Review Article

Electric Morcellation-related Reoperations After Laparoscopic Myomectomy and Nonmyomectomy Procedures Nigel Pereira, MD*, Tommy R. Buchanan, MD, Kayla M. Wishall, MD, Sarah H. Kim, BS, Irene Grias, DO, Scott D. Richard, MD, and Carl R. Della Badia, DO From the Department of Obstetrics and Gynecology (Drs. Pereira, Buchanan, Wishall, Richard, and Badia, and Ms. Kim), Division of Gynecologic Oncology (Dr. Richard), Division of Minimally Invasive Gynecologic Surgery (Dr. Badia), Drexel University College of Medicine, Philadelphia, Pennsylvania, and Division of General Gynecology, Penn Presbyterian Medical Center, Philadelphia, Pennsylvania (Dr. Grias).

ABSTRACT Study Objective: To identify, collate, and summarize the most common causes and pathologies of electric morcellationrelated reoperations after laparoscopic myomectomy and nonmyomectomy procedures. Design: A systematic review of published medical literature from January 1990 to February 2014 reporting morcellationrelated reoperations after laparoscopic myomectomy and nonmyomectomy procedures involving the use of intracorporeal electric tissue morcellators. Publications were included in this review if patients underwent a second surgical procedure because of the onset of new clinical symptoms after a primary surgical procedure that involved intracorporeal morcellation or if histopathology of the morcellated surgical specimen revealed malignancy (Canadian Task Force classification II-3). Setting: All case reports and case series were reported from community and academic hospitals in the United States and the rest of the world. Patients: We identified 66 patients from 32 publications. Interventions: Reoperation after laparoscopic myomectomy and nonmyomectomy procedures involving intracorporeal electric tissue morcellation. Measurements and Main Results: For patients who presented with new clinical symptoms requiring reoperation, we recorded the follow-up period, nature and duration of the new symptoms, details of the second surgical procedure, intraoperative findings during the second surgical procedure, and the final histopathologic diagnosis. When histopathology of the morcellated specimen revealed malignancy, we recorded the specific type of malignancy, the corresponding surgical treatment that the patient underwent, and the follow-up period. Percentages and 95% confidence intervals were calculated for all categoric variables. Twenty-four (36.4%) patients underwent laparoscopic myomectomies, of which 19 (79.2%) and 5 (20.8%) patients required a second surgical procedure because of new clinical symptoms and the diagnosis of malignancy in the morcellated surgical specimen, respectively. Forty-two (63.6%) patients underwent laparoscopic hysterectomies; of these, 25 (59.5%) patients required a second surgical procedure because of the onset of new clinical symptoms, whereas the remaining 17 (40.5%) patients underwent a second surgical procedure because of the diagnosis of malignancy in the morcellated surgical specimen. The most common benign pathology was parasitic leiomyomata (22 patients, 33.3%). The most common malignant pathology was leiomyosarcoma (16 patients, 24.2%). Conclusion: Dispersion of tissue fragments into the peritoneal cavity at the time of morcellation continues to be a concern. It was previously thought that morcellated tissue fragments are resorbed by the peritoneal cavity; however, there is some evidence highlighting the long-term sequelae related to the growth and propagation of these dispersed tissue fragments in the form of parasitic leiomyomata, iatrogenic endometriosis, and cancer progression. Yet, the majority of laparoscopic myomectomy and nonmyomectomy procedures involving the use of intracorporeal electric tissue morcellators are uncomplicated, and institutions having no women with endometriosis or cancer are very

Carl R. Della Badia is a research investigator for AbbVie. Presented at the AAGL 41st Global Congress of Minimally Invasive Gynecology, Las Vegas, NV, November 5-9, 2012. Corresponding author: Nigel Pereira, MD, Department of Obstetrics and Gynecology, 245 N 15th Street, MS 495, New College Building, 16th Floor, Philadelphia, PA 19102. 1553-4650/$ - see front matter Ó 2015 AAGL. All rights reserved. http://dx.doi.org/10.1016/j.jmig.2014.09.006

E-mail: [email protected] Submitted March 1, 2014. Accepted for publication September 6, 2014. Available at www.sciencedirect.com and www.jmig.org

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unlikely to report surgical outcomes of uneventful electric morcellation. Thus, prospective studies are still required to validate the role of electric intracorporeal tissue morcellation in the pathogenesis of parasitic leiomyomata, iatrogenic endometriosis, and cancer progression. Journal of Minimally Invasive Gynecology (2015) 22, 163–176 Ó 2015 AAGL. All rights reserved. Keywords:

