Uterine Sparring Operative for Adenomyosis

ORIGINAL ARTICLE: FERTILITY PRESERVATION

Uterus-sparing operative treatmentfor adenomyosis
Grigoris F. Grimbizis, M.D., Ph.D., Themistoklis Mikos, M.D., M.Sc., Ph.D., and Basil Tarlatzis, M.D., Ph.D.
1st Department of Obstetrics and Gynecology, Aristotle University of Thessaloniki, Thessaloniki, Greece

Objective: To review systematically the literature on uterus-sparing surgical treatment options for adenomyosis.Design: Systematic literature review.Setting: Tertiary academic center.Patient(s): Women with histologically proven adenomyosis treated with uterus-sparing surgical techniques.Intervention(s): Conservative uterine-sparing surgery for adenomyosis classified as (1) complete excision of adenomyosis, (2)cytoreductive surgery or incomplete removal of the lesion, or (3) nonexcisional techniques, with studies selected if women withadenomyosis were treated surgically without performing hysterectomy.Main Outcome Measure(s): The cure rate after interventional strategies, the rate of symptom (dysmenorrhea and menorrhagia) con-trol, and pregnancy rate in each group of intervention.Result(s): A quality assessment tool was used to assess the scientific value of each study. In total, 64 studies dealing with 1,049 patientswere identified. After complete excision, the dysmenorrhea reduction, menorrhagia control, and pregnancy rate were 82.0%, 68.8%,and 60.5%, respectively. After partial excision, the dysmenorrhea reduction, menorrhagia control, and pregnancy rate were 81.8%,50.0%, and 46.9%, respectively.Conclusion(s): Uterine-sparing operative treatment of adenomyosis and its variants appear to be feasible and efficacious. Well-

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designed, comparative studies are urgently needed to answer the multiple questions arisingfrom this intriguing intervention. (Fertil Steril� 2014;101:472–87. �2014 by AmericanSociety for Reproductive Medicine.)Key Words: Adenomyoma, adenomyosis, cytoreductive surgery, juvenile cystic adenomyoma,uterus-sparing surgery

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I n 1860, von Rokitansky was one ofthe first to describe a conditioncharacterized by the heterotopic

occurrence of islands of endometriumscattered throughout the myometrium(1, 2), specified by Frankl in 1932 as‘‘adenomyosis interna’’ (3). Quite afew reports since the beginning ofthe previous century have outlinedthe feasibility of uterine-sparing sur-gery in women with postoperativelyproven adenomyosis causing subfer-tility (2). The term ‘‘hysteroplasty’’has been proposed to describe the

Received May 27, 2013; revised and accepted OctobeG.F.G. has nothing to disclose. T.M. has nothing to di

travel grants, and honoraria fromMerck Sharp aand honoraria from IBSA and Ferring.

Reprint requests: Grigoris F. Grimbizis, M.D., Ph.D., A1st Department of Obstetrics and Gynecology,niki, Thessaloniki, Greece 54623 (E-mail: grigor

Fertility and Sterility® Vol. 101, No. 2, February 2014Copyright ©2014 American Society for Reproductivehttp://dx.doi.org/10.1016/j.fertnstert.2013.10.025

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conservative operation in whichchildbearing function is preserved inyoung women with extensive adeno-myosis (4). During the last decades,there is an increasing trend of gettingpregnant at a later age. Adenomyosis,a disease mostly diagnosed between30 and 45 years of age, increasinglycomplicates the fertility potential ofwomen in this age group (5). Minimalaccess surgery techniques and organ-preserving surgery is a parallel trendthat characterizes modern gynecology(6). Thus, the need for uterus-

r 15, 2013; published online November 26, 2013.sclose. B.T. received unrestricted research grants,nd Dohme and Merck Serono, and travel grants

ssistant Professor in Obstetrics and Gynecology,Aristotle University of Tsimiski 51 Str., [email protected]).

0015-0282/$36.00Medicine, Published by Elsevier Inc.

preserving surgery in women withsymptomatic adenomyosis warrants aconservative operative managementof the disease.

Adenomyosis is defined as thepresence of endometrial tissue (glandsand stroma) within the myometrium;heterotopic endometrial tissue foci areassociated with a variable degree ofsmooth muscle cell hyperplasia. Ad-enomyosis can either be diffuse orlocalized (focal), depending on theextend of myometrial invasion. More-over, adenomyotic lesions may have ahistologic spectrum from mostly solidto mostly cystic (7).

Adenomyosis is enigmatic interms of etiology, diagnosis, and clin-ical significance. Regarding the etiol-ogy of the disease, the current trendin thought is that adenomyosis or ad-enomyoma results as a down-growthand invagination of the endometrial

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basalis into the adjacent myometrium after disruption of thenormally intact boundary between them. The incidence ofadenomyosis is increased after uterine surgery (i.e., myo-mectomy), cesarean delivery, postpartum endometritis, preg-nancy, uterine trauma, and endometrial interventions (i.e.,endometrial ablation, dilation and curettage, or dilationand evacuation of products of conception). Uterine manipu-lations appear to be a crucial factor predisposing the inva-sion of endometrial cells in the myometrium (8). Adysfunction at the endometrial-myometrial junction is spec-ulated that might be the causative factor of adenomyosis, acondition that could theoretically link the disease to endo-metriosis as well (9).

There is no consensus on the appropriate managementof symptomatic adenomyosis in women seeking fertility.This is because [1] the causative relationship between ad-enomyosis and subfertility has not been fully confirmed,and [2] the incidence of subfertility in women with adeno-myosis has not been defined (10). The concept of conserva-tive, uterine-sparing surgery for adenomyosis is increasingas fertility preservation and quality-of-life improvementcan be achieved in this group of patients (11). Nevertheless,conservative surgery has not become the standard treatmentfor adenomyosis. This is mainly because adenomyotic tissueinvades the uterine muscle layer in a way that make the bor-ders of the lesion unclear, so complete excision of theaffected area remains inaccurate (11). Moreover, the exci-sion of adenomyotic tissue is always accompanied by exci-sion of myometrium, so it is partly destructive for theuterine wall: the advantages of removing an affected areamust be balanced against the disadvantages of leaving apossibly defective uterine wall. Hence, there is a recognizeddifficulty in establishing the state-of-the-art conservativesurgical technique for uterine-sparing management of ad-enomyosis, and operative options include nonstandardizedcytoreductive approaches (12). Additionally, initial experi-ence with simple excision of adenomyotic lesions andcovering or simply closing the myometrium was reportedto be disappointing because this group of patients had quickrecurrences and soon needed hysterectomy (13). Our study isa systematic review of the literature about uterus-sparingsurgical treatment options for adenomyosis [1] aiming to re-view and categorize the available proposals of surgicaluterus-sparing techniques (open or laparoscopic) for thetreatment of symptomatic adenomyosis, and [2] to assessthe effect of each type of surgical treatment on symptomsand future fertility, according to the best available data inthe literature.

MATERIALS AND METHODSClinical/Histologic Classification of Adenomyosis

Until now, a clear classification of adenomyosis has notexisted. This is further complicated by the histologic di-versity, and the differences in the extent and location ofthe disease. However, categorization of the patients isnecessary to evaluate the results of surgical treatment.Thus, taking into account the histologic characteristicsand the extent of the myometrial invasion, adenomyosis


could be classified into the following clinical/histologicvariants:

1. Diffuse adenomyosis. The extensive form of the disease,characterized by foci of endometrial mucosa (glandsand stroma) scattered throughout the uterine muscula-ture (14).

2. Focal adenomyosis. A restricted area of hypertrophic anddistorted endometrium and myometrium, usuallyembedded within the myometrium (14, 15). Thehistologic characteristics of focal adenomyosis maydiffer from patient to patient, from almost solid to onlycystic (adenomyotic cysts); thus, this form could besubdivided to:a. Adenomyoma. Any disease that infiltrates a restricted

area of the myometrium with more or less clear bordersand with mainly solid characteristics. Practically, theterm adenomyoma seems to be used for grossly circum-scribed adenomyotic masses (15, 16).

b. Cystic adenomyosis. An extreme form of adenomyosischaracterized mainly by the presence of a single ad-enomyotic cyst within myometrium (8).

