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Springer Science+Business Media, LLC 2012 Abdom Imaging (2013) 38:193200

Abdominal Published online: 15 April 2012 DOI: 10.1007/s00261-012-9896-0

Imaging

Pelvic inflammatory disease: evaluation of


diagnostic accuracy with conventional MR with
added diffusion-weighted imaging
Wenhua Li,1 Yuzhen Zhang,1 Yanfen Cui,1 Ping Zhang,2 Xiangru Wu3
1
Department of Radiology, Xinhua Hospital Affiliated to Shanghai JiaoTong University School of Medicine, 1665 KongJiang
Road, Shanghai 200092, China
2
Department of Obstetrics and Gynecology, Xinhua Hospital Affiliated to Shanghai JiaoTong University School of Medicine, 1665
KongJiang Road, Shanghai 200092, China
3
Department of Pathology, Xinhua Hospital Affiliated to Shanghai JiaoTong University School of Medicine, 1665 KongJiang
Road, Shanghai 200092, China

Abstract Magnetic resonance (MR) imaging of the pelvic cavity


has gained increasing attention as a powerful diagnostic
Purpose: To determine the incremental value of magnetic tool for the assessment of pelvic diseases [14]. Ultraso-
resonance (MR) diffusion-weighted (DW) imaging for nography (US) is the first-line noninvasive technique
the diagnosis of pelvic inflammatory diseases (PID). for detecting pelvic inflammatory disease (PID), but it is
Materials and methods: We added DW sequences to less accurate for the characterization of complex pelvic
conventional MR imaging in 187 patients with clinically lesions, even when combined with color Doppler
suspected PID. The imaging findings included shape, Imaging. MR imaging has been shown to be more spe-
signal intensity on T1-weighted, T2-weighted, and DW cific and accurate than US assessment for PID, with a
imaging, shade in the peripheral lesions, free pelvic fluid, sensitivity of 95%, a specificity of 89%, and an accuracy
and lymphadenopathy. of 93%, compared with a sensitivity of 81%, a specificity
Results: Laparoscopic and pathological findings con- of 78%, and an accuracy of 80% for US [5].
firmed the diagnosis in all patients. Conventional MR Little data is available on the contribution of MR
findings were consistent with a diagnosis of PID in 90.7% diffusion-weighted (DW) imaging to the accuracy of
(117/129) and of non-PID in 93.3% (28/30) of the 159 diagnosis in PID. DW imaging and the calculated
patients. The sensitivity, specificity, positive predictive apparent diffusion coefcient (ADC) were originally
value, negative predictive value, and accuracy of con- used to demonstrate early ischemic changes in brain tis-
ventional MR imaging findings vs. the addition of DW sue and have also been applied for characterization of
imaging to conventional MR protocols for predicting brain, abdominal, and pelvic tumors [211].
PID were 90.7%, 93.3%, 98.3%, 70.0%, and 91.2% and The purpose of our study, therefore, was to pro-
98.4%, 93.3%, 98.4%, 93.3%, and 97.5%, respectively. spectively evaluate the potential of the addition of DW
Conclusion: The addition of DW sequences to conven- imaging to a conventional MR imaging protocol for
tional MR imaging can improve the accuracy of accurate characterization of PID, using laparoscopy and
diagnosis in PID. surgery as the reference standard.

Key words: OvaryPelvic inammatory disease Materials and methods


Pelvic abscessDiffusion-weighted imaging
Patients
The study was approved by our institutional ethics com-
mittee and written informed consent was obtained from all
patients. Between January 2007 and October 2011, a
DW imaging sequence was added to conventional MR
Correspondence to: Wenhua Li; email: wenhualimyj@sohu.com imaging for each woman with clinically suspected PID.
194 W. Li et al.: Pelvic inflammatory disease