DISCUSS

Complications; Hysterectomy; Laparoscopy; Morcellation; Myomectomy; Reoperation

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Gynecologic surgery has truly become minimally invasive because of the refinement of laparoscopic techniques and instrumentation. Large uteri or leiomyomata that were previously removed through laparotomy are now morcellated, facilitating removal through smaller incisions [1]. The first documented uterine morcellation procedure was performed in 1840 by Ammasut of France to deliver a leiomyomatous uterus through the vagina [2]. In 1899, William Pryor of New York described the systematic technique of transvaginal wedge morcellation of enlarged uteri [1]. After several variations of hand morcellation and the success of laparoscopic hysterectomies in the early 1990s, Steiner et al [3] developed a prototype electrical morecellator that could be used during laparoscopic surgery. This morcellator consisted of a 12-mm cylindrical sheath with a rotating blade at its intra-abdominal end and an electrical microengine at the other end. Cylindrical blocks of tissue were cut out of the original surgical specimen and removed from the peritoneal cavity through the instrument using grasping forceps [3]. Although modern morcellators are variations of Steiner et al’s original design consisting of a sheath, grasper, and cutting blade that produces cores of tissue that can be retrieved through smaller incisions, the most recent morcellator uses bipolar energy to cut tissue instead of a blade [2]. The newer and easier-to-use electric morcellators have contributed to the rise in number of hysterectomies and myomectomies performed via the laparoscopic approach; however, some morcellators have been associated with injury to the abdominal and pelvic organs at the time of morcellation [4–6]. A recent review by Milad and Milad [6] identified 55 morcellator-related injuries over the past 15 years. These injuries involved the bowel, bladder, kidney, ureters, and the diaphragm [6]. Eleven injuries involved more than 1 organ, and 6 deaths were directly attributed to morcellator-related injuries [6]. Another growing concern of morcellation involves dispersion of morcellated tissue fragments into the peritoneal cavity at the time of morcellation. There are several publications linking the pathogenesis of parasitic leiomyomata, iatrogenic endometriosis, and disseminated peritoneal leiomyomatosis (DPL) to morcellator-related surgical spillage and dispersion of tissue fragments in the peritoneal cavity [4,5,7–10]. More importantly, morcellation of surgical specimens containing occult malignancy can lead

to seeding of cancerous tissue in the abdominal and pelvic cavity, possibly leading to decreased cancer survival [7–10]. Although morcellation-related complications are becoming more frequently reported, systematic data summarizing the most common causes or pathologies of morcellationrelated reoperations during laparoscopic myomectomy and nonmyomectomy procedures remain scarce. The primary objective of this systematic review is to identify, collate, and summarize the most common causes and pathologies of morcellation-related reoperations after laparoscopic myomectomy (LM), laparoscopic supracervical hysterectomy (LSCH), and total laparoscopic hysterectomy (TLH) involving the use of electric intracorporeal tissue morcellation. Materials and Methods Inclusion Criteria We searched PubMed, Ovid, EMBASE, and Google Scholar for all English language peer-reviewed publications published from January 1990 to February 2014 with the search terms ‘‘uterine morcellation,’’ ‘‘complications,’’ ‘‘laparoscopy,’’ ‘‘myomectomy,’’ and ‘‘hysterectomy.’’ We also searched the US Food and Drug Administration’s Manufacturer and User Facility Device Experience database with search terms ‘‘morcellation,’’ ‘‘complications,’’ and ‘‘adverse events.’’ The authors independently reviewed the preliminary search results. Of the initial pool of publications, relevant studies reporting morcellation-related reoperations were identified and read by all authors. Studies were included in this systematic review if patients underwent a second surgical procedure for 1 of the following indications: (1) onset of new clinical symptoms after a primary LM, LSCH, or TLH during which intracorporeal tissue morcellation was performed or (2) histopathology of the intracorporeally morcellated surgical specimen revealed malignancy. When patients presented with new clinical symptoms, it was imperative for the authors to attribute these symptoms and any subsequent intraoperative findings to the use of a morcellator during the primary surgical procedure. Exclusion Criteria Studies in which hysterectomies and myomectomies were performed abdominally or vaginally were excluded

Pereira et al.

Electric Morcellation-related Reoperations

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Fig. 1 A flowchart showing the distribution of identified publications and patients.

from our systematic review. We also excluded studies in which manual, transvaginal, or hysteroscopic morcellators were used. Finally, we also eliminated reports in which there was incomplete patient information or reoperations because of reasons deemed unrelated to intracorporeal tissue morcellation. Measurements and Statistical Analyses Demographic data recorded included the patient’s age, initial clinical symptoms, original surgical procedure, and indication for surgery. When patients presented with new clinical symptoms necessitating a second surgical procedure, we recorded the follow-up period, nature and duration of the new symptoms, details of the second surgical procedure that the patient underwent, intraoperative findings during the second surgical procedure, and the final histopathologic diagnosis. Benign pathologies included the following: (1) parasitic leiomyomata defined as histologyconfirmed leiomyomata within the peritoneal cavity separate from the uterus with a blood supply distinct from the uterus [11], (2) iatrogenic endometriosis defined as histologyconfirmed abdominopelvic implants of endometrial glands [7], (3) adenomyosis defined as histology-confirmed abdominopelvic implants of endometrial and smooth muscle tissue within the same implant [12], and (4) DPL defined as histology-confirmed abdominopelvic peritoneal nodules of smooth muscle [8]. When histopathology of the morcellated specimen revealed occult malignancy, the specific type of malignancy, the corresponding surgical treatment if any, and the follow-up period were recorded. Percentages and corresponding 95% confidence intervals (CI) were calculated for all categoric variables. The Student’s t test and Fisher exact tests were performed when appropriate. Results A total of 165 publications were initially identified, and the authors reviewed all corresponding abstracts. Of these, 32 (19.4%) publications met inclusion criteria, from which 66 patients were identified (Fig. 1). These publications included 23 case reports (71.9%), 8 case series (25.0%), and 1 case-control study (3.1%). Patients identified through these publications varied in their ages (range, 24–60), parity,