I. In women younger than 30 years old, focal cysticadenomyosis is described as juvenile cystic ad-enomyosis (JCA). For this variant, Takeuchiet al. (17) proposed the following diagnosticcriteria: age less than 30 years, cystic lesion >1cm clearly independent of the endometrium,and severe dysmenorrhea.

3. Polypoid adenomyomas. Circumscribed endometrialmasses composed of predominantly endometrioid glandsand a stromal component predominantly of smoothmuscle (15).a. Typical polypoid adenomyomas. Polypoid adenomyo-

mas without architectural or cellular atypia (15).b. Atypical polypoid adenomyomas. A rare variant of

polypoid adenomyomas characterized by atypicalendometrial glands, often squamous metaplasia, anda cellular smooth muscle stroma (18).

4. Other forms.a. Adenomyomas of the endocervical type. Rare forms of

adenomyomatous polyps in the uterine cervix thatcontain epithelial component of endocervical type.These lesions are important because they must bedifferentiated from adenoma malignum (19).

b. Retroperitoneal adenomyomas. Adenomyotic nodulesthat are thought to arise from metaplasia of m€ullerianremnants beneath the peritoneum and in the area of up-per rectovaginal septum (7).

Classification of Uterine-Sparing Techniques

For most cases of adenomyosis, the lesion presents with a mi-nor or major degree of myometrial infiltration. In these cases,removal of healthy myometrium happens inevitably duringexcision of the lesion. It seems sound to stipulate that anyclassification of the currently available surgical techniquesregarding the excision of adenomyosis should be based onthe extent of removal of adjacent healthy myometrium and

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the preservation of the integrity (and subsequently the func-tionality) of the uterine wall. Accordingly, one could classifythe currently available uterine preserving surgical options foradenomyosis as following:

1. Complete excision of adenomyosis.a. Adenomyomectomy. Preferably used in cases of local-

ized adenomyosis (adenomyoma) but also in selectedcases of more diffuse adenomyosis with reconstructionof the uterine wall. This includes the complete removalof all clinically recognizable non-microscopic lesions.The integrity of uterine wall is maintained (20).

b. Cystectomy. Used in cases of cystic focal adenomyosis,including the entire removal of the adenomyotic cyst(17, 21).

2. Cytoreductive surgery/partial adenomyomectomy. Used incases of diffuse adenomyosis, including the partialremoval of the clinically recognizable non-microscopic le-sions because complete removal of the lesion would lead tothe concomitant excision of critical amount of healthymyometrium, which could lead to ‘‘functional’’ hysterec-tomy (13, 22).

3. Nonexcisional techniques. Used in interventions whereremoval of adenomyotic tissue is not included (22–24).

Selection Criteria

Studies were selected if women with adenomyosis weretreated surgically without performing a hysterectomy. Forthe constellation of systematic review that examines theoutcome of conservative surgical methods of treatment of ad-enomyosis, we included randomized trials, cohort studies,case-control studies, case series, and case reports. Both pro-spective and retrospective studies were included. Studieswere excluded if the outcome was not clearly stated. Non-English studies, duplicate publications, and studies publishedonly in abstract form were excluded.

Special issues of ambiguity were the mode of final diag-nosis of adenomyosis before the intervention, the control ofthe disease, and the reproductive outcome. Definitive diag-nosis of adenomyosis is made with a biopsy (14). Preoperativediagnosis of adenomyosis has been performed with ultra-sound and/or magnetic resonance imaging (MRI); however,MRI seems to exhibit higher sensitivity and specificitycompared with other diagnostic modalities (25, 26). In ourreview, all articles where histology was not obtained wereexcluded.

The control of the disease was evaluated by the reductionof pain, menorrhagia, or symptoms. There was no restrictionon the modality of how the outcome was reported, whether itwas in a form of a questionnaire or was clinician of patientreported. The reproductive outcome was measured by thenumber and type of conceptions in patients who wished tobecome pregnant, the pregnancy outcome, and the numberof babies taken home.

Study Selection

Studies were included in the systematic review after a two-stage process (Supplemental Fig. 1, available online). First,

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the titles and abstracts from the electronic searches wereexamined by two reviewers (T.M. and G.G.), and full manu-scripts of all articles that met the selection criteria wereretrieved. Second, full manuscripts were examined to makefinal inclusion or exclusion decisions. Any disagreement inthe inclusion/exclusion stage was resolved by arbitrationfrom a third reviewer (B.C.T.).

All selected articles were assessed for the following: studydesign, adequate description of patient characteristics,completeness of information in the data sets, preoperativeor intraoperative diagnosis of adenomyosis, use of validatedassessment method of symptoms, pain, and bleeding, ratesand types of intraoperative complications, rates of recurrenceof adenomyosis and need for further interventions, and post-interventional rates of conception and full-term pregnancy.

Data Extraction

Two assessors (T.M. and G.G.) independently reviewed the ti-tles and abstracts of all identified citations. From full text ar-ticles and using a standardized data collection form, thereviewers independently extracted data regarding the studydesign, the number of patients, the characteristics of theparticipants, the modality of the initial diagnosis, the primaryintervention, the duration of follow-up observation, the post-operative outcomes in terms of symptom reduction, the painreduction, the uterine volume reduction, and the reproductiveoutcome. The reproductive outcome after the primary inter-vention was recorded in terms of the number wishing toconceive, the number of natural conceptions or conceptionsafter assisted reproduction techniques (ART), and the numberof terminations of pregnancies (TOP), miscarriages, ongoingpregnancies, preterm and full-term deliveries, including themode of delivery.

Quality Assessment of Studies

All of the studies were evaluated and consequently ranked toascertain the specific power of each, based on certain criteria.This was performed solely to assist the reader in assessingobjectively the scientific value of each study. These criteriaare reported and explained in Supplemental Table 1 (availableonline). The criteria were selected and modified from alreadyproposed quality assessment tools (Newcastle-Ottawa QualityAssessment Scale) for clinical studies. Each criterion could begraded either as 0 (study not meeting the criterion) or 1 (studymeeting the criterion). Each study was then graded with ascore ranging from 0 (poorest performance, minimum totalscore) to 9 (best performance, maximum total score), depend-ing on the fulfillment of the criteria. Studies that scored 5 ormore the trials with powerful evidence in their results; theywere selected for further analysis. Studied that scored lessthan 4 were trials with poor evidence; they were not includedin subsequent analysis.

Statistical Analysis

Statistical analyses were performed to establish the cure rateafter interventional strategies, the rate or recurrence of symp-toms, the hysterectomy rate, and the pregnancy and the



delivery rate in each intervention group. For analysis, the logrates were pooled, weighting each study by the inverse of itsvariance, and the summary estimates were calculated. Thestatistical analysis was performed using Microsoft Exceland MedCalc 11.4.4 (MedCalc Software).

RESULTSCurrently Available Methods of Uterine-SparingSurgical Treatment

Adenomyomectomy for diffuse or focal adenomyosis, cytore-ductive surgery (partial adenomyomectomy), or a variety ofnonexcisional techniques has been described thoroughly inthe literature for the uterine-sparing surgical treatment ofadenomyosis. The described proposals, classified accordingto the radicality of the excision of the adenomyotic tissueare shown in Table 1.

Complete Excision of Adenomyosis/Adenomyomectomy

Classic technique. An adenomyomectomy (open or laparo-scopic) includes the same steps as myomectomy (open orlaparoscopic). This technique involves [1] recognition of thelesion's location and borders by inspection and/or palpation,[2] longitudinal incision of the uterine wall along the adeno-myoma (Fig. 1Aa), [3] sharp and blunt dissection of the lesionwith scissors, graspers, and/or diathermy in a fashion similarto the removal of a fibroid (Fig. 1Ab), [4] suturing of the

TABLE 1

Classification of uterine sparing surgical techniques and of their variants.

