Eur Radiol (2008) 18: 1215–1223 DOI 10.1007/s00330-008-0881-5
GASTRO INTESTINAL
Sonja Buhmann-Kirchhoff Reinhold Lang Chlodwig Kirchhoff Heinrich Otto Steitz Karl Walter Jauch Maximilian Reiser Andreas Lienemann
Functional cine MR imaging for the detection and mapping of intraabdominal adhesions: method and surgical correlation
Received: 7 May 2007 Revised: 17 December 2007 Accepted: 17 January 2008 Published online: 15 February 2008 # European Society of Radiology 2008
C. Kirchhoff Department of Surgery, University Hospital Munich-Innenstadt, Nussbaumstrasse 20, 80336 Munich, Germany
Sonja Buhmann and Reinhold Lang contributed equally to this work. S. Buhmann-Kirchhoff (*) . M. Reiser . A. Lienemann Department of Clinical Radiology, University Hospital Grosshadern, Ludwig-Maximilians-University Munich, Marchioninistrasse 15, 81377 Munich, Germany e-mail:
[email protected] Tel.: +49-89-70953663 Fax: +49-89-70958832 R. Lang . H. O. Steitz . K. W. Jauch Department of Surgery, University Hospital Munich-Großhadern, Marchioninistrasse 15, 81377 Munich, Germany
Abstract The purpose of this study was to evaluate the presence and localization of intraabdominal adhesions using functional cine magnetic resonance imaging (MRI) and to correlate the MR findings with intraoperative results. In a retrospective study, patients who had undergone previous abdominal surgery with suspected intraabdominal adhesions were examined. A true fast imaging with steady state precession sequence in transverse/sagittal orientation was used for a section-by-section dynamic depiction of visceral slide on a 1.5Tesla system. After MRI, all patients underwent anew surgery. A ninesegment abdominal map was used to document the location and type of the adhesions. The intraoperative results were taken as standard of reference.
Introduction Intraabdominal adhesions are a common cause for abdominal pain, bowel obstruction, especially of the small bowel in up to 75%, and for mechanical ileus in adult patients [1]. Almost half of the patients who complain about chronic pelvic pain have adhesions [2]. Mostly these intraabdominal adhesions consist of fibrous bands or fibrous fatty tissue and develop between bowel loops or at the parietal peritoneum, mainly interconnecting the
Ninety patients were enrolled. During surgery 71 adhesions were detected, MRI depicted 68 intraabdominal adhesions. The most common type of adhesion in MRI was found between the anterior abdominal wall and small bowel loops (n=22, 32.5%) and between small bowel loops and pelvic organs (n=14, 20.6%). Comparing MRI with the intraoperative findings, sensitivity varied between 31 and 75% with a varying specificity between 65 and 92% in the different segments leading to an overall MRI accuracy of 89%. Functional cine MRI proved to be a useful examination technique for the identification of intraabdominal adhesions in patients with acute or chronic pain and corresponding clinical findings providing accurate results. However, no differentiation for symptomatic versus asymptomatic adhesions is possible. Keywords Adhesions . MRI . Surgical correlation . Abdomen
abdominal wall and the subperitoneal organs [3, 4]. Adhesions in the abdominal cavity as a result of previous abdominal or pelvic surgery or infection are predisposing factors to injury intraabdominal organs during trocar insertion. Therefore, surgeons planning the surgical approach for laparoscopy or laparotomy have to consider the presence and distribution of adhesions in patients who underwent previous abdominal or pelvic surgery. Thus, an accurate diagnosis of intraabdominal adhesions would be highly valuable [5]. The use of real-time
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ultrasound (US) to visualize visceral slide for the identification of intraabdominal adhesions has been described by several authors [6, 7]. Using US during initial needle or trocar placement for laparoscopy has been proposed by Kodama et al. [8] to avoid visceral injury. However, US exploration of the entire abdomen is often difficult due to the patients’ physique (e.g., obese patients) or overlay of intestinal gas. Also regarding sensitivity poor results were reported for adhesion detection in the subumbilical and pelvic area [8]. Other radiological methods, such as small bowel enteroclysis, are rather insensitive regarding the detection of fibrous bands manifesting as consecutive luminal narrowing or failure to separate adjacent bowel loops by manually applied pressure to the abdomen [9]. However, in the year 2000 the detection of visceral slide using functional cine MRI was introduced as an accurate, reliable, and non-invasive tool for the identification of adhesions [10]. Therefore, the aim of this study was to further evaluate the potential of functional cine MRI for the detection and mapping of intraabdominal adhesions and to correlate the MR results with surgical, intraoperative findings.