ethnicity, and their initial diagnostic workup. Overall, 24 (36.4%) patients underwent LMs, and 42 (63.6%) patients underwent nonmyomectomy procedures (Fig. 1). Of the patients who underwent nonmyomectomy procedures, 34 (80.9%) patients underwent LSCHs, whereas the remaining 8 (19.1%) patients underwent TLHs (Fig. 1). Table 1 summarizes the clinical, surgical, and pathologic details as well as follow-up periods for all 24 patients who underwent reoperations after LMs involving electric intracorporeal tissue morcellation. Table 2 lists the initial clinical symptoms in all patients undergoing LMs. Of the 24 patients, 19 (79.2%) patients presented with new clinical symptoms requiring a second surgical procedure (Fig. 2A). The pathology identified during the second surgical procedure in these patients included: 15 cases of parasitic leiomyomata (78.9%; CI, 60.5%–97.2%) and 4 cases of DPL (21.05%; CI, 2.7%–39.4%) (Fig. 2B and Table 1). The follow-up period for these patients ranged from 3 months (patient 14) to 16 years (patient 15). The remaining 5 (20.8%) patients were found to have leiomyosarcoma in the intracorporeally morcellated surgical specimen (Fig. 2A and C). The time interval between the diagnosis of malignancy and reoperation was 63 days for patient 5, 15 days for patient 23, 36 days for patient 24, and unknown for patients 21 and 22. Only patient 24 died during a follow-up period of 37.5 months after the second surgical procedure. Table 3 summarizes the clinical, surgical, and pathologic details and follow-up periods for all 42 patients who underwent reoperations after laparoscopic nonmyomectomy procedures involving electric intracorporeal tissue morcellation. Table 4 lists the initial clinical symptoms in all patients undergoing LSCHs and TLHs. Twenty-five (59.5%) patients of the 42 patients who initially underwent laparoscopic nonmyomectomy procedures presented with new clinical symptoms necessitating a second surgical procedure (Fig. 3A). In these patients, the pathology identified during the second surgical procedure was as follows: 7 cases of parasitic leiomyomata (28%; CI, 10.4%–45.6%), 9 cases of adenomyosis (36%; CI, 17.2%–54.8%), 4 cases of iatrogenic endometriosis (16%; CI, 1.6%–30.7%), 2 cases of DPL (8%; CI, 22.6% to 18.6%), and 3 cases of mixed pathology (12%; CI, 20.74% to 24.7%) (Fig. 3B and Table 3). Seventeen (40.5%) patients who underwent

166

Table 1 Electric morcellator-related reoperations after laparoscopic myomectomy (n 5 24) Age (yr)/menopause (yes/no)/ presenting symptoms

Initial pathology

Second clinical presentation/ second surgery

1

28/no/urinary retention

Leiomyoma

2

33/no/not reported

Leiomyoma

3

24/no/not available

Leiomyoma

4

31/no/menorrhagia

Leiomyoma

5

Not available/not available/ not available

Uterine leiomyosarcoma

Not available/total abdominal hysterectomy and staging

6

29/no/menorrhagia

Leiomyoma

Pelvic pain/laparoscopic myomectomy

7–12

Leiomyoma

Pelvic pain/excision of parasitic leiomyomata

13

33, 38, 50, 43, 40, and 32/no/pain (4 patients), dyspareunia (1 patient), and menorrhagia (1 patient) 36/no/not reported

Leiomyoma

Pain/excision of leiomyomata

14

42/no/not reported

Benign leiomyoma with ischemic necrosis and areas of hyaline degeneration,

Progressive abdominal distention, nodule at the umbilicus, and severe pallor for 2 weeks/no

Dyspareunia, dysuria, and pelvic pain/excision of parasitic leiomyomata Asymptomatic pelvic mass during routine examination/ laparoscopic excision of tumors Abdominal distention and breathlessness for 2 mo/ excision of abdominopelvic mass and 3 leiomyomata through laparotomy Palpable 2.7 ! 1.7 cm round mass in the left lower quadrant of abdomen/ excision of the mass

Follow-up period

Reference

Iatrogenic parasitic peritoneal leiomyomata DPL

2.5 yr

[13]

6 yr

[14]

DPL

1 yr

[15]

Iatrogenic parasitic leiomyomata

3 yr

[16]

Uterine leiomyosarcoma

30 mo (median), 2–90 mo (range) 18 mo

[4]

Intraoperative findings

Final pathology

Multiple parasitic leiomyomata Multiple tumors in pelvic cavity

20 ! 30 cm abdominopelvic mass attached to omentum, 5–6 leoimyomata attached to peritoneum near uterus, leiomyomatous uterus 3.2 ! 2.2 ! 2.0 cm mass located in the subfascial area of the abdominal wall, near the trocar site of the previous myomectomy Not available