The consecutive population included 187 women, who pathological ndings, in two steps. In the rst step, the
satised the following inclusion criteria: (a) a history of radiologists reviewed the conventional MR images. In
acute pelvic or lower abdominal pain of <3 weeks duration the second step, they reviewed the conventional MR and
with or without fever; (b) the presence of lower abdominal DW images. For both steps, the observers characterized
tenderness; (c) bilateral adnexal tenderness and cervical lesions as PID or non-PID. Discrepancies in interpreta-
motion tenderness; and (d) elevation of C-reactive protein tion were resolved by consensus.
(>10 mg/L). The MR imaging database was reviewed, Conventional MR ndings, including signal intensity
and subjects who subsequently underwent laparoscopy characteristics and morphological appearance of lesions,
and surgery were selected. Patients with endometriomas were evaluated. The normal outer myometrium was used
(n = 17), mature teratomas (n = 6), free pelvic fluid only as a signal intensity (grade 3: low, iso- or intermediate,
(n = 2), and DW imaging artifacts (n = 3) were excluded and high) reference on T1-weighted, T2-weighted and
to limit selection bias. For endometriomas, mature terato- DW images. The diagnosis of PID can be made in the
mas, and free pelvic fluid, conventional MR imaging can presence of the following ndings: a uid-lled tube
provide an appropriate diagnosis. (FFT) in acute salpingitis was diagnosed when a sausage-
The nal cohort included 159 patients (premenopau- like or tortuous, slightly dilated FFT with wall thickening
sal 103 and postmenopausal 56; mean age, 43.5 years; and enhancement, with the tubal content demonstrating
age range, 1872 years). Of the 159 patients, 81.1% (129/ low signal intensity on T1-weighted images and high
159) had laparoscopic and pathologically proven PID. signal intensity on T2-weighted images. A pyosalpinx was
Thirty subjects (18.9%) were shown not to have PID and diagnosed when a dilated tubular structure with thick
were randomly selected to serve as control subjects. enhancing walls was identied with lack of internal
enhancement, and with signal intensity characteristics
similar to those of the FFT. A hydrosalpinx has a similar
MR image acquisition
appearance to the pyosalpinx, with C-, S-, or cystic
In all patients, imaging was performed with a 1.5-T clin- shading with or without plica, but with thin walls. A
ical MR imaging system (Twinspeed, GE Medical Sys- tubo-ovarian or ovarian abscess was dened as an
tems, Milwaukee, WI, USA), using a pelvic phased-array ill-dened adnexal mass with thick regular or irregular
coil. All sequences were acquired with saturation bands enhanced walls containing uid. It usually had low signal
placed anteriorly and posteriorly to eliminate the high intensity on T1-weighted images, high signal intensity on
signal from subcutaneous fat. The imaging protocol was T2-weighted and on DW images, but the signal intensity
comprised of axial non-contrast T1-weighted (TR/TE can vary from low signal intensity on T1-weighted images
range, 400600/1014 ms) and axial T2-weighted (TR/TE to intermediate or high signal intensity on T2-weighted
range, 40006000/100120 ms) imaging performed with a images. An adnexal mass was dened as one that could
chemical shift-selective fat saturation pulse using the fol- not be condently categorized into either an abscess or a
lowing parameters: slice thickness, 6 mm; gap, 1 mm; eld site of origin. A diagnosis of hematosalpinx or fallopian
of view (FOV), 3242 cm; matrix, 256 9 256; and exci- tubal torsion was made on the basis of a blood-containing
tation, 2. Sagittal T1-weighted and T2-weighted (TR/TE dilated tube with high signal intensity on T1-weighted
range, 30006000/100110 ms) fast spin-echo imaging images and high or low signal intensity on T2-weighted
without chemical shift-selective fat saturation pulse was images with possible shading or layering [58].
also performed, as well as post-contrast enhanced-axial All ADC measurements of tubal uid and high signal
and sagittal T1-weighted imaging using the same param- intensity areas of adnexal masses on DW images were
eters described above except that a slice thickness of made by one radiologist, at an Advantage Windows
57 mm was used. DW MRI was acquired in the axial workstation 4.2 (GE Healthcare, Milwaukee, WI), by
plane before administration of contrast medium by using placing freehand regions of interest (ROIs) on DW
a single-shot echo-planar imaging sequence (TR/TE images. ROIs were placed carefully within the center of the
effective range, 800010,000/70100; slice thickness, tubal uid and the high signal intensity areas. To minimize
6 mm; gap, 1 mm; FOV, 3242 cm; matrix, 128 9 128; variability, the largest possible ROIs, which varied from 18
excitation, 2). B values of 0 and 1000 s/mm2 were also to 120 mm2, were manually placed in the target area. When
applied in three orthogonal (Z, Y, and X) directions. the lesion exhibited multiple high signal intensity areas,
ROIs were drawn within the targeted components and the
mean ADC value was used for the results.
MR image analysis
Conventional MR data was analyzed on an Advantage
Windows workstation 4.2 (GE Healthcare, Milwaukee,
Statistical analysis
WI) by two radiologists (who had 11 and 12 years of Laparoscopic and pathological ndings were used as the
experience in pelvic MR imaging, respectively), without reference standard. Mean ADC values were compared
knowledge of clinical presentation and laparoscopic and using a one way analysis of variance and an unpaired t test
W. Li et al.: Pelvic inflammatory disease 195

