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(Radiology. 2000;217:421-425.)
© RSNA, 2000


Gastrointestinal Imaging

Detection and Mapping of Intraabdominal Adhesions by Using Functional Cine MR Imaging: Preliminary Results1

Andreas Lienemann, MD, Dorothee Sprenger, MD, Heinrich Otto Steitz, MD, Matthias Korell, MD and Maximillian Reiser, MD

1 From the Departments of Diagnostic Radiology (A.L., D.S., M.R.), Surgery (H.O.S.), and Obstetrics and Gynecology (M.K.), Klinikum Grosshadern, Ludwig-Maximilians-University Munich, Marchioninistr 15, D-81377 Munich, Germany. Received July 7, 1999; revision requested September 9; revision received January 14, 2000; accepted January 27. Address correspondence to A.L. (e-mail: andreasliene@compuserve.com).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To identify and map intraabdominal adhesions by using functional cine magnetic resonance (MR) Imaging.

MATERIALS AND METHODS: Twenty-seven patients suspected of having intraabdominal adhesions were examined. Section-by-section dynamic depiction of induced visceral slide throughout the whole abdomen was achieved by using a transverse or sagittal true fast imaging with steady-state precession sequence. Location and type of diagnosed adhesions were documented by using the nine segments of the abdominal map. These criteria and intraoperative results were compared in 13 patients.

RESULTS: MR images depicted a total of 42 intraabdominal adhesions; 21 (50%) were in the lower abdomen. The most common types of adhesions were located between the ventral abdominal wall and small-bowel loops (n = 10 [24%]) and between adjacent small-bowel loops (n = 9 [21%]). Comparison with the intraoperative results showed a sensitivity of 87.5% and a specificity of 92.5%. MR imaging was most accurate in depicting adhesions to the abdominal wall (15 [94%] of 16) and subperitoneal space (eight [100%] of eight). The presence of adhesions between bowel loops was overestimated.

CONCLUSION: Detection of visceral slide at functional cine MR imaging is easy to perform and represents a well-tolerated and accurate procedure for use in the identification of intraabdominal adhesions in patients with chronic pain and equivocal clinical findings.

Index terms: Abdomen, abnormalities, 70.293, 70.458, 70.89 • Abdomen, MR, 70.121419 • Intestines, stenosis or obstruction, 74.723 • Magnetic resonance (MR), cine study, 70.121419 • Magnetic resonance (MR), functional imaging, 70.121419 • Peritoneum, abnormalities, 70.293 • Peritoneum, MR, 70.121419


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Intraabdominal adhesions are nonspecific complications related to prior abdominal surgery. They are the main cause of small-bowel obstruction and mechanical ileus in adults. Most often, acute or chronic abdominal complaints are the only symptoms (1,2). Abdominal adhesions consist of fibrous bands or fibrous fatty tissue. Adhesions interconnect loops of bowel or stick to the parietal peritoneum, mainly the abdominal wall and the subperitoneal organs (3,4).

The correct diagnosis of the presence and extent of adhesions is of great importance regarding the indication for and planning of an operation (5). Real-time ultrasonography (US) can be used to depict the movement of abdominal viscera next to the abdominal wall. Abdominal wall adhesions produce a restriction of visceral slide that is detectable with this modality (6). Therefore, US localization of adhesions is most useful in guiding the insertion of the trocar at laparoscopic surgery (7). Small-bowel enteroclysis will occasionally show fibrous bands with luminal narrowing. In addition, manual pressure externally applied to the abdomen may fail to cause separation of adjacent bowel loops (8).

Our study was performed to evaluate the potential of functional cine magnetic resonance (MR) imaging in the detection of adhesions and to compare our preliminary results with the intraoperative findings.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Between January 1998 and November 1998, 27 consecutive patients (22 women and five men; mean age, 50.2 years; age range, 21–62 years) were examined at functional cine MR imaging. At the time of admission, 25 patients had episodes of chronic abdominal pain but no signs of obstruction. In the remaining two patients, the initial complaints were caused by pelvic floor dysfunction with organ descent. All patients had undergone prior abdominal surgery. In nine (36%) patients, previous surgery had been necessary because of obstruction caused by intraabdominal adhesions. The time between the last surgical intervention and MR examination ranged from 6 months to 12 years.

Intraoperative results of 13 patients were available for comparison. A laparoscopic approach was used in eight patients suspected of having intraabdominal adhesions. Laparotomy was performed in two patients with coincidental pelvic organ descent.