2 pendunculated leiomyomata (anterior uterine wall and fundus) and 2 parasitic leiomyomata (omentum and sigmoid colon) Parasitic leiomyomata located in sigmoid, rectovaginal septum, bladder, and bowel mesentery

Iatrogenic parasitic leiomyomata

[17]

Iatrogenic parasitic leiomyomata

75 mo (median), 2–204 mo (range)

[11]

Multiple extrauterine leiomyomata in pelvic cavity No surgical intervention

DPL

2 yr

[18]

DPL

3 mo

[19]

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Patient

57/yes/not reported

16

44/no/severe pelvic pain

Leiomyoma

Severe pelvic pain/ laparoscopic excision of the mass

17–20

41, 35, 36, and 48/no/ asymptomatic (2 patients), abdominal mass with pain (1 patient), and dyspareunia with left-sided tenderness (1 patient)

Leiomyoma

21

Not available/not available/ not available

Uterine leiomyosarcoma

Abdominal pain, dyspareunia (1 patient each), no symptoms (2 patients)/laparoscopic excision of parasitic leiomyomata (3 patients) and excision of parasitic leiomyoma during cesarean delivery (1 patient) Not reported/surgical staging

22

42/not available/not available Not available/not available/ not available

Uterine leiomyosarcoma Uterine leiomyosarcoma

Persistent vaginal spotting/ TLH, BSO, and excision of leiomyoma

Not reported/surgical staging Not reported/surgical staging

Necrosed and partially calcified mummified leiomyoma Leiomyoma without atypia

16 yr

[20]

8 yr

[20]

Iatrogenic parasitic leiomyomata

69 mo (median), 24–108 mo (range)

[21]

Not reported

Uterine leiomyosarcoma

[22]

No intra-abdominal dissemination Not reported

Uterine leiomyosarcoma Uterine leiomyosarcoma

27 mo (median), 2–119 mo (range) 42 mo

Pedunculated oval myomalike mass in the pouch of Douglas, mobile and attached to the peritoneum with a thin vascular stalk 7-cm myomalike pedunculated lesion attached to the right infundibulopelvic ligament by a vascular pedicle Leiomyomata found attached to pelvic parietal peritoneum, left paracolic fossa, and peritoneum at the level of the promontory of the sacrum

38 mo (patient 23) and 37.5 mo (patient 24)

Electric Morcellation-related Reoperations

15

23, 24*

Pereira et al.

surgical intervention; palliative therapy administered

without evidence of mitotic activity, cellular atypia, or malignant disease Leiomyoma

[23] [24]

BSO 5 bilateral salpingo-oophorectomy; DPL 5 disseminated peritoneal leiomyomatosis. * Deaths during follow-up period: patient 24 (37.5 months).

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Table 2 Initial clinical symptoms in patients undergoing laparoscopic myomectomy (n 5 24) Asymptomatic Abdominopelvic pain Abnormal uterine bleeding Palpable mass Mixed Other Unknown

2 (8.3) 5 (20.8) 3 (12.5) 0 2 (8.3) 2 (8.3) 10 (41.8)

Data are presented as n (%).

previous laparoscopic hysterectomies required a second surgical procedure because of the diagnosis of malignancy in the intracorporeally morcellated surgical specimen (Fig. 3A). The malignancies identified were 3 cases of uterine adenocarcinoma (17.6%; CI, 20.5% to 35.7%), 11 cases of uterine leiomyosarcoma (64.8%; CI, 42.0%–87.4%), and 3 cases of endometrial stromal sarcoma (17.6%; CI, 20.5% to 35.7%) (Fig. 3C and Table 3). Six of the 17 patients diagnosed with a malignancy in the intracorporeally morcellated surgical specimen died during the follow-up period after the second surgical procedure (Table 3). The follow-up periods for these patients were 1 year (patient 1), 8 months (patient 5), 14 months followed by 6 cycles of chemotherapy (patient

32), 3 months (patient 36), 5.1 months (patient 37), and 48 months (patient 38). The overall distribution of pathologies was as follows: 18 cases of parasitic leiomyomata (27.3%; CI, 16.5%–37.9%), 9 cases of adenomyosis (13.6%; CI, 5.3%–21.9%), 8 cases of endometriosis (12.1%; CI, 4.2%–20.0%), 6 cases of DPL (9.1%; CI, 2.2%–16.0%), 3 cases of mixed benign pathology (4.5%; CI, 20.5% to 9.5%), and 22 cases of malignancy (33.3%; CI, 21.9%–44.7%) (Fig. 4). A subanalysis of all patients undergoing laparoscopic myomectomy and nonmyomectomy procedures for symptoms related to leiomyomata was also performed (Table 5). Twenty-seven (64.3%) patients in the nonmyomectomy group underwent LSCHs and TLHs. As evident in Table 5, patients who underwent laparoscopic myomectomy procedures were younger compared with patients in the nonmyomectomy group (i.e., 38.4 6 8.2 years vs 44.1 6 5.6 years [p 5 .005]). The incidence of parasitic leiomyomata was higher in the laparoscopic myomectomy group (62.5% vs 29.6%, p 5 .02) compared with the nonmyomectomy group during the second surgical procedure. In contrast, the incidence of adenomyosis was lower in the laparoscopic myomectomy group (0% vs 33.4%, p 5 .001) compared with the nonmyomectomy group. There was no difference in the incidence of iatrogenic endometriosis (0% vs 3.7%), DPL (16.7% vs 7.4%), mixed pathologies (0% vs 7.4%), and malignancy (20.8% vs 18.5%) when comparing the 2 groups.

