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doi:10.1111/jog.12093

J. Obstet. Gynaecol. Res. Vol. 39, No. 11: 15131517, November 2013

AllenMasters syndrome: Do the classic risk factors also apply in patients with endometriosis?
Dietmar Haas1,4, Peter Oppelt1,4, Omar Shebl2, Radek Chvatal1, Andreas Shamiyeh3, Richard Mayer2 and Helge Binder5
1 Department of Obstetrics and Gynecology, Linz General Hospital, Linz, 2Linz Womens General Hospital, Linz, 3Ludwig Boltzmann Institute for Operative Laparoscopy, 2nd Surgical Department, Linz General Hospital, Linz, Austria; 4Department of Gynecology, Erlangen University Hospital, Erlangen, Germany; and 5Kantonsspital Uri, Department of Obstetrics and Gynecology, Altdorf, Switzerland

Abstract
Aim: To evaluate whether the classic risk factors for AllenMasters syndrome, such as body mass index (BMI) and spontaneous births, are in fact responsible for the condition in patients with endometriosis. Methods: A total of 26 women who underwent a laparoscopic procedure due to chronic pelvic pain, Allen Masters syndrome and endometriosis from 20092011 were enrolled in this study from an endometriosis competence center specializing in minimally invasive surgery. This was a retrospective cohort study (Canadian Task Force classication II-2). Results: Only eight of the 26 patients (30.77%; 95% condence interval [CI], 14.3351.79%) had the classic risk factors (BMI >25 kg/m2 and/or at least one spontaneous birth). The mean age in the study group was 32.08 years (SD 5.45). The patients had a mean BMI (kg/m2) of 19.61 (SD 3.07). The means for the patients clinical data were 0.88 (SD 1.53) pregnancies, 0.81 (SD 1.23) for parity, 0.27 (SD 0.60) for cesareans and 0.54 (SD 0.99) for spontaneous births. The revised American Society for Reproductive Medicine (rASRM) stage showed a median of grade III. The left side of the posterior compartment was more often affected (73.1% of cases) than the right side in all patients. Conclusion: In all, 69.23% of the cases (95% CI, 48.2185.67%) were not explained by the classic risk factors. In view of the absence of other diseases and otherwise unremarkable parameters, we consider mechanical damage of the lesser pelvis not to be solely responsible for AMS. Further observations in patients with AMS, with and without endometriosis, may be able to contribute to research into the actual etiology of the condition. Key words: AllenMasters syndrome, body mass index, chronic pelvic pain, endometriosis, laparoscopy.

Introduction
In a study published in 1955, Allen and Masters described traumatic laceration of uterine support as a syndrome characterized by a laceration in the posterior leaf of the broad ligament.1 AllenMasters syndrome

(AMS) is associated with an abnormally mobile cervix, described as having a universal joint type of mobility. The condition is mainly attributed to traumatic lacerations of the broad ligament during birth. In AMS, the peritoneum loses its elasticity, becomes thin and is often missing completely. Body mass index (BMI) and

Received: December 5 2012. Accepted: February 1 2013. Reprint request to: Dr Dietmar Haas, Allgemeines Krankenhaus Linz, Abteilung fr Gynkologie und Geburtshilfe, Krankenhausstrasse 9, A-4021 Linz, Austria. Email: dr.haas@hotmail.com The paper has not previously been presented at any meeting or conference. Conicts of interest: The authors hereby state that there were no conicts of interest. Funding support: None.

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spontaneous birth are considered to be major contributing factors.2 Clinically, AMS is associated with chronic pelvic pain (CPP), dyspareunia, menstrual disturbances and back pain.1,3 Due to the similar clinical symptoms in AMS and endometriosis, several studies have been carried out on the connections between AMS, endometriosis and CPP. The results have shown sometimes quite widely differing views on the etiology of AMS.4 Zivi et al. and Tischendorf traced AMS to traumatic lacerations of the uterine supporting apparatus during birth.5,6 Chatman described 25 cases of AMS diagnosed during 635 diagnostic laparoscopies carried out when investigating CPP. He attributed the etiology of AMS to endometriosis, which was strongly associated with AMS in 68% of the cases.7 Priou et al. reported a 22.2% prevalence of endometriosis and a 3.2% prevalence of AMS in patients with chronic pelvic pain.8 The aim of the present study was to assess whether the classic risk factors for AMS, such as BMI and spontaneous birth, do also apply in patients with endometriosis. For this purpose, endometriosis patients with AMS and CPP were examined for possible inuencing factors.