Surgical category Techniques

Complete excision Adenomyomectomy

Cystectomy Classic technique

Partial excision (cytoreductive surgery) Partial adenomyomectomy

Nonexcisional techniques Combined with excisional

Nonexcisional only

Hysteroscopic

Others

Grimbizis. Uterus sparing surgery for adenomyosis. Fertil Steril 2014.


uterine wall in a seromuscular layer (16, 27) or in two ormore layers (4, 10) (Fig. 1Ad), and suturing of theendometrial cavity with absorbable suture when necessary.In cases of laparoscopic adenomyomectomy (Fig. 1Ac), theadenomyotic mass is removed with the use of a morcellator(16). In cases where intraoperative recognition of theadenomyotic lesion is arduous, the use of ultrasoundguidance has been proposed, either in the form ofhydroultrasonographic monitoring or in the form oftranstrocar ultrasonography (28, 29).

Modification in wall reconstruction: U-shaped suturing. Inthis laparoscopic modification, after removal of adenomyom-atous tissue, the wall's cavelike wound is approximated by U-shape sutures at the muscle layer; the seromuscular layer isclosed by figure-eight sutures (30).

Modification in wall reconstruction: overlapping flaps. Inthis laparoscopic modification, a transverse incision is madein the adenomyotic tissue, and the lesion is excised with amo-nopolar needle. The remaining seromuscular layers are over-lapped and sutured to counteract the lost muscle layer of theuterus (Fig. 1Ba–d) (31).

Triple-flap method. This laparotomy technique involves [1]extraperitonealization of the uterus and rubber tourniquetplacement for hemostasis; [2] bisection of the uterus in themidline and in the sagittal plane with a scalpel until the uter-ine cavity is reached (Fig. 1Ca); [3] opening of the endometrialcavity to permit the introduction of the index finger to guideduring excision of adenomyotic tissues; [4] use of Martin

Described variant

1. Classic technique (Hyams 1952; Grimbizis et al., 2008; Wanget al. 2009)/plus intraoperative ultrasound guidance(Nabeshima et al. 2003; Nabeshima et al. 2008)

Modifications:U-shaped suturing (Sun et al. 2011)Overlapping flaps (Tacheshi et al. 2006)

2. Triple flap method (Osada et al. 2011)

1. Classic technique (Fujishita et al. 2004)2. Transverse H incision (Fujishita et al. 2004)3. Wedge resection of the uterus (Sun et al. 2011)4. Asymmetric dissection of the uterus (Nishida et al. 2010)

Uterine artery ligation together with adenomyomectomy (Kanget al. 2009)

1. Uterine artery ligation (Wang et al. 2002)2. Electrocoagulation of myometrium (Wood, 1998; Philips,

1996)1. Endometrial resection (Wood, 1998; Fernandez et al. 2007;

Kumar et al. 2007; Maia et al. 2007)2. Endometrial ablation (Preuthhupan et al. 2010)3. Hysteroscopic cystectomy1. High-frequency ultrasound (HIFU) (Yang et al. 2009)2. Alcohol instillation for cystic adenomyosis (Furman et al. 2007)3. Endometrial nonhysteroscopic ablation

Radiofrequency (Ryo et al. 2006)Microwave (Kanaoka et al. 2004)Balloon (Chan et al. 2001)

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forceps to grasp adenomyotic tissues and to excise them fromsurrounding myometrium, leaving a myometrial thickness of1 cm from serosa above and endometrium below (Fig. 1Cb);[5] closure of the endometrium with 3–0 Vicryl (Fig. 1Cc);and [6] closure of the flaps of the uterine wall approximatingthe myometrium and serosa of the one side of the bisecteduterus in the anteroposterior planewith interrupted 2–0Vicryl(Fig. 1Cd), while the contralateral side of the uterine wall isbrought over the reconstructed first side in such a way as tocover it (Fig. 1Ce) (20).

Cytoreductive Surgery/PartialAdenomyomectomy

Classic technique: excision of diffused adenomyosis. Cy-toreductive surgery for adenomyosis includes the followingsteps: [1] a vertical or transverse incision is applied in themiddle of the anterior or the posterior uterine wall; [2]Ford T clamps (or an equivalent instrument) are applied tothe wound edges so as myometrium of the subserous layer,which is rarely affected by adenomyosis (up to �10 mm),can be preserved; [3] the uterine wall is inspected for clini-cally recognizable non-microscopic adenomyotic lesions(coarse, white trabeculations), which are excised piece bypiece with as much of the adjacent normal myometrium aspossible being preserved; [4] if adenomyosis is extended tothe contralateral wall of the uterus as well, the incision isextended over the top of the uterus and down toward the uri-nary bladder of the pouch of Douglas. Closure of myome-trium is performed in one or more layers and closure of theserosa in one layer with interrupted sutures. Attention istaken to not leave any uterine defect that could increasethe risk of hematoma (12).

Transverse H incision technique. In this laparotomy modifi-cation, mainly described for anterior uterine wall adenomyo-sis, ligation of the uterine cervix throughout the broadligament and vasoconstricting agents are used to minimizeblood loss. A vertical incision is made in the uterine wall,and two transverse incisions are applied perpendicularly tothe initial incision along the upper and lower edges of theuterus (H incision). A 5-mm thickness of the uterine serosais resected from the uterine myometrium along the verticalincision. This resection is extended, and the uterine serosa iswidely opened bilaterally at the area under the H incision.Then, slices of adenomyotic tissue are removed, using manualpalpation to define the borders of healthy myometrium. Chro-mopertubation test using indigo-carmine allows assessmentof endometrial perforation. As above, closure of myometriumis performed in one or more layers and closure of the serosa inone layer with interrupted sutures (12).

Wedge resection of the uterine wall. In this technique (openor laparoscopic), the part of the seromuscular layer whereadenomyosis is located is removed by wedge resection ofthe uterine wall. The operation is completed with traditionalclosure of the uterine wounds as described in the classic tech-nique of partial adenomyomectomy (30).

Asymmetric dissection of uterus. In this laparotomy tech-nique, the uterus is dissected longitudinally with a surgical

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electric knife in an asymmetrical fashion to divide the insidefrom the outside, preserving both the uterine cavity andbilateral uterine arteries. From this incision, the myome-trium is dissected diagonally, as if hollowing out the uterinecavity. With a transverse incision, the uterine cavity is thenopened; the index finger is inserted into the cavity, and ad-enomyotic lesions are excised using a loop electrode to athickness of 5 mm of the inner myometrium. The procedurecontinues with excision of adenomyosis to a thickness of 5mm of the serosal myometrium. Then the endometrial cavityis closed, and the uterine flaps are rejoined in layers (muscleand serosa) (13).

Laparoscopically assisted vaginal excision. In this tech-nique, the surgeon initially confirms that the uterus is freeof any adhesions. A laparoscopic bilateral uterosacral liga-ment removal is performed, and a posterior colpotomyfollows. Through the vaginal incision, the uterus is extracted,and under direct manipulation the surgeon removesadenomyotic fragments verified by touch using monopolarcautery. The residual myometrium is closed in two layers.The advantages of this method are comparable to open adeno-myomectomy because of excising adenomyotic tissue distin-guished by touch and knotting manually with adequatetension (32).

Nonexcisional Techniques

The following groups of nonexcisional techniques have beendescribed in the literature for the uterine-sparing manage-ment of adenomyosis.

1. Combination of excisional and nonexcisional techniques.Kang et al. (33) described a technique of performing lapa-roscopic resection of diffuse adenomyosis after laparo-scopic uterine artery occlusion.

2. Laparoscopic nonexcisional techniques. These techniquesinclude laparoscopic electrocoagulation of the myome-trium (22, 23, 34) and laparoscopic uterine arteryligation (24).

3. Hysteroscopic nonexcisional techniques. These techniquesinclude operative hysteroscopy (35), rollerball endometrialablation (36), transcervical resection of the endometrium(37, 38), and endomyometrial resection (22).

4. Other techniques. These techniques include ablation offocal adenomyosis with high frequency ultrasound(HIFU) (39), alcohol instillation under ultrasound guidancefor the treatment of cystic adenomyosis (40), radiofre-quency ablation of focal adenomyosis (41), microwaveendometrial ablation (42), and balloon thermoablation(43) for diffuse adenomyosis.