Fig. 2 (A) The distribution of patients with previous laparoscopic myomectomy (n 5 24) who underwent a second surgical procedure. (B) The distribution of benign pathologies identified during the second surgery in all patients (n 5 19) who had a previous laparoscopic myomectomy. (C) The distribution of malignant pathologies identified during the second surgery in all patients (n 5 5) who had a previous laparoscopic myomectomy.

Pereira et al.

Table 3 Electric morcellator-related reoperations after laparoscopic nonmyomectomy procedures (n 5 42)

Initial pathology

1*

46/no/abnormal vaginal bleeding

Small solid formations of epithelial tumor cells attached to the surface of the endocervical epithelium in the endocervical core specimen

2

Not available/not available/abdominal and pelvic pain

Leiomyoma

3

30s/no/menorrhagia and dysmenorrhea

Leiomyoma without evidence of adenomyosis or endometriosis

4

36/no/menorrhagia

Leiomyoma

5*

40/no/not reported

Leiomyoma without features of atypia

6

48/no/menorrhagia

Leiomyoma

7

44/no/menorrhagia

Leiomyoma

Second clinical presentation/second surgery Pelvic mass protruding through anterior vaginal vault/partial colpectomy, hemicolectomy, omentectomy, lymphadenectomy, BSO Increased abdominal pain over 3 weeks/excision of leiomyoma though laparotomy Cyclic pelvic pain 6 mo later/laparoscopic trachelectomy, LSO, and excision of endometrial implants Dyspareunia, terminal dysuria and pelvic pain/ laparoscopic resections of implants, cystoscopy Abdominal distention 6 mo later/excision of pelvic and intraabdominal masses, infracolic omentectomy, bilateral oophorectomy and pelvic lymphadenectomy Dyspareunia and moderate pelvic pain, 4-cm retrocervical mass/excision of pelvic mass, dissection of adhesions

First surgery/follow-up period

Reference

Undifferentiated adenocarcinoma

LSCH/1 yr

[25]

Leiomyoma lodged in region of gallbladder and liver

Leiomyoma

LSCH/3 wk

[26]

Endometrial implants in pelvis

Iatrogenic endometriosis

LSCH/15 mo

[7]

Five scattered, white and dark, firm lesions in pelvis

Implanted benign leiomyomata, fibrosis

TLH/10 mo

[27]

Large mass in the rectovesical pouch and multiple tumor deposits over the omentum and abdominal peritoneum

High-grade leiomyosarcoma

TLH/8 mo

[28]

Severe adhesions between mass, peritoneum, and rectum

Iatrogenic adenomyosis

LSCH, BSO/5 yr

[12]

Intraoperative findings

Final pathology

10-cm tumor involving vagina and cecum

LSCH, 5 yr

169

[29] (Continued)

Electric Morcellation-related Reoperations

Number

Age (yr)/menopause (yes/ no)/presenting symptoms

170

Table 3 Continued

Number

Age (yr)/menopause (yes/ no)/presenting symptoms

Initial pathology

40–48/no/menorrhagia

Leiomyoma

16, 17

Not available/not available/not available

Patient 16: Uterine endometrioid cancer; patient 17: uterine leiomyosarcoma

18

48/no/abdominal and pelvic pain

Leiomyoma

19

30/no/menorrhagia

Low-grade endometrial stromal sarcoma

20

48/no/menorrhagia and pelvic pressure

Leiomyoma

Pelvic pain for 4 yr/ bilateral tuboovarian adhesiolysis, BSO, sigmoidal adhesiolysis, right ureteral dissection, rectal dissection with excision of anterior rectal wall, trachelectomy, closure of the vaginal cuff, and Cystoscopy Deep dyspareunia and pelvic pain/excision of pelvic masses, dissection of adhesions Not available/patient 16: trachelectomy, staging, and excision of port sites; patient 17: trachelectomy and staging Abdominal and pelvic pain/trachelectomy, BSO, omentectomy, and excision of gross lesions on peritoneum Pathology showed lowgrade endometrial sarcoma/trachelectomy, BSO Asymptomatic pelvic mass during routine examination 7 yr later/ exploratory laparotomy, BSO, trachelectomy, and small bowel resection with resection of

First surgery/follow-up period

Reference

Iatrogenic adenomyosis

LSCH/2–9 yr (range)

[30]

Not available

Patient 16: uterine endometrioid cancer; patient 17: uterine leiomyosarcoma

LSCH/34 mo (patient 16); 30 mo (patient 17)

[4]

Multiple coalescent nodules of varying sizes on omentum and pelvic peritoneum

DPL

LSCH/not reported

[31]

Enlarged left ovary and tumor adherent to infundibulopelvic ligament 16 discrete tumor masses throughout the abdomen and pelvis ranging in size from 0.6–9.0 cm

Low-grade endometrial stromal sarcoma

LSCH/11 mo

[32]

