOI:https://doi.org/10.1016/j.ajog.2014.12.002

      Objective

      The purpose of this study was to describe the incidence and risk factors for uterine sarcomas and parasitic myomas at the time of power morcellation.

      Study Design

      We performed a retrospective review of 3523 women who underwent laparoscopic hysterectomy from 2001-2012. Univariate analyses were used for the morcellation cases to identify potential risk factors. Multivariable logistic regression was performed.

      Results

      Nine hundred forty-one patients underwent power morcellation at the time of hysterectomy; 10 of 941 patients (1.1%) were diagnosed subsequently with uterine sarcomas or parasitic myomas. The overall incidence of uterine sarcoma was 6 of 941 (0.6%), with a median age of 47 years (range, 41–52 years). There was no association among any of the factors analyzed and uterine sarcoma. Three of 6 patients had sarcoma diagnosed on initial pathologic evaluation of the morcellated specimen; 3 patients had delayed diagnosis of sarcoma with benign disease at the time of the initial procedure (median time to second evaluation, 6 years). For parasitic myomas (n = 4), the median age was 35 years (range, 32–40 years), and the median time to second evaluation was 5 years. On multivariate analysis, age <40 years (odds ratio, 26; 95% confidence interval, 2.7015–261.9; P ≤ .01) was associated with higher risk of the development of parasitic myomas.

      Conclusion

      Uterine sarcoma was found in 0.6% of patients who underwent power morcellation but was not found to be associated significantly with any preoperative factors. All 6 cases were noted to have apparent fibroid tumors as an indication for their hysterectomy. Age <40 years was a risk factor for parasitic myomas after power morcellation. Patients should be counseled about these complications before power morcellation.

      Key words

      See related editorial, page 553
      More than 600,000 hysterectomies are performed in the United States annually, with 40% performed laparoscopically.
      • Warren L.
      • Ladapo J.A.
      • Borah B.J.
      • Gunnarsson C.L.
      Open abdominal versus laparoscopic and vaginal hysterectomy: analysis of a large United States payer measuring quality and cost of care.

      Center for Disease Control National Center for Health Statistics, National Hospital Discharge Summary 2010 [Internet]. 2010 [cited 2014 May 26]. Available at: http://www.cdc.gov/nchs/data/nhds/4procedures/2010pro4_numberrate.pdf. Accessed Aug. 1, 2014.

      Laparoscopic hysterectomy is associated with fewer postoperative complications, less blood loss, less postoperative pain, decreased hospital stay, and faster recovery time when compared with the open abdominal approach.
      • Warren L.
      • Ladapo J.A.
      • Borah B.J.
      • Gunnarsson C.L.
      Open abdominal versus laparoscopic and vaginal hysterectomy: analysis of a large United States payer measuring quality and cost of care.
      • Walsh C.A.
      • Walsh S.R.
      • Tang T.Y.
      • Slack M.
      Total abdominal hysterectomy versus total laparoscopic hysterectomy for benign disease: a meta-analysis.
      Power morcellation is performed during laparoscopic supracervical hysterectomy, laparoscopic myomectomy, and laparoscopic total hysterectomy when the uterus is too large to pass through the vaginal canal.
      • Jacobson G.F.
      • Shaber R.E.
      • Armstrong M.A.
      • Hung Y.-Y.
      Hysterectomy rates for benign indications.
      It involves the division of uterine tissue with the use of a rotating circular blade to facilitate removal of the specimen. Power morcellation has raised concern for potential dissemination of benign or malignant tissue. The Food and Drug Administration (FDA) recently issued a warning discouraging the use of power morcellation with uterine fibroid tumors.
      Press Announcement
      FDA discourages use of laparoscopic power morcellation for removal of uterus or uterine fibroids.
      Spindle cell neoplasms are tumors of the uterine smooth muscle or endometrial stroma. They include parasitic myomas and uterine sarcomas. Uterine sarcomas are malignant tumors of uterine connective tissue and include leiomyosarcoma, endometrial stromal sarcoma, carcinosarcoma, and undifferentiated sarcoma, with a reported incidence of 0.2%.
      Press Announcement
      FDA discourages use of laparoscopic power morcellation for removal of uterus or uterine fibroids.
      • Seidman M.A.
      • Oduyebo T.
      • Muto M.G.
      • Crum C.P.
      • Nucci M.R.
      • Quade B.J.
      Peritoneal dissemination complicating morcellation of uterine mesenchymal neoplasms.

      American College of Obstetricians and Gynecologists. Power morcellation and occult malignancy in gynecologic surgery: a special report [Internet]. [cited 2014 May 26]. Available at: http://www.acog.org/Resources_And_Publications/Task_Force_and_Work_Group_Reports/Power_Morcellation_and_Occult_Malignancy_in_Gynecologic_Surgery. Accessed Dec. 1, 2014.

      They often behave more aggressively and are associated with a poorer prognosis than endometrial cancers.
      • Harlow B.L.
      • Weiss N.S.
      • Lofton S.
      The epidemiology of sarcomas of the uterus.
      • Kim W.Y.
      • Chang S.-J.
      • Chang K.-H.
      • et al.
      Uterine leiomyosarcoma: 14-year two-center experience of 31 cases.
      There are no specific symptoms or signs or reliable diagnostic modalities to differentiate benign from malignant uterine tumors before they are morcellated and removed.
      • Park J.-Y.
      • Park S.-K.
      • Kim D.-Y.
      • et al.
      The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma.
      • Park J.-Y.
      • Kim D.-Y.
      • Kim J.-H.
      • Kim Y.-M.
      • Kim Y.-T.
      • Nam J.-H.
      The impact of tumor morcellation during surgery on the outcomes of patients with apparently early low-grade endometrial stromal sarcoma of the uterus.
      Parasitic myomas are defined as leiomyomas that are not attached to the uterus and are “parasitic” because they receive their blood supply from surrounding organs.
      • Leren V.
      • Langebrekke A.
      • Qvigstad E.
      Parasitic leiomyomas after laparoscopic surgery with morcellation.
      They have a reported incidence of 0.12-0.9% after laparoscopic surgery with power morcellation.
      • Leren V.
      • Langebrekke A.
      • Qvigstad E.
      Parasitic leiomyomas after laparoscopic surgery with morcellation.
      • Nezhat C.
      • Kho K.
      Iatrogenic myomas: new class of myomas?.
      • Donnez O.
      • Squifflet J.
      • Leconte I.
      • Jadoul P.
      • Donnez J.
      Posthysterectomy pelvic adenomyotic masses observed in 8 cases out of a series of 1405 laparoscopic subtotal hysterectomies.
      • Cucinella G.
      • Granese R.
      • Calagna G.
      • Somigliana E.
      • Perino A.
      Parasitic myomas after laparoscopic surgery: an emerging complication in the use of morcellator? Description of four cases.
      The objectives of this study were (1) to describe the rates of spindle cell neoplasm formation after power morcellation and (2) to identify risk factors for formation of either uterine sarcoma or parasitic myomas at the time of laparoscopic hysterectomy with power morcellation.