Synopsis of the Literature that Deals with Uterine-Sparing Treatment of Adenomyosis

In total, 64 studies dealing with 1,049 patients treated withuterine-sparing surgical methods for adenomyosis wereanalyzed. Complete excision of adenomyosis was describedin 20 studies (488 patients) (Supplemental Table 2); of these,9 studies (469 patients) scored R5 during quality assess-ment (4, 10, 11, 16, 20, 30, 31, 44–56) (Table 2). Partial


FIGURE 1



excision of adenomyosis was described in 11 studies (128patients) (Supplemental Table 3); of these, 3 studies (83patients) scored R5 during quality assessment (10, 12, 13,22, 30, 32, 57–61). Complete excision of cysticadenomyomas was described in 22 studies (38 patients)(see Supplemental Table 4); of these, 2 studies (13


patients) scored R5 during quality assessment (8, 17, 21,28, 29, 62–77)(Table 2). Nonexcisional methods foradenomyosis were applied in 15 studies (395 patients) (seeSupplemental Table 5); of these, 4 studies (342 patients)scored R5 during quality assessment (22–24, 33, 35–43,78)(Table 2).

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FIGURE 1 Continued

(A) Complete adenomyomectomy classic technique: (a) Longitudinal incision along the adenomyoma. (b) Sharp and blunt dissection with scissors,graspers and/or diathermy. (c) Suturing of the endometrial cavity. (d) Suturing of the uterine wall. (B) Complete adenomyomectomy classictechnique with overlapping flaps: (a) Transverse incision. (b) The lesion is excised with monopolar needle. (c, d) The remaining seromuscularlayers are overlapped and sutured to counteract the lost muscle layer of the uterus. (C) Complete adenomyomectomy with triple flaptechnique: (a) Bisection of the uterus in the midline and in the sagittal plane. (b) Opening of the endometrial cavity and excision ofadenomyotic tissues leaving a myometrial thickness of 1 cm. (c) Closure of the endometrium. (d) Closure of the flaps approximating themyometrium and serosa of the one side of the bisected uterus in the anteroposterior plane. (e) The contralateral side of the uterine wall isbrought over the reconstructed first side in such a way as to cover it.Grimbizis. Uterus sparing surgery for adenomyosis. Fertil Steril 2014.


Results after complete excision of adenomyosis/adenomyo-

mectomy. In 9 studies, 469 patients were treated withcomplete excision of adenomyosis/adenomyomectomy(Supplemental Table 2, available online). Overall, the meanpatient age was 37.5 years old (�1.5 years), and the mean

478

follow-up period was 25.1 months (�7.0 months). The meanreduction of pain was 82.0% (�5.4%), and the mean reduc-tion of bleeding was 68.8% (�14.8%) (see Table 3). Afterexcluding the studies where fertility preservation was notthe primary outcome, 147 out of 341 patients wishing to


TABLE 2

Uterus sparing surgical treatment of adenomyosis: quality assessment of the relevant studies.

Author, year

Study

design

No. of

patients

Modality of initial

diagnosis/definition of extent of

the disease

Representativeness

of the cases

Ascertainment of exposure/detailed

surgical technique

Outcome

evaluation

Follow

up/adequate

length

Adequacy

of follow-up

of cohorts

Statistical

analysis

Total

grade

Completeadenomyomectomy

Dai et al. 2012 Pro 1 38 1 U/S Focaladenomyosis(adenomyoma)

1 Consecutive 1 Surgicalrecords

Openexcision/classictechnique

1 Structuredquestionnaire

1 24/12 1 Yes 1 Yes 1 9

Osada et al. 2011 Pro 1 104 1 U/S, MRI Diffuse/focaladenomyosis


Openexcision/tripleflap technique


1 24/12 1 Yes 1 Yes 1 9

Wang et al. 2009 Pro 1 165 1 U/S Focaladenomyosis(adenomyoma)


Open or lapexcision/classictechnique


1 24/12 1 Yes 1 Yes 1 9

Takeuchi et al. 2006 Pro 1 14 0 MRI Focaladenomyosis(adenomyoma)


Lapexcision/uterinewall reconstructionwith overlappingflaps


1 NA 0 No 0 Yes 1 6

Al Jama et al. 2011 Retro 0 18 0 U/S, MRI Focal adenomyosis(adenomyoma)



1 Selfreport

0 36/12 1 Yes 1 Yes 1 6

Koo et al. 2011 Retro 0 18 0 U/S Focal adenomyosis(adenomyoma)




1 9/12 0 Yes 1 Yes 1 6

Sun et al. 2011 Retro 0 40 0 NA Focal adenomyosis(adenomyoma)


Open or lapcompleteexcision/classictechnique withadditional U-shapesuturing

1 Selfreport

0 27/12 1 Yes 1 Yes 1 5

Grimbizis et al. 2008 Retro 0 6 0 U/S Focal adenomyosis(adenomyoma)


Lapexcision/classictechnique


1 13/12 0 Yes 1 No 0 5

Fedele et al. 1993 Retro 0 18 1 Histology Focaladenomyosis(adenomyoma)



1 Selfreport

0 53/12 1 Yes 1 No 0 4

Partial excision ofadenomyosis/partialadenomyomectomy

Sun et al. 2011 Retro 0 13 0 NA Focaladenomyosis(adenomyoma)


Lap partialexcision/classicreconstruction

1 Selfreport

0 20/12 0 Yes 1 Yes 1 4

Nishida et al. 2010 Retro 0 44 1 MRI Diffuse adenomyosis 1 Consecutive 1 Surgicalrecords

Openexcisiona/asymmetricdissection of uterus


1 12/12 0 Yes 1 No 0 6

Wang et al. 2009 Retro 0 28 1 U/S Diffuseadenomyosis


Openexcisiona/classictechnique


1 36/12 1 Yes 1 Yes 1 8

Fujishita et al. 2004 Retro 0 11 0 U/S, MRI Diffuseadenomyosis


Open partialexcision/modifiedH incision

1 Selfreport

0 36/12 1 Yes 1 Yes 1 6

Wood, 1998 Retro 0 25 1 NA Diffuse/focaladenomyosis

0 NA 0 Surgicalrecords

Lapexcisiona/classictechnique

1 Selfreport

0 24/12 1 Yes 1 No 0 4


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TABLE 2

Continued.

Author, year

Study

design

No. of

patients

Modality of initial

diagnosis/definition of extent of

the disease

Representativeness

of the cases

Ascertainment of exposure/detailed

surgical technique

Outcome

evaluation

Follow

up/adequate

length

Adequacy

of follow-up

of cohorts

Statistical

analysis

Total

grade

Cysticadenomyomas andjuvenile cysticadenomyomas

Takeuchiet al. 2010

Retro 1 9 0 U/S, MRI JCA 1 Consecutive 1 Surgicalrecords



1 35/12 1 Yes 1 Yes 1 8

Kriplaniet al. 2011




1 18/12 0 Yes 1 No 0 5

Nonexcisionaltechniques

Kang et al. 2009 Retro 0 37 1 U/S Diffuse/focaladenomyosis


Laparoscopicpartial resectionof adenomyosisþ UAO


1 12/12 0 Yes 1 Yes 1 7

Wang et al. 2002 Pro 1 20 0 U/S, MRI Uncleardescriptionof lesion


Laparoscopicuterine arteryligation


1 8/12 0 Yes 1 Yes 1 6



Myometrialelectrocoagulation

1 Self report 0 24/12 1 Yes 1 No 0 3

Philips et al. 1996 Pro 1 10 0 MRI Uncleardescriptionof lesion


Laparoscopicbipolarcoagulation


Preutthupanet al. 2010

Retro 0 190 1 U/S Diffuse/focaladenomyosis


Rollerballendometrialablation

1 Self report 0 60/12 1 Yes 1 Yes 1 7

Maia et al. 2003 Retro 0 95 1 U/S Uncleardescriptionof lesion


TCRE � Mirena 1 Self report 0 12/12 0 Yes 1 Yes 1 5



Endomyometrialresection


Note: HIFU ¼ high-intensity focal ultrasound; HSG ¼ hysterosalpingogram; Lap ¼ Laparoscopic; MEA ¼ microwave endometrial ablation; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective, Retro ¼ retrospective; TCRE ¼ transcervical endo-metrial resection, UAO ¼ uterine artery occlusion; U/S ¼ ultrasound.a Unclear description of the radicality of adenomyotic tissue excision.