DPL

LSCH/7 yr

[8]

Intraoperative findings

Final pathology

Adhesions of sigmoid colon to left fallopian tube, ovary, and cervical stump; large right ovarian endometriotic cyst; and an attached 3-cm mass

Iatrogenic implantation of multiple leiomyomata, adenomyosis, and endometriosis

Latero- and retrocervical masses

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8–15

Second clinical presentation/second surgery

Myometrial fragments with adenomyosis, proliferative endometrium with slightly polypoid configuration

22–24

Not available/not available/not available 46, 50, and 49/no/vaginal bleeding

Endometriosis

25–27

Leiomyoma

28

39/no/vaginal bleeding

Leiomyoma

29

56/yes/vaginal bleeding

Leiomyoma

30

Not available/not available/Not available 48/not available/not available 56/no/menorrhagia and pelvic pain

Low-grade endometrial stromal sarcoma Endometrial stromal sarcoma Weakly proliferative endometrium without atypia, adenomyosis, and leiomyoma in the uterus

60/yes/not reported

Leiomyoma

31 32*

33

Resection of tumor implants and cervical stump

Ovarian tissue, endometriosis, and complex atypical endometrial hyperplasia in sigmoid mesentery mass

LSCH, BSO/7 yr

[33]

Excision of endometrial implants Leiomyomata in different regions of abdomen and pelvis

Endometriosis

LSCH/3 yr

[34]

Iatrogenic parasitic leiomyomata

2 LSCH, 1 LSCH with RSO/3 yr 6 mo (patient 25); 3 yr 9 mo (patient 26); 8 yr (patient 27) TLH/6 yr

[35]

[20]

6-cm solid cystic lesion intimately attached to the presacral peritoneum

Adenomyosis, parasitic leiomyoma

Anterior vaginal prolapse, 3 ! 5 cm solid round mass in the anterior vaginal wall Not reported

Iatrogenic parasitic leiomyoma

TLH/3 yr

[20]

Low-grade endometrial stromal sarcoma Endometrial stromal sarcoma Grade 3 endometrioid adenocarcinoma

TLH/73 mo (median), 3– 124 mo (range) TLH/34 mo

[36] [23]

LSCH, BSO/.14 mo

[37]

Negative for residual disease

LSCH/1 yr

[38]

No intraabdominal dissemination 9-cm left pelvic mass

Two hot and blue sentinel nodes detected in the ventral aspect of the left external iliac vessels and in the right

171

(Continued)

Electric Morcellation-related Reoperations

55/no/dysmenorrhea, menorrhagia, and anemia

Pereira et al.

21

peritoneal tumor masses Left and right lower quadrant pelvic pain, urinary frequency, abdominal bloating, and tenderness/ovarian remnant on the left pelvis sidewall, myometrial implants in the right pelvis and culde-sac, and a tumorlike mass on the mesentery of the sigmoid Pain and bleeding/ endometrial implants Abdominal pain in first 2, suspicion of ovarian cyst in third/excision of tumors Pelvic pain and pelvic tumor during routine pelvic exam/ laparoscopic excision of the mass Genital bulge and presence of mass protruding from vagina/ excision of the mass Not reported/surgical staging Not reported/exploratory laparotomy Left lower quadrant pain and persistent cough with shortness of breath/Surgery deferred because of advancedstage disease Pathology showed poorly differentiated endometrial adenocarcinoma/ laparoscopic

[24] 2 TLHs, 7 LSCHs/27 mo (median), 1.8–93.1 mo (range) superficial common iliac lymph node

Not available/not available/not available

Uterine leiomyosarcoma

trachelectomy, sentinel lymph node detection, pelvic lymphadenectomy Not reported/surgical staging 34–42*

Number

Not reported

Uterine leiomyosarcoma

First surgery/follow-up period Final pathology Intraoperative findings Initial pathology

Second clinical presentation/second surgery Age (yr)/menopause (yes/ no)/presenting symptoms Continued

Table 3

BSO 5 bilateral salpingo-oophorectomy; DPL 5 disseminated peritoneal leiomyomatosis; LSCH 5 laparoscopic supracervical hysterectomy; LSO 5 left salpingo-oophorectomy; RSO 5 right salpingo-oophorectomy; TLH 5 total laparoscopic hysterectomy. * Deaths during follow-up period: patient 1 (1 year), patient 5 (8 months), patient 32 (14 months followed by 6 cycles of chemotherapy), patient 36 (3 months), patient 37 (5.1 months), and patient 38 (48 months).

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Reference

172

Table 4 Initial clinical symptoms in patients undergoing laparoscopic nonmyomectomy procedures (n 5 42) Asymptomatic Abdominopelvic pain Abnormal uterine bleeding Palpable mass Mixed Other Unknown

0 1 (2.4) 18 (42.9) 0 4 (9.5) 0 19 (45.2)

Data are presented as n (%).