with a P < 0.05 considered statistically significant. Table 2. Performance of the two blinded observers for the detection of
PID
Quadratic K coefficients were calculated to assess the
interobserver agreement between conventional MR imag- Parameter cMR imaging alone cMR and DW imaging
ing and the combination of conventional MR and DW No. of TP findings 117 127
imaging readers with regard to lesion characterization. A k No. of TN findings 28 28
value of 0.610.80 was indicative of substantial agreement No. of FP findings 2 2
No. of FN findings 12 2
and a value of 0.80 reflected almost perfect agreement. Sensitivity (%) 90.7 98.4
Specificity (%) 93.3 93.3
Results PPV (%) 98.3 98.4
NPV (%) 70.0 93.3
Clinical demographics Accuracy (%) 91.2 97.5

One hundred and fty-nine patients met our inclusion TP true positive, TN true negative, FP false positive, FN false negative,
cMR conventional MR, PPV positive predictive value, NPV negative
criteria. Laparoscopy and surgery were performed within predictive value
2 weeks of MR imaging, and histological ndings are
shown in Table 1.
The signal characteristics of an abscess can demon-
strate considerable variability in MR imaging ndings on
Comparison of conventional MR T1-weighted and T2-weighted images. Among 40 tubo-
and conventional MR with added DW imaging ovarian and ovarian abscess patients, 52.5% (21/40) had
The results in all 159 patients with suspected PID low signal intensity on T1-weighted images and high
revealed considerable variability in MR imaging ndings. signal intensity on T2-weighted images. Of these patients,
However, there was almost complete agreement between 37.5% (15/40) had intermediate or high signal intensity
the radiologists in lesion characterization between con- on T1-weighted images and high signal intensity on
ventional MR imaging and the combination of conven- T2-weighted images, and 35.0% (14/40) had intermediate
tional MR with DW imaging (k = 0.893). Conventional or high signal intensity on T1-weighted images and inter-
MR findings were consistent with a diagnosis of PID in mediate signal intensity (pseudosolid) on T2-weighted
90.7% (117/129) and of non-PID in 93.3% (28/30) of the images. Associated pelvic abscess formation was observed
159 patients. The sensitivity, specificity, positive predic- in 27.5% (11/40). Conventional MR imaging also revealed
tive value (PPV), negative predictive value (NPV), and thickening of the uterosacral ligaments in 68.2% (88/129),
accuracy of conventional MR imaging findings for pre- periovarian stranding and enhancement of the peritoneum
dicting the nature of suspected PID were 90.7%, 93.3%, in 29.5% (38/129), and free pelvic uid in 100% (129/129)
98.3%, 70.0%, and 91.2%, respectively. When DW of patients with PID. Pelvic lymphadenopathy was
imaging was added to conventional MR protocols, the observed in 35.7% (5/14) of those with fallopian tube and
sensitivity, specificity, PPV, NPV, and accuracy of MR ovarian cancers.
imaging findings for predicting PID were 98.4%, 93.3%, Among 12 misclassied patients using conventional
98.4%, 93.3%, and 97.5%, respectively. Thus, the com- MR imaging, 1 pyosalpinx was misclassied as acute
bined imaging strategy may increase the accuracy, sen- salpingitis with a FFT correctly reclassied by taking
sitivity, and NPV of MR imaging for distinguishing PID into account the high signal intensity of luminal uid
from non-PID (Table 2). on DW images with a low ADC value (Fig. 1). Two

Table 1. Summary of patient characteristics (n = 159)


Characteristic Patient no. Distribution Mean ADC value

Patients with PID (n = 129)


FFT with salpingitis 35 Unilateral 21; bilateral 14 2.49 0.24a
Hydrosalpinx 41 Unilateral 9; bilateral 32 2.57 0.21a
Pyosalpinx 13 Unilateral 5; bilateral 8 0.78 0.26b
TOA 19 Unilateral 15; bilateral 6 0.73 0.29b
Ovarian abscess 21 Unilateral 11; bilateral 10 0.74 0.25b
Patients with non-PID (n = 30)
Hematosalpinx 7 Unilateral 7 0.79 0.11b
Tubal torsion 6 Unilateral 6 0.91 0.17b
Tube ligation 2 Bilateral 2 2.57 0.08a
FTC 2 Unilateral 2 2.51 0.06a
Ovarian cancer 12 Unilateral 12 2.41 0.22a