      Materials and Methods

      This was an institutional review board–approved, retrospective study of women who underwent laparoscopic hysterectomy at Kaiser Permanente San Diego from 2001-2012.
      Patient charts were reviewed after cases were identified with the use of surgical case logs. Demographic and clinical characteristics, surgical techniques, pathology reports, and perioperative complications were abstracted by physician reviewers and individually entered into an Access Database (Microsoft Access 2007; Microsoft Inc, Seattle, WA). Baseline characteristics were collected: age, gravidity, parity, ethnicity, body mass index, presence of diabetes mellitus, hypertension, collagen vascular disease, use of tobacco, alcohol, or drugs, presence of sexual activity, menopausal status, use of hormones, use of leuprolide or the progestin intrauterine device, number of vaginal deliveries, and history of pelvic surgery or endometrial ablation. Pathology reports were carefully reviewed and coded for the presence of fibroid tumors, endometriosis, adenomyosis, endometrial hyperplasia, cervical dysplasia, or malignancy. Operative techniques, removal of the ovaries, uterine specimen weight, estimated blood loss, and complications were also abstracted.
      Total laparoscopic hysterectomy was defined as removal of the uterus and cervix. If the uterine body was too large to fit through the vagina, it was often morcellated laparoscopically to facilitate retrieval. Laparoscopic supracervical hysterectomy was defined as removal of the uterus above the level of the cervix followed by laparoscopic morcellation to remove the uterine body. In this study, bags were not used to contain morcellated contents.
      To address our primary objective, we evaluated patients who underwent power morcellation and identified those diagnosed with either uterine sarcoma or parasitic myomas. Fisher exact test and Mann Whitney U test were used to conduct univariate analyses to identify potential risk factors for parasitic myomas and for uterine sarcoma. The 28 baseline characteristics listed previously were analyzed as potential risk factors. Multivariable logistic regression was used to assess the independent risk factors. Variables were included if they had a probability value of < .10 on univariate analysis or if the variable was determined to be an important biologic risk factor. Odds ratios (ORs) and 95% confidence intervals (CIs) were reported. A probability value of < .05 was considered statistically significant. Statistical analysis was performed with SPSS software (version 18.0, SPSS Inc, Chicago, IL).

      Results

      A total of 3523 women underwent laparoscopic hysterectomy. Of these, 941 women underwent power morcellation. Of those who had power morcellation, 10 women were subsequently diagnosed with uterine sarcoma or parasitic myomas, for an overall incidence of 1.1% (10/941 women).

