1 Departments of Obstetrics and Gynaecology and 2 Radiology I, Klinikum Darmstadt, Academic Teaching Hospital to the University of Frankfurt, Darmstadt, Germany
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Abstract |
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Key words: adenomyosis/archimetra/endometriosis/junctional zone/uterine sonography
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Introduction |
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Materials and methods |
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Of these women 41 (aged 1944 years; mean 32) had a history of infertility of 110 years (mean 4) duration and were suffering from endometriosis as demonstrated by laparoscopy. Almost half of these patients were suffering from minimal or mild endometriosis (n = 20) and the rest from moderate or severe endometriosis (n = 21), according to the revised classification of the American Society of Reproductive Medicine (ASRM) (American Fertility Society, 1985). No additional factors responsible for the infertility could be demonstrated in these patients.
The control group consisted of 33 healthy women (aged 2043 years; mean 32) with their husbands suffering from andrological infertility. In all controls the absence of endometriosis was confirmed by laparoscopy. Patients with irregular menstrual cycles, bleeding disorders or abnormalities of the uterine structure such as fibromas or malformations were excluded from the study. None of the healthy women complained of dysmenorrhoea.
Endovaginal sonography
The sonographic measurements were performed during the follicular (n = 47) and luteal phases (n = 27) of the cycles in both groups. The women were examined before the laparoscopic fertility work-up, hence before the diagnosis of endometriosis was established or excluded.
The analysis of the subendometrial myometrium was performed with a 7.5 MHz vaginal probe (Logiq 500, Kranzbühler, Solingen, Germany). After placing the probe in the dorsal fornix of the vagina, the dominant follicle or corpus luteum was localized. Then a mid-sagittal section of the uterus was adjusted and the endometrium and the myometrial layers were visualized. The layer comprising the subendometrial myometrium could be documented either as a sonographically hypoechoic band (`halo'), which regularly encircled the endometrium as well as the isthmical and cervical parts of the cervical canal, or, on the level of the uterine cavity, as a band with varying echogenicity and width.
The EVS real-time measurements were performed on the height of the transition between the upper and the lower half of the dorsal wall of the uterine corpus. There the diameters of the subendometrial myometrium (`halo') and of the total myometrium were documented by electronic calipers and expressed in millimetres. The sonographic measurements were performed by two investigators (G.K., G.L.). During most of the measurement both investigators were present and there was always consensus with respect to the placement of the calipers.
After each scan a venous blood sample was drawn in order to determine oestradiol and progesterone serum concentrations.
Magnetic resonance imaging
In 15 women with endometriosis aged 2636 years (mean 32) and in five healthy women aged 2536 years (mean 32) the uteri were examined by means of MRI.
The uteri were imaged during the proliferative phase of the cycle by means of a superconducting magnet at 1.0 T (Magnetom Impact, Siemens, Erlangen, Germany) with the use of the body coil. T2-weighted fat-saturated turbospin echo sequences were used (TR/TE 35003800/9099 ms, four acquisitions, slice thickness 34 mm, slice gap 0.1 mm) to obtain sagittal, axial and coronal planes. The image matrix consisted of 256 elements in frequency-encoded direction and of 154220 elements in phase-encoded direction. The field of view was 263x350 mm. All examinations were performed in supine position. In order to compensate for artefacts due to respiratory movements, the abdominal wall was compressed by a broad belt. All patients received an antispasmodic intravenously (hyoscine butylbromide; Buscopanâ; Boehringer, Ingelheim, Germany) to decrease bowel peristalsis. The measurements of total myometrium and the diameters of the subendometrial myometrium (`junctional zone') were performed, as in EVS, in a mid-sagittal plane on the height of the transition between the upper and the lower half of the dorsal wall of the uterine corpus. There the diameters of the subendometrial myometrium and of the total myometrium were documented by electronic calipers and expressed in millimetres.
Hormone measurements
For the measurement of the serum oestradiol and progesterone concentrations, a commercially available radioimmunoassay kit was used (Serono Diagnostics GmBH, Freiburg, Germany).
Statistical analysis
The diameters of the `halo' and the `junctional zone' as well as of the total myometrium, as measured by EVS and MRI respectively, of infertile women with endometriosis were compared with those of women without endometriosis. The statistical analysis was performed using Student's t-test and significance was assumed when P < 0.05.
