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Ultrasonographic Difference between Salmonella Enterocolitis and Rotavirus Gastroenteritis in Children
M.C. Lee and L.H. Lin
Ultrasonographic Difference between Salmonella Enterocolitis and Rotavirus Gastroenteritis in Children Ming-Che Lee and Lung-Huang Lin
Background: Salmonella is an important cause of severe bacterial enterocolitis in children. Results of traditional diagnostic culture methods take at least 24 to 72 hours. Due to the easy availability and noninvasiveness of ultrasonography, we investigated whether or not imaging studies could provide faster results. Materials and Methods: From November 1, 2000 to October 25, 2001, we collected 48 continuous patients with Salmonella enterocolitis as the study group and 52 continuous patients with rotavirus gastroenteritis as the control group. We measured the thickness of the right lower quadrant colonic wall and sought to learn whether or not there were ascites behind the bladder and/or in Douglas’s pouch. Thickness of the colonic wall greater than 5 mm was defined as abnormal. Results: The mean thickness of the colonic wall of the study group was greater than that of the control group (p < 0.01). A total of 41 patients in the study group had colonic wall thickening, but only one patient in the rotavirus control group had thickening (p < 0.01). The mean C-reactive protein, white blood cell (WBC) count and percentage of neutrophils in the WBC differential classification were statistically different between the study and control groups (p < 0.01, p = 0.04, p = 0.02, respectively). A total of 41 patients in the study group had occult blood (≥ ±) in their stool; 17 patients in the control group had stool occult blood (p < 0.01). Conclusion: We emphasize that, although ultrasonography did not enable us to make a definitive diagnosis of Salmonella enterocolitis, it could be used to identify the pathologic changes in the bowel and intraabdominal lesions, and to grade the degree of enterocolitic invasion. (J Med Ultrasound 2002;10:76–79) KEY WORDS: • colonic wall thickness • enterocolitis • gastroenteritis • rotavirus • Salmonella • ultrasonography
Received: March 29, 2002. Accepted: June 3, 2002. Department of Pediatrics, Cathay General Hospital, Taipei, Taiwan. Address correspondence and reprint requests to: Dr. Lung-Huang Lin, Department of Pediatrics, Cathay General Hospital, 280, Section 4, Jen-Ai Road, Taipei, Taiwan.
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J Med Ultrasound 2002 • Vol 10 • No 2
Sonography in Enterocolitis
INTRODUCTION Acute gastroenteritis is a common disease in young children throughout the world. In developing countries, the incidence ranges from 3.5 to 7.0 episodes per child per year during the first 2 years of life and from two to five episodes per child per year for the first 5 years [1]. In Taiwan, diarrhea occurs in about 11.4% of pediatric admissions [2]. Salmonella spp. are known to cause mainly community-acquired diarrhea and are common pathogens of acute diarrhea among hospitalized children [3, 4]. Salmonella infection can cause gastroenteritis, meningitis, bacteremia or even enteric fever [5]. The traditional diagnostic method is bacterial culture, which takes at least 24 to 72 hours. The white blood cell (WBC) count and other inflammatory parameters can only offer indirect evidence of infection. Due to the easy availability and noninvasiveness of ultrasonography, we investigated whether or not imaging studies could provide faster results of Salmonella enterocolitis infection. Because rotavirus infection is the most common viral etiology of severe, acute diarrhea among children [1], we used rotavirus gastroenteritis patients as the control group for comparison of the imaging differences between children with Salmonella enterocolitis and rotavirus infections.
PATIENTS
AND
than 5 mm was defined as abnormal [6]. Additionally, we also determined C-reactive protein (CRP) levels, WBC count and stool occult blood (OB) within the first 3 days after initial presentation with diarrhea. Student’s t-distribution, the χ2 test and F-test were used for statistical analysis.