      Uterine sarcoma

      Of the 10 women who received a diagnosis of spindle cell neoplasms, 6 tumors (0.6%) were uterine sarcomas. Demographic characteristics are shown in Table 1. Three of the 6 uterine sarcomas were endometrial stromal sarcomas, and 3 were leiomyosarcomas (2 low-grade and 1 high-grade; Table 2). Only 3 of the 6 patients received a diagnosis of uterine sarcoma on pathologic evaluation at the time of hysterectomy with morcellation. These 3 patients underwent subsequent exploratory laparotomy, trachelectomy, and bilateral salpingo-oophorectomy (if not performed at time of hysterectomy). One patient required resection of metastatic implants, omentectomy, appendectomy, and adjuvant therapy with the use of Megace (Table 3; patients #1-3). The other 3 patients were examined from 2-7 years after hysterectomy with ≥1 pelvic masses; pathologic evaluation of these recurrent masses revealed uterine sarcoma (patients #4-6). There were no significant associations among any of the potential risk factors and uterine sarcoma.
      Table 1Demographic characteristics of subjects with uterine sarcoma who underwent morcellation
      VariableUterine sarcomaP value
      No (n = 935)Yes (n = 6)
      Mean age, y
      Data are given as mean ± standard deviation
      46 ± 644 ± 5.65
      Mann Whitney U test
      Body mass index, kg/m2
      Data are given as mean ± standard deviation
      29 ± 630 ± 12.73
      Mann Whitney U test
       <25 kg/m2, n (%)222 (26)3 (50).18
      Fisher exact test
       ≥25 kg/m2, n (%)642 (74)3 (50)
      Ethnicity, n (%).61
      Fisher exact test
       White530 (57)4 (67)
       Hispanic200 (21)2 (33)
       African American129 (14)0
       Asian/other/unknown76 (8)0
      Smoking (current), n (%)95 (11)0.40
      Fisher exact test
      Diabetes mellitus, n (%)49 (5)0.56
      Fisher exact test
      Hypertension, n (%)224 (24)1 (17).67
      Fisher exact test
      Menopausal, n (%)73 (8)1 (17).43
      Fisher exact test
      Hormones (at time of history and physical), n (%)215 (26)2 (33).23
      Fisher exact test
      Use of leuprolide, n (%)327 (39)2 (33).66
      Fisher exact test
      Use of progestin intrauterine device, n (%)18 (2)0.76
      Fisher exact test
      Type of laparoscopic hysterectomy performed, n (%).54
      Fisher exact test
       Total laparoscopic hysterectomy262 (28)1 (17)
       Supracervical laparoscopic hysterectomy673 (72)5 (83)
      One or both ovaries left intact, n (%)608 (65)3 (50).37
      Fisher exact test
      Uterine weight, g
      Data are given as mean ± standard deviation
      333 ± 261458 ± 248.25
      Mann Whitney U test
       >350 g, n (%)262 (28)3 (50).36
      Fisher exact test
      Fibroid tumors (pathologic specimen), n (%)802 (86)5 (83)
      All 6 patients who were diagnosed with uterine sarcoma had apparent fibroid tumors before surgery. Five patients had fibroid tumors noted on pathologic specimen from initial surgery (represented in this variable); 1 patient had only sarcoma without mention of fibroid tumors on specimen.
      .87
      Fisher exact test
      Adenomyosis (pathologic specimen), n (%)240 (26)1 (17).61
      Fisher exact test
      Endometriosis (pathologic specimen), n (%)64 (7)0.51
      Fisher exact test
      Not all variables are shown; none of the variables were significant.
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.
      a Data are given as mean ± standard deviation
      b Mann Whitney U test
      c Fisher exact test
      d All 6 patients who were diagnosed with uterine sarcoma had apparent fibroid tumors before surgery. Five patients had fibroid tumors noted on pathologic specimen from initial surgery (represented in this variable); 1 patient had only sarcoma without mention of fibroid tumors on specimen.
      Table 2Details of procedures of the 6 patients who were diagnosed with uterine sarcoma after power morcellation
      PatientAge, yMenopausal at time of hysterectomyIndication for hysterectomyPreoperative endometrial biopsyPreoperative ultrasound scanProcedureUterine weight, gDisease at initial procedure
      147NoFibroid tumors, menorrhagiaBenignEnlarged uterus (20 × 10 × 9 cm), fundal fibroid tumor (8 × 9 × 10 cm)Laparoscopic supracervical hysterectomy, bilateral salpingo-oophorectomy720Low-grade endometrial stromal sarcoma
      241NoFibroid tumors, menorrhagiaBenignFibroid uterus, abnormal heterogeneity of the endometriumLaparoscopic supracervical hysterectomy218Low-grade endometrial stromal sarcoma
      351YesFibroid tumors, postmenopausal bleedingNone: frozen section curettage done at time of procedure (benign)Enlarged uterus (14 × 5 × 7 cm), 2 fibroid tumors (3 × 4 × 4 cm) and (5 × 5 × 4 cm)Laparoscopic supracervical hysterectomy, bilateral salpingo-oophorectomy285Leiomyosarcoma, grade II-III
      445NoFibroid tumors, menorrhagia, abdominal discomfortBenignNoneTotal laparoscopic hysterectomy with uterine morcellation, left salpingo-oophorectomy787Cellular leiomyoma, usual type leiomyoma

      (review of disease: endometrial stromal sarcoma)
      541NoFibroid tumors, pelvic panNoneNoneLaparoscopic supracervical hysterectomy486Pieces of leiomyoma
      648NoFibroid tumors, menorrhagiaBenignSlightly enlarged uterus (10 × 7 × 8 cm), 6 cm posterior fibroid tumorLaparoscopic supracervical hysterectomy, bilateral salpingo-oophorectomy250Pieces of leiomyoma, adenomyosis
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.
      Table 3Survival status of the 6 patients who were diagnosed with uterine sarcoma after power morcellation
      PatientSarcoma diagnosed at initial procedureTime to second evaluationSymptomsRestagingTumor typeAdjuvant treatmentFollow up, moSurvival status
      1YesN/AN/AYes: exploratory laparotomy, trachelectomy, resection of metastatic implants, omentectomy, appendectomyLow-grade endometrial stromal sarcomaMegace135Alive; no disease
      2YesN/AN/AYes: exploratory laparotomy, trachelectomy, bilateral salpingo-oophorectomy; no evidence of diseaseLow-grade endometrial stromal sarcomaNone48Alive; no disease
      3YesN/AN/AYes: exploratory laparotomy, trachelectomy; no evidence of diseaseLeiomyosarcoma, grade II-IIINone31Alive; no disease
      4No23 moPelvic painYes: exploratory laparotomy, bilateral salpingo-oophorectomy, resection of pelvic masses, omentectomy; bowel resection and anastomosisLow-grade endometrial stromal sarcomaMegace75Alive; no disease
      5No7 yPelvic pressureYes: exploratory laparotomy, resection of abdominopelvic mass, bilateral salpingo-oophorectomyLow-grade leiomyosarcomaNone51Alive; no disease
      6No6 yAbdominal painYes: exploratory laparotomy, resection of pelvic masses, appendectomyHigh-grade leiomyosarcomaChemotherapy, radiation, additional excision of recurrent masses36Died of disease
      N/A, not applicable.
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.