MR imaging was performed with a 1.5-T system (Vision; Siemens, Erlangen, Germany). The examination was performed by using a body-array surface coil with the patient in supine position. No premedication or opacification of organs was used. Informed consent was obtained in all patients for the MR imaging examinations. Our university ethical board indicated that its approval was not required for this study.

A coronal localizer with a superimposed grid was used as a reference for screening the whole abdomen. In all patients, we used a single-section true fast imaging with steady-state precession (FISP) sequence (5.8/2.5 [repetition time msec/echo time msec], flip angle of 70°, matrix of 192 x 256, field of view of 400 mm, section thickness of 7 mm). One cycle consisted of 10 consecutive measurements in the same position, with one frame acquired every 1.3 seconds.

In the first three patients, as part of a pilot study, the cycle in the midsagittal position of the abdomen was acquired twice: First, the patients were asked to increase intraabdominal pressure by straining and to subsequently relax (Fig 1). Then, they were asked to breathe deeply while performing the same cycle. The decision about which type of induced visceral slide to use ultimately was based on only the visual facts.



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Figure 1. Transverse true FISP MR images (5.8/2.5, 70° flip angle) obtained with the same section position in the middle abdomen illustrate one cycle of straining and relaxing (top row left to bottom row right). Next to the ventral and left lateral abdominal wall, part of a small-bowel loop (s) does not move out of the imaging plane during straining. In addition, there is no separation of these structures at any time. In contrast, note the vast movement of the large bowel (L) and right kidney (R) in and out of the imaging plane.

 
The previously mentioned cycle was repeated in sequence until both transverse and sagittal images of the whole abdomen were acquired. The mean distance or gap between two consecutive cycles was half the space of the grid, that is, 1.5 cm. A total of 300–400 images of the whole abdomen were acquired. The overall examination time was 30 minutes on average.

At the completion of the examination, the sequences of functional cine image were spliced together to make an infinite loop and recorded with a standard videotape recorder.

To facilitate comparison of these results with the intraoperative results, a map of the abdomen was created. This map was divided into nine segments with bilateral vertical lines along the border of the rectus abdominis muscle, a transverse line across the inferior costal margins, and a transverse line across the iliac crest.

The criteria for the diagnosis of adhesions at MR imaging were the following (Fig 2): distortion of adjacent organs (Fig 3) and preserved visceral slide of adjacent structures in the same direction with missing separation between them (Fig 4) and with missing excursion along the peritoneal layer within the section orientation (Figs 5, 6).



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Figure 2. Diagram depicts the criteria for detection of adhesions at functional cine MR imaging. Sagittal and transverse section orientation is represented by the two planes, whereas arrows indicate the main directions of induced visceral slide. Adhesions between the omentum and anterior abdominal wall (A) may be visible only as a parallel alignment of mesenteric vessels that proceed perpendicularly to the wall. Adhesions involving two or more bowel loops (B) show visceral slide but no separation during straining. In contrast, adhesions next to the retroperitoneum (C) or anterior wall (F) show neither slide nor separation. Distortion, especially of subperitoneal organs (D, E), is common with adhesions.

 


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Figure 3. Midsagittal true FISP MR image (5.8/2.5, 70° flip angle) of the lower abdomen shows an adhesion between a small-bowel loop (s) and bladder (b) as tether (arrow) to the bladder wall.

 


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Figure 4. Midsagittal true FISP MR image (5.8/2.5, 70° flip angle) of the abdomen shows that, during straining, no visceral slide and no separation (arrowhead) occur between the uterus (U) and small-bowel loop (s).

 


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Figure 5. Parasagittal true FISP MR image (5.8/2.5, 70° flip angle) of the abdomen shows several small-bowel loops (s) as part of a large adhesional plate next to the anterior abdominal wall (a). There is a missing separation of the structures during straining, and some small-bowel loops exhibit pointed angles (arrowheads).

 


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Figure 6a. Transverse true FISP MR images (5.8/2.5, 70° flip angle) of the pelvis obtained at the level of the acetabula. (a) Image shows an ovarian cyst (O), a fluid level (arrow) in the right lower pelvis, a pouchlike mass (P) with an area of 4.0 x 4.5 cm, and a large-bowel loop as part of the sigmoid colon (c) dorsal and medial to the mass. (b) Image of intraoperative site in the same patient shows multiple adhesions between small-bowel loops (arrows). Additional adhesions involving the cecum and sigmoid colon (not shown) led to a cranial displacement of the cecum and formation of a valvelike mechanism. In fact, the patient had to apply manual pressure to the right lower abdomen to ease his pain and promote digestion.