Numbers are expressed as mean SD, or range of ADC values. There is a significant difference between a and b group (P < 0.05). ADC is unit
910-3 mm2/s. The ADC value in the ovarian cancer group is that of the cystic component
PID pelvic inflammatory disease, FFT fluid-filled tube, TOA tubo-ovarian abscess, FTC fallopian tube carcinoma
196 W. Li et al.: Pelvic inflammatory disease

Fig. 1. A 46-year-old woman with a right pyosalpinx. A Axial thickening and enhancement similar to that in acute salpigitis.
T1-weighted image shows a sausage-like tubal structure with D Axial DW images shows a tubal content of high signal
low signal intensity (arrow). B Axial T2-weighted image intensity, representing pus with a low ADC value
reveals that the dilated tube has high signal intensity. C Axial (ADC = 0.763 9 10-3 mm2/s).
contrast-enhanced MR image shows the tube with wall

fallopian tube ligations with hydrosalpinx were misclas- correctly reclassified by taking into account the fact that
sified as chronic salpingitis with hydrosalpinx, and were all intermediate and high signal intensity areas on
not correctly reclassified by the addition of DW imaging T2-weighted images were high signal intensity on DW
to conventional MR protocols. Both of these patients imaging with low ADC values (Fig. 2). Of these 40 tubo-
had similar low signal intensity on T1-weighted and high ovarian and ovarian abscess patients, 72 abscesses were
signal intensity on T2-weighted images, and low signal revealed by DW imaging, but only 46 abscesses were
intensity on DW images as PID patients with hydrosal- confidently found as the missed abscesses were of inter-
pinx and high ADC values. Among nine conventional mediate signal intensity (misclassified as solid components
MR imaging findings misclassified as adnexal tumors, all of ovarian tumors) on T2-weighted images (Fig. 3).
areas detected were low and intermediate signal intensity
on T1-weighted images, with heterogeneous (intermedi-
ADC analysis
ate and high mixed) signal intensity on T2-weighted
images within the masses. The area exhibiting interme- The mean ADC values of contained uid in PID and
diate signal intensity on T1-weighted images and non-PID patients are presented in Table 1. There are
T2-weighted images were regarded as soft-tissue many overlaps between the ADC values for both groups.
(pseudosolid) within the mass. These 9 patients were The mean ADC values did not differ significantly
W. Li et al.: Pelvic inflammatory disease 197

Fig. 2. A 49-year-old woman with a right TOA. A Axial enhancing walls and septa. D Axial DW images show an
T1-weighted image shows an iso- and mildly high mixed sig- S-like structure and high signal intensity, and an ovoid high
nal intensity mass in the right side of the pelvic cavity. B Axial signal intensity area within a complex mass, findings that are
T2-weighted image reveals that the mass has heterogeneous compatible with TOA (circle 1 ADC = 0.636 9 10-3 mm2/s,
high signal intensity. C Axial contrast-enhanced MR image circle 2 ADC = 1.28 9 10-3 mm2/s, circle 3 ADC = 1.35 9
shows complex cystic and solid mass with thick, irregular 10-3 mm2/s in the outer myometrium).

between the FFT group, the hydrosalpinx group, the combination with conventional MR imaging is not only
fallopian tube ligation with hydrosalpinx group, the sensitive and specic for establishing the diagnosis of
fallopian tube carcinoma (FTC) group, and the cystic PID, but also for distinguishing PID from other patho-
component in the ovarian cancer group (P > 0.05). The logic processes. With the use of ADC measurements and
mean ADC values of contained fluid did not differ sig- signal characteristics, MR imaging can lead to the cor-
nificantly between the pyosalpinx, tubo-ovarian abscess rect assessment of PID with a higher degree of accuracy.
(TOA), ovarian abscess, hematosalpinx, and tubal tor- DW imaging has already been used to improve con-
sion groups (P > 0.05), but there was a statistically ventional MR imaging by allowing the identication of
significant difference in mean ADC values between specic criteria for diagnosis according to tissue speci-
groups a and b (P < 0.05) (Table 1). cities of various brain, breast, prostate, and abdominal
tumors [1218]. However, until now no such data has
been available for PID patients. To the best of our
Discussion knowledge, this is the first study to evaluate the role of
Our results demonstrate that dilated fallopian tubes can DW imaging in conjunction with signal characteristics to
be identied on MR imaging, and that DW imaging in further characterize PID. Acute tubo-ovarian or ovarian
198 W. Li et al.: Pelvic inflammatory disease

