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1
Department of Diagnostic Imaging and Radiology, Children's National Medical
Center, 111 Michigan Ave., N.W., Washington, DC 20010.
2
Department of Pediatrics, Children's National Medical Center, Washington, DC
20010.
3
Present address: Department of Radiology, MCHK-DR, Tripler Army Medical
Center, 1 Jarrett White Rd., Honolulu, HI 96859-5000.
4
Department of Gastroenterology, Children's National Medical Center,
Washington, DC 20010.
5
Present address: Division of Pediatric Gastroenterology and Nutrition,
Pasquerilla Healthcare Center, 2nd Fl., 3800 Reservoir Rd., N.W., Washington,
DC 20007.
Received September 23, 1999;
accepted after revision December 15, 1999.
Address correspondence to L. Ruess.
Abstract
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SUBJECTS AND METHODS. Eighty-eight sonograms were obtained of 23 bowel segments in 17 children and young adults (age range, 10-21 years; mean, 16 years) with new or recurrent inflammatory bowel disease. Sixteen segments were involved with Crohn's disease and seven with ulcerative colitis. Serial sonography (range, two to eight examinations; mean, four per segment) was performed while patients underwent treatment. Bowel wall thickness measurements and color and power Doppler sonography grading were recorded and compared with clinical data.
RESULTS. All 17 patients had at least one abnormal bowel segment on initial sonography. The correlation was significant (p < 0.01). Agreement was 91% on direction of change over time between bowel wall thickness and Doppler grades, with 100% correlation between color and power Doppler sonography grades. In patients with Crohn's disease, the correlation was significant (p < 0.05) between bowel wall thickness and Doppler grades with two of seven and four of seven clinical parameters, respectively. In patients with ulcerative colitis, the correlation was significant (p < 0.05) between bowel wall thickness and Doppler sonography grades with four of seven and three of seven clinical parameters, respectively. The erythrocyte sedimentation rate correlated with all sonographic measurements in both patient groups. Combining bowel wall thickness and Doppler sonography, the percentage of agreement was significant in the direction of change, with five of seven clinical parameters in both patient groups.
CONCLUSION. Gray-scale and color or power Doppler sonography can show changes in disease activity in children and young adults undergoing treatment for inflammatory bowel disease.
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The initial diagnosis of inflammatory bowel disease is usually confirmed with contrast-enhanced radiographic studies and endoscopy. The diagnosis of recurrent disease is usually made clinically. The grayscale sonographic findings of inflammatory bowel disease have been described in adults [2,3,4] and children [5, 6], with both small-bowel and colonic disease. However, these findings, including bowel wall thickening, are also seen in other diseases, limiting the use of gray-scale sonography as a diagnostic tool [6, 7]. More recently, investigators have used color Doppler sonography in the diagnosis of inflammatory bowel disease and the differentiation of this disease from other extrinsic inflammatory conditions in children [6, 8]. Reduction in bowel wall thickness has been documented after treatment of Crohn's disease [9]. The purpose of this study was to determine whether sonography, including gray-scale measurement of bowel wall thickness and color and power Doppler sonography, is useful in the assessment of disease activity during treatment in children with inflammatory bowel disease.
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All sonographic examinations were performed on an HDI 3000 (Advanced Technology Laboratories, Bothell, WA) using a 7-MHz linear transducer. All studies were performed by one of two registered diagnostic medical sonographers and one of the authors, without knowledge of the laboratory test results or treatment history. Each examination included gray-scale and color and power Doppler sonography of all four quadrants of the abdomen and any areas of pain or tenderness indicated by the patient. The areas of the abdomen imaged in each patient were recorded. Follow-up examinations in each patient included examination of the same areas (or bowel segments). Longitudinal and transverse images were obtained. The study times ranged from 5 to 15 min. Images were electronically magnified. Sensitivity was maximized; and color gain was adjusted to maximize visualization of vessels (70-80%) and was kept constant for the follow-up studies for each patient. Color persistence was adjusted to the medium setting and the bandpass filter was adjusted to the lowest setting. Pulse repetition frequency was set at 1000 MHz.