 


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Figure 6b. Transverse true FISP MR images (5.8/2.5, 70° flip angle) of the pelvis obtained at the level of the acetabula. (a) Image shows an ovarian cyst (O), a fluid level (arrow) in the right lower pelvis, a pouchlike mass (P) with an area of 4.0 x 4.5 cm, and a large-bowel loop as part of the sigmoid colon (c) dorsal and medial to the mass. (b) Image of intraoperative site in the same patient shows multiple adhesions between small-bowel loops (arrows). Additional adhesions involving the cecum and sigmoid colon (not shown) led to a cranial displacement of the cecum and formation of a valvelike mechanism. In fact, the patient had to apply manual pressure to the right lower abdomen to ease his pain and promote digestion.

 
Adhesions depicted on functional cine MR images were classified according to their location in the nine segments and according to the structures involved.

The previously mentioned criteria were assessed by two experienced abdominal radiologists (A.L., D.S.) for each sagittal and transverse cycle.

Surgery was used as the standard. The two readers were blinded to the intraoperative results. Comparison of findings with both modalities included evaluation of the location and type of adhesion found in the nine segments of the abdominal map. Interpretation was made by means of consensus reading.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Images in all 27 MR imaging examinations were regarded to be diagnostic, with no evident artifacts. In the pilot study, we found that an increase in intraabdominal pressure caused by straining proved to be superior to that due to respiratory excursions alone. Thus, all patients were asked to perform the straining maneuver during the examination.

Figures 7 and 8 show the results of MR imaging. Mapping of the adhesions showed that most of them were in the lower abdomen, which corresponded to segments 7–9.



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Figure 7. Bar graph shows the number and location of intraabdominal adhesions found at MR imaging compared with those found at surgery. Most adhesions occurred in the lower abdomen, with almost an equal number of findings identified with both modalities. (Numbers in parentheses are segment numbers.)

 


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Figure 8. Bar graph shows the different types of adhesions found at surgery and MR imaging. MR imaging had the best results in the depiction of adhesions between the peritoneum and adjacent organs but caused overestimation of the number of adhesions between small-bowel loops. Adhesions involving the omentum were missed in most patients.

 
In all patients, MR images depicted a total of 42 intraabdominal adhesions throughout the abdomen (Table). The most common types of adhesions were interconnections between the ventral abdominal wall and small-bowel loops (n = 10 [24%]) and those between adjacent small-bowel loops (n = 9 [21%]).


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Diagnosis of Intraabdominal Adhesions at MR Imaging and Surgery
 
Agreement between MR imaging and intraoperative results concerning the segments involved with adhesions was achieved in 21 segments; this finding resulted in a sensitivity of 87.5% and a specificity of 92.5% (total of 117 segments, with false-positive findings in seven segments and false-negative findings in three segments).

When we compared the different types of adhesions, as detected by means of MR imaging and surgery (Fig 8), MR imaging was most accurate in depicting adhesions to the abdominal wall (15 [94%] of 16) (Fig 1) and subperitoneal space (eight of [100%] eight) (Fig 4).

The presence of adhesions between bowel loops was overestimated at MR imaging evaluation. Adhesions involving the omentum were missed in most patients.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In a prospective study, Ivarson et al (9) concluded that adhesions are a serious, common, and costly complication of abdominal surgery. Ellis (1) mentioned the considerable workload created by problems resulting from postoperative adhesions. The increasing number of publications on adhesion prevention with the use of noninflammatory agents, gel, or bioresorbable membranes indicate the importance of adhesion-related problems (10,11).

Patients with a history of intraabdominal inflammatory disease not treated with surgery, multiple abdominal operations, or previous postoperative intraabdominal complications are most likely to experience adhesion formation (12,13). The types of surgery that represent risk factors include colonic (especially rectal) surgery, appendectomy, and gynecologic procedures (1,14). Unequivocal symptoms and signs of bowel obstruction and bowel ischemia are advanced stages of adhesion-related problems (5). However, recurrent abdominal pain with or without a reproducible sensitive spot are most often the only complaints of the patient.

