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AJR 2003; 180:1291-1296
© American Roentgen Ray Society


Fast Breath-Hold T2-Weighted MR Imaging Reduces Interobserver Variability in the Diagnosis of Adenomyosis

Marc Bazot1, Emile Daraï2, Sébastien Clément de Givry1, Frank Boudghène1, Serge Uzan2 and Alain Ferdinand Le Blanche1

1 Department of Radiology, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris, 4 rue de la Chine, 75020 Paris, France.
2 Department of Obstetrics and Gynecology, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris, 75020 Paris, France.

Received April 15, 2002; accepted after revision September 26, 2002.

 
Address correspondence to M. Bazot.


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. We compared two rapid MR imaging T2-weighted pulse sequences with high-resolution turbo spin-echo for the diagnosis of adenomyosis, and we evaluated interob-server variability.

SUBJECTS AND METHODS. Fifty-six consecutive patients referred for hysterectomy prospectively underwent MR imaging. Two fast pulse sequences using a breath-hold technique—true fast imaging with steady-state free precession (FISP) and turbo inversion recovery—and turbo spin-echo T2-weighted images of the pelvis were obtained in each patient. The images were analyzed in a blinded manner and independently by three reviewers with different levels of experience for the accuracy of adenomyosis diagnosis, image quality, anatomic visualization, and image artifacts. The accuracy for the diagnosis of adenomyosis on turbo spin-echo T2-weighted imaging combined with one or two fast pulse sequences was evaluated for each reviewer.

RESULTS. Twenty-four patients (42.9%) had a histologic diagnosis of adenomyosis. The accuracy for the diagnosis of adenomyosis for reviewers 1, 2, and 3 using turbo spin-echo T2-weighted, true FISP, and turbo inversion recovery sequences was 83.9%, 67.8%, 75%; 83.9%, 67.8, 78.5%; and 87.5%, 73.2%, and 75%, respectively. A difference in the accuracy rate was found among the observers for the three sequences (p < 0.001). Whatever the pulse sequence, the accuracy rate was higher for the reviewer with more experience in gynecologic imaging. The combination of turbo spin-echo T2-weighted imaging with at least one rapid sequence increased the accuracy of observers with little experience in gynecology. With turbo inversion recovery sequences, the image quality score was low for the three reviewers compared with turbo spin-echo T2-weighted and true FISP sequences. The combination of turbo spin-echo T2-weighted and true FISP sequences gave the highest image quality scores.

CONCLUSION. Breath-hold T2-weighted sequences optimize the accuracy of MR imaging for the diagnosis of adenomyosis and reduce interobserver variability.


Introduction
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Adenomyosis, a common gynecologic disorder, is defined by the presence of ectopic endometrial glands and stroma in the myometrium. Adenomyosis is a source of pain, dysmenorrhea, and menometrorrhagia [1]. The diagnosis of adenomyosis is based on clinical symptoms and is confirmed by further investigations. Sonography is the primary imaging method used to investigate suspected adenomyosis [2]. In selected women with isolated menometrorrhagia, Fedele et al. [3] reported a high accuracy of transvaginal sonography (sensitivity and specificity of 80% and 74%, respectively). However, in unselected patients and in women with associated gynecologic disorders, the sensitivity and specificity of transvaginal sonography for the diagnosis of adenomyosis range from 53% to 89% and from 50% to 89%, respectively [2, 3, 4, 5, 6].

To improve the diagnosis of adenomyosis, most authors recommend the use of MR imaging, particularly in patients with associated gynecologic disorders [6, 7]. Various MR imaging criteria have been proposed, including the thickness of the junctional zone, the presence of an ill-defined, relatively homogeneous low-signal-intensity area of myometrium, and the presence of high-intensity foci in the myometrium [4, 5, 6]. Nevertheless, the sensitivity and specificity of MR imaging for the diagnosis of adenomyosis range from 77.5% to 89% and from 67% to 92.5% [4, 5, 6]. These discrepancies could be explained by differences in the pathologic criteria used for adenomyosis, MR imaging criteria and techniques, and the gynecologic experience of radiologists.