Discussion Electric intracorporeal tissue morcellation has helped gynecologic surgeons to overcome the problem of retrieving large surgical specimens through small incisions by allowing fragmentation of larger specimens into smaller pieces [39]. During laparoscopic surgery, morcellated tissue fragments are routinely dispersed into the peritoneal cavity [4]. It was previously thought that these tissue fragments, which are devoid of vascular supply, are resorbed by the peritoneal cavity [4]. However, there is evidence documenting the longterm sequelae related to growth and propagation of these dispersed tissue fragments in the peritoneal cavity [4]. Our review adds to the body of evidence suggesting that morcellated tissue fragments dispersed in the peritoneal cavity can contribute to the pathogenesis of parasitic leiomyomata, iatrogenic endometriosis, adenomyosis, and DPL. The pathogenesis of iatrogenic parasitic leiomyomata is thought to be caused by the seeding and implantation of dispersed tissue fragments produced at the time of morcellation, with its incidence after laparoscopic surgery ranging from 0.12% to 0.57% [11,35,38]. Kho and Nezhat [11] performed a retrospective chart review of 12 patients with parasitic leiomyomata and found that 8 patients had prior morcellation procedures; 6 of these procedures were performed laparoscopically. Endometriosis and adenomyosis may also occur in atypical sites such as the umbilicus or vagina because of the implantation and growth of morcellated tissue fragments [7]. Although it may be postulated that the dispersion of endometrial and myometrial tissue fragments in the peritoneal cavity during intracorporeal morcellation can contribute to the pathogenesis of iatrogenic endometriosis and adenomyosis, it also important to recognize the possibility that the pathology was present but went unrecognized during the first surgical procedure. DPL belongs to a rare group of smooth muscle tumors characterized by discrete nodules of smooth muscle scattered throughout the peritoneal cavity [8]. It is considered as a distinct entity from parasitic leiomyomata, exhibiting unusual growth patterns and occasionally mimicking peritoneal carcinomatosis macroscopically [8]. Although the true pathogenesis of DPL remains unknown, several cases of intraperitoneal seeding

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173

Fig. 3 (A) The distribution of patients with previous laparoscopic nonmyomectomy procedures (n 5 42) who underwent a second surgical procedure. (B) The distribution of benign pathologies identified during the second surgery in all patients (n 5 25) who had a previous laparoscopic nonmyomectomy procedure. (C) The distribution of malignant pathologies identified during the second surgery in all patients (n 5 17) who had a previous laparoscopic nonmyomectomy procedure.

caused by morcellator use have been reported in the medical literature [8,14,15,18]. Inadvertent morcellation of surgical specimens containing malignancy is another important aspect that our review addresses. Previous studies have investigated the impact of

morcellation on the risk of disseminating unexpected malignancy and its corresponding impact on cancer progression and survival [4,23,24]. In a retrospective case series of 17 patients with uterine malignancy who had previously undergone surgery for presumed benign disease, Einstein

Fig. 4 Overall distribution of all pathologies during the second surgery in all patients (N 5 66) who had a previous laparoscopic myomectomy and nonmyomectomy procedures.

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Table 5 Subanalysis of patients undergoing laparoscopic myomectomy and nonmyomectomy procedures for leiomyomata

Laparoscopic myomectomy

Laparoscopic supracervical hysterectomy/total laparoscopic hysterectomy

Age (yr) 38.4 6 8.2 Pathology (n 5 24) Parasitic leiomyomata 15 (62.5%) Adenomyosis 0% Iatrogenic endometriosis 0% DPL 4 (16.7%) Mixed pathology 0% Malignancy 5 (20.8%)

Age (yr) 44.1 6 5.6 Pathology (n 5 27) Parasitic leiomyomata 8 (29.6%) Adenomyosis 9 (33.4%) Iatrogenic endometriosis 1 (3.7%) DPL 2 (7.4%) Mixed pathology 2 (7.4%) Malignancy 5 (18.5%)

p value .005 .02 .001 .53 .28 .28 .56

Data are presented as mean 6 standard deviation and n (%).

et al [4] found that patients who underwent early and complete surgical restaging and were not upstaged appeared to have a good prognosis. Although our review identifies 66 patients who underwent morcellation-related reoperations after laparoscopic myomectomy and nonmyomectomy procedures, we recognize that this number could be underestimated for a few reasons. First, this review included only English language studies that involved intracorporeal morcellation during LMs, LSCHs, and TLHs. A larger number of patients may have been identified if non–English language studies or hysterectomies and myomectomies that were performed abdominally and vaginally were included. Second, not all gynecologic surgeons report surgical complications, which, in turn, can result in an underestimation of patients undergoing morcellator-related reoperations. Finally, our study includes a variety of case reports and case series, which, in turn, reflect variations in surgical technique and intraoperative use of a morcellator. To maintain uniformity in surgical technique, we excluded any hysterectomies and myomectomies that involved the use of manual, transvaginal, or hysteroscopic morcellators. We also recognize that this review may be prone to publication bias because of its focus on electric morcellation-related reoperations. Gynecologic surgeons continue to use laparoscopic techniques because they offer quicker recovery, less postoperative pain, fewer wound complications, and better cosmesis compared with open procedures [39]. Patients being considered for laparoscopic surgery who may require intracorporeal morcellation should undergo thorough preoperative evaluation for coexisting uterine or cervical malignancy [39,40]. As evident from the data collated in this review, patients must also understand that there is no reliable preoperative constellation of symptoms or screening tool to differentiate between benign