the pelvis affected by AMS, and the revised American Society for Reproductive Medicine (rASRM) score (grades IIV). To begin with, the data for the overall group were analyzed; the group was then divided into a subgroup typical for AMS (BMI >25 and/or at least one spontaneous birth) and a subgroup atypical for AMS (BMI 25). The BMI cut-off point was selected on the basis of the World Health Organization categories.9 Measures of location and dispersion, and frequencies with exact two-sided 95% condence intervals, were calculated for the two subgroups. Finally, statistical comparison of the subgroups was carried out.

Methods
Institutional review board approval was obtained (K-21-12). A total of 26 endometriosis patients with AMS and CPP underwent laparoscopic surgery in the Department of Gynecology and Obstetrics at Linz General Hospital between 1 January 2009 and 31 December 2011 (n = 26, study group). Criteria for inclusion in the study were: endometriosis with postoperative histological conrmation; CPP, dened as lower abdominal pain that had persisted for at least 6 months; clinical cervical hypermobility and intraoperatively identied AMS with peritoneal defects and photographic documentation. Operative photographs were reviewed for all cases by two different surgeons, each of whom had previously carried out at least 200 laparoscopies. Exclusion criteria were any other diseases diagnosed that could lead to pelvic pain and any previous operations capable of leading to iatrogenic lesions of the broad ligament. The clinical parameters for which data were collected preoperatively were age, BMI (kg/m2), number of pregnancies, total number of births, number of cesarean sections, number of spontaneous births, the side of

Statistics Exact two-sided 95% condence intervals (95% CI) were calculated for prevalence. All datasets for metric variables were tested for normal distribution using the KolmogorovSmirnov test with Lilliefors signicance correction (type I error = 10%). As none of these datasets showed a normal distribution, the exact MannWhitney U-test was used for subgroup comparisons both of metric variables and of variables measured on ordinal scales. Data for dichotomous variables were compared using Fishers exact test. All of the tests were two-tailed, with a condence level of 95% (P < 0.05). No adjustment for type I error was made, and the relevant P-values are therefore only descriptive. The statistical program BIAS 10.0 was used for the calculations.

Results
The mean age in the study group (n = 26) was 32.08 years (standard deviation [SD] 5.45). The patients had a mean BMI (kg/m2) of 19.61 (SD 3.07). The means for the patients clinical data were 0.88 (SD 1.53) pregnancies, 0.81 (SD 1.23) parity, 0.27 (SD 0.60) cesarean sections and 0.54 (SD 0.99) spontaneous births. All of the pregnancies were achieved spontaneously, without the aid of assisted reproductive techniques. The rASRM stage showed a median of grade III. Seven patients (26.9%) had a history including at least one spontaneous birth. BMI of more than 25 kg/m2 was noted in two patients (7.7%). One of these patients had both a spontaneous birth and also BMI of more than 25 kg/m2, and there was thus a typical AMS (tAMS) subgroup of eight patients. The other 18 patients had no spontaneous births (73.1%)

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Table 1 Distribution of spontaneous births in the typical AllenMasters syndrome subgroup Spontaneous births (n) 0 1 2 3 Total
Body mass index > 25 kg/m2.

Patients n 1 2 3 2 8 % 12.5 25.0 37.5 25.0 100.0

Table 2 The revised American Society for Reproductive Medicine (rASRM) score in the typical and atypical AllenMasters syndrome subgroups (tAMS and aAMS) rASRM score n 1 2 3 4 Total 1 1 4 2 8
t