Gray-scale, color Doppler, and power Doppler images were recorded on paper. Total bowel wall thickness was electronically measured in millimeters on gray-scale images at the time of the examination. Measurements were made on either a transverse or a longitudinal image of the bowel. The thickness of the bowel wall was measured from the edge of the outer wall to the inner echogenic lumen, which contained air, or to the central echogenic mucosal stripe (Fig. 1). Abnormal bowel segments were identified as those with thickened bowel wall (bowel wall thickness >3 mm) and increased color and power Doppler signal in the bowel wall. The presence or absence of color or power Doppler signal was recorded at the time of the examination. We assessed each bowel segment with both color and power Doppler sonography using a scale for both measurements similar to that used by Patriquin et al. [10] in their color Doppler studies of appendiceal inflammation. Vascularity of the bowel as depicted by color and power Doppler sonography was graded on a scale of 1-4 (1 = no vascularity, 2 = minimal vascularity or 1-5 pixels of color per centimeter, 3 = moderate vascularity or >5 scattered foci of color or power signal per centimeter, and 4 = marked or severely increased vascularity with color and power Doppler signal present throughout the length of the involved segment, including discrete elongated vessels and areas of confluent vascularity). Color prints of each examination were interpreted by one author for standardization of Doppler vascularity grading.
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Clinical data were collected and recorded for each visit, which occurred within 3 days of a sonographic examination. The following parameters were recorded: diagnosis, treatment, presence and character of abdominal pain, frequency and character of stools, hematocrit, erythrocyte sedimentation rate, abdominal tenderness, presence or absence of a mass, and WBC. The amount of abdominal pain, degree of stool abnormality, abdominal tenderness with or without mass, hematocrit, and erythrocyte sedimentation rate were scored using the system used to calculate the pediatric Crohn's disease activity index [11] (Table 1). For statistical purposes, these parameters were scored on a scale of 1-3. Records were also reviewed for the results of other diagnostic studies, including upper gastrointestinal series with small-bowel follow-through, abdominal CT, and endoscopy.
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Patients were divided into groups by diagnosis (Crohn's disease and ulcerative colitis) for statistical analysis. Correlation analysis was made between each of the sonographic parameters (bowel wall thickness, color Doppler sonography grade, and power Doppler sonography grade) and between each of the sonographic parameters and each of the seven clinical parameters recorded. This correlation was performed using JMP version 3.1 statistical software (SAS Institute, Cary, NC). Percentage of agreement for direction of change from initial to last sonography for each patient was evaluated comparing each of the three sonographic parameters with one another and with each of the clinical parameters.
In statistically evaluating the agreement in the direction of change, we assumed random distribution of a 33.3% probability that any pair of parameters would change in the same direction—that is, increase, decrease, or remain unchanged. We assumed a 66.6% probability that the pair would not change in the same direction—that is, one may improve while the other remains unchanged. Thus, if we observed that in six of seven instances both parameters changed in the same direction, 87.5% was compared with 33.3% by the Exact Binomial Probability test (NCSS version 6.0, Jerry L. Hintze, Kaysville, UT).
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All patients underwent initial baseline sonography that revealed at least one abnormal, thickened, hyperemic segment of the bowel (Figs. 1 and 2A). In six patients (four with Crohn's disease and two with ulcerative colitis), more than one abnormal bowel segment was identified on initial sonography. A total of 23 abnormal bowel segments were found: 16 segments involved with Crohn's disease and seven with ulcerative colitis. Serial sonography was performed to follow up these abnormal segments during treatment with a variety of antiinflammatory therapies. Each abnormal bowel segment was examined two to eight times (mean, four examinations per segment). There were 6-95 days (mean, 36 days) between the first and last sonography. A total of 88 sonograms were obtained: 61 in the Crohn's disease group and 27 in the ulcerative colitis group.