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Results |
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No relationship was observed between the stage of the endometriotic disease and the mean diameter of the expanded halo.
In individual sonographic scans in women with endometriosis, particularly during the luteal phase, the halo was focally disrupted by areas of higher echogenicity (Figures 3 and 4), while in women without endometriosis the halo was usually intact (Figure 1
top). The disruptions were mostly localised on or close to the sagittal line of the uterine wall.
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Discussion |
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In MRI the endometrium is surrounded by a similar contour of similar width characterized by low signal intensity (Figures 5 and 8). It had been termed the `junctional zone' (Hricak et al., 1983
) because it was considered to represent a hypodense interface between endometrium and myometrium. The stratum subvasculare, however, is directly adjacent to the endometrium (Werth and Grusdew, 1898
; Wetzstein, 1965
; Fujii et al., 1989
; Scoutt et al., 1991
). Thus, the `junctional zone' in MRI represents the archimyometrium (Werth and Grusdew, 1898
; Noe et al., 1999
) as does the halo in sonography (Mitchell et al., 1990
; Reinhold et al., 1996
). The archimyometrium as measured by MRI, however, appears to be broader as measured by EVS (Figures 2 and 8
) (Mitchell et al., 1990
).
The low signal intensity of the archimyometrium in MRI and the apparent difference to the outer myometrial layers, the stratum vasculare and the stratum supravasculare have been discussed by several authors (Lee et al., 1985; Brown et al., 1991
; Scoutt et al., 1991
; Reinhold et al., 1998
; Brosens et al., 1998
). The subendometrial myometrium differs in various respects from the outer two layers. These differences include embryology (Werth and Grusdew, 1898
; Leyendecker et al., 1998
; Noe et al., 1999
), function and activity during the menstrual cycle (Kunz et al., 1996
; Leyendecker et al., 1996
) as well as cellular (Wetzstein, 1965
; Schwalm and Dubrauszky, 1966
; Fujii et al., 1989
; Scoutt et al., 1991
) and biochemical composition (Campbell et al., 1998
; Noe et al., 1999
). Of the myometrial wall only the stratum subvasculare is of paramesonephric origin (Werth et al., 1898; Noe et al., 1999
) and it is the only myometrial layer that is, with its cyclically changing peristaltic contractions, active during the menstrual cycle (Lyons et al., 1991
; Kunz et al., 1996
; Lesny et al., 1998a
,b
). A decrease of the relative content of connective tissue within the myometrium from the two outer to the inner layer (Schwalm and Dubrauszky, 1966
; Brown et al., 1991
) in addition to the more densely packed myocytes of the subendometrial myometrium (Scoutt et al., 1991
) might be related to the specific embryology and function of the stratum subvasculare and might result in the specific image in MRI as well as in the hypoechogenic halo in EVS.
In women with endometriosis this halo or band of low signal intensity is significantly expanded in EVS (Figures 1 and 2) and MRI respectively (Figures 68
). While this could be easily documented in MRI, it was more difficult in EVS and required real-time measurement (Ascher et al., 1994
; Reinhold et al., 1995
, 1996
). In EVS, the expanded halo was in some cases hypoechoic (Figure 1
), in other cases of intermediate echogenicity (Figure 4
) or isoechoic in comparison to the middle layer of the myometrium. With real-time measurements, however, it was always possible to determine the boundary between the expanded halo and the outer myometrium.
There was no relationship between the thickness of the halo in EVS and the stage of the disease. These alterations, however, appear to progress with age since the expanded halo was significantly broader in women older than 31 years as compared to younger women. The thickness of the whole myometrium did not differ between women with and without endometriosis, suggesting that the widening of the halo in women with endometriosis represents, as in adenomyosis, infiltrative growth of endometrium. In all 10 hysterectomy specimens examined from women with endometriosis, infiltrations of endometrial glands with endometrial stroma into the myometrium resulting in the morphological picture of adenomyosis could be observed (M.Herbert, M.Loe, G.Kunz, et al., unpublished observations). Moreover, our findings obtained with EVS and MRI in women with external endometriosis are similar to or do not differ from the respective findings obtained in adenomyosis (Fleischer et al., 1986; Brosens et al., 1995
, 1998
; Reinhold et al., 1995
, 1996
, 1998
), supporting the view that our findings in endometriosis represent endometrial infiltrations into the underlying myometrium.
These data add further evidence to the notion that endometriosis is primarily a disease of the archimetra (Leyendecker et al., 1998) with external endometriosis being a secondary phenomenon, which had been suggested previously on the basis of functional (Leyendecker et al., 1996
), biochemical (Noble, et al, 1996
; Jolicoeur et al., 1998
), immunocytochemical (Wingfield et al., 1995
) and immunological (Leiva et al., 1994
; Ota et al., 1996
, 1997
, 1998
) alterations of the uterus and the eutopic endometrium, respectively, in women with endometriosis.
Moreover, the data provide evidence that endometriosis and adenomyosis are merely clinical variants of the same disease process (Leyendecker et al., 1998), which have been separated from each other in the past due to various reasons such as the prevailing theories of the pathogenesis of endometriosis as well as clinical bias. The theory of transtubal shedding of normal endometrial cells and tissue elements by retrograde menstruations as well as the theory of coelomic metaplasia, (Sampson, 1927
) directed research efforts to the peritoneum as the primary site of disease development. In addition, histological examination of the uterus is usually impossible when endometriosis is diagnosed in a sterile patient and it is unlikely that in the past, when hysterectomies were performed due to symptoms related to adenomyosis, the peritoneum was looked at for endometriotic foci or scars with the same scrutiny as it is done today by laparoscopy during a sterility work-up. That is probably why the reported association between adenomyosis and endometriosis and vice versa varies considerably over a large range (Emge, 1962
; Bird et al., 1972
; Pratt, 1972
). Moreover, strict morphological criteria are required for the diagnosis of adenomyosis that exclude minor infiltrations of endometrium and stroma into the myometrium as insignificant (Emge, 1962
; Bird et al., 1972
; Ferenszy, 1998). Since the adenomyotic nodules, however, communicate with the uterine cavity (Otto, 1957
), pathophysiologically, a continuous process from beginning to deep infiltration must exist. Our data suggest that the process of myometrial infiltration in endometriosis progresses with age.
Whether or not adenomyosis is accompanied by endometriosis may also largely depend on the localization of the active core of the adenomyotic nodule with respect to the proliferative and infiltrative potential of the cells. If this is, as in the beginning of the disease (adenomyosis sub-basalis; Bird et al., 1972), localized in or near the uterine cavity, there may be a great likelihood of transtubal seeding of altered endometrial tissue, which may even be enhanced by hyperperistalsis (Leyendecker et al., 1996) and increased intrauterine pressure (Mäkäräinen, 1988
; Buletti et al., 1997). The transtubal seeding of altered tissue might be impeded when the active core of adenomyosis has grown into the depth of the myometrial wall or may even be terminated when the process of adenomyotic proliferation has `burnt out'. This might be the pathophysiological basis of the notion (Evers, 1994
) that all women might have endometriosis once in their lives. Eventually, an adenomyotic nodule might penetrate the uterine serosa with ensuing massive pelvic endometriosis (Jones and Jones, 1981
).
In view of the fact that normal endometrium exhibits high signal intensity in MRI, which is even higher than that of the middle layer of the myometrium, the question has to be addressed more closely as to why the myometrial area of endometrial infiltration displays low signal intensity similar to the subendometrial myometrium, resulting in the impression of an expanded junctional zone.
Adenomyotic nodules are composed of endometrial glands, stroma and surrounding hyperplastic myometrium (Emge, 1962; Bird et al., 1972
; Ferenszy, 1998; Reinhold et al., 1998
). According to a prior report (Schwalm and Dubrauszky, 1966
), the relative content of muscular versus connective tissue within the myometrium is increasing during pregnancy probably as a consequence of increasing steroid action. In adenomyosis as well as in endometriotic lesions and in the eutopic endometrium of women with endometriosis, a pathological expression of P450-aromatose resulting in elevated tissue concentrations of oestrogen has been demonstrated (Yamamoto et al., 1993
; Noble et al., 1996
, 1997
; Kitawaki et al., 1997
). Thus the lower signal intensity of the myometrium around adenomyotic nodules could result from increased local oestrogenic stimulation and hyperplasia. During pregnancy, however, there is no decrease in the signal intensity of the stratum vasculare. In contrast, the signal intensity of the subendometrial myometrium increases and the zonal differences become indistinct (Willms et al., 1995
).
Alternatively, the hyperplastic myometrium around the adenomyotic nodules may be of paramesonephric origin, as previously suggested (Brosens et al., 1998), thus displaying the same structural characteristics as the stratum subvasculare of the myometrium with its low intensity appearance in MRI. This latter assumption may be derived from the observation that the archimyometrium is a differentiation of the endometrial stroma during embryology (Werth and Grusdew, 1898
) and that during the menstrual cycle constant metaplastic changes between muscular and stromal cells are taking place at the myometrialstromal interface (Fujii et al., 1989
) that could also occur on the level of the infiltrating endometrial glands. Thus, adenomyotic/endometriotic infiltrations into the outer myometrium would consist according to this assumption of all archimetrial components, glandular and stromal endometrium as well as archimyometrium (Leyendecker et al., 1998
; Noe et al., 1999
). This conjecture has been recently supported by our observation that the muscular tissue of the adenomyotic nodules expanding and penetrating into the outer myometrium displays the same cyclic changes of steroid hormone receptor expression as the normal subendometrial myometrium, while the respective receptor expression of the surrounding outer myometrium remains on a constantly high level (Noe et al., 1999; M.Herbertz, M.Noe, G.Kunz, G.Mall, G.Leyendecker, unpublished observations). This characterizes adenomyosis as a disease of the archimetra (Leyendecker et al., 1998
; Noe et al., 1999
). In recto-vaginal endometriosis, with endometrial glands stroma and smooth muscle cells, all three components of the archimetra can be demonstrated. Recto-vaginal endometriosis, however, is believed to result from Müllerian remnants rather than from transplanted endometrium (Nisolle and Donnez, 1997
).
It is well known that the composition of the adenomyotic nodules with respect to the relative distribution of endometrial and myometrial components varies to a large degree (Emge, 1962; Bird et al., 1972
; Ferenszy, 1998; Brosens et al., 1998
; Reinhold et al., 1998
) as does the amount of remaining neometrial myometrium (Noe et al., 1999
) in between the penetrating archimetrial myometrium (M.Herbertz, M.Noe, G.Kunz, G.Mall, G.Leyendecker, unpublished observations). This appears to have a differential impact on the images obtained with MRI and EVS respectively. While in MRI the expanded archimetra usually displays low signal intensity or may appear somewhat patchy (Reinhold et al., 1998; Figure 7
) in comparison to the more homogeneous appearance of the normal subendometrial myometrium, in EVS, the echogenicity of the adenomyotic structures may vary considerably between patients and may even become similar to the surrounding myometrium allowing the determination of the boundary between adenomyotic and normal tissue only by real-time measurements.
This may also explain the finding that the normal archimyometrium appears to be thicker by MRI than by EVS measurement (Figures 2 and 8). In a transitional zone, muscular fibres of the archimyometrium blend with those of the stratum vasculare (Werth and Grusdew, 1898
; Noe et al., 1999
). The changing composition of the tissue within this transitional zone might differentially influence the images produced by MRI and EVS respectively. This might be the morphological basis of the finding that the boundary between the archimyometrium and the outer myometrium is different with MR imaging versus ultrasound (Mitchell et al., 1990
).
We assume that, in the process of developing adenomyosis, archimyometrial expansion is secondary to endometrial infiltration. In MRI, early endometrial infiltration into the archimyometrium should result in focally increased signal intensity. Only following extensive metaplastic change of the endometrial stroma into archimetrial myometrium does either a patchy (Figure 7) image or an image with low signal intensity (Figure 6
) result. In EVS, particularly during the luteal phase, when endometrium exhibits high echogenicity, early infiltration of the endometrium into the underlying myometrium results in the disruption of the normal archimyometrial halo (Figures 3 and 4
). According to our studies, a halo of normal thickness with no signs of focal infiltration is predictive of the absence of endometriosis (Figure 1
top).
In conclusion, infertile women with endometriosis show alterations of the myometrial wall in that, in both EVS and MRI, the archimetra is significantly expanded. These alterations are similar to or identical with those obtained in women with adenomyosis. These data further support the notion that endometriosis is primarily a uterine disease (Leyendecker et al., 1998).
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Notes |
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References |
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Submitted on February 1, 1999; accepted on September 28, 1999.