The aims of this prospective study were to evaluate, in addition to turbo spin-echo T2-weighted sequences, the accuracy of breath-hold fast sequences using turbo inversion recovery and true fast imaging with steady-state free precession (FISP) for the diagnosis of adenomyosis, and intra- and interobserver variability with these methods.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Patients
From October 1997 to December 1998, 293 patients at our institution underwent MR imaging for gynecologic disorders. Of these, 63 underwent hysterectomy. Fifty-six of the 63 women underwent MR imaging with turbo spin-echo T2-weighted, turbo inversion recovery, and true FISP sequences. The 56 women composing the study population had a mean age of 51 years (range, 38-73 years). Among the 56 women, 48 (85.7%) were premenopausal and eight (14.3%), postmenopausal. The indications for surgery were menorrhagia or metrorrhagia (n = 37), postmenopausal bleeding (n = 9), adnexal masses (n = 4), genital prolapse (n = 2), and cervical intraepithelial neoplasia (n = 4). All hysterectomies were performed between 1 day and 3 months after MR imaging.

MR Imaging Technique
MR imaging was performed on a 1.5-T system (Magnetom Vision; Siemens, Erlangen, Germany) with a phased array body coil. Patients were required to fast for 3 hr before MR imaging. Antispasmodic drugs were not used. T2-weighted turbo spin-echo images were acquired in the sagittal and oblique axial or coronal planes (short axis of the uterus) with the following parameters: TR/TE, 4500/128; echo-train length, 23; slice thickness, 5 mm; interslice gap, 10%; rectangular field of view, 280 x 245 mm; and matrix, 224 x 512. The phaseencoding axis was in the anteroposterior direction for sagittal images and right-to-left for axial images. Using abdominal compression, we acquired MR imaging sections every 5 mm with a gap of 1 mm. These parameters yielded 16 sections in 3 min 58 sec. Respiratory compensation and fat suppression were not used.

In addition, two breath-hold fast T2-weighted pulse sequences, one true FISP sequence, and one turbo inversion recovery sequence in the sagittal and axial planes were performed. The true FISP sequence was acquired with the following parameters: 6.3/3; flip angle, 70°; slice thickness, 5 mm; rectangular field of view, 320 x 240 mm; and matrix, 256 x 198. These parameters yielded 12 sections in 18 sec. The turbo inversion recovery sequence was acquired with the following parameters: 3905/76; inversion time, 150 msec; echo-train length, 150; slice thickness, 7 mm; rectangular field of view, 320 x 240 mm; and matrix, 256 x 224. These parameters yielded 11 sections in 20 sec.

MR Imaging Criteria for Diagnosing Adenomyosis
Adenomyosis was defined as a junctional zone of at least 12 mm or an ill-defined low-signal-intensity area of myometrium or punctuate high-intensity myometrial foci [5]. Adenomyosis was classified according to its uterine location and size, but no attempt was made to grade the depth of myometrial involvement in this study.

Accuracy of MR Imaging Diagnosis
MR images were analyzed by three reviewers, radiologists who had different levels of experience in MR imaging of the female pelvis. Reviewer 1 (an M.D.) was highly experienced in female pelvic imaging, reviewer 2 (an M.D./Ph.D.) was highly experienced in upper abdominal and vascular MR imaging, and reviewer 3 (a fellow) was being trained in MR imaging but had performed more than 150 MR imaging examinations of the female pelvis over a 6-month period. The diagnosis of adenomyosis was based on previously described criteria. To ensure consistency, before reviewing the study images, the three reviewers were presented with five selected nonstudy cases serving as examples. The reviewers were informed of the sequence type.

The accuracy rate of each reviewer for the diagnosis of adenomyosis was evaluated, in light of the histologic results, separately for the turbo spinecho T2-weighted, turbo inversion recovery, and true FISP sequences.

For combinations of two MR imaging sequences, the diagnosis of adenomyosis was made when one sequence suggested the diagnosis. For the combination of the three MR imaging sequences, the diagnosis of adenomyosis was made when at least two sequences suggested the diagnosis.

Qualitative Image Analysis
Qualitative analysis was performed by three radiologists who were unaware of the patients' clinical histories and pathologic results. Initially, sets of images acquired with each of the three sequences were randomly presented independently to each of the three radiologists, who assigned image quality scores of 0, 1, 2, or 3, for poor, moderate, good, and excellent image quality and anatomic visualization (delineation of the contours and depiction of the zonal anatomy of the uterus). The presence of image artifacts (respiratory and peristalsis artifacts, artifacts due to pulsation of large vessels, and chemical shift artifacts) was scored 0, 1, 2, or 3, representing severe, moderate, mild, or absent artifacts. For each patient and each sequence, the image quality, anatomic visualization, and image artifacts scores were calculated.