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Fourteen of the 17 patients (11 with Crohn's disease and three with ulcerative colitis) had disease activity confirmed with another diagnostic study within 7 days (range, 0-7 days; mean, 1 day) of the initial sonography. Seventeen (94%) of these 18 diagnostic studies had positive, or abnormal, results related to the disease. These positive studies included seven upper gastrointestinal studies with small-bowel follow-throughs, five CTs, and five endoscopies. Five patients with Crohn's disease had two studies with positive findings: two underwent both upper gastrointestinal studies with small-bowel follow-through and endoscopy, two underwent both CT and endoscopy, and one underwent both upper gastrointestinal studies with small-bowel follow-through and CT. One patient with Crohn's disease had equivocal CT results but positive endoscopic findings at the time of initial sonography. Three patients with ulcerative colitis underwent endoscopy within 6 days (range, 0-6 days; mean, 1 day) of initial sonography. All three of these endoscopies had positive findings for active disease.
Three patients with Crohn's disease underwent another diagnostic study within 2 days of the last sonography. One patient underwent CT on the day of the last sonography, which, like the sonography, had normal findings. In one patient, CT showed improvement similar to the sonographic findings. In one patient, endoscopic findings were abnormal at the time of the last sonography, which had normal findings. This patient required surgical resection for abnormal bleeding. No patients with ulcerative colitis underwent follow-up diagnostic studies at the time of the last sonography.
Correlation between color Doppler and power Doppler vascularity grading was 100% in all sonograms obtained; hence, we use the term "Doppler sonography" to refer to both of these methods. Correlation was significant between bowel wall thickness and Doppler sonography in both the Crohn's disease (r = 0.602, p < 0.01) and ulcerative colitis (r = 0.623, p < 0.01) patient groups. When bowel wall thickness was greater than 3 mm, the Doppler grade was increased. In the patients with Crohn's disease, the bowel wall thickness measurements and Doppler grades from 61 sonograms were correlated with seven clinical parameters, when available (Table 2). In the ulcerative colitis group, sonographic measurements from 27 sonograms were correlated with the seven clinical parameters, when available (Table 2).
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We performed follow-up examinations in our patients at frequent intervals (every 1-2 weeks). We saw a decrease in both bowel wall thickness and Doppler grade as early as 6 days after initial sonography in one patient. The mean time for a decrease in Doppler grade with a decrease or no change in bowel wall thickness occurred at 25 days (range, 6-72 days) in the 19 bowel segments that showed improvement (Fig. 2B). No change in either bowel wall thickness or Doppler grade was ever documented in four bowel segments. The patients with no change included two patients who each had one moderately inflamed segment that showed improvement and another mildly involved segment that did not appear to improve with therapy. Two other patients who were possibly noncompliant or did not respond to treatment, had evidence of significant inflammation in a single bowel segment on initial sonography that was unchanged on last sonography.
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The percentage of agreement on the direction of change was evaluated using the first and last sonograms obtained on each patient during enrollment in the study. These two studies typically represented before and after treatment. At the time of the last sonography with normal findings, the patient was clinically improved and was no longer undergoing corticosteroid treatment, or therapies were being tapered. Of two patients who did not show improvement, one patient was lost to follow-up early in the treatment of the recurrent disease (8 days), and compliance was questionable in the other patient.
The percentage of agreement was the same for each bowel wall thickness and Doppler sonography grade with the clinical parameters because the two points of disagreement between these two sonographic parameters did not have clinical values. In the patients with Crohn's disease, the percentage of agreement was significant (p < 0.05) in the direction of change of both bowel wall thickness and Doppler sonography grade for five of seven clinical parameters: abdominal pain score, hematocrit score, erythrocyte sedimentation rate, erythrocyte sedimentation rate score, and abdominal tenderness score. In the patients with ulcerative colitis, the percentage of agreement was significant (p < 0.05) in the direction of change between the sonographic parameters and five of seven clinical parameters: abdominal pain score, erythrocyte sedimentation rate, erythrocyte sedimentation rate score, abdominal tenderness score, and WBC.