A noninvasive tool for use in the diagnosis of adhesions is desirable, as the widely used laparoscopic exploration itself may result in the formation of adhesions (1,15). The detection of intraabdominal adhesions is based on indirect signs or abnormal visceral slide.

Computed tomography (CT) has proved to be a valuable diagnostic modality in the detection of advanced adhesion-related problems such as bowel obstruction and bowel ischemia (1618). In the absence of concomitant diseases, an abrupt transition from dilated to collapsed bowel segments may be the only hint of the presence of adhesions that can be depicted on CT scans (16).

Enteroclysis studies are advocated in patients with equivocal clinical symptoms or negative findings at CT (16,19). Indirect signs include hyperperistalsis, distortion of folds with luminal narrowing, or kinking of an entire loop (20). Visible crossing bands or a missing separation of adjacent loops with external manual compression are direct signs of adhesions (8). Therefore, this procedure can be used to more accurately identify the location and the cause of the obstruction (19). Nevertheless, the procedure is time-consuming and is often unpleasant for the patient. Besides, palpation of the small-bowel loops in the lower abdomen remains unsatisfactory because of limited access, multiple superimpositions, and missing identification of surrounding structures.

US performed with the visceral slide technique was first introduced by Sigel et al (6). The visualization of respiration-induced visceral slide beneath the ventral peritoneum proved to be useful in planning the site of entry prior to abdominal surgery. Sensitivity and specificity were reported to be as high as 95% and 100%, respectively (7,21). Although adhesions frequently involve the abdominal wall, an exploration of the whole abdomen may be obscured in many ways (eg, by intestinal gas or by subcutaneous fat in obese patients) (21).

We adjusted the before-mentioned method (6) to develop an adequate MR imaging technique. The main elements of our method may be summarized as a section-by-section functional cine depiction of induced visceral slide throughout the whole abdomen (Fig 1).

The procedure requires no premedication or preparation. Although filling of bowel loops with fluid would add to the identifiability and demarcation of the intestine, we did not use orally administered contrast medium for several reasons. As in bowel preparation before colonoscopy, consumption of large amounts of fluid is time-consuming, is unpleasant for the patient, and may cause diarrhea.

Compared with spontaneous movements (eg, peristalsis), induced visceral slide is more controllable; the shift is marked and involves all intraabdominal (and even retroperitoneal) organs. Repeated straining proved to be superior to repeated deep breathing in this regard. Besides, this type of movement is best depicted on sagittal and transverse images.

To combine high spatial resolution with a sufficient temporal resolution, we used a true FISP sequence. A cycle of 10 consecutive measurements in each section positioned with the superimposed grid on the localizer was the most easy to handle and permitted us to standardize the procedure.

Our criteria for the detection of intraabdominal adhesions rely on the absence of either movement or separation of adjacent structures. On one hand, these effects are best depicted if one of the involved structures is stationary. On the other hand, a certain freedom of movement in intraabdominal and retroperitoneal structures is required. As our results show, the best correlation was achieved with adhesions to the ventral abdominal wall or subperitoneal space (Figs 3, 5, 8). Due to the restricted movement of bowel loops deep within the small pelvis and/or parts of the large bowel (ascending and descending colon), adhesions between these structures and the retroperitoneum were difficult to assess. The extensive mobility of small-bowel loops, on the other hand, requires an extremely thorough reading of images obtained in both orientations in adjacent sections. Adhesions involving the omentum were most difficult to detect. The most likely reason for this is the same signal intensity of both the omentum and mesenteric fat.

With a cooperative and normal-weight to slightly obese patient, our method of detection and mapping of intraabdominal adhesions proved to be a reliable tool for use by the surgeon prior to laparoscopy or laparotomy. Therefore, indications for this generally easy-to-perform and well-tolerated examination may include the clinical confirmation of intraabdominal adhesions in patients with a known history of adhesions and in those with chronic abdominal pain but no signs of obstruction or bowel ischemia. In such patients, MR imaging examination performed according to our protocol may provide relevant preoperative information regarding the identification and localization of structures involved with adhesions.