Materials and methods Between January 2001 and May 2006, 90 patients (15 men, 75 women, mean age 50.8 years, SD 32 years, age range 19–83 years) from the department of surgery of our University Hospital, who were suffering from complaints due to adhesions were examined using functional cine MRI and enrolled in this study. All patients had undergone prior abdominal or pelvic surgery and were suffering from definite acute or chronic abdominal pain with the most common symptoms following abdominal pain being pain after food intake, constipation or colic pain. In many cases, adhesions were already suspected in US performed by the treating surgeon. However, other causes of symptoms were in most cases excluded using different examination techniques, such as computed tomography. The initial complaints in many female patients were pelvic floor dysfunction. Functional cine MRI was performed prior to anew surgical treatment with the time interval between the MR examination and subsequent surgery ranging from 2 days to 8 months. Functional cine MRI MRI was performed on 1.5-Tesla systems (Sonata/Avanto; Siemens Medical Solution, Erlangen, Germany). Two body-array surface coils covering the abdomen/pelvis of the patient lying in a supine position were used. No premedication or contrast agent were administered. The university board of ethics indicated that an approval of this
study was not required. The MRI examination for adhesion detection presents a routine examination at our University Hospital. However, written informed consent was obtained from all enrolled patients. The MR protocol used had previously been described in the literature [10] After a coronal localizer, a single-slice true fast imaging with steady state precession sequence (trueFISP) (field of view 400 mm, matrix of 256×256, flip angle 50°, slice thickness 5 mm) was used. One cycle consisted of ten consecutive measurements in the same position; one frame was acquired every 1.3 s. During one cycle the patients were asked to increase the intraabdominal pressure by straining and to relax subsequently. The above-mentioned cycle was repeated in sequence at different slice positions covering the entire abdomen, both in cranio-caudal (axial), and from right to left direction (sagittal). The mean distance of gap between two consecutive cycles was 1.5 cm. Depending on the size of the patient 300–400 images were acquired in order to cover the entire abdomen (for the axial slices beginning at the level of the liver down to the pelvic area). Thus, the overall examination time varied between 20 and 30 min. Mapping of intraabdominal/pelvic adhesions To facilitate the above-mentioned correlation with the intraoperative surgical data, a map of the abdomen was created dividing the entire abdomen into nine segments employing bilateral vertical lines along the borders of the rectus abdominis muscle, a transverse line across the inferior costal margins, and another transverse line across the iliac crest (see Table 1, Fig. 1). MRI criteria Criteria on MRI for the diagnosis of adhesions can be best explained figuratively when compared with a swing. When two persons are sitting on the swing, they represent two independent bowel loops, whereas the scaffold symbolizes the abdominal border. The degree of exercise of the two persons stands for the movement induced by the valsalva maneuver. Without present adhesions a single bowel loop will move back and forth in a mainly cranio-caudal direction during the valsalva maneuver (Figs. 2, 3). The presence of adhesions will significantly alter this movement. First, this bowel loop will no longer move in and out of an image plane perpendicular to the direction of the movement. Secondly, there will be an impediment of the movement next to non-varyingly structures like the peritoneal border.
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Table 1 Abdominal map showing sensitivity/specificity of each evaluated segment Segments
TP
FP
FN
TN
I II III IV V VI VII VIII IX
5 3 3 10 20 8 14 22 23
6 8 7 8 10 11 10 19 10
7 1 4 22 13 12 23 13 15
72 78 76 50 47 59 43 36 42
The corresponding raw data for calculating sensitivity and specificity segment-wise is also provided in Fig. 1 TPtrue positive findings; MRI=positive/Surgery=positive FPfalse positive findings: MRI=positive/surgery=negative FNfalse negative findings: MRI=negative/surgery=positive TNtrue negative findings: MRI=negative/surgery=negative
Third, if two or more adjacent structures (e.g., other bowel loops) are involved, no separation between the single organs will occur. This may account for pseudo-ramification of bowel loops. In addition, the typical artifact, which normally can be seen on tissue interfaces on trueFISP sequences, will disappear. Direct signs like distortion of adjacent organs may also be noticed (see Figs. 4, 5, 6, 7, 8). Surgical criteria For surgery either laparoscopy or conventional open laparotomy was performed. During both treatment options the localization of adhesions intraoperatively were docu-
Fig. 2 These figures present an anatomical example of normal visceral slide on MRI in sagittal orientation still (a) and during (b) straining
Fig. 1 Abdominal map showing sensitivity/specificity of each evaluated segment
mented according to Zuehlke’s criteria [11]. Eighty-five percent of the patients were operated on by two surgeons with expertise in adhesiolysis and great general experience in visceral surgery. Before performing surgery the surgeons were aware of the MR results, of course influencing their decision towards laparoscopic versus open surgery.