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TABLE 3

Postoperative results, pregnancy rates, and pregnancy outcomes after uterus-sparing surgery for adenomyosis.

Author, year

No. of

patients

Reduction

of symptoms

(%)

Reduction

of pain (%)

Reduction of

bleeding (%)

Patients wishing

to conceive

(n, %)

Natural

Conceptions

(n, %)

Conceptions

after ART

(n, %)

Total

Conceptions

(n, %)

Miscarriages

(n, %)

Ongoing

pregnancy

(n, %)

Preterm

(n, %)

Full-term

(n, %)

Total

deliveries

(n, %) Comment

Complete adenomyomectomyDai et al. 2012 38 NA >80% >80% — — — — — — — — — Recurrence � 7Osada et al. 2011 104 NA VAS: 10–1.6 VAS: 10–2.8 26 4 12 16 2 — — 14 14 No uterine

ruptureWang PH

et al. 2009Surgical group 51 NA VNRS-6:

3.8–1.1Scale: 3.08–1.2 27 20 (74.1%) — 20 3 (11.1%) — 2 (7.4%) 15 (55.6%) 17 Adenomyoma

relapse 49.0%Surgical-

medical114 NA VNRS: 6:

3.9–0.7Scale: 3.68–0.9 44 35 (79.5%) — 35 3 (6.8%) — 5 (11.4%) 27 (61.4%) 32 Adenomyoma

relapse 28.1%Takeuchi et al.

200614 NA NA VAS: 10–2.5 8 2 — 2 — 1 — 1 2 VD � 1

Al Jama et al.2011

18 NA NA NA 18 8 — 8 2 — — 6 6 C/S � 6/18;TAH � 3

Koo et al. 2011 18 NA NRS: 8.1–1.3 MVJ: 4.3–3.2 — — — — — — — — — GnRH therapy;uterine scardehiscence

Sun et al. 2011 40 NA 91.2% 40% 24 3/13 (23.1%) 5/11 (45.5%) 8 5 — — 3 3 U/S relapserate 15.0%

Grimbizis et al.2008

6 Cure Cure Cure — — — — — — — — — None

Subtotal(Symptoms)

— 82.00 68.79

Subtotal(Fertilityoutcome)

341 147/341(43.11)

72/147(48.98)

17/147(11.56)

89/147(60.54)

15/89(16.85)

1/89(1.13)

7/89(7.87)

66/89(74.16)

74/89(83.15)

Partial adenomyomectomyNishida

et al. 201044 NA VAS: 9.4–0.8 Improve — — — — — — — — — Report of 2

incidentalpregnancies;recurrence � 3

Wang PHet al. 2009

28 NA VNRS-6:4.9–1.8

NA 28 13 (46.4%) — 13 4 (14.3%) — — 9 (32.1%) 9 GnRH-a � 6/12

Fujishitaet al. 2004(modified)

6 55% NA NA 4 2 — 2 — 1 — 1 2 C/S � 1,Recurrence �1;endometriumperforation �1

Fujishitaet al. 2004(classic)

5 18% NA NA — — — — — — — — — Recurrence � 4;endometriumperforation �2

Subtotal(symptoms)

56.11 81.78 50.00

Subtotal(fertilityoutcome)

34 32/34(94.12)

15/32(46.88)

0/32(0.00)

15/32(46.88)

4/15(26.67)

1/15(6.67)

0/15(0.00)

10/15(66.67)

11/15(73.33)

Complete adenomyomectomy (JCA)Takeuchi

et al. 20109 NA Pain score:

10–2NA 3 3 — 3 — — — 3 3 V/D � 2; C/S � 1

Kriplaniet al. 2011

4 Cure Pain score:9.75–0.25

NA — — — — — — — — — None


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Fertilityand

Sterility®

TABLE 3

Continued.

Author, year

No. of

patients

Reduction

of symptoms

(%)

Reduction

of pain (%)

Reduction of

bleeding (%)

Patients wishing

to conceive

(n, %)

Natural

Conceptions

(n, %)

Conceptions

after ART

(n, %)

Total

Conceptions

(n, %)

Miscarriages

(n, %)

Ongoing

pregnancy

(n, %)

Preterm

(n, %)

Full-term

(n, %)

Total

deliveries

(n, %) Comment

Subtotal(symptoms)

86.13 84.62 —

Nonexcisional techniquesKang

et al. 200937 NA Median

Pain score8/11–4/11

MedianPBAC:158–59

— — — — — — — — — Hysterectomy � 2;reduction ofvolume (%):224.6–91.6(59.2)

Wanget al. 2002

20 NA Pain score2.4–1.1

(53% red)

PBAC:516–263(49% red)

— — — — — — — — — Hysterectomy � 3;45%dissatisfied;reduction ofvolume (%):268–217(12%)

Preutthupanet al. 2010

190 NA NA Reduced/healed:165 (86.8%)

— — — — — — — — — Hysterectomy � 3;GnRHpretreatment

Maiaet al. 2003(Mirena)

53 NA NA 20% — — — — — — — — — RepeatTCRE � 4;hysterectomy� 4

Maia, 2003(no Mirena)

42 NA NA 90% — — — — — — — — — None

Subtotal(symptoms)

— 54.62 73.68

Total (fertilityoutcome)

384 182/384(47.39)

90/182(49.45)

17/182(9.34)

107/182(58.79)

19/107(17.76)

2/107(1.87)

7/107(6.54)

79/107(73.83)

88/107(82.24)

Note:C/S¼ cesarean section;MVJ¼Mansfield-Voda-Jorgensenmenstrual bleeding scale; NA¼ not applicable; NRS¼ numerical rating scale; PBAC¼ pictorial blood loss assessment chart; TAH¼ total abdominal hysterectomy; TCRE¼ transcervical endometrial resection;U/S¼ ultrasound; VAS ¼ Visual Analogue Score; VD ¼ vaginal delivery; VNRS ¼ verbal numeric rating scale.


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conceive (43.1%) were found; these patients achieved 89 con-ceptions (pregnancy rate: 60.5%) and delivered 74 babies(delivery rate: 83.1%) (see Table 3).

Results after partial excision of adenomyosis/cytoreductive

surgery. In 3 studies, 83 patients underwent open or laparo-scopic partial excision of adenomyosis/adenomyomas(Supplemental Table 3, available online). All were retrospec-tive cohort studies; the mean age of patients was 35.4 years(�1.9 years), and the mean follow-up period was 24.1 months(�13.3 months). In this group of patients, the mean reductionof pain was 81.8% (�0.0), and the mean reduction of bleedingwas 50.0% (�0.0) (see Table 3). After excluding the studieswhere fertility preservation was not the primary outcome,there were 32 out of 34 patients wishing to conceive(94.1%), who achieved 15 conceptions (46.9%) and gave birthto 11 babies (73.3%) (see Table 3).

Results after complete excision of cystic adenomyomas

(including juvenile cystic adenomyomas). In 2 studies [13patients, mean age 23.1 (�3.2) years, follow-up period 29.8(�8.2) months], there was a reported 86.1% (�9.6%) reduc-tion of symptoms and 84.6% (�7.2%) reduction of pain afterexcision of cystic adenomyomas (see Table 3; SupplementalTable 4, available online). Out of three patients wishing toconceive, there were three conceptions and three deliveries(see Table 3).

Results after nonexcisional techniques. In 4 studies [342patients, mean age 42.03 (�1.65) years, follow-up period38.43 (�24.17) months], there was a reported 54.6%(�1.2%) reduction of pain and 73.7% (�23.6%) reduction ofbleeding (see Table 3; Supplemental Table 5, available online).Out of 9 patients wishing to conceive, there were 5 (55.6%)conceptions and 1 delivery (50.0%).

DISCUSSIONUterine-sparing treatment of adenomyosis appears to befeasible and efficacious. The reduction of dysmenorrhea afterconservative surgery ranges from 54.6% (nonexcisionaltechniques) to 84.6% (complete adenomyomectomy). Thereduction of menorrhagia ranges from 50.00% (partial adeno-myomectomy) to 68.8% or even 73.68% (nonexcisional tech-niques). The pregnancy rate ranges from 46.9% (partialadenomyomectomy) to 60.5% (complete adenomyomectomy).