RESULTS Among the 48 patients in the study group, there were 33 boys and 15 girls; their mean age was 22.3 ± 18.0 months. Among the 52 patients in the control group, there were 20 boys and 32 girls; their mean age was 36.9 ± 26.2 months. The mean thickness of the colonic wall was 5.39 ± 0.81 (standard deviation, SD) mm in the study
A
METHODS
From November 1, 2000 to October 25, 2001, we enrolled 48 continuous patients with Salmonella enterocolitis into the study group; Salmonella infection was confirmed by stool bacterial culture. Another 52 continuous patients with rotavirus gastroenteritis served as the control group; rotavirus gastroenteritis was confirmed by a latex agglutinin test. We performed abdominal sonography within the first 3 days after the initial presentation of diarrhea. All patients were examined by the same experienced pediatric gastroenterologist. Ultrasonography was performed using high-resolution, real-time computed sonography with an Acuson 128XP with 5, 6 and 7 MHz transducers (Mountain View, CA, USA). We measured the thickness of the colonic wall in the right lower quadrant and sought to learn whether or not there was ascites behind the bladder and/or in Douglas’ pouch (see the Figure for representative sonographs). Thickness of the colonic wall greater J Med Ultrasound d 2002 • Vol 10 • No 2
B
Figure. Ultrasonography of the right lower quadrant in (A) a study group patient with Salmonella enterocolitis showing colonic wall thickening (thickness = 6.2 mm) and (B) a control group patient showing normal colonic wall thickness (1.7 mm).
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M.C. Lee and L.H. Lin
Table 1. Thickness of the colonic wall and laboratory results of the study and control groups Study group (n = 48) Colonic wall thickness (mm) CRP (mg/dL) WBC count (/μL) Neutrophils (%)
5.39 ± 0.81 9.45 ± 9.62 10,533 ± 4,106 54.2 ± 17.7
Control group (n = 52)
t
p
± ± ± ±
25.79 6.10 2.07 –2.34
< 0.01 < 0.01 0.04 0.02
1.73 1.24 9,036 62.9
0.60 1.25 3,098 19.3
The study group comprised patients with Salmonella enterocolitis; the control group comprised patients with rotavirus gastroenteritis. CRP = C-reactive protein; WBC = white blood cell.
group, and 1.73 ± 0.60 mm in the control group (Table 1). The difference in mean thickness of the colonic wall was statistically significant (p < 0.01). There were 41 study group patients with colonic wall thickening (≥ 5 mm), but there was only one patient with thickening in the control group (p < 0.01, Table 2). There was no ascites noted in either group. The mean CRP levels in the study and control groups were 9.45 ± 9.62 mg/dL and 1.24 ± 1.25 mg/dL, respectively (p < 0.01). The mean WBC counts were 10,533 ± 4,106/μL and 9,036 ± 3,098/μL in the study and control groups, respectively (p = 0.04) (Table 1). While the percentage of neutrophils (WBC differential classification) was significantly different between the study and control groups (p = 0.02, Table 1), the mean neutrophil percentages of both groups fell within the normal range (54%–62%). This may mean that the application of neutrophil differential percentage has little function in distinguishing between Salmonella and rotavirus infection. There were 41 patients with stool OB (≥ ±) in the study group and 17 patients with OB in the control group (p < 0.01). Only one patient in the control group had stool OB of 3+ (Table 2).
DISCUSSION The sensitivity of ultrasonography to detect bowel wall thickening is about 75% [7]. Bowel wall thick-
ening can be seen in a variety of bowel diseases, including infectious enterocolitis, inflammatory bowel disease, bleeding disorders, infiltrative disease, neutropenic colitis, ischemic enteritis, leukemic or lymphomatous infiltration and pseudomembranous colitis [8–15]. The mechanism of inflammatory changes in bowel wall thickening involves mucosal or transmural hyperemia [10]. In acute diarrhea, viral pathogens generally produce injury to the proximal small bowel and bacterial pathogens usually cause colonic injury [16]. In our study, we compared the ultrasonographic differences in colonic wall thickness between patients with Salmonella enterocolitis and patients with rotavirus gastroenteritis. Of the 48 patients in the study group, seven did not show colonic wall thickening. The mean CRP of these seven patients was 1.43 mg/dL (range, 0.41–4.6 mg/dL; SD = 1.45 mg/dL), which was significantly lower than the other 41 patients in the study group (p < 0.01). This might be because these seven patients had less severe Salmonella infections than the other study group patients [17, 18]. There was one control group patient with colonic wall thickening (5.6 mm). The CRP of this patient was 5.5 mg/dL. One possible explanation for this unexpected thickening is that this patient might have been coinfected with a rotavirus and a bacterium, but the bacterial etiologic agent failed to be isolated. There were no patients in our study group with ascites. This result differed from that of Ueda et al [8].