      Uterine sarcoma with initially benign pathologic evidence

      Three of the women in the uterine sarcoma group had benign leiomyoma on initial pathologic evaluation and then had a delayed presentation of ≥1 abdominal or pelvic masses that subsequently were found to be uterine sarcoma. Incidence of this presentation was 0.3% (3/941 women). The median age of these patients at the time of initial procedure was 45 years, and the median uterine weight at the time of morcellation was 486 g. The median amount of time to second evaluation was 6 years. All patients were imaged with a computed tomography scan, which revealed single or multiple pelvic masses, the largest of which was 15 × 16 cm (Figure 1). All patients underwent exploratory laparotomy and resection of masses. On final pathologic evaluation, 1 patient was diagnosed with endometrial stromal sarcoma, and 2 patients were diagnosed with leiomyosarcoma (1 low grade; 1 high grade.) Associated risk factors were not found to be significant.
      Figure thumbnail gr1
      Figure 1A 15 × 16 cm recurrent uterine sarcoma with initially benign fibroid tumors on pathologic examination
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.
      Two of these 3 patients had their original pathologic specimens reviewed at the time of the second evaluation. It was determined on re-review that patient #4 who was originally reported to have a cellular leiomyoma on her morcellated specimen actually had a low-grade endometrial stromal sarcoma at the time of initial surgery. This report was officially amended. Patient #5 did not have an amended pathology report, and the tissue specimen was no longer available for review at the time of this study. It was unclear from the records whether that pathology report was reviewed officially and left unchanged or never reviewed. Patient #6 (high-grade leiomyosarcoma, 6 years after initial surgery) had her disease reviewed, and high-grade leiomyosarcoma was not found on the available tissue specimen of her original morcellated uterus.
      At the time of the study conclusion, 5 of the 6 patients who had morcellation of uterine sarcoma were living without evidence of recurrent disease, with a minimum of 31 months of follow up. The patient with high-grade leiomyosarcoma had died of the disease 3 years after diagnosis (patient #6).

      Uterine sarcoma in patients who did not undergo morcellation

      Our primary objective was to describe the incidence of uterine sarcomas and parasitic myomas at the time of power morcellation. However, we thought it would be interesting to also report the incidence of sarcoma in the patients who did not undergo morcellation in our laparoscopic hysterectomy population. During the same study period, a total of 2582 women underwent laparoscopic hysterectomy but did not have power morcellation. All women underwent total hysterectomy at a mean age of 46 ± 8 years and uterine weight 189 ± 141 g. Of these, 5 women received a diagnosis of uterine sarcoma (0.19%; 5/2582 women). Two women received a diagnosis of low-grade endometrial stromal sarcoma, 1 with carcinosarcoma and 2 with leiomyosarcoma (1 high-grade, 1 grade not specified). In addition, 2 patients received a diagnosis of smooth muscle tumor of uncertain malignant potential. At the time of study conclusion, 4 of the 5 patients with a diagnosis of sarcoma and the 2 patients with smooth muscle tumor of uncertain malignant potential were alive without evidence of disease at a minimum of 37 months of follow up. The patient with high-grade leiomyosarcoma died of the disease 2 years after diagnosis. The details of the clinical courses of these patients can be found in Table 4.
      Table 4Clinical characteristics of patients who were diagnosed with uterine sarcoma and smooth muscle tumor of uncertain malignant potential and who did not undergo power morcellation
      PatientAgeMenopausal at time of hysterectomyIndicationPreoperative endometrial biopsyPreoperative ultrasound scanProcedureUterine weight, gTumor typeAdjuvant treatmentFollow up, moSurvival
      181YesEndometrial biopsy with adenosarcomaAdenosarcomaNoneTotal laparoscopic hysterectomy, bilateral salpingo-oophorectomy109AdenosarcomaNone37Alive; no disease
      249NoFibroid tumors, pelvic painBenignEnlarged uterus (15 × 4 × 7 cm), left posterior fibroid tumor (3 × 3 × 4 cm)Total laparoscopic hysterectomy, right salpingo-oophorectomy154Low-grade endometrial stromal sarcomaNone65Alive; no disease
      349NoEnlarged uterus, abnormal uterine bleedingBenignEnlarged uterus (11 × 8 × 7 cm)Total laparoscopic hysterectomy, bilateral salpingo-oophorectomyUnknownLow-grade endometrial stromal sarcomaNone40Alive; no disease
      466YesPostmenopausal bleedingBenign

      (1 y previously)
      Fundal fibroid tumor (7 × 7 × 7 cm)Total laparoscopic hysterectomy, bilateral salpingo-oophorectomy383Leiomyosarcoma (grade not specified)None37Alive; no disease
      554YesFibroid uterus, postmenopausal bleedingBenignEnlarged uterus (14 × 8 × 8 cm), multiple fibroid tumors, largest 5.2 cmTotal laparoscopic hysterectomy, bilateral salpingo-oophorectomy268High-grade leiomyosarcomaMultiple rounds and agents of chemotherapy23Died of disease
      644NoFibroid tumors, ovarian mass, cervical dysplasiaBenignMultiple fibroid tumors, largest (5 × 5 × 3 cm)Total laparoscopic hysterectomy, bilateral salpingo-oophorectomy184Smooth muscle tumor of uncertain malignant potentialNone52Alive; no disease
      733NoSmooth muscle tumor of uncertain malignant potential on endometrial biopsyLeiomyoma vs stromal lesion, favor smooth muscle tumor of uncertain malignant potentialLower uterine fibroid tumor (4 × 5 × 4 cm)Laparoscopic assisted vaginal hysterectomy96Smooth muscle tumor of uncertain malignant potentialNone46Alive; no disease
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.