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The gray-scale sonographic findings in inflammatory bowel disease include bowel wall thickening, reduced bowel compressibility, loss of distinction of normal wall stratification, and loss of colonic haustrations [2, 3, 9, 13, 14]. Most investigators have found sonographic findings to be nonspecific indicators of bowel inflammation [13, 15, 16], but others believe sonography has a role in the differentiation of Crohn's disease and ulcerative colitis [17, 18]. Sheridan et al. [19] used gray-scale sonography in the primary investigation of adult patients with suspected Crohn's disease or recurrent Crohn's disease and reported up to 87% sensitivity and 91% specificity for detection of disease. In children, most authors have concentrated on diagnosis of primary and recurrent disease with sonography. Quillin and Siegel [6] studied a small group of children with acute abdominal pain using color Doppler sonography and suggested that mucosal or transmural hypervascularity on color Doppler sonography can be seen in several inflammatory bowel processes. Siegel et al. [8] also reported that gray-scale and color Doppler sonography helped in the differentiation of causes of bowel wall thickening in children but was most useful when considered with the clinical situation, particularly the age of the patient and location of the disease.
We confirmed that bowel wall inflammation can be revealed on sonography by thickening of the bowel wall (bowel wall thickness >3 mm) and by increased color Doppler and power Doppler signals in the bowel wall. On initial sonography, at least one abnormal bowel segment was identified in all our patients. Most patients were able to identify an area of abdominal tenderness that corresponded to an abnormal segment on sonography. These findings correlated well with those of other diagnostic imaging or endoscopic studies, if these studies were performed.
We compared color Doppler and power Doppler sonography in the evaluation of gastrointestinal inflammation with associated hypervascularity. Power Doppler sonography is more sensitive than color Doppler sonography to low-velocity flow [20] and might be expected to be the preferred method of studying bowel wall vascularity. Clautice-Engle et al. [21] suggested that power Doppler sonography improved visualization of intramural gastrointestinal vascularity, increasing their level of confidence in distinguishing ischemic from nonischemic lesions. In our study, correlation between color Doppler and power Doppler grading was 100% in all examinations, including initial sonography, follow-up sonography, and last sonography with normal findings. Thus, power Doppler sonography did not offer any statistical advantage over color Doppler sonography. However, we noted that subjective visual comparison of the two techniques suggested a more intense confluent pattern of enhancement with power Doppler sonography and it was the preferred imaging method for assessing bowel vascularity in our study.
Previous studies have shown improvement in disease activity in patients with inflammatory bowel disease by changes in bowel wall thickness on sonography 2-4 months after antiinflammatory therapy [9]. In adult patients with ulcerative colitis, response to therapy was documented at 10 days with sonographic measurements of bowel wall thickness and extent (segment length) of disease [22]. In our series, the agreement between bowel wall thickness measurements and the Doppler grade was significant in all examinations. When bowel wall thickness was greater than 3 mm, the Doppler grade was always increased. In addition, we saw a decrease in both bowel wall thickness and Doppler grade as early as 6 days after initial sonography. These results suggest that sonography can be a useful noninvasive tool to assess disease activity during treatment in children with inflammatory bowel disease.
Children with inflammatory bowel disease are treated at diagnosis or at the time of recurrence with multidrug therapy. This frequently includes an empiric course of corticosteroid antiinflammatory therapy. There is no standard end point for this treatment, which may be marked by signs of steroid toxicity. In addition, antiinflammatory agents may mask signs of residual active disease and can have long-term toxic effects. Many attempts have been made to quantify the clinical assessment of disease activity in inflammatory bowel disease. The first Crohn's disease activity index was published in 1976 [23]. Subsequently, multiple indexes have been developed, including a pediatric Crohn's disease activity index [24,25,26,27]. The pediatric Crohn's disease activity index is a cumbersome scoring system, developed primarily for research purposes; however, the authors of the pediatric Crohn's disease activity index have shown that readily available laboratory parameters including erythrocyte sedimentation rate, hematocrit, and albumin, as well as a pediatric gastroenterologist's global assessment, appear to adequately reflect disease activity in most patients with Crohn's disease [11]. Lloyd-Still and Green [28] developed a clinical scoring system for chronic inflammatory bowel disease (both Crohn's disease and ulcerative colitis) in children. They found that albumin as a single laboratory parameter correlated well with disease activity. There are other scoring systems for ulcerative colitis alone, but none has been specifically designed for pediatric patients [29,30,31].
No specific scoring system is used to follow up either disease at our institution. A history, physical examination, and laboratory examination are routinely obtained and recorded in the patient's record at each visit. Because most of the published activity indexes for both Crohn's disease and ulcerative colitis include some if not all the clinical and laboratory parameters routinely recorded, we compared these existing clinical data with our sonographic data.