Histopathologic Findings
Histopathologic examination was performed by a single pathologist who was unaware of MR imaging data. Gross and microscopic histopathologic examinations were performed according to the method of Siegler and Camillien [8]. Specimens were oriented by a fixed mark on the anterior uterine wall. Uterus weight, macroscopic appearance, and associated pathologic abnormalities were recorded. Fundal, anterior, posterior, right, and left maximal uterine wall thickness were measured.

Macroscopically, adenomyosis was diagnosed in the presence of an enlarged uterus, a globular and asymmetric uterus, and a dense anarchically fasciculated unlimited myometrium with small cavities (0.5-10 mm). Focal adenomyosis was defined as the presence of adenomyoma (circumscribed nodular lesion) mimicking intramural myoma, or when lesions were restricted to one uterine wall (localized adenomyosis). In other cases, adenomyosis was defined as diffuse lesions.

Block sections were taken from the fundal, anterior, posterior, right, and left uterine walls, and from macroscopically abnormal areas. The number of slides ranged from five to 15, depending on myometrial thickness.

Histopathologic criteria for the diagnosis of adenomyosis included the presence of ectopic endometrial tissue in the myometrium located 2.5 mm beyond the endometrial-myometrial junction. The presence of smooth-muscle cells surrounding ectopic endometrial areas was noted. Adenomyosis was graded according to the depth of myometrial involvement, grades 1, 2, and 3 corresponding respectively to adenomyotic involvement of the inner third (superficial adenomyosis), two thirds, or entire (deep adenomyosis) myometrial thickness. Adenomyosis was also graded as mild, moderate, or severe according to the number of endometrial islets observed (one to three, four to nine, or 10 or more foci, respectively).

Statistical Analysis
Sensitivity, specificity, and positive and negative predictive values were calculated for each pulse sequence for each observer. Statistical analysis was performed using the chi-square, Kruskall-Wallis, and Mann-Whitney tests, as appropriate. Values for p of less than 0.05 were considered to denote significance.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Histopathologic Findings
Twenty-four patients (42.9%) had a histologic diagnosis of adenomyosis. Adenomyomas were found in four (16.7%) of the 24 patients. The adenomyosis was fundal in 14 patients, posterior in 13, anterior in 12, left-sided in six, and right-sided in five.

Fifteen (62.5%) of the 24 patients had diffuse adenomyosis, including two patients with associated adenomyoma. Nine (37.5%) of the 24 patients were diagnosed with focal adenomyosis, including two women with an adenomyoma and seven with localized adenomyosis.

The adenomyosis was grade 1 in six patients, grade 2 in nine, and grade 3 in nine, respectively. The degree of adenomyosis was minimal in nine patients, moderate in seven, and severe in eight.

Adenomyotic uteri were associated with other pelvic disorders in 20 patients (83.3%). Of these patients, 17 (85%) had uterine myomas.

MR Imaging Diagnosis of Adenomyosis
The sensitivity, specificity, and positive and negative predictive values of turbo spin-echo T2-weighted imaging, turbo inversion recovery, and true FISP for the diagnosis of adenomyosis are given in Table 1 for each observer.


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TABLE 1 Performance of Turbo Spin-Echo T2-Weighted, True FISP, and Turbo Inversion Recovery MR Imaging for Diagnosis of Adenomyosis

 

On turbo spin-echo T2-weighted imaging, the numbers of false-negative findings were six, 12, and 12, respectively, for reviewers 1, 2, and 3. The numbers of false-positive findings were three, six, and two, respectively, for reviewers 1, 2, and 3. The accuracy rates for the diagnosis of adenomyosis differed significantly among the three reviewers (p < 0.0001). The accuracy was higher for reviewer 1 than for reviewers 2 and 3 (p < 0.01) and higher for reviewer 3 than for reviewer 2 (p < 0.01).

On true FISP sequences, the number of false-negative findings was seven for each reviewer.

The numbers of false-positive findings were two, 10, and five, respectively, for reviewers 1, 2, and 3. For the diagnosis of adenomyosis, the accuracy rate differed significantly among the three reviewers (p < 0.0001). The accuracy rate was higher for reviewer 1 than for reviewers 2 and 3 (p < 0.01) and higher for reviewer 3 than for reviewer 2 (p < 0.01).