      Parasitic myomas

      The remaining 4 of 10 women diagnosed with spindle cell neoplasms were found to have parasitic myomas (0.4%; 4/941 women). The demographic characteristics of these patients are shown in Table 5. All women with parasitic myomas received the diagnosis many years after their laparoscopic hysterectomy; the median amount of time to evaluation was 5 years. The most common symptom was a self-palpated mass, followed by abdominal pain. One patient was asymptomatic, and the recurrent myomas were noted at the time of surgery for pelvic organ prolapse repair. All of the patients who had symptoms underwent computed tomography scanning, which showed single or multiple pelvic masses, the largest of which was 18 × 18 cm (Figure 2). All patients underwent subsequent reoperation with resection of pelvic masses; 2 of the women had laparoscopy, and 2 women underwent exploratory laparotomy. Final pathologic evidence for all of these patients showed benign leiomyoma, and all patients were living without evidence of recurrence at the time of the study conclusion.
      Table 5Demographic characteristics of subjects with parasitic myomas after morcellation
      VariableParasitic myomasP value
      No (n = 937)Yes (n = 4)
      Age, y
      Data are given as mean ± standard deviation
      45.5 ± 6.236.5 ± 4< .01
      Significant probability values ≤ .05
      Mann Whitney U test
       <40 y, n (%)109 (12)3 (75)< .01
      Significant probability values ≤ .05
      Fisher exact test
      Variables included in the multivariate regression model based on probability value of < .1 or biological plausibility.
      Body mass index, kg/m2
      Data are given as mean ± standard deviation
      29.1 ± 6.427.5 ± 4.9.62
      Data are given as mean ± standard deviation
      Ethnicity, n (%).49
      Fisher exact test
       White532 (57)2 (50)
       Hispanic200 (21)2 (50)
       African American129 (14)0
       Asian/other/unknown76 (8)0
      Smoking (current), n (%)95 (10)0.50
      Fisher exact test
      Diabetes mellitus, n (%)49 (5)0.64
      Fisher exact test
      Hypertension, n (%)224 (24)1 (25).97
      Fisher exact test
      Menopausal, n (%)75 (8)0.55
      Fisher exact test
      Hormones (at time of history and physical), n (%)217 (26)0.23
      Fisher exact test
      Use of leuprolide, n (%)327 (39)2 (50).66
      Fisher exact test
      Use of progestin intrauterine device, n (%)18 (2)0.76
      Fisher exact test
      Type of laparoscopic hysterectomy performed, n (%).21
      Fisher exact test
       Total laparoscopic hysterectomy263 (28)0
       Supracervical laparoscopic hysterectomy674 (72)4 (100)
      One or both ovaries left intact, n (%)607 (65)4 (100).14
      Fisher exact test
      Uterine weight, g
      Data are given as mean ± standard deviation
      334 (261)383 (394).71
      Mann Whitney U test
       >350 g, n (%)314 (38)3 (75).12
      Fisher exact test
      Variables included in the multivariate regression model based on probability value of < .1 or biological plausibility.
      Fibroid tumors (pathologic specimen), n (%)803 (86)4 (100).41
      Fisher exact test
      Adenomyosis (pathologic specimen), n (%)241 (26)0.24
      Fisher exact test
      Endometriosis (pathologic specimen), n (%)64 (7)0.59
      Significant probability values ≤ .05
      Not all variables are shown.
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.
      a Data are given as mean ± standard deviation
      b Significant probability values ≤ .05
      c Mann Whitney U test
      d Fisher exact test
      e Variables included in the multivariate regression model based on probability value of < .1 or biological plausibility.
      Figure thumbnail gr2
      Figure 2An 18 × 18 cm parasitic myoma years after power morcellation
      Tan-Kim. Uterine sarcomas, parasitic myomas, and power morcellation. Am J Obstet Gynecol 2015.
      On multivariate analysis, age <40 years was found to be a significant risk factor (OR, 26; 95% CI, 2.7–261.9; P = .005) for the development of parasitic myomas. There was a trending association between uterine weight >350 g and parasitic myomas; however, this approached but did not meet statistical significance (OR, 7.0; 95% CI, 0.7–69.4; P = .098).

      Comment

      Our study represents one of the largest series of laparoscopic hysterectomies performed in a large health maintenance organization (HMO) setting with long-term follow up. With regards to uterine sarcoma, the number of cases was too small to show an association with the potential risk factors. It should be noted that all 6 of the patients with sarcoma were thought to have fibroid uteri during their preoperative evaluations. Five of the patients with uterine sarcoma had fibroid tumors noted on their initial pathologic specimen with or without sarcoma. Only 1 patient had sarcoma without mention of fibroid tumors. We also found age <40 years to be associated with a higher risk for the development of parasitic myomas after laparoscopic hysterectomy with power morcellation.
      The incidence of uterine sarcoma in patients who have undergone hysterectomy for presumed benign fibroid tumors has been investigated recently by several national organizations that include the FDA and the American Congress of Obstetrics and Gynecology (ACOG). The FDA published a total incidence of uterine sarcoma of 0.28% (1/352 cases) and an incidence of leiomyosarcoma of 0.20% (1/498 cases) based on 9 studies of women who underwent hysterectomy or myomectomy for presumed benign leiomyoma.
      Press Announcement
      FDA discourages use of laparoscopic power morcellation for removal of uterus or uterine fibroids.
      ACOG published an estimated incidence of uterine sarcoma of 0.2% (2/1000 cases), based on a review and analysis of the available scientific evidence on power morcellation and occult malignancy in gynecologic surgery.

      American College of Obstetricians and Gynecologists. Power morcellation and occult malignancy in gynecologic surgery: a special report [Internet]. [cited 2014 May 26]. Available at: http://www.acog.org/Resources_And_Publications/Task_Force_and_Work_Group_Reports/Power_Morcellation_and_Occult_Malignancy_in_Gynecologic_Surgery. Accessed Dec. 1, 2014.