AMS % 12.5 12.5 50.0 25.0 100.0

n 2 3 3 10 18

AMS % 11.1 16.7 16.7 55.6 100.0

n 3 4 7 12 26

Total % 11.5 15.4 26.9 46.2 100.0

and BMI of 25 kg/m2 or less (92.3%). These 18 patients formed an atypical AMS (aAMS) subgroup. The mean ages in the tAMS and aAMS subgroups were 32.38 (SD 5.41) and 31.94 (SD 5.41) years, respectively. The mean BMI was 20.66 kg/m2 (SD 4.00) in the tAMS group and 19.14 (SD 2.55) kg/m2 in the aAMS group. Three patients in the aAMS subgroup had a history including one cesarean, and one patient had had two cesareans. The numbers of spontaneous births in the tAMS subgroup are shown in Table 1. Overall, the left side of the posterior compartment was more often affected (73.1% of cases; tAMS 75.0%, aAMS 72.2%) than the right side. The rASRM stages in the two subgroups are shown in Table 2. Table 3 presents subgroup comparisons between the tAMS and aAMS groups. The statistical proportion of AMS patients who had the classic risk factors of BMI and spontaneous birth (tAMS) was 30.77% (95% CI, 14.3351.79%). The proportion of atypical patients was 69.23% (95% CI, 48.2185.67%).

Discussion
Remarkably, only eight of the 26 patients (30.77%; 95% CI, 14.3351.79%) had the classic risk factors (BMI >25 kg/m2 and/or at least one spontaneous birth). No signicant differences were observed in the subgroup

analysis between this risk group (tAMS) and the atypical group (aAMS) with regard to clinical data. Age, the side affected, and also the rASRM scores showed no signicant differences (Table 3). The signicant parameters of spontaneous birth, parity and pregnancy only reect the distribution into these two subgroups based on spontaneous births. The result showing that BMI did not differ signicantly between the two groups is all the more surprising, although this was also a factor in assignment to the tAMS group. This is because the mean BMI in the tAMS subgroup was only 20.66 kg/m2 (SD 4.00). Only 30.77% (95% CI, 14.33 51.79%) of the cases can thus be explained on the basis of the classic symptoms. Cases of AMS without the typical risk factors and trauma have previously been reported in the published work.3,10 The selection of the study group has both advantages and disadvantages. Many of the previous studies on the topic were based on the symptom of CPP. However, CPP can have many possible causes7,8,11 and involves a heavy selection bias. As a cardinal symptom of AMS, CPP has similarities with endometriosis, often described in the previous studies as a comorbid condition. To reduce the selection bias, the present study only included endometriosis patients with CPP and AMS, with other diseases being treated as an exclusion criterion. Based on De Lanceys anatomy12 of the lesser pelvic suspensory apparatus and the new systematization of the parametria to lateral, dorsal and ventral aspects, the description of traumatic lacerations of the broad ligament during birth does not stand up as well as the theory of purely mechanical damage. If AMS were a result of mechanical damage, then the causes of pathological traction would have to be apparent all over the endopelvic fascia. It is not only a descriptive problem, but a functional one as well. The fascia endopelvina consists of connective tissue of varying density that lls the spaces between the individual parts of the levator and obturator muscles. It continues to the pelvic wall (fascia endopelvina parietalis). It lines the preformed pathways for neurovascular bundles. In this way, it afxes the organs elastically and allows limited motion along all of the axes (fascia endopelvina conjugans). In AMS, the peritoneum loses its elasticity, becomes thin and is often missing completely, and the defect continues as far as the paravesical fossa. In extreme cases, the round ligament lies isolated, and the two compartments anterior and posterior are connected. The defect is often isolated, with a clear left-side prevalence (73.1%). The reason for this is unclear, but it

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Table 3 Subgroup comparisons between the typical and atypical AllenMasters syndrome groups (tAMS and aAMS; mean + SD) Parameter Age (years) BMI (kg/m2) Pregnancies (n) Parity (n) Cesarean sections (n) Spontaneous births (n) Right side affected by AMS Left side affected by AMS rASRM (median stage)
t

AMS

AMS

P value 0.538 0.452 0.001 0.001 0.896 <0.001 0.216 >0.999 0.365

32.38 (SD 5.93) 20.66 (SD 4.00) 2.25 (SD 2.12) 2.00 (SD 1.51) 0.25 (SD 0.71) 1.75 (SD 1.04) 25.0% 75.0% 3

31.94 (SD 5.41) 19.14 (SD 2.55) 0.28 (SD 0.57) 0.28 (SD 0.57) 0.28 (SD 0.57) 0.00 55.6% 72.2% 4

BMI, body mass index; rASRM, revised American Society for Reproductive Medicine.