Comments on Quality of Data

The main problem of an attempt to systematically reviewthese procedures is that there are few good quality studies.In an effort to qualify the data of each study, a 9-item qualityassessment tool was created. This tool was based on theNewcastle-Ottawa Quality Assessment scale. Based on thistool, data from only 17 out of the 64 studies were used tocalculate the results after uterus-sparing surgery for adeno-myosis, in terms of dysmenorrhea reduction, menorrhagiareduction, and pregnancy outcome. In fact, a small numberof prospective studies deal with the conservative surgicaltreatment of adenomyosis, and there has been no uniformdesign and/or outcome, so the feasibility of pooling the resultsmay be suboptimal. Overall, the quality of the results may be


inferior, especially regarding therapies such as partial exci-sion of adenomyosis (no prospective studies identified, smallnumber of patients), the complete excision of cystic adeno-myomas (one prospective study, but the total number ofpatients was very small for eliciting secure results), and thenonexcisional techniques (three prospective studies, but thetreatments were totally different, so the results cannot becombined).

On the other hand, for the treatment of adenomyosiswith complete excision of the lesion, we found four prospec-tive studies and a total of 8 studies scoring R5 afterapplying the assessment tool. In this subgroup, the investi-gators reported the use of surgical techniques based on thesame operative principles, so a total of 469 treated patientsaccumulated, which offered good quality data for furtheranalysis. In this subgroup of patients, both treatment andfertility rates appear to be increased (dysmenorrhea control:82.0%; menorrhagia control: 68.8%; pregnancy rate:60.5%).

Comments on the Control of Symptoms

In terms of dysmenorrhoea control, the main contemporarytechniques applied for the uterine-sparing techniques for thetreatment of adenomyosis appear to yield comparable clin-ical results. After complete excision of adenomyosis, partialexcision of adenomyosis, and complete excision of cysticadenomyomas, the reduction of dysmenorrhoea was foundto be 82.0%, 81.8%, and 84.6%, respectively (P ¼ not statis-tically significant). It seems that the excision of the bulk ofadenomyosis controls the pain even if some amount of resid-ual lesion has been left, as happens in cases of cytoreductivesurgery. However, all the series included are studies wherespecially designed cytoreductive techniques were applied,such as the triple flap Osada technique (20), and these resultscould not be generalized across all the techniques used forthe conservative surgery (such as the ‘‘wedge’’ resectiontechnique, represented in this review by only a few casereports).

In terms of menorrhagia control, the results differed afterpartial excision of adenomyosis (50.00% reduction) and com-plete excision of adenomyosis (68.79% reduction). With non-excisional techniques, the control of menorrhagia appears tobe better compared with the partial excision techniques, andto be comparable to that of the complete excision techniques(73.7%). Nonexcisional techniques is an heterogeneous groupof operations including many cases of hysteroscopic ablation.In these cases, the control of bleeding is achieved through thedestruction/excision of endometrium, resulting in loss of thefertility of the patient; in addition, in the group of nonexci-sional techniques, control of symptoms is achieved indirectlyand without treatment of the primary disease. Furthermore, itseems that, especially after partial excision of adenomyosis,the residual lesion adjacent to the endometrium continuesto cause bleeding symptoms. This is an implication for clinicalpractice: in cases of diffuse adenomyosis with menorrhagia,cytoreductive partial excision of the lesion is less effectivecompared with complete excision techniques or nonexci-sional techniques where fertility may be lost.

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Comments on Fertility after Treatment

Overall, there was a restriction in the design of the studiesincluded in this review regarding the fertility potential afteruterine-sparing surgery for adenomyosis. Most of the studieswere not primarily designed to address this issue, as the studypopulations were mainly women with adenomyosis but notnecessarily and subfertility. On the other hand, uterus-sparing surgery for adenomyosis involves techniques thatmodify the anatomy of the uterus (i.e., pelvic adhesions, uter-ine deformities, intrauterine adhesions, or reduced uterinecapacity). These deformities may contribute to a declinedpostoperative pregnancy rate (13). Nevertheless, not onlywas fertility finally preserved, but any subfertility related toadenomyosis appears largely to be treated after cytoreductivesurgery, considering that the crude delivery rate appears to behigher than 70%. In view of the fact that pregnancy rates aftersurgical treatment of fibroids appear to be�50%, the postop-erative fertility outcome after excision of adenomyosis shouldbe considered satisfactory (79). Nevertheless, although theexisting evidence for the burden on clinical pregnancy anddelivery rate caused by intramural fibroids is based oncomparative studies (the common odds ratio [95% confidenceinterval] is 0.8 [0.6–0.9] and 0.7 [0.5–0.8], respectively),research of similar design (prospective, controlled) for theburden on fertility caused by adenomyosis is lacking (79).

According to the findings of this review, the conceptionrates do not appear to be statistically significantly differentbetween partial excision of adenomyosis (46.8%) and com-plete excision of adenomyosis (60.5%) (P¼ .22). These resultsare in agreement with analogous research published in theliterature about the role of treatment of adenomyosis in sub-fertility (80). Similar results have been accumulated about thedelivery rate after partial (73.3%) and complete (83.1%) exci-sion of adenomyosis (P¼ .58), and the miscarriage rate afterpartial (26.7%) and complete (16.9%) excision of adenomyo-sis (P¼ .58). No comment upon the achievement of pregnancyafter nonexcisional techniques can be made because of thelack of reliable data. It appears that there is a trend forincreased fertility after surgery for adenomyosis in the com-plete excision group, but more data are needed to elicit saferesults for clinical practice.

Pregnancy Issues

Intervention to conception time. In most of the studies thatdealt with pregnancy after surgery for adenomyosis, attemptsfor conception were permitted at least 3 months after theintervention (13, 62).

Implication to ART methods. It has been reported that ARTmethods show increased pregnancy rates compared with nat-ural cycles after an operative intervention for adenomyosis(30). Moreover, a single-embryo transfer policy ensures lessrisk of uterine rupture, because a twin pregnancy generatesuterine activity at an earlier gestational age, which maylead to this devastating event (32). Although the data dealingwith this issue are still scarce, our results do not support theuse of a particular technique to increase the conception ratesafter ART methods in women with adenomyosis.

484

Complications

Adenomyosis and uterine rupture. A spontaneous uterinerupture during pregnancy in gravid uteri complicated byadenomyosis has been recorded in isolated case reports,even with no prior cytoreductive surgery (2). Furthermore,there is a recognized risk of uterine rupture during pregnancyor labor after conservative surgery for adenomyosis (32).However, the risk of rupture accompanies all types of uterinesurgery: the incidence of symptomatic uterine rupture duringvaginal birth after cesarean delivery (VBAC) or laparoscopicmyomectomy is reported to be 0.27% and 1.0%, respectively(27, 81). After adenomyomectomy, it is speculated thatsubsequent uterine scars may conceal dense residualadenomyotic foci, and as a consequence the tensile strengthof the uterus may decline leading to possible rupture ofpregnant uterus (82). Wang et al. (48) described this risk asbeing as high as one out of eight women experiencinguterine rupture in pregnancy/labor after cytoreductivesurgery for adenomyosis. Moreover, there are some studieswhere alternative operative procedures are proposed for theadequate healing of uterine wound after this type ofintervention to prevent major complications such as uterinerupture during labor (11).

Adenomyosis and delivery. Although most of the reporteddeliveries have been completed by cesarean delivery, therehave been a few reports vaginal deliveries being allowed. Spo-radic reports have outlined the risk of severe atonic post-partum hemorrhage in women with known adenomyosis,which can necessitate a peripartum hysterectomy (2). Becauseof the absence of data and experience, an elective caesariandelivery after adenomyomectomy seem preferable for patientsafety, especially in nonorganized centers.

General Comments

Conservative surgical intervention: first-line approach for

adenomyosis. This study shows that conservative surgicalintervention is quite likely to improve symptoms from diffuseadenomyosis, and in cases of focal adenomyosis there is agood possibility of permanent treatment. So it is sound toselect the appropriate treatment for the right patient: in casesof focal adenomyosis, laparoscopic excision appears to be thefirst-line approach; in women with diffuse adenomyosis whoare interested in a future pregnancy, aggressive excision ofthe lesion with secure restoration of the uterine wall thicknessmight offer the best results.