      Neither of these data analyses was able to include only cases in which power morcellation was performed. Our study describes the incidence of uterine sarcoma with power morcellation to be 0.6% with 95% confidence intervals 0.3–1.4%. In order to understand the percentage risk, we must first closely evaluate the denominator of this study compared to other studies. This study is the first to evaluate a subgroup of patients who all underwent power morcellation. This risk does not apply to all women or all women who had hysterectomies. Power morcellation is a technique used to remove uteri laparoscopically that would otherwise not be able to be removed via a smaller incision. In many cases, these are enlarged fibroid uteri. Not surprisingly, this primary subgroup analyzed in our study of subjects who underwent power morcellation had a median uterine weight which was 2-3 times higher than the other hysterectomy specimens that did not require morcellation. This subgroup can be considered a “higher risk” group because these larger uteri would be more at risk for harboring sarcoma. Additionally, this higher apparent incidence may also be explained by the inclusions of 3 patients who had a delayed evaluation of uterine sarcoma when initial disease was benign and whose disease was discovered because of the captive nature of the Kaiser Healthcare System. These 3 patients were evaluated and treated at the same institution, despite a median of 6 years until second evaluation.
      When we evaluate the entire laparoscopic hysterectomy cohort, the incidence of occult uterine sarcoma is similar to previous reports (11/3523, 0.3%). In our study, there were no cases of morcellated endometrial or cervical cancer. In the Kaiser system, patients are monitored closely for preventative maintenance and are likely to be up-to-date on screening tests such as Papanicolaou smears or have been evaluated previously for symptoms such as irregular bleeding.
      One major disadvantage to power morcellation is the loss of the gross appearance of the specimen. Generally, pathologic specimens are examined grossly, and the most suspicious areas are investigated microscopically. Morcellation increases the possibility of missing the most suspicious areas for microscopic evaluation. In one case (patient #4), the initial pathology report of cellular leiomyoma was later confirmed to be the same tissue type as the endometrial stromal sarcoma that was resected at the time of second evaluation. Morcellation results in distortion of normal tissue that makes diagnosis more difficult and increases the possibility of dissemination of cellular material (benign or malignant) throughout the peritoneal cavity. It is not known whether the 2 patients (patients #5 and #6) who were diagnosed with disseminated leiomyosarcoma years after their initial disease was benign had uterine sarcoma in the original specimen that was missed or had malignant transformation of disseminated leiomyoma. It is our opinion that pathologists should be alerted to the possibility of missing a uterine sarcoma in a morcellated specimen, especially that of a large uterus.
      It has been suggested that supracervical hysterectomy leads to decreased operative complications, decreased sexual dysfunction, and urinary issues compared with total hysterectomy, but these advantages have not been confirmed.
      • Learman L.A.
      • Summitt R.L.
      • Varner R.E.
      • et al.
      A randomized comparison of total or supracervical hysterectomy: surgical complications and clinical outcomes.
      • Thakar R.
      • Ayers S.
      • Clarkson P.
      • Stanton S.
      • Manyonda I.
      Outcomes after total versus subtotal abdominal hysterectomy.
      • Gimbel H.
      • Zobbe V.
      • Andersen B.M.
      • Filtenborg T.
      • Gluud C.
      • Tabor A.
      Randomised controlled trial of total compared with subtotal hysterectomy with one-year follow up results.
      • Kuppermann M.
      • Summitt R.L.
      • Varner R.E.
      • et al.
      Sexual functioning after total compared with supracervical hysterectomy: a randomized trial.
      In female pelvic reconstructive surgery, supracervical hysterectomy has been associated with lower vaginal cuff mesh erosion rates than total hysterectomy during minimally invasive laparoscopic sacrocolpopexy (5% vs 23%).
      • Tan-Kim J.
      • Menefee S.A.
      • Luber K.M.
      • Nager C.W.
      • Lukacz E.S.
      Prevalence and risk factors for mesh erosion after laparoscopic-assisted sacrocolpopexy.
      • Osmundsen B.C.
      • Clark A.
      • Goldsmith C.
      • et al.
      Mesh erosion in robotic sacrocolpopexy.
      When performed at the time of a sacrocolpopexy, the indication for hysterectomy is usually prolapse, not an enlarged fibroid uterus. In this specialized group, the risks of mesh complications need to be weighed against the risks of power morcellation.
      In December of 2013, a high-profile case in the Boston area, in which a patient experienced disseminated uterine sarcoma after morcellation of an apparent fibroid uterus, was reported in the national media,

      Brody JE. A surgical procedure’s risks, unmentioned–NYTimes.com [Internet]. 2014 [cited 2014 May 26]. Available at: http://well.blogs.nytimes.com/2014/03/17/a-surgical-procedures-risks-unmentioned/?_php=true&_type=blogs&_r=0. Accessed Dec. 1, 2014.

      which called the morcellation procedure into question. Subsequently, on April 17, 2014, the United States FDA issued a communication that discouraged the use of morcellation at the time of hysterectomy for uterine fibroid tumors, because of the possibility of an undiagnosed uterine sarcoma.
      Press Announcement
      FDA discourages use of laparoscopic power morcellation for removal of uterus or uterine fibroids.
      The FDA’s statement caused considerable concern in the gynecologic surgery community in light of the low incidence of uterine sarcoma and the recognized benefits of minimally invasive surgery, which sometimes requires morcellation for patients with large uterine fibroid tumors. In response, ACOG published a special report in May 2014 entitled “Power Morcellation and Occult Malignancy in Gynecologic Surgery” that reviewed the available literature and emphasized patient counseling and informed consent and the development of technology and training to reduce the risk of disseminated tissue.

      American College of Obstetricians and Gynecologists. Power morcellation and occult malignancy in gynecologic surgery: a special report [Internet]. [cited 2014 May 26]. Available at: http://www.acog.org/Resources_And_Publications/Task_Force_and_Work_Group_Reports/Power_Morcellation_and_Occult_Malignancy_in_Gynecologic_Surgery. Accessed Dec. 1, 2014.

      In December 2013, the Society of Gynecologic Oncology published a position statement on power morcellation that did not discourage the use of morcellation in all cases but that recommended communication with patients regarding risks, benefits, and alternatives.

      SGO Position Statement: morcellation [Internet]. 2014 [cited 2014 May 26]. Available at: https://www.sgo.org/newsroom/position-statements-2/morcellation/. Accessed Dec. 1, 2014.

