Ultrasound in the diagnosis of Typhoid fever
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《美国医学杂志》
1 Department of Radiodiagnosis, Asian Institute of Gastroenterology & Nitya Diagnostic Centre, Hyderabad, India
2 Department of Radiodiagnosis, Nitya Diagnostic Centre, Hyderabad, India
3 Department of Radiodiagnosis, Gandhi Hospital, Hyderabad, India
4 Department of Radiodiagnosis, Asian Institute of Gastroenterology, Hyderabad, India
Abstract
Objectives. To establish the efficacy of ultrasound (US) of the abdomen as a diagnostic test in Typhoid. To determine the ultrasound diagnostic criteria in cases of Typhoid. Methods. The Widal test is the most commonly used method of detecting Typhoid fever, but does not provide results until a week after onset of fever due to the need for enough antibodies to develop to render a positive result. Abdominal Ultrasound was performed within three days of the onset of fever in 80 cases suspected to be having Typhoid fever. Subsequent follow -up scans were performed at five days, ten days and fifteen days. Subsequently, all 80 cases were found to be Widal positive and Salmonella culture was positive in 32 cases. We present our findings in 26 patients in the age group between 4 to 20 years in whom both Widal test and Salmonella culture was subsequently positive. Results. The US findings were as follows: splenomegaly (n-26, 100%); Bowel wall thickening (n-22, 85%); mesenteric lymphadenopathy(n-20,77%); hepatomegaly with normal parenchymal echotexture (n-8, 31%); thickened gall bladder (n-16, 62%); biliary sludge (n-6, 23%); positive US Murphy's sign (n-7, 27%); pericholecystic edema with increased vascularity (n-6, 23%); mucosal ulceration in the wall of the gall bladder (n-1, 3.8%). Conclusion. In endemic areas