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The second reader was a 3rd-year resident with also good experience in reading adhesion MRI; however, with general experience on abdominal MRI. Both readers were blinded to the intraoperative results. Surgical findings were defined as the “gold standard”. The evaluation was performed in a consensus read. The location and type of adhesion found in the defined ninesegment map of the abdomen were assessed in functional cine MRI and surgery. For each segment, sensitivity and specificity was calculated separately. The matching of MRI and surgery results was performed by a third independent reader who was not involved in the evaluation of the MR examination or in performing surgery/laparoscopy. Outcome Regarding the outcome of the patients after surgery, the standard Medical Outcome Study SF-36 Health Survey was answered by the patients. This questionnaire consists of eight health-quality domains: physical and social functioning, body pain, general health perception, physical and emotional role limitations, vitality and mental health. The scores for each domain range from 0 to 100, whereas higher scores indicate better quality of life. The SF36 scores are presented as means in comparison to the healthy German population controls computed from the German Federal Health Survey from 1998 [12].
Results All 90 MRI examinations were considered to be diagnostic without presenting substantial artifacts. All 90 enrolled
Fig. 3 These figures also show the normal visceral slide in axial orientation with a single bowel loop moving back and forth in mainly cranio-caudal direction, again still (a) and during (b) the valsalver maneuver
Correlation Two experienced radiologists evaluated both the transverse and the sagittal cycles of all 90 functional cine MRI data sets. The first reader was a general radiologist with an expertise on abdominal MRI and also great experience in reading such MRI examinations for detection of adhesions.
Fig. 4 Present adhesions will alter the movement shown in Figs. 2 and 3. These sagittal trueFISP MR images demonstrate that parts of the small bowel loops do not move out of the imaging plane during straining, whereas no separation of the small bowel loops and the ventral abdominal wall is recognizable (see black arrow) as well as between the small bowel and the urinary bladder (see white arrow). The intraoperative image shows the most common detected type of adhesions between small bowel loops as well as suggested adhesions of the small bowel to the uterus and urinary bladder
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adhesion were interconnections between small bowel loops and the anterior abdominal wall (n=22; 32.5%), as found intraoperatively. In contrast to the standard of reference, the second most common adhesions were found between small bowel loops and pelvic organs (n=14, 20.6%) (see Table 2, Figs. 4, 5, 6, 7). After dividing the abdomen into the “nine-segment map”, MRI reached sensitivity values between 31 and 75% and, respectively, specificity values between 65 and 92%, segment-wise (see Table 1/Fig. 1 for more details). In 80 of the 90 patients enrolled, MRI and the intraoperative findings were concordant, whereas in only ten patients discrepant findings resulted. Thus, MRI reached an overall accuracy of 89%. MRI overestimated adhesions between small bowel loops, whereas adhesions between the omentum majus and intraabdominal organs were missed in two cases with intraoperative findings (see Table 2). Regarding the evaluation of the postoperative outcome, the used questionnaire was answered by 62 of the enrolled 90 patients at an average of 6–9 months after surgery. In comparison with a German population normal cohort for all life quality parameters, no significant difference in lifequality index was found with the operated patients (see Table 3).