Table 2. Differences between the study and control groups in colonic wall thickening and stool occult blood appearance
Colonic wall thickening (≥ 5 mm) Stool occult blood ≥ ± Stool occult blood ≥ + Stool occult blood ≥ 2+ Stool occult blood ≥ 3+
Study group (n = 48)
Control group (n = 52)
χ2
p
41/48 41/48 22/48 8/48 1/48
1/52 17/52 6/52 2/52 1/52
73.83 40.98 19.21 6.12 —
< 0.01 < 0.01 < 0.01 0.013 —
The study group comprised patients with Salmonella enterocolitis; the control group comprised patients with rotavirus gastroenteritis.
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J Med Ultrasound 2002 • Vol 10 • No 2
Sonography in Enterocolitis
Table 3. Correlation between thickness of the colonic wall and C-reactive protein (CRP) in the study group Thickness of colonic wall & CRP
r
F
p
0.432
10.54
0.002
The OB appearance (≥ ±) between the study group and control group differed significantly. Nonetheless, the degree of stool OB in the study group was not severe (Table 2). There was only one patient in the study group and one in the control group with stool OB greater than or equal to 3+. In the study group, the thickness of the colonic wall and the CRP level showed significant correlation (p < 0.01, Table 3). This suggests that ultrasonography may be a useful noninvasive diagnostic tool for grading the severity of enterocolitis. The application of ultrasonography to other bowel diseases includes tuberculosis and vascular bowel disease [8, 19]. Moreover, the ultrasonographic features of other bacterial etiologic agents of enterocolitis such as Shigella, Campylobacter, Yersinia and Escherichia coli need further study in order to gain more information on the significance of these ultrasonographic changes. In conclusion, we emphasize that, although ultrasonography does not enable us to make a definitive diagnosis of Salmonella enterocolitis, it can be used to identify the pathologic changes in the bowel and intraabdominal lesions, and to evaluate the invasiveness of the enterocolitis.
REFERENCES 1. Black RE. Epidemiology of diarrheal disease: implications for control by vaccines. Vaccine 1993;11: 100–6. 2. Lee MC, Lin LH, Hung KL, et al. Oral bacterial therapy promotes recovery from acute diarrhea in children. Acta Pediatr Taiwan 2001;42:301–5. 3. Rohner P, Pittet D, Pepey B, et al. Etiology agents of infectious diarrhea: implications for requests for microbial culture. J Clin Microbiol 1997;35: 1427–32. 4. Biswas R, Lyon DJ, Nelson EAS, et al. Aetiology of acute diarrhea in hospitalized children in Hong Kong. Trop Med Int Health 1996;1:679–83. 5. Alessio F. Intestinal infections. In: Walker WA, Durie PR, Hamilton JR, et al, Eds. Pediatric Gastrointestinal
J Med Ultrasound 2002 • Vol 10 • No 2
Disease, 3rd ed. Canada: BC Decker, 2000:465–7. 6. Fleischer AC, Muhletaler CA, James AE Jr. Sonographic assessment of the bowel wall. AJR Am J Roentgenol 1981;136:887–91. 7. Siegel MJ, Friedland JA, Hildebolt CF. Bowel wall thickening in children: differentiation with US. Radiology 1997;203:631–5. 8. Ueda D, Sato T, Yoshida M. Ultrasonographic assessment of Salmonella enterocolitis in children. Pediatr Radiol 1999;29:469–71. 9. Philpotts LE, Heiken JP, Westcott MA, et al. Colitis: use of CT findings in differential diagnosis. Radiology 1994;190:445–9. 10. Quillin SP, Siegel MJ. Gastrointestinal inflammation in children: color Doppler ultrasonography. J Ultrasound Med 1994;13:751–6. 11. Downey DB, Wilson SR. Pseudomembranous colitis: sonographic features. Radiology 1991;180:61–4. 