      Indeed, the incidence of uterine sarcoma is rare, and leiomyosarcoma accounts for only 30% of all uterine sarcomas.
      • Park J.-Y.
      • Park S.-K.
      • Kim D.-Y.
      • et al.
      The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma.
      In 2009, Park et al
      • Park J.-Y.
      • Park S.-K.
      • Kim D.-Y.
      • et al.
      The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma.
      • Park J.-Y.
      • Kim D.-Y.
      • Kim J.-H.
      • Kim Y.-M.
      • Kim Y.-T.
      • Nam J.-H.
      The impact of tumor morcellation during surgery on the outcomes of patients with apparently early low-grade endometrial stromal sarcoma of the uterus.
      found that tumor morcellation was associated with higher abdominopelvic recurrence and decreased disease-free survival for both leiomyosarcoma and endometrial stromal sarcoma but only with decreased survival for leiomyosarcoma. In our study, there were 6 patients who underwent morcellation and who were subsequently diagnosed with uterine sarcoma, either immediately or several years later. Five of these 6 patients remained disease-free at a minimum of 31 months of follow up, and only the patient with high-grade leiomyosarcoma died of the disease (3 years after diagnosis). High-grade leiomyosarcoma has a very poor prognosis, even when specimens are removed intact, with a recurrence rate of at least 50% even in disease that is limited to the uterus at the time of diagnosis.
      • Reed N.S.
      • Mangioni C.
      • Malmström H.
      • et al.
      Phase III randomised study to evaluate the role of adjuvant pelvic radiotherapy in the treatment of uterine sarcomas stages I and II: an European Organisation for Research and Treatment of Cancer Gynaecological Cancer Group Study (protocol 55874).
      It is unknown whether the ultimate fate of this patient was altered by the use of power morcellation. In the 2582 patients in this database who did not undergo morcellation, one patient was also diagnosed with high-grade uterine leiomyosarcoma. This patient’s uterus was removed intact, and she also died of the disease 2 years after diagnosis. Only 3 of the 9 studies in the FDA’s recent analysis included uterine sarcomas that were morcellated, and only 2 studies specified the number of morcellated sarcomas compared with the total number of patients.
      • Seidman M.A.
      • Oduyebo T.
      • Muto M.G.
      • Crum C.P.
      • Nucci M.R.
      • Quade B.J.
      Peritoneal dissemination complicating morcellation of uterine mesenchymal neoplasms.
      • Sinha R.
      • Hegde A.
      • Mahajan C.
      • Dubey N.
      • Sundaram M.
      Laparoscopic myomectomy: do size, number, and location of the myomas form limiting factors for laparoscopic myomectomy?.
      • Leung F.
      • Terzibachian J.-J.
      Re: “The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma.”.
      In these 2 studies, there were 5 uterine sarcomas (3 of which were leiomyosarcoma) of 1596 patients total. At the time of the publication of those studies, all 5 of those patients who had morcellation of a uterine sarcoma were alive with no apparent evidence of disease.
      • Seidman M.A.
      • Oduyebo T.
      • Muto M.G.
      • Crum C.P.
      • Nucci M.R.
      • Quade B.J.
      Peritoneal dissemination complicating morcellation of uterine mesenchymal neoplasms.
      • Sinha R.
      • Hegde A.
      • Mahajan C.
      • Dubey N.
      • Sundaram M.
      Laparoscopic myomectomy: do size, number, and location of the myomas form limiting factors for laparoscopic myomectomy?.
      The incidence of parasitic myomas currently reported ranges from 0.12–0.9%, with a lower incidence being shown when the dataset includes a higher number of patients.
      • Leren V.
      • Langebrekke A.
      • Qvigstad E.
      Parasitic leiomyomas after laparoscopic surgery with morcellation.
      • Nezhat C.
      • Kho K.
      Iatrogenic myomas: new class of myomas?.
      • Donnez O.
      • Squifflet J.
      • Leconte I.
      • Jadoul P.
      • Donnez J.
      Posthysterectomy pelvic adenomyotic masses observed in 8 cases out of a series of 1405 laparoscopic subtotal hysterectomies.
      • Cucinella G.
      • Granese R.
      • Calagna G.
      • Somigliana E.
      • Perino A.
      Parasitic myomas after laparoscopic surgery: an emerging complication in the use of morcellator? Description of four cases.
      In our study, we report the incidence of parasitic leiomyomas to be 0.4% of 941 patients. Although their prognosis is very good, reoperation for diagnosis and treatment represents a significant morbidity. Data on these patients was also presented so that it is noted that recurrent masses after laparoscopic hysterectomy with morcellation may be benign.
      The strengths of this study include the analysis of a large cohort of patients over an 11-year period who underwent laparoscopic morcellation within a mature laparoscopic program at a large HMO. Our study population consisted of patients within a captive HMO that limits the bias introduced by loss to follow up.
      The primary limitation is the very small number of uterine sarcomas and parasitic myomas, which limits the strength of the conclusions that can be drawn from this study. Associations between the disease and potential risk factors did not reach statistical significance. Also, this study does not include patients who underwent vaginal morcellation, who underwent morcellation through a minilaparotomy incision without a power morcellator, or who had laparoscopic myomectomy. Finally, the incidence of these conditions may actually be higher than what is reported in this study because of lead time.
      This study contributes to the growing literature regarding this relatively rare and unpredictable disease process. When a patient is to undergo a minimally invasive procedure with possible power morcellation, the patient should be counseled about the possible consequences of morcellation of an undiagnosed malignancy. The patient should be offered alternatives such as a minilaparotomy for removal of an intact specimen or an open procedure. Given the well-known advantages of laparoscopic surgery compared with open procedures and the rarity of uterine sarcomas, we do not believe that the risk of morcellation of occult malignancy is sufficient to abandon power morcellation completely.

      References

        • Warren L.
        • Ladapo J.A.
        • Borah B.J.
        • Gunnarsson C.L.
        Open abdominal versus laparoscopic and vaginal hysterectomy: analysis of a large United States payer measuring quality and cost of care.
        J Minim Invasive Gynecol. 2009; 16: 581-588
      1. Center for Disease Control National Center for Health Statistics, National Hospital Discharge Summary 2010 [Internet]. 2010 [cited 2014 May 26]. Available at: http://www.cdc.gov/nchs/data/nhds/4procedures/2010pro4_numberrate.pdf. Accessed Aug. 1, 2014.