Discussion In general surgery, laparoscopic approaches play an important role principally because of reduced pain and discomfort associated with the surgical procedure as well as shorter periods of time of recovery. However, abdominal
Fig. 5 This sagittally oriented abdominal MR trueFISP image demonstrates also that no separation between small bowel loops, omentum and uterus occurs (see white arrow)
patients were operated, whereas 59 patients underwent laparotomy and 31 patients were operated using laparoscopy. One of these patients required surgery for a herniated scar after Billroth-II resection. Intraoperatively, this patient revealed no adhesions correlating to the preoperative cineMRI results. The intraoperative findings revealed a total of 71 adhesions. The most common type of adhesion was detected between small bowel loops and the anterior abdominal wall (see Fig. 4). The second most common type of adhesion was in between small bowel loops (see Table 2). MRI depicted a total of 68 intraabdominal adhesions throughout the entire abdomen. The most common type of
Fig. 6 Parasagittal trueFISP MR image of the abdomen showing adhesions between small bowel loops as well as between small bowel loops and the upper urinary bladder and/or uterus (see white arrow). There is a missing separation of the structures during straining (see black arrow). On the right, the intraoperative situs is shown presenting adhesion formation between pelvic organs and small bowel loops
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Fig. 7 The axial MR image also presents inter-small-bowel-loop adhesions (see black arrows) in the pelvis minor, which corresponds very well with the intraoperative findings
organs are at risk of injury when the trocar is blindly inserted. Even if this presents an uncommon complication, it is associated with serious morbidity [13]. This risk is most pronounced in patients who underwent previous surgery [14]. Not only patients who had undergone intraabdominal or pelvic surgery but also those suffering from inflammatory diseases or postoperative intraabdominal complications are most likely to experience adhesions [15, 16]. The most common symptoms or clinical signs of adhesions, mainly resulting from colonic surgery, appendectomy and gynecological surgical procedures, are unspecific acute or chronic abdominal pain. Unequivocal signs and symptoms of bowel obstruction or bowel
ischemia present advanced stages of adhesion-related problems [5]. Therefore, it would be highly desirable to have a noninvasive examination method to assess intraabdominal adhesions [3, 17]. When intraabdominal adhesions result in bowel obstruction or ischemia in terms of an emergency situation, computed tomography (CT) enables sensitive detection. Abrupt transition from dilated to collapsed bowel segments is another indirect sign of intraabdominal adhesions, easily detected on CT images [18–20]. MR enteroclysis requires extensive patient preparation and should be performed utilizing an intraabdominal tube for complete distension of the small bowel loops [21]. Therefore, it is not well tolerated and accepted by patients
Fig. 8 It has to be mentioned that MRI also presented additional findings; as in this case, an adeno-carcinoma was suspected in MRI and confirmed by the intraoperative findings
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Table 2 Differentiation of adhesion findings in MRI versus surgery Type of adhesion
MRI
Surgery
Abdominal wall-small bowel Abdominal wall-large bowel Abdominal wall-omentum Abdominal wall-bladder Small bowel-small bowel Small bowel-large bowel Small bowel-retroperitoneum Small bowel-bladder Small bowel-uterus Small bowel-vaginal vault Small bowel-other abdominal organs Small bowel-omentum Large bowel-retroperitoneum Large bowel-bladder Large bowel-vaginal vault Total
22 4 1 0 13 5 0 6 14 1 1 0 2 0 0 68
21 4 6 0 13 4 0 2 8 2 4 2 3 0 1 71
suffering from acute abdominal symptoms. Moreover, MR enteroclysis does not provide dynamic information concerning mobility of intraabdominal organs. US may also allow for an identification of adhesions of intraabdominal viscera and the abdominal wall [6], when the movement of the abdominal viscera is restricted in relation to the abdominal wall. This visceral slide may occur spontaneously as a result of respiratory movements or due to manual ballottement. However, for a US examination, intestinal gas or obesity may prevent for the assessment of the whole abdomen [22]. In our study, a section-by-section functional cine MRI for the depiction of visceral slide throughout the entire abdomen, which was first introduced by Lienemann et al. [10], was used. As criteria for the detection of intraabdominal adhesions, the absence of movement or separation of adjacent structures were employed. Adhesions to the abdominal wall or subperitoneal space could be detected most accurately. However, due to restricted movement of the bowel loops within the pelvis minor and/or parts of the large bowel, adhesions between these structures are difficult to assess. Adhesions to the omentum were most difficult to detect which might be due to the same signal intensity of mesenteric fat and the omentum itself. However, as it can be expected also that the habitus of the patient had some influence on adhesion detection on MRI, so that in patients with prominent intraabdominal fat, adhesions can be detected more easily. In normal-shaped patients showing typical clinical signs of adhesions as well as in patients with slight obesity with normal cooperation the previously introduced functional cine MR examination technique has again been proven as a