12. Teefey SA, Roarke MC, Brink JA, et al. Bowel wall thickening: differentiation of inflammation from ischemia with color Doppler and duplex US. Radiology 1996;198:547–51. 13. Khaw KT, Yeoman LJ, Saverymuttu SH, et al. Ultrasonic patterns in inflammatory bowel disease. Clin Radiol 1991;43:171–5. 14. Glass-Royal MC, Choyke PL, Gootenberg JE, et al. Sonography in the diagnosis of neutropenic colitis. J Ultrasound Med 1987;6:671–3. 15. Bolondi L, Ferrentino M, Trevisani F, et al. Sonographic appearance of pseudomembranous colitis. J Ultrasound Med 1985;4:489–92. 16. Semeao E, Mulberg AE. Diarrhea acute. In: Schwartz MW, Bell LM, Bingham PM, et al, eds. The 5-Minute Pediatric Consult, 2nd ed. Philadelphia: Lippincott Williams & Wilkins, 2000:326–7. 17. Olubuyide IO, Brown NM, Higginson J, et al. The value of C-reactive protein in the diagnosis of intestinal perforation in typhoid fever. Ann Clin Biochem 1989; 26:246–8. 18. Lin PY, Huang YC, Chang LY, et al. C-reactive protein in childhood non-typhi Salmonella gastroenteritis with and without bacteria. Pediatr Infect Dis J 2000;19:754–5. 19. Bomelburg T, Claasen U, Von Lengerke HJ. Intestinal ultrasonographic findings in Schonlein-Henoch syndrome. Eur J Pediatr 1991;150:158–60.
79
Ultrasonographic Difference between Salmonella Enterocolitis and Rotavirus Gastroenteritis in Children Ming-Che Lee and Lung-Huang Lin
Background: Salmonella is an important cause of severe bacterial enterocolitis in children. Results of traditional diagnostic culture methods take at least 24 to 72 hours. Due to the easy availability and noninvasiveness of ultrasonography, we investigated whether or not imaging studies could provide faster results. Materials and Methods: From November 1, 2000 to October 25, 2001, we collected 48 continuous patients with Salmonella enterocolitis as the study group and 52 continuous patients with rotavirus gastroenteritis as the control group. We measured the thickness of the right lower quadrant colonic wall and sought to learn whether or not there were ascites behind the bladder and/or in Douglas’s pouch. Thickness of the colonic wall greater than 5 mm was defined as abnormal. Results: The mean thickness of the colonic wall of the study group was greater than that of the control group (p < 0.01). A total of 41 patients in the study group had colonic wall thickening, but only one patient in the rotavirus control group had thickening (p < 0.01). The mean C-reactive protein, white blood cell (WBC) count and percentage of neutrophils in the WBC differential classification were statistically different between the study and control groups (p < 0.01, p = 0.04, p = 0.02, respectively). A total of 41 patients in the study group had occult blood (≥ ±) in their stool; 17 patients in the control group had stool occult blood (p < 0.01). Conclusion: We emphasize that, although ultrasonography did not enable us to make a definitive diagnosis of Salmonella enterocolitis, it could be used to identify the pathologic changes in the bowel and intraabdominal lesions, and to grade the degree of enterocolitic invasion. (J Med Ultrasound 2002;10:76–79) KEY WORDS: • colonic wall thickness • enterocolitis • gastroenteritis • rotavirus • Salmonella • ultrasonography
Received: March 29, 2002. Accepted: June 3, 2002. Department of Pediatrics, Cathay General Hospital, Taipei, Taiwan. Address correspondence and reprint requests to: Dr. Lung-Huang Lin, Department of Pediatrics, Cathay General Hospital, 280, Section 4, Jen-Ai Road, Taipei, Taiwan.