In our study, bowel wall thickness and Doppler grades both correlated with the erythrocyte sedimentation rate (and the erythrocyte sedimentation rate score) in all patients. In the patients with Crohn's disease, correlation was also significant between the Doppler grade and the abdominal pain score and stools score. In our patients with ulcerative colitis, the bowel wall thickness measurements also correlated with abdominal pain and stools scores, and the Doppler grade also correlated with the abdominal pain score.
When evaluating change in disease activity as depicted on sonography compared with clinical parameters, both sonographic measurements correlated with more than the erythrocyte sedimentation rate. Abdominal pain and abdominal tenderness scores also correlated with bowel wall thickness and Doppler sonographic findings, with a change in the same direction (improved, worsened, or no change) in patients with Crohn's disease and in those with ulcerative colitis. However, in one patient with Crohn's disease, the correlation was poor, with decreased bowel wall thickness and lower Doppler grade with a worsening clinical prognosis, despite therapy. This patient, in whom treatment was considered a failure, eventually underwent bowel resection for persistent bleeding.
One potential flaw in our study is related to the retrospective collection of clinical data. We used data points for correlation analysis if the clinical points were collected within 3 days of the sonography. Furthermore, the use of clinical and laboratory parameters in patients with Crohn's disease as an indicator of disease activity may not always be reliable. Normal erythrocyte sedimentation rate values have been noted in those with severely active disease [11].
Another potential problem is that measurement of bowel wall thickness is sometimes difficult on sonography. At times, the lumen may be difficult to identify, or multiple diseased adherent loops of small bowel may make accurate measurement of one bowel wall difficult. This has also been reported by other authors [18]. In this circumstance, we found that the overall thickness of the diseased loops of the bowel decreased with clinical improvement of the patient. One concern about the use of sonography in patients with inflammatory bowel disease was the possibility that the entire extent of bowel disease may not be identified. However, one could infer that if a response to treatment is seen in one segment, a similar response might be anticipated in other areas of involvement.
Another limitation was the lack of an independent gold standard confirming resolution of bowel inflammation. Fluoroscopy, CT, and endoscopy each have inherent limitations in defining the severity and extent of disease. Repeated CT or fluoroscopy would increase the radiation dose to the patient, and endoscopy is difficult to justify in patients with clinical signs of improvement. However, at least one study has reported correlation between sonography and the gold standard, endoscopy, at both the time of diagnosis and of recurrence in children with both Crohn's disease and ulcerative colitis [32]. Recently, 99mTc WBC scintigraphy has been shown to be an accurate diagnostic test for extent and distribution of inflammation in children with inflammatory bowel disease [33]. This examination is more invasive and time-consuming, but may be an additional method of assessing response.
Our study shows that sonography can reveal inflammatory bowel disease and its apparent improvement or lack of improvement with treatment. The noninvasive and relatively quick direct visualization of the diseased segment adds information not obtainable by indirect assessment of splanchnic perfusion [34] or by laboratory studies and physical examination and is similar to sonographic assessment of other disease states such as pyloric stenosis, intussussception, and pelvic inflammatory disease. Potential clinical applications include confirming or excluding an active site of disease when a palpable abdominal fullness is present on follow-up, adding a level of certainty to the sometimes difficult clinical diagnosis of a flare in disease activity; confirming the presence of abnormal bowel in a patient in whom the diagnosis of inflammatory bowel disease has not yet been definitively established; and replacing upper gastrointestinal series with small-bowel follow-through examinations to assess response to treatment. Whether sonography can be used independently of laboratory studies in guiding therapy remains to be evaluated.
In conclusion, bowel wall thickness and Doppler grading of bowel wall vascularity correlate with common laboratory and clinical parameters of disease activity in patients with Crohn's disease and ulcerative colitis. Sonography shows therapy-induced changes in bowel disease activity in patients with inflammatory bowel disease and may have a future role in directing therapy.
Acknowledgments
We thank John R. Claybaugh for statistical advice and analysis, Patricia
Ganley for her assistance with patient recruitment, and Cathy Brown-Jones and
Linda Rebolo for their assistance in performing the sonography.
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