has been reported in previous studies.13 The peritoneum lining the defects has a lower density and is sometimes missing altogether. It may be difcult or completely impossible to obtain histological conrmation, due to the absence of material. Another factor that needs to be taken into account is that laparoscopy, with the magnied images it provides, has led to a marked improvement in the visualization of disease conditions during the last few decades. Using diagnostic laparoscopy, for example, several cases of atypical AMS have already been claried and treated which it was not possible to diagnose purely clinically. The authors of these published cases advise that laparoscopy should be used as the diagnostic standard.4,10,14 With detailed imaging and magnication, it is already possible to demonstrate preliminary stages of AMS that present only as thin peritoneum. Further advantages include visualization with the corresponding photographic documentation, and also the exclusion of possible concomitant diseases such as endometriosis. As no other diseases were present and other parameters such as prior trauma were unremarkable, endometriosis appears to be a risk factor in the pathogenesis of AMS. However, the study design does not make it possible to determine the causality or even to assess the extent to which such alleged risk factors and AMS may be associated in patients with endometriosis in general. Requiring both AMS and endometriosis to be present as inclusion criteria and then stating that one leads to the other is not meaningful. There have been studies reporting that inammatory components present in endometriosis are responsible for peritoneal defects and AMS.15 However, it must be noted that it is only the complex of symptoms including an abnormally mobile cervix, CPP and peritoneal defects that fully meets the criteria for AMS.

An absolute limitation in the present study is the fact that its applicability is limited to the study group investigated. However, it was shown that the classic risk factors such as BMI and spontaneous birth are not responsible for AMS in patients with endometriosis in this study group. Further observations with an appropriate study design in larger groups of patients with AMS, with and without endometriosis, may be able to contribute to research into the actual etiology of the condition.

References
1. Allen WM, Masters WH. Traumatic laceration of uterine support; the clinical syndrome and the operative treatment. Am J Obstet Gynecol 1955; 70: 500513. 2. Lukanova M, Tatarova S, Popov I. Diagnostic approach to AllenMasters syndrome. Akush Ginekol (Soia) 2005; 44 (Suppl 2): 715. Bulgarian. 3. Gupta R, Elakkary E, Sadek M, Lakra Y. Masters Allen syndrome: A review. Dig Dis Sci 2007; 52: 17491751. 4. Ventolini G, Neiger R. AllenMasters syndrome detected at the time of a cesarean delivery: A case report and a review of the literature. J Gynecol Surg 2007; 23: 117120. 5. Zivi E, Maor-Sagy E, Ben-Shushan A, Rojansky N. Chronic pelvic pain and AllenMasters syndrome. Harefuah 2009; 148: 424426. 477. Hebrew. 6. Tischendorf D. The AllenMasters syndrome. Zentralbl Gynakol 1977; 99: 11971199. German. 7. Chatman DL. Pelvic peritoneal defects and endometriosis: AllenMasters syndrome revisited. Fertil Steril 1981; 36: 751 756. 8. Priou G, Arvis P, Rind A, Fraisse E, Grall JY. The diagnostic value of celioscopy in the evaluation of chronic pelvic pain. Apropos of 184 cases. J Gynecol Obstet Biol Reprod (Paris) 1984; 13: 395402. French. 9. WHO. Obesity: Preventing and Managing the Global Epidemic. Report of A WHO Consultation. (WHO Technical Report Series 894). Geneva: World Health Organization, 2000. 10. Onida S, Lynes K, Ozdemir BA, Whitehouse PA. Unexpected ndings at diagnostic laparoscopy: Caecal incarceration with

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concurrent appendicitis in a patient with bilateral broad ligament defects. Ann R Coll Surg Engl 2010; 92: W19W20. 11. Fauconnier A, Dubuisson JB, Foulot H et al. Mobile uterine retroversion is associated with dyspareunia and dysmenorrhea in an unselected population of women. Eur J Obstet Gynecol Reprod Biol 2006; 127: 252256. 12. De Lancey JO. Surgical anatomy of the female pelvis. In: Rock JA, Jones HW (eds). Te Lindes Operative Gynecology, 9th edn. Philadelphia: Lippincott, Williams, and Wilkins, 2003; 6393.

13. Batt RE. AllenMasters syndrome is caused by trauma, not by endometriosis. J Am Assoc Gynecol Laparosc 1995; 2: 245 247. 14. Agresta F, Michelet I, Candiotto E, Bedin N. Incarcerated internal hernia of the small intestine through a breach of the broad ligament: Two cases and a literature review. JSLS 2007; 11: 255257. 15. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril 2012; 98: 511519.

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