76
J Med Ultrasound 2002 • Vol 10 • No 2
Sonography in Enterocolitis
INTRODUCTION Acute gastroenteritis is a common disease in young children throughout the world. In developing countries, the incidence ranges from 3.5 to 7.0 episodes per child per year during the first 2 years of life and from two to five episodes per child per year for the first 5 years [1]. In Taiwan, diarrhea occurs in about 11.4% of pediatric admissions [2]. Salmonella spp. are known to cause mainly community-acquired diarrhea and are common pathogens of acute diarrhea among hospitalized children [3, 4]. Salmonella infection can cause gastroenteritis, meningitis, bacteremia or even enteric fever [5]. The traditional diagnostic method is bacterial culture, which takes at least 24 to 72 hours. The white blood cell (WBC) count and other inflammatory parameters can only offer indirect evidence of infection. Due to the easy availability and noninvasiveness of ultrasonography, we investigated whether or not imaging studies could provide faster results of Salmonella enterocolitis infection. Because rotavirus infection is the most common viral etiology of severe, acute diarrhea among children [1], we used rotavirus gastroenteritis patients as the control group for comparison of the imaging differences between children with Salmonella enterocolitis and rotavirus infections.
PATIENTS
AND
than 5 mm was defined as abnormal [6]. Additionally, we also determined C-reactive protein (CRP) levels, WBC count and stool occult blood (OB) within the first 3 days after initial presentation with diarrhea. Student’s t-distribution, the χ2 test and F-test were used for statistical analysis.
RESULTS Among the 48 patients in the study group, there were 33 boys and 15 girls; their mean age was 22.3 ± 18.0 months. Among the 52 patients in the control group, there were 20 boys and 32 girls; their mean age was 36.9 ± 26.2 months. The mean thickness of the colonic wall was 5.39 ± 0.81 (standard deviation, SD) mm in the study
A
METHODS
From November 1, 2000 to October 25, 2001, we enrolled 48 continuous patients with Salmonella enterocolitis into the study group; Salmonella infection was confirmed by stool bacterial culture. Another 52 continuous patients with rotavirus gastroenteritis served as the control group; rotavirus gastroenteritis was confirmed by a latex agglutinin test. We performed abdominal sonography within the first 3 days after the initial presentation of diarrhea. All patients were examined by the same experienced pediatric gastroenterologist. Ultrasonography was performed using high-resolution, real-time computed sonography with an Acuson 128XP with 5, 6 and 7 MHz transducers (Mountain View, CA, USA). We measured the thickness of the colonic wall in the right lower quadrant and sought to learn whether or not there was ascites behind the bladder and/or in Douglas’ pouch (see the Figure for representative sonographs). Thickness of the colonic wall greater J Med Ultrasound d 2002 • Vol 10 • No 2
B
Figure. Ultrasonography of the right lower quadrant in (A) a study group patient with Salmonella enterocolitis showing colonic wall thickening (thickness = 6.2 mm) and (B) a control group patient showing normal colonic wall thickness (1.7 mm).
77
M.C. Lee and L.H. Lin
Table 1. Thickness of the colonic wall and laboratory results of the study and control groups Study group (n = 48) Colonic wall thickness (mm) CRP (mg/dL) WBC count (/μL) Neutrophils (%)
5.39 ± 0.81 9.45 ± 9.62 10,533 ± 4,106 54.2 ± 17.7
Control group (n = 52)
t
p
± ± ± ±
25.79 6.10 2.07 –2.34
< 0.01 < 0.01 0.04 0.02
1.73 1.24 9,036 62.9
0.60 1.25 3,098 19.3
The study group comprised patients with Salmonella enterocolitis; the control group comprised patients with rotavirus gastroenteritis. CRP = C-reactive protein; WBC = white blood cell.