It is of outmost important to preoperatively [1] ensure thedefinite diagnosis of adenomyosis, and [2] assess the locationand the size of each adenomyotic focus. Magnetic resonanceimaging assists in the achievement of both of these preoper-ative goals and helps the surgeon to remove completely eachfocus of adenomyosis (26, 51).

Preoperative and postoperative use of GnRH agonist thera-

py. The role of combination approach to adenomyosis withcytoreductive surgery and administering a gonadotropin-releasing hormone (GnRH) agonist in the management ofpatients wishing to preserve their uterus is not clear. It ishypothesized have a synergistic effect because during



cytoreductive surgery the affected tissues with relatively poorblood supply are removed and the response of the remainingadenomyosis to hormone treatment is therefore enhanced(83). The advantages of preoperative use of GnRH-agonisttherapy include the reduction of uterine vascularity, thecorrection of anemia, and the reduction of operative bleeding(facilitates laparoscopy rather than laparotomy) (12).

The disadvantages of preoperative use of GnRH-agonisttherapy are that normal size uteri recognizing adenomyotic tis-sues after GnRH treatment is difficult, assessing the demarca-tion between adenomyosis and normal myometrium isdifficult, the risk of endometrial perforation is increased, andremoving a large amount of adenomyotic lesions becomesdifficult (an adverse effect of GnRH-agonist therapy) (12).

Laparotomy or Laparoscopy

Traditionally, laparotomy has been used for the surgical treat-ment of adenomyosis because of the extension of the diseasewithin the myometrium and the difficulty in suturing theremaining uterine wedges after the excision. The main advan-tage of laparotomy remains the ability of the surgeon topalpate and recognize the adenomyotic lesions intraopera-tively. However, when the adenomyotic lesion can be clearlyoutlined via MRI, laparoscopy is feasible either for ablation ofthe adenomyotic foci or for excision of adenomyomas,whereas laparoscopic suturing presents no more difficultycompared with suturing after myomectomy (16, 51).

Which Technique is Better?

There is no strong evidence to indicate a technique thatsecures the best clinical and reproductive performance. Eachinvestigator describes the theoretical advantages of his orher technique, but in practice the results show no statisticallysignificant clinical differences. Mainly, most of the modifica-tions aim [1] to maximize the amount of adenomyosis excisedduring surgery by offering an increased area where surgicalmanipulations can be performed, and [2] to empower the uter-ine wall integrity so that a future pregnancy can be sustainedwithout uterine rupture.

CONCLUSIONUterine-sparing operative treatment of adenomyosis and itsvariants appears to be feasible and efficacious. Control ofsymptoms is achieved in more than 81% (dysmenorrhea con-trol) and 50% (menorrhagia control) of the patients, and thepregnancy rates appear to be higher than 46%. Nevertheless,data supporting this type of intervention are still suboptimal,and prospective, well-designed, comparative studies areurgently needed to answer multiple questions arising fromthis intriguing intervention.

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SUPPLEMENTAL FIGURE 1

Flow diagram of search strategy.Grimbizis. Uterus sparing surgery for adenomyosis. Fertil Steril 2014.


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SUPPLEMENTAL TABLE 1

Criteria for evaluation of the studies included in the review.

Criteria for study evaluation Grading

Selection1. Type of study design Prospective 1

Retrospective 02. No. of patients >25 1

<25 03. Is the definition of the extent of the adenomyosis

adequate?Clinical/not reported 1MRI or U/S and clinical 0

Is the definition of the type of adenomyosisadequate?

Yes 1No 0

4. Representativeness of the cases Consecutive or obviously representative series of cases 1Potential for selection biases or not stated 0

Exposure5. Ascertainment of surgical technique Secure record (e.g., surgical records) 1

Written self report of medical record only 0No description 0

Is there a detailed description of the surgicaltechnique?

Yes 1No 0

Outcome6. Outcome evaluation Structured questionnaire 1

Self report/No description 07. Was follow-up long enough for outcomes to

occur?>24 months 1<24 months 0

8. Adequacy of follow-up of cohorts Complete follow-up/all subjects accounted for 1Subjects lost to follow-up unlikely to introduce bias,

small number lost1

Inadequate follow-up rate 0No statement 0

9. Statistical analysis Existence of statistical analysis 1Absence of statistical analysis 0

Maximum grading 9/9Note: Studies accumulating a scoreR5 were considered as trials with powerful evidence of their results, but those with a score <5 were considered as poor. MRI ¼magnetic resonance imaging;U/S ¼ ultrasound.


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Complete adenomyomectomy: quality assessment of the relevant studies.

Author, yearStudydesign

No. ofpatients

Modality of initialdiagnosis/definition

of extent ofthe disease

Representativenessof the cases

Ascertainment ofexposure/detailed surgical technique

Outcomeevaluation

Followup/adequate

length

Adequacy offollow-upof cohorts

Statisticalanalysis

Totalgrade

Prospectivestudies

Dai2012/EJOGRB

Pro 1 38 1 U/S Focaladenomyosis(adenomyoma)




1 24/12 1 Yes 1 Yes 1 9

Osada2011/RBM

Pro 1 104 1 U/S, MRI Diffuse/focaladenomyosis


Openexcision/tripleflap technique


1 24/12 1 Yes 1 Yes 1 9

Wang PH2009/FS

Pro 1 165 1 U/S Focaladenomyosis(adenomyoma)




1 24/12 1 Yes 1 Yes 1 9

Takeuchi2006/JMIG

Pro 1 14 0 MRI Focaladenomyosis(adenomyoma)


Lap excision/uterine wallreconstructionwith overlappingflaps


1 NA 0 No 0 Yes 1 6

Retrospective studiesAl Jama

2011/OmanRetro 0 18 0 U/S, MRI Focal

adenomyosis(adenomyoma)


Open or Lapexcision/classictechnique

1 Self-report 0 36/12 1 Yes 1 Yes 1 6

Koo2011/Pak JMS

Retro 0 18 0 U/S Focaladenomyosis(adenomyoma)


Open or Lapexcision/classictechnique


1 9/12 0 Yes 1 Yes 1 6

Sun2011/Chin MJ

Retro 0 40 0 NA Focaladenomyosis(adenomyoma)


Open or Lapcompleteexcision/classictechnique withadditional U-shape suturing


Grimbizis2008/FS





1 13/12 0 Yes 1 No 0 5

Fedele1993/HR

Retro 0 18 1 Histology Focaladenomyosis(adenomyoma)



1 Self-report 0 53/12 1 Yes 1 No 0 5

Case reportsWang

CJ 2006/FSRetro 0 2 0 U/S Focal

adenomyosis(adenomyoma)



1 Self-report 0 25/12 1 NA 0 No 0 3

Ferrero2005, AOG




1 Self-report 0 NA 0 NA 0 No 0 2


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N


Continued.


No. ofpatients


of extent ofthe disease

Representativenessof the cases

Ascertainment ofexposure/detailed surgical technique

Outcomeevaluation

Followup/adequate

length


Statisticalanalysis

Totalgrade

La Fianza2004/JCU


1 NA 0 Medicalrecord



Morita2004/JAAGL

Retro 0 3 0 MRI Focaladenomyosis(adenomyoma)




Wei 2004,Gyn Oncol

Retro 0 1 0 Clinical Focaladenomyosis(adenomyoma)




Ozaki1999/IJFWM





Kataoka1998, JCAT





Hoffman1989/O&G

Retro 0 1 0 HSG Focaladenomyosis(adenomyoma)




Honore1988/JRM





Hyams 1952 Retro 0 2 0 Clinical Diffuseadenomyosis


Openexcision/classictechnique(hysteroplasty)


Coghlin1947/CMJ

Retro 0 1 0 Clinical Focaladenomyosis(adenomyoma)




Note: HSG ¼ hysterosalpingogram; Lap ¼ laparoscopic; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; U/S ¼ ultrasound.a Unclear description of the radicality of adenomyotic tissue excision.


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Partial excision of adenomyosis/partial adenomyomectomy: quality assessment of the relevant studies.