Fig. 3. A 54-year-old woman with right ovarian abscess. A signal intensity area that mimics a soft-tissue (pseudosolid)
Axial T1-weighted image shows a low heterogeneous signal signal (long arrow). D Axial DW images show that the
intensity mass in the right side of the pelvic cavity. B Axial T2- pseudosolid and high signal intensity area on the T2-weighted
weighted image reveals that the mass has intermediate signal image are all high signal intensity, compatible with purulent
intensity and a small cystic component (high signal intensity cavities with low ADC values (circle 1 ADC = 0.555 9 10-3
area). C Axial contrast-enhanced MR image shows a complex mm2/s, circle 2 ADC = 0.519 9 10-3 mm2/s).
cystic and solid mass with thick enhancing walls and a low

abscesses may produce very complex masses with wall images with low ADC values. These results confirm that
thickening and pseudosolid areas. The pseudosolid areas the addition of DW imaging enabled us to increase the
can demonstrate low, intermediate, or high signal diagnostic confidence of conventional MR imaging in up
intensity on T1-weighted images and low or intermediate to 22.5% (9/40) of tubo-ovarian and ovarian abscesses.
signal intensity on T2-weighted images, and are similar This positive result is mainly due to the fact that the
to those of soft-tissue or mucinous components of ad- addition of DW imaging to conventional MR imaging
nexal masses. The signal characteristics of pseudosolid can confidently differentiate pseudosolids (pus) from
areas may be related to the presence of high inflamma- other conditions based on signal characteristics. When a
tory cellularity, a matrix of proteins, cellular debris, and high signal intensity area is depicted on DW imaging
bacteria in high viscosity purulent fluids, as well as large with low ADC values, our results demonstrate that high
molecules playing a key role in restricting the diffusion or intermediate signal intensity on T2-weighted images of
of protons in pus. These can demonstrate marked this area without enhancement is the best criteria for
enhancement, thereby mimicking malignancy. The clini- predicting the presence of an abscess. These findings are
cal features of acute pelvic infection and malignancy similar to previous reports that demonstrated the rela-
usually differ, though some chronic infections such as tionship between high signal intensity with low ADC
TOA may exactly mimic malignancy. In our patients, all values in the central part of a brain abscess and the
abscess cavities initially had high signal intensity on DW presence of pus [12, 13].
W. Li et al.: Pelvic inflammatory disease 199

Our results also showed that the signal intensity non-PID patients. Finally, the variable concentrations
of fallopian tube uid is associated with pathological of inammatory cells and bacteria with different path-
conditions, and the combination of T1-weighted, ogenic organisms, the age of an abscess and blood
T2-weighted, DW, as well as morphology, allowed us to parameters might inuence the uid viscosity, resulting
further characterize lesions that were clinically suspected in variations of signal intensity and ADC values. As a
to be PID. In acute salpingitis, the fallopian tubes are result, conclusions drawn from the results observed in
often revealed as sausage-like, slightly dilated FFTs with this cohort might not be generally applicable. A con-
wall thickening and enhancement. The tubal content has tinued evaluation of the clinical utility and indications of
low signal intensity on T1-weighted, DW, and high signal combined DW and MRI, therefore, still needs to be
intensity on T2-weighted images. On MR images, both investigated, especially as there are few reports of the
hydrosalpinx and pyosalpinx appear as dilated, uid-l- use of ADC values for the differential diagnosis of pa-
led, and tubal structures. With pyosalpinx, the wall of a tients with PID.
dilated fallopian tube may be thickened, and it has var- In conclusion, the ndings in this study demonstrate
iable signal intensity on T1-weighted images and heter- that DW imaging in combination with conventional MR
ogeneous signal intensity on T2-weighted images. In imaging is a useful tool for improving the characteriza-
general, a pyosalpinx cannot be reliably differentiated tion of clinically suspected PID. With the use of ADC
from a hydrosalpinx on conventional MR images. The measurements and signal characteristics, MR imaging
combination of T1-weighted, T2-weighted, and DW can lead to a more accurate assessment of adnexal
images allowed us to further characterize and differen- lesions.
tiate both entities, with hydrosalpinx demonstrating low
signal intensity and pyosalpinx high signal intensity on
DW images. This is explained by the fact that the vis-
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