group, and 1.73 ± 0.60 mm in the control group (Table 1). The difference in mean thickness of the colonic wall was statistically significant (p < 0.01). There were 41 study group patients with colonic wall thickening (≥ 5 mm), but there was only one patient with thickening in the control group (p < 0.01, Table 2). There was no ascites noted in either group. The mean CRP levels in the study and control groups were 9.45 ± 9.62 mg/dL and 1.24 ± 1.25 mg/dL, respectively (p < 0.01). The mean WBC counts were 10,533 ± 4,106/μL and 9,036 ± 3,098/μL in the study and control groups, respectively (p = 0.04) (Table 1). While the percentage of neutrophils (WBC differential classification) was significantly different between the study and control groups (p = 0.02, Table 1), the mean neutrophil percentages of both groups fell within the normal range (54%–62%). This may mean that the application of neutrophil differential percentage has little function in distinguishing between Salmonella and rotavirus infection. There were 41 patients with stool OB (≥ ±) in the study group and 17 patients with OB in the control group (p < 0.01). Only one patient in the control group had stool OB of 3+ (Table 2).
DISCUSSION The sensitivity of ultrasonography to detect bowel wall thickening is about 75% [7]. Bowel wall thick-
ening can be seen in a variety of bowel diseases, including infectious enterocolitis, inflammatory bowel disease, bleeding disorders, infiltrative disease, neutropenic colitis, ischemic enteritis, leukemic or lymphomatous infiltration and pseudomembranous colitis [8–15]. The mechanism of inflammatory changes in bowel wall thickening involves mucosal or transmural hyperemia [10]. In acute diarrhea, viral pathogens generally produce injury to the proximal small bowel and bacterial pathogens usually cause colonic injury [16]. In our study, we compared the ultrasonographic differences in colonic wall thickness between patients with Salmonella enterocolitis and patients with rotavirus gastroenteritis. Of the 48 patients in the study group, seven did not show colonic wall thickening. The mean CRP of these seven patients was 1.43 mg/dL (range, 0.41–4.6 mg/dL; SD = 1.45 mg/dL), which was significantly lower than the other 41 patients in the study group (p < 0.01). This might be because these seven patients had less severe Salmonella infections than the other study group patients [17, 18]. There was one control group patient with colonic wall thickening (5.6 mm). The CRP of this patient was 5.5 mg/dL. One possible explanation for this unexpected thickening is that this patient might have been coinfected with a rotavirus and a bacterium, but the bacterial etiologic agent failed to be isolated. There were no patients in our study group with ascites. This result differed from that of Ueda et al [8].
Table 2. Differences between the study and control groups in colonic wall thickening and stool occult blood appearance
Colonic wall thickening (≥ 5 mm) Stool occult blood ≥ ± Stool occult blood ≥ + Stool occult blood ≥ 2+ Stool occult blood ≥ 3+
Study group (n = 48)
Control group (n = 52)
χ2
p
41/48 41/48 22/48 8/48 1/48
1/52 17/52 6/52 2/52 1/52
73.83 40.98 19.21 6.12 —
< 0.01 < 0.01 < 0.01 0.013 —
The study group comprised patients with Salmonella enterocolitis; the control group comprised patients with rotavirus gastroenteritis.
78
J Med Ultrasound 2002 • Vol 10 • No 2
Sonography in Enterocolitis
Table 3. Correlation between thickness of the colonic wall and C-reactive protein (CRP) in the study group Thickness of colonic wall & CRP
r
F
p
0.432
10.54
0.002
The OB appearance (≥ ±) between the study group and control group differed significantly. Nonetheless, the degree of stool OB in the study group was not severe (Table 2). There was only one patient in the study group and one in the control group with stool OB greater than or equal to 3+. In the study group, the thickness of the colonic wall and the CRP level showed significant correlation (p < 0.01, Table 3). This suggests that ultrasonography may be a useful noninvasive diagnostic tool for grading the severity of enterocolitis. The application of ultrasonography to other bowel diseases includes tuberculosis and vascular bowel disease [8, 19]. Moreover, the ultrasonographic features of other bacterial etiologic agents of enterocolitis such as Shigella, Campylobacter, Yersinia and Escherichia coli need further study in order to gain more information on the significance of these ultrasonographic changes. In conclusion, we emphasize that, although ultrasonography does not enable us to make a definitive diagnosis of Salmonella enterocolitis, it can be used to identify the pathologic changes in the bowel and intraabdominal lesions, and to evaluate the invasiveness of the enterocolitis.