        • Walsh C.A.
        • Walsh S.R.
        • Tang T.Y.
        • Slack M.
        Total abdominal hysterectomy versus total laparoscopic hysterectomy for benign disease: a meta-analysis.
        Eur J Obstet Gynecol Reprod Biol. 2009; 144: 3-7
        • Jacobson G.F.
        • Shaber R.E.
        • Armstrong M.A.
        • Hung Y.-Y.
        Hysterectomy rates for benign indications.
        Obstet Gynecol. 2006; 107: 1278-1283
        • Press Announcement
        FDA discourages use of laparoscopic power morcellation for removal of uterus or uterine fibroids.
        Center for Devices and Radiological Health, US Food and Drug Administration Center for Devices and Radiological Health; Silver Spring, MD2014
        • Seidman M.A.
        • Oduyebo T.
        • Muto M.G.
        • Crum C.P.
        • Nucci M.R.
        • Quade B.J.
        Peritoneal dissemination complicating morcellation of uterine mesenchymal neoplasms.
        PLoS One. 2012; 7: e50058
      2. American College of Obstetricians and Gynecologists. Power morcellation and occult malignancy in gynecologic surgery: a special report [Internet]. [cited 2014 May 26]. Available at: http://www.acog.org/Resources_And_Publications/Task_Force_and_Work_Group_Reports/Power_Morcellation_and_Occult_Malignancy_in_Gynecologic_Surgery. Accessed Dec. 1, 2014.

        • Harlow B.L.
        • Weiss N.S.
        • Lofton S.
        The epidemiology of sarcomas of the uterus.
        J Natl Cancer Inst. 1986; 76: 399-402
        • Kim W.Y.
        • Chang S.-J.
        • Chang K.-H.
        • et al.
        Uterine leiomyosarcoma: 14-year two-center experience of 31 cases.
        Cancer Res Treat. 2009; 41: 24-28
        • Park J.-Y.
        • Park S.-K.
        • Kim D.-Y.
        • et al.
        The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma.
        Gynecol Oncol. 2011; 122: 255-259
        • Park J.-Y.
        • Kim D.-Y.
        • Kim J.-H.
        • Kim Y.-M.
        • Kim Y.-T.
        • Nam J.-H.
        The impact of tumor morcellation during surgery on the outcomes of patients with apparently early low-grade endometrial stromal sarcoma of the uterus.
        Ann Surg Oncol. 2011; 18: 3453-3461
        • Leren V.
        • Langebrekke A.
        • Qvigstad E.
        Parasitic leiomyomas after laparoscopic surgery with morcellation.
        Acta Obstet Gynecol Scand. 2012; 91: 1233-1236
        • Nezhat C.
        • Kho K.
        Iatrogenic myomas: new class of myomas?.
        J Minim Invasive Gynecol. 2010; 17: 544-550
        • Donnez O.
        • Squifflet J.
        • Leconte I.
        • Jadoul P.
        • Donnez J.
        Posthysterectomy pelvic adenomyotic masses observed in 8 cases out of a series of 1405 laparoscopic subtotal hysterectomies.
        J Minim Invasive Gynecol. 2007; 14: 156-160
        • Cucinella G.
        • Granese R.
        • Calagna G.
        • Somigliana E.
        • Perino A.
        Parasitic myomas after laparoscopic surgery: an emerging complication in the use of morcellator? Description of four cases.
        Fertil Steril. 2011; 96: e90-e96
        • Learman L.A.
        • Summitt R.L.
        • Varner R.E.
        • et al.
        A randomized comparison of total or supracervical hysterectomy: surgical complications and clinical outcomes.
        Obstet Gynecol. 2003; 102: 453-462
        • Thakar R.
        • Ayers S.
        • Clarkson P.
        • Stanton S.
        • Manyonda I.
        Outcomes after total versus subtotal abdominal hysterectomy.
        N Engl J Med. 2002; 347: 1318-1325
        • Gimbel H.
        • Zobbe V.
        • Andersen B.M.
        • Filtenborg T.
        • Gluud C.
        • Tabor A.
        Randomised controlled trial of total compared with subtotal hysterectomy with one-year follow up results.
        BJOG. 2003; 110: 1088-1098
        • Kuppermann M.
        • Summitt R.L.
        • Varner R.E.
        • et al.
        Sexual functioning after total compared with supracervical hysterectomy: a randomized trial.
        Obstet Gynecol. 2005; 105: 1309-1318
        • Tan-Kim J.
        • Menefee S.A.
        • Luber K.M.
        • Nager C.W.
        • Lukacz E.S.
        Prevalence and risk factors for mesh erosion after laparoscopic-assisted sacrocolpopexy.
        Int Urogynecol J. 2011; 22: 205-212
        • Osmundsen B.C.
        • Clark A.
        • Goldsmith C.
        • et al.
        Mesh erosion in robotic sacrocolpopexy.
        Female Pelvic Med Reconstr Surg. 2012; 18: 86-88
      3. Brody JE. A surgical procedure’s risks, unmentioned–NYTimes.com [Internet]. 2014 [cited 2014 May 26]. Available at: http://well.blogs.nytimes.com/2014/03/17/a-surgical-procedures-risks-unmentioned/?_php=true&_type=blogs&_r=0. Accessed Dec. 1, 2014.

      4. SGO Position Statement: morcellation [Internet]. 2014 [cited 2014 May 26]. Available at: https://www.sgo.org/newsroom/position-statements-2/morcellation/. Accessed Dec. 1, 2014.

        • Reed N.S.
        • Mangioni C.
        • Malmström H.
        • et al.
        Phase III randomised study to evaluate the role of adjuvant pelvic radiotherapy in the treatment of uterine sarcomas stages I and II: an European Organisation for Research and Treatment of Cancer Gynaecological Cancer Group Study (protocol 55874).
        Eur J Cancer. 2008; 44: 808-818
        • Sinha R.
        • Hegde A.
        • Mahajan C.
        • Dubey N.
        • Sundaram M.
        Laparoscopic myomectomy: do size, number, and location of the myomas form limiting factors for laparoscopic myomectomy?.
        J Minim Invasive Gynecol. 2008; 15: 292-300
        • Leung F.
        • Terzibachian J.-J.
        Re: “The impact of tumor morcellation during surgery on the prognosis of patients with apparently early uterine leiomyosarcoma.”.
        Gynecol Oncol. 2012; 124: 172-173