On the turbo inversion recovery sequence, the numbers of false-negative findings were seven, 12, and 11, respectively, for reviewers 1, 2, and 3. The respective numbers of false-positive findings were three, five, and three. Accuracy for the diagnosis of adenomyosis differed significantly among the three reviewers (p < 0.0001). Accuracy was significantly higher for reviewer 1 than for reviewers 2 and 3 (p < 0.001); no difference was found between reviewers 2 and 3.

No intraobserver variability was observed according to the type of MR imaging sequence.

Accuracy for the Diagnosis of Adenomyosis with Combinations of the Three MR Imaging Sequences
The sensitivity, specificity, and positive and negative predictive values of turbo spin-echo T2-weighted combined with turbo inversion recovery sequences, of turbo spin-echo T2-weighted combined with true FISP images, and of turbo spin-echo T2-weighted combined with turbo inversion recovery and true FISP sequences, are given in Tables 2 and 3 for each reviewer.


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TABLE 2 Performance of Combinations of MR Imaging Sequences in Patients in Whom at Least One Sequence Indicated Adenomyosis

 

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TABLE 3 Performance of Combinations of MR Imaging Sequences in Patients in Whom Two Sequences Indicated Adenomyosis

 

Compared with turbo spin-echo T2-weighted imaging alone, the combination of turbo spin-echo T2-weighted and turbo inversion recovery imaging, and the combination of turbo spin-echo T2-weighted and true FISP imaging, increased the accuracy of reviewer 3 (Table 2).

Compared with turbo spin-echo T2-weighted imaging alone, the combination of the three MR imaging sequences increased the accuracy of reviewer 2 but not that of reviewers 1 and 3.

Quality Scores of Three MR Imaging Sequences
The image quality, anatomic visualization, and image artifacts obtained with turbo spin-echo T2-weighted, turbo inversion recovery, and true FISP sequences are given in Table 4 for each reviewer.


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TABLE 4 Imaging Quality of Three MR Imaging Techniques

 

With turbo spin-echo T2-weighted images, image quality (p = 0.037) and anatomic visualization (p = 0.01) scores differed among the three reviewers. No difference was found for image artifacts among the reviewers (Figs. 1A and 2A).



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Fig. 1A. MR imaging in 44-year-old woman with adenomyosis. Ill-defined hypointense area containing high-intensity spots in posterior myometrium (arrow) is visible on turbo spin-echo T2-weighted image.

 


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Fig. 2A. MR imaging in 40-year-old woman with interstitial posterior and submucosal myomas (arrows) but no adenomyosis. Ghosting artifact seen on turbo spin-echo T2-weighted sequence impairs image quality.

 

With turbo inversion recovery sequences, image quality differed among the three reviewers (p = 0.0001). Anatomic visualization also differed among the three reviewers (p = 0.0002). No difference in image artifacts was noted among the three reviewers (Figs. 1B and 2B).



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Fig. 1B. MR imaging in 44-year-old woman with adenomyosis. Image quality and anatomic visualization are poor on turbo inversion recovery sequence.

 


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Fig. 2B. MR imaging in 40-year-old woman with interstitial posterior and submucosal myomas (arrows) but no adenomyosis. Blurring on turbo inversion recovery sequence impairs image quality.

 

With true FISP sequences, image quality (p = 0.0001), anatomic visualization (p = 0.0001), and image artifacts (p = 0.0001) differed among the three reviewers (Figs. 1C and 2C).



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Fig. 1C. MR imaging in 44-year-old woman with adenomyosis. Anterior image artifacts (arrow) are present on true fast imaging with steady-state free precession.

 


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Fig. 2C. MR imaging in 40-year-old woman with interstitial posterior and submucosal myomas (arrows) but no adenomyosis. True fast imaging with steady-state free precession gives high image quality.

 

With true FISP sequences, scores for image artifacts and image quality were higher for the reviewers with low experience in gynecologic imaging than for turbo inversion recovery or turbo spin-echo sequences. High-quality scores were obtained for image quality and anatomic visualization with both turbo spin-echo T2-weighted and true FISP sequences. Image artifacts were higher with true FISP than with turbo spin-echo T2-weighted imaging. The combination of turbo spin-echo T2-weighted and true FISP sequences gave the highest image quality scores.