No. ofpatients


of extent of the diseaseRepresentativeness

of the cases

Ascertainment ofexposure/detailedsurgical technique

Outcomeevaluation

Followup/adequate

length


Statisticalanalysis

Totalgrade

Retrospectivestudies

Sun2011/Chin MJ

Retro 0 13 0 NA Focaladenomyosis(adenomyoma)


Lappartialexcision/classicreconstruction


Nishida 2010/FS Retro 0 44 1 MRI Diffuseadenomyosis


Openexcisiona/Asymmetricdissection of uterus


1 12/12 0 Yes 1 No 0 6

Wang PH2009/JOGR

Retro 0 28 1 U/S Diffuseadenomyosis




1 36/12 1 Yes 1 Yes 1 8

Fujishita2004/GOI

Retro 0 11 0 U/S, MRI Diffuseadenomyosis


Openpartialexcision/modifiedH incision


Wood1998/HRU

Retro 0 25 1 NA Diffuse/focaladenomyosis


Lapexcisiona/classictechnique


Case reportsWada

2006/JMIGRetro 0 1 0 MRI Unclear

descriptionof lesion


Lap assisted vaginalexcisiona/classictechnique


Lin 2000/CMJa Retro 0 2 0 U/S Uncleardescriptionof lesion


Lap excision/classictechnique


Huang 1998, CMJ Retro 0 1 0 NA Uncleardescriptionof lesion


Open excisiona/classictechnique


Kammerer-Doak1996/JRM

Retro 0 1 0 CT Uncleardescriptionof lesion


Open excisiona/classictechnique


Van PraaghCJMA, 1965

Retro 0 1 0 Clinical Diffuseadenomyosis


Open excision/classictechnique


Naidu 1958 Retro 0 1 0 Clinical Diffuseadenomyosis


Openexcision/wedgeresection

1 Self-report 0 <24/12 0 NA 0 No 0 1

Note: HSG ¼ hysterosalpingogram; Lap ¼ laparoscopic; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; U/S ¼ ultrasound.a Unclear description of the radicality of adenomyotic tissue excision.


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Cystic adenomyomas and juvenile cystic adenomyomas: quality assessment of the relevant studies.


No. ofpatients

Modality of initialdiagnosis/definitionof extent of the

diseaseRepresentativeness

of the casesAscertainment of exposure/detailed

surgical techniqueOutcomeevaluation

Followup/adequate

length


Statisticalanalysis

Totalgrade

Retrospectivestudies

Takeuchi2010/FS




1 35/12 1 Yes 1 Yes 1 8

Kriplani2011/JMIG




1 18/12 0 Yes 1 No 0 5

Cases: JuvenileAcien 2012/HR Retro 0 3 0 U/S, MRI JCA (reported

as ACUM)1 NA 0 Surgical

recordsOpen excisiona 1 Self-report 0 2/12 0 NA 0 No 0 2

Chun2011/JLAST

Retro 0 <5 1 MRI JCA 1 NA 0 Surgicalrecords



Acien2010/O&G

Retro 0 <25 2 U/S, MRI JCA (reportedas ACUM)


Open excisiona 1 Self-report 0 18/12 0 NA 0 No 0 2

Akar2010/F&S

Retro 0 <25 1 U/S JCA 1 NA 0 Surgicalrecords

Roboticexcision/classictechnique


Liang2010/F&S

Retro 0 <25 1 U/S JCA (reportedas ACUM)



Ball2009/GynSurg

Retro 0 <25 1 U/S JCA 1 NA 0 Surgicalrecords



Ho2009/JPAG

Retro 0 <25 1 U/S, MRI JCA 1 NA 0 Surgicalrecords

Open excisiona 1 Self-report 0 NA 0 NA 0 No 0 2

Dogan2008/AOG

Retro 0 1 0 MRI JCA 1 NA 0 Surgicalrecords



Nabeshima2008/JMIG




Kamio2007/JOGR


Openexcisiona


Takeda2007/JMIG




Nabeshima2003/JAAGL




Potter 1998/F&S Retro 0 1 0 U/S JCA (reportedas ACUM)



Tamura1996/TJEM

Retro 0 1 0 U/S, MRI JCA 1 NA 0 Surgicalrecords


Cases: adults


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Continued.


No. ofpatients

Modality of initialdiagnosis/definitionof extent of the

diseaseRepresentativeness

of the casesAscertainment of exposure/detailed

surgical techniqueOutcomeevaluation

Followup/adequate

length


Statisticalanalysis

Totalgrade

Acien2010/O&G

Retro 0 1 0 U/S, MRI Cysticadenomyoma(reported asACUM)



Ors 2009/Anatol Retro 0 1 0 U/S, MRI Cysticadenomyoma(Focaladenomyosis)




Protopapas2008

Retro 0 3 0 U/S Cysticadenomyoma(Focaladenomyosis)



Wang JH2007/FS





Iribarne1994, JCUS





Parulekar1990/JPGM





Note: HSG ¼ hysterosalpingogram; JCA ¼ juvenile cystic adenomyoma; Lap ¼ laparoscopic; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; U/S ¼ ultrasound.a Unclear description of the radicality of adenomyotic tissue excision.


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Nonexcisional techniques of surgical treatment of adenomyosis: quality assessment of the relevant studies.


No. ofPatients


of extent of the diseaseRepresentativeness

of the cases

Ascertainment ofexposure/detailedsurgical technique

Outcomeevaluation

Followup/adequate

length


Statisticalanalysis

Totalgrade

Kang2009/JMIG



Laparoscopicpartial resectionof adenomyosisþ UAO


1 12/12 0 Yes 1 Yes 1 7

Wang2002/JAAGL

Pro 1 20 0 U/S, MRI Uncleardescription of lesion


Laparoscopicuterine arteryligation


1 8/12 0 Yes 1 Yes 1 6

Wood1998/HRU



Myometrialelectrocoagulation


Philips1996/JAAGL

Pro 1 10 0 MRI Unclear descriptionof lesion


Laparoscopic bipolarcoagulation


Preutthupan,2010/JOGR



Rollerball endometrialablation


Fernadez2007/JMIG

Retro 0 1 0 U/S Diffuse adenomyosis 1 NA 0 Surgicalrecords

Operativehysteroscopy


Kumar2007/JMIG

Retro 0 1 0 Clinical Unclear descriptionof lesion


TCRE 1 Self-report 0 18/12 0 NA 0 No 0 1

Giana2005/EJGO

Retro 0 1 0 U/S Focaladenomyosis (cysticadenomyoma)


Resectoscope 1 Self-report 0 6/12 0 NA 0 No 0 2

Maia2003/JAAGL

Retro 0 95 1 U/S Unclear descriptionof lesion


TCRE � Mirena 1 Self-report 0 12/12 0 Yes 1 Yes 1 5

Wood1998/HRU



Endomyometrialresection


Yang 2009/FS Pro 1 7 0 U/S Focal adenomyosis 1 Consecutive 1 Surgicalrecords

Open HIFU 1 NA 0 NA 0 NA 0 Yes 1 4

Furman2007/UOG

Retro 0 1 0 U/S Focal Adenomyosis(cystic adenomyoma)


U/S aspiration,alcohol instillation


Ryo 2006/JRM Retro 0 1 0 U/S Focal Adenomyosis(cystic adenomyoma)


Radiofrequencyablation


Kanaoka2004/Osaka

Retro 0 1 0 MRI Diffuse adenomyosis 1 NA 0 Surgicalrecords

MEA 1 Self-report 0 12/12 0 NA 0 No 0 2

Chan2001/Med JMalaysia

Retro 0 1 0 U/S Diffuse adenomyosis 1 NA 0 Surgicalrecords

Balloonthermoablation


1 36/12 1 NA 0 No 0 4

Note: HIFU ¼ high-intensity focal ultrasound; HSG ¼ hysterosalpingogram; JCA ¼ juvenile cystic adenomyoma; Lap ¼ laparoscopic; MEA ¼microwave endometrial ablation; MRI ¼magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retro-spective; TCRE ¼ transcervical endometrial resection; UAO ¼ uterine artery occlusion; U/S ¼ ultrasound.


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Uterine Sparring Operative for Adenomyosis