    FOOTNOTES
 
Abbreviation: FISP = fast imaging with steady-state precession

Author contributions: Guarantor of integrity of entire study, A.L.; study concepts, A.L., H.O.S., M.K.; study design, D.S., A.L.; definition of intellectual content, A.L., H.O.S., M.K.; literature research, D.S.; clinical studies, A.L., D.S.; data acquisition, D.S., A.L.; data analysis, A.L., H.O.S., M.K.; statistical analysis, A.L.; manuscript preparation, A.L., D.S.; manuscript editing, H.O.S., M.K.; manuscript review, M.R.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Ellis H. The clinical significance of adhesions: focus on intestinal obstruction. Eur J Surg Suppl 1997; 577:5-9.
  2. Stovall TG, Elder RF, Ling FW. Predictors of pelvic adhesions. J Reprod Med 1989; 34:345-348.[Medline]
  3. Levrant SG, Bieber EJ, Barnes RB. Anterior abdominal wall adhesions after laparotomy or laparoscopy. J Am Assoc Gynecol Laparosc 1997; 4:353-356.[Medline]
  4. Cox MR, Gunn IF, Eastman MC, Hunt RF, Heinz AW. The operative aetiology and types of adhesions causing small bowel obstruction. Aust NZ J Surg 1993; 63:848-852.[Medline]
  5. Freys SM, Fuchs KH, Heimbucher J, Thiede A. Laparoscopic adhesiolysis. Surg Endosc 1994; 8:1202-1207.[Medline]
  6. Sigel B, Golub RM, Loiacono LA, et al. Technique of ultrasonic detection and mapping of abdominal wall adhesions. Surg Endosc 1991; 5:161-165.[Medline]
  7. Caprini JA, Arcelus JA, Swanson J, et al. The ultrasonic localization of abdominal wall adhesions. Surg Endosc 1995; 9:283-285.[Medline]
  8. Bartram CI. Radiologic demonstration of adhesions following surgery for inflammatory bowel disease. Br J Radiol 1980; 53:650-653.[Abstract/Free Full Text]
  9. Ivarson ML, Holmdahl L, Franzen G, Risberg B. Cost of bowel obstruction resulting from adhesions. Eur J Surg 1997; 163:679-684.[Medline]
  10. Beck DE. The role of Seprafilm bioresorbable membrane in adhesion prevention. Eur J Surg Suppl 1997; 577:49-55.
  11. Rodgers KE, Girgis W, Campeau JD, diZerega GS. Reduction of adhesion formation by intraperitoneal administration of anti-inflammatory peptide 2. J Invest Surg 1997; 10:31-36.[Medline]
  12. Luijendijk RW, de Lange DC, Wauters CC, et al. Foreign material in postoperative adhesions. Ann Surg 1996; 223:242-248.[Medline]
  13. Brill AI, Nezhat F, Nezhat CH, Nezhat C. The incidence of adhesions after prior laparotomy: a laparoscopic appraisal. Obstet Gynecol 1995; 85:269-272.[Medline]
  14. Stovall TG, Elder RF, Ling FW. Predictors of pelvic adhesions. J Reprod Med 1989; 34:345-348.
  15. Levrant SG, Bieber EJ, Barnes RB. Anterior abdominal wall adhesions after laparotomy or laparoscopy. J Am Assoc Gynecol Laparosc 1997; 4:353-356.
  16. Makanjuola D. Computed tomography compared with small bowel enema in clinically equivocal intestinal obstruction. Clin Radiol 1998; 53:203-208.[Medline]
  17. Ha HK, Kim JS, Lee MS, et al. Differentiation of simple and strangulated small-bowel obstructions: usefulness of known CT criteria. Radiology 1997; 204:507-512.[Abstract/Free Full Text]
  18. Maglinte DD, Gage SN, Harmon BH, et al. Obstruction of the small intestine: accuracy and role of CT in diagnosis. Radiology 1993; 188:61-64.[Abstract/Free Full Text]
  19. Shrake PD, Rex DK, Lappas JC, Maglinte DD. Radiographic evaluation of suspected small bowel obstruction. Am J Gastroenterol 1991; 86:175-178.[Medline]
  20. Caroline DF, Herlinger H, Laufer I, Kressel HY, Levine MS. Small-bowel enema in diagnosis of adhesive obstructions. AJR Am J Roentgenol 1984; 142:1133-1139.[Abstract/Free Full Text]
  21. Steitz HO, Meyer G, Schildberg FW. Ultrasonography of adhesions prior to laparoscopic procedures after previous Abdominal operations. In: Farthmann EH, Meyer C, Richter HA, eds. Current aspects of laparoscopic colorectal surgery. New York, NY: Springer, 1997; 210-216.



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