valuable diagnostic tool for the surgeons prior to laparascopy or laparotomy. Regarding the presented results, in 80 of 90 enrolled patients a complete agreement of MR and intraoperative findings was found, whereas in only ten patients discrepant findings resulted, leading to an overall accuracy of 89%. In this study no overall sensitivity and specificity were evaluated because certain parts—such as the upper (segment 1, 3) and lower part (segment 7, 9) of the abdomen being affected by intraabdominal, mostly respiratory, movements—are difficult to inspect closely, especially during surgery, thus possibly resulting in low overall sensitivity. Therefore, the decision was made to perform a segment-per-segment analysis. The sensitivity values resulting for MRI in the segments varied between 35 and 72%, thus not presenting the sensitivity to be expected. However, during the blind reading of the MR examinations, slight progress was recognizable towards an increased detection of adhesions. This point was, however, not a focus of the study in terms of a statistical analysis and, therefore, not mentioned in the results section. However, it needs to be stressed that there exist no clear clinical criteria up to now for the differentiation between symptomatic and asymptomatic adhesions. Recurrent painful episodes in one circumscribed area of the abdomen are considered as the only hint for the presence of adhesions. In the literature, there exists only one study— from the ethical point of view very questionable—when strain has been put on adhesions during surgical exploration and the patients were asked about their perception [23]. In consequence, the surgeons however will always attempt to detect all adhesions interconnecting adjacent structures with only one exception in terms of risking the perforation of luminal structures in the absence of an imminent ileus. Therefore, looking for adhesions in the entire abdomen is not an exception but the rule, at least at Table 3 SF36 Health Survey Scores after surgery in comparison to the age-stratefied German population as means of the male and female population Patients
German population Means of male/female
PF RP BP GH SF RE VT MH
78.0 75.3 56.5 59.4 80.5 79.2 58.9 71.1
81.5 77.1 61.6 62.3 84.7 86.5 59.6 71.4
PFphysical functioning, SFsocial functioning, GHgeneral health perception, RPphysical role limitation, REemotional role limitation, BPbody pain, VTvitality, MHmental health
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our university settings. Thus, especially from the MRaspect alone, the differentiation between symptomatic and asymptomatic adhesions is not possible at all. Nevertheless, in this study the intention was set towards the same surgeons operating on all enrolled patients to enforce the exploration of the entire abdomen for adhesion detection, and to overcome the fact that clinical disciplines tend to only look at their specific target organs. In general, the use of oral fluid intake for the MR examination would probably diminish the degree of adhesion detection due to enlarged bowel lumen and consecutively narrowed space to be examined; therefore, it is not advisable. In addition, in patients suffering from acute abdominal pain it is difficult to apply oral fluid, not only due to their condition but also not to prevent consecutive surgery. In the context of the current literature, Mussack et al. [24] compared adhesion detection rates of functional cine MRI versus high-resolution US. In comparing the rate of adhesion detection in MRI, our results underline their results, at least regarding the location and type of found adhesions. This means that the most common type of detected adhesions were in both studies between small bowel loops and the anterior abdominal wall. The second most common type was found between small bowel loops. Regarding the location, in both studies most adhesion was found in the mid-center and lower center segments. Another recently published work by Fischer et al. [25] studied the use of functional cine MRI for the assessment of implanted synthetic mesh after incisional hernia repair. In comparing the presented results regarding the detection and location of adhesions with their results, again the most common location of adhesions was the mid-center segments, followed by the lower center segments. In terms of the most common adhesion type detected, mostly adhesions between small bowel loops and the anterior abdominal wall were also reported in their study. In general, our presented results also punctuate the results published by Fischer et al. [25]. The outcome of the patients after surgery was assessed by the SF-36 Health Survey form. This assay yields an
eight-scale profile of functional health and well-being scores, which has been translated in many languages. Unfortunately no specific questionnaire for patients with adhesions or adhesion-related problems and consecutive surgery exists. In general, a specific form would be better than a generic one; however, the SF-36 has been proven to provide reliable and valid information on clinical outcome in normal subjects and also in patients suffering from other diseases [26]. In our patient collective, no significantly different findings regarding life quality parameters compared with the age-stratified German population resulted after surgery, at least no better results for the mental as well as the social part were found. This is in accordance with the general opinion that adhesions and adhesions-related problems present a major health as well as economical problem which can in general not be solved by surgical adhesiolysis.
Conclusion In general, the results published by Lienemann et al. [10] in 2000 were confirmed and indications for this easy-toperform and well-tolerated examination technique include the clinical confirmation of intraabdominal adhesions in patients with known history of adhesions or with chronic abdominal pain without any signs of obstruction or ischemia. In addition, our study provides MR results of a larger patient cohort compared with the initial study by Lienemann and co-workers. Moreover, this study had the opportunity to directly compare the number and type of adhesions depicted in MRI and assessed during surgery, which was defined as the standard of reference so that it can be concluded that MRI presents an accurate examination technique for the detection of adhesions; however, without providing a separation between symptomatic and asymptomatic adhesions. Of course, this study also suffers from a limitation in terms of a lack of a reproducibility study to be overcome in further investigations.
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