Discussion
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
In our study, the histologic rate of adenomyosis (42.9%) was in keeping with the reported prevalence in the general population (24-44%) [5, 6, 9, 10]. The value of preoperative imaging for the diagnosis of adenomyosis varies according to the method used. Sonography, which remains the primary imaging method for suspected adenomyosis, has a sensitivity and specificity of 52.9-89% and 50-89%, respectively [2, 3, 4, 9, 11]. The variable accuracy of transvaginal sonography depends mainly on the sonographic criteria used and on the presence of associated gynecologic disorders such as myomas [6]. To limit false-positive and false-negative diagnoses of adenomyosis in patients with inconclusive sonographic findings, most authors recommend the use of MR imaging [4, 5, 6, 9]. However, the use of MR imaging is limited by its being less available than sonography [12]. As with sonography, the accuracy of MR imaging in the diagnosis of adenomyotic lesions depends on the imaging criteria and the MR imaging technique.

In our study, the sensitivity and specificity of turbo spin-echo T2-weighted sequences for the diagnosis of adenomyosis was 50-75% and 81.2-90.9%, respectively. Our results are partly in agreement with those of previous reports of the sensitivity and specificity of T2-weighted or turbo spin-echo T2-weighted sequences (77.5-89% and 67-92.5%, respectively) [4, 5, 6]. In our experience, the sensitivity of turbo spin-echo T2-weighted sequences for the diagnosis of adenomyosis is relatively low. This wide range of values could be explained by interobserver variability. Our results show that the main factor influencing accuracy was the radiologist's experience in MR imaging of the female pelvis and the MR imaging sequence used. Indeed, the accuracy of reviewer 2 (highly experienced, but not in gynecologic imaging) was lower with turbo spin-echo T2-weighted or true FISP sequences than with turbo inversion recovery sequences.

Radiologists such as reviewer 2 who specialize in upper abdominal MR imaging, prefer rapid MR imaging sequences. As noted in other publications [13, 14], our data suggest that reviewer experience is an important component in achieving high accuracy in the MR imaging diagnosis of adenomyosis. Multicoil high-resolution turbo spin-echo MR imaging is considered the gold standard for investigating the female pelvis [15, 16, 17]. Turbo spin-echo T2-weighted imaging suffers from the long acquisition time and image degradation caused by motion artifacts. Turbo inversion recovery and true FISP sequences eliminate motion artifacts, improve patient acceptance, and are more rapid [12]. In our study, intraobserver accuracy for the diagnosis of adenomyosis was similar whether turbo spin-echo T2-weighted, turbo inversion recovery, or true FISP sequences were used. Recently, the ultrafast half-Fourier single-shot turbo spin-echo sequence has been suggested for female pelvic imaging [18, 19]. Further studies are necessary to evaluate turbo inversion recovery and true FISP sequences compared with the ultrafast half-Fourier single-shot turbo spin-echo sequence.

With turbo spin-echo T2-weighted imaging, we found a difference among the three reviewers in image quality and anatomic visualization but not in the intensity of artifacts. Although turbo spin-echo T2-weighted imaging is associated with high image quality, the incidence of artifacts is high. Our data are in keeping with previous reports that the main limitations of turbo spin-echo T2-weighted imaging in both upper abdominal and pelvic imaging are pulsation artifacts and the magnetic heterogeneity caused by intestinal gas and respiratory motion [13, 15, 16, 20, 21, 22]. Various methods have been recommended to avoid these artifacts, such as abdominal compression and the IV administration of glucagon. Respiratory triggering of the MR acquisition (not available in our unit at the time of this study) requires a longer examination time [23]. Another way of reducing artifacts is to use fast breath-hold MR imaging sequences. In our study, turbo inversion recovery received poor image quality scores for radiologists experienced in gynecologic imaging. In contrast, despite interobserver variability in subjective image quality and artifact intensity, the imaging quality of true FISP appeared to improve the diagnosis of adenomyosis.

We also evaluated the diagnostic value of combining various MR imaging sequences. The combination of turbo spin-echo T2-weighted and turbo inversion recovery sequences, compared with turbo spin-echo T2-weighted sequences alone, increased the accuracy rate of only the reviewer with extensive gynecologic imaging experience. Similar results were obtained with the combination of turbo spin-echo T2-weighted and true FISP sequences. However, with the reduction in motion artifacts on true FISP sequences compared with turbo spin-echo T2-weighted sequences, our results suggest that the best option for the diagnosis of adenomyosis is a combination of turbo spin-echo T2-weighted and true FISP sequences. Further studies are necessary to validate these preliminary results.


References
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

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