REFERENCES 1. Black RE. Epidemiology of diarrheal disease: implications for control by vaccines. Vaccine 1993;11: 100–6. 2. Lee MC, Lin LH, Hung KL, et al. Oral bacterial therapy promotes recovery from acute diarrhea in children. Acta Pediatr Taiwan 2001;42:301–5. 3. Rohner P, Pittet D, Pepey B, et al. Etiology agents of infectious diarrhea: implications for requests for microbial culture. J Clin Microbiol 1997;35: 1427–32. 4. Biswas R, Lyon DJ, Nelson EAS, et al. Aetiology of acute diarrhea in hospitalized children in Hong Kong. Trop Med Int Health 1996;1:679–83. 5. Alessio F. Intestinal infections. In: Walker WA, Durie PR, Hamilton JR, et al, Eds. Pediatric Gastrointestinal
J Med Ultrasound 2002 • Vol 10 • No 2
Disease, 3rd ed. Canada: BC Decker, 2000:465–7. 6. Fleischer AC, Muhletaler CA, James AE Jr. Sonographic assessment of the bowel wall. AJR Am J Roentgenol 1981;136:887–91. 7. Siegel MJ, Friedland JA, Hildebolt CF. Bowel wall thickening in children: differentiation with US. Radiology 1997;203:631–5. 8. Ueda D, Sato T, Yoshida M. Ultrasonographic assessment of Salmonella enterocolitis in children. Pediatr Radiol 1999;29:469–71. 9. Philpotts LE, Heiken JP, Westcott MA, et al. Colitis: use of CT findings in differential diagnosis. Radiology 1994;190:445–9. 10. Quillin SP, Siegel MJ. Gastrointestinal inflammation in children: color Doppler ultrasonography. J Ultrasound Med 1994;13:751–6. 11. Downey DB, Wilson SR. Pseudomembranous colitis: sonographic features. Radiology 1991;180:61–4. 12. Teefey SA, Roarke MC, Brink JA, et al. Bowel wall thickening: differentiation of inflammation from ischemia with color Doppler and duplex US. Radiology 1996;198:547–51. 13. Khaw KT, Yeoman LJ, Saverymuttu SH, et al. Ultrasonic patterns in inflammatory bowel disease. Clin Radiol 1991;43:171–5. 14. Glass-Royal MC, Choyke PL, Gootenberg JE, et al. Sonography in the diagnosis of neutropenic colitis. J Ultrasound Med 1987;6:671–3. 15. Bolondi L, Ferrentino M, Trevisani F, et al. Sonographic appearance of pseudomembranous colitis. J Ultrasound Med 1985;4:489–92. 16. Semeao E, Mulberg AE. Diarrhea acute. In: Schwartz MW, Bell LM, Bingham PM, et al, eds. The 5-Minute Pediatric Consult, 2nd ed. Philadelphia: Lippincott Williams & Wilkins, 2000:326–7. 17. Olubuyide IO, Brown NM, Higginson J, et al. The value of C-reactive protein in the diagnosis of intestinal perforation in typhoid fever. Ann Clin Biochem 1989; 26:246–8. 18. Lin PY, Huang YC, Chang LY, et al. C-reactive protein in childhood non-typhi Salmonella gastroenteritis with and without bacteria. Pediatr Infect Dis J 2000;19:754–5. 19. Bomelburg T, Claasen U, Von Lengerke HJ. Intestinal ultrasonographic findings in Schonlein-Henoch syndrome. Eur J Pediatr 1991;150:158–60.
79