and malignant pathologies, especially uterine leiomyosarcomas or endometrial stromal sarcomas [39,40]. Preoperative preparation of patients should also include detailed informed consent regarding the risks of intracorporeal morcellation. Gynecologic surgeons must inform patients that morcellators have been associated with injury to abdominopelvic organs [6]. As highlighted in our review, patients should be aware that morcellated tissue fragments are dispersed into the peritoneal cavity and have been implicated in the pathogenesis of parasitic leiomyomata, iatrogenic endometriosis, and DPL. It is also imperative to counsel patients that the majority of laparoscopic myomectomy and nonmyomectomy procedures involving the use of intracorporeal electric tissue morcellators are uncomplicated and that institutions having no women with parasitic leiomyomata, iatrogenic endometriosis, adenomyosis, DPL, or malignancy are very unlikely to report surgical outcomes of uneventful electric morcellation. The risks of developing the aforementioned pathologies are unknown, largely because of the fact that the precise frequency of morcellator use in gynecologic surgery still remains unknown [39]. At some tertiary referral centers, electric morcellation has been used in up to 93% and 40% of laparoscopic myomectomies and hysterectomies, respectively [21]. Electric morcellator-associated pathology must be suspected in patients who present with new clinical symptoms after any surgery in which a morcellator was used. Patients should be also be aware that inadvertent morcellation of surgical specimens containing occult malignancy can lead to the dissemination of cancerous cells in the peritoneal cavity, necessitating reoperation for complete staging [4,23,24]. It is likely that the time interval between the initial surgery and the staging surgery is an important factor in determining the outcome for malignancies. The lack of prospective data or the rarity of an adverse event should not preclude a discussion of potential complications [39]. For optimal cosmesis, it is desirable to retrieve surgical specimens through the smallest possible incision; yet, retrieval of an intact surgical specimen should still be considered paramount [9]. Alternatives to electric intracorporeal tissue morcellation such as laparoscopic-assisted minilaparotomy and tissue retrieval through a vaginal incision can be considered [39,40]. If morcellation is required, then manual morcellation within an endoscopic bag can also be attempted although there is insufficient evidence to establish its superiority over electric morcellation [39,40]. If electric intracorporeal tissue morcellation is used, the rotating blades should be used at lower velocities to decrease tissue dispersion [23]. Copious irrigation must be performed to decrease the retention of dispersed tissue fragments intraperitoneally [7]. Before surgical closure, a meticulous survey of the peritoneal cavity must also be undertaken to identify any residual tissue fragments. If any preoperative or intraoperative findings are suspicious for malignancy, morcellation is contraindicated. Given the potential for

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dissemination of cancerous cells in the peritoneal cavity during intracorporeal morcellation, the Society for Gynecologic Oncology asserts that morcellation is contraindicated in the presence of documented or highly suspected malignancy and may be inadvisable in premalignant conditions or riskreducing surgery [40]. Future Research Despite some evidence highlighting the long-term sequelae of morcellated tissue fragments in the peritoneal cavity and morcellation-related reoperations, large-scale prospective data are still required to validate the role of electric intracorporeal tissue morcellation in the pathogenesis of parasitic leiomyomata, endometriosis, DPL, and cancer progression. One such example is a single-center study of 423 women who underwent laparoscopic myomectomy and nonmyomectomy procedures involving the use of an electric morcellator in which the prevalence of parasitic leiomyomata was 0.9% (CI, 0.3%–2.2%) [21]. Another recent single-center case-control study comparing 277 cases of LSCHs with morcellation with 187 cases of transabdominal or transvaginal hysterectomies without morcellation showed that 1.4% of patients were newly diagnosed with endometriosis after hysterectomy, with a similar incidence in both groups [34]. It is also important to recognize that malignancies such as uterine leiomyosarcomas or endometrial stromal sarcomas are associated with poor prognoses even when surgical specimens are removed intact [40]. Therefore, total abandonment of laparoscopic techniques and banning of electric intracorporeal tissue morcellation seem hasty and premature [39]. Conclusion As more gynecologic surgeons use minimally invasive approaches and possibly tissue morcellators to remove larger uteri and leiomyomata, morcellator-associated reoperations will become more relevant [4,6]. Rare complications may become more apparent as prospective data are assimilated [39]. The creation of a nationwide database of gynecologic surgeries, including data on electric intracorporeal tissue morcellation, its associated outcomes, and complications, would be a critical step toward evidence-based action [39]. References 1. Pelosi MA 3rd, Pelosi MA. The Pryor technique of uterine morcellation. Int J Gynaecol Obstet. 1997;58:299–303. 2. Streicher LF. A gynecologist’s guide to laparoscopic morcellation. Female Patient. 2010;35:26–35. 3. Steiner RA, Wight E, Tadir Y, Haller U. Electrical cutting device for laparoscopic removal of tissue from the abdominal cavity. Obstet Gynecol. 1993;81:471–474. 4. Einstein MH, Barakat RR, Chi DS, et al. Management of uterine malignancy found incidentally after supracervical hysterectomy or uterine morcellation for presumed benign disease. Int J Gynecol Cancer. 2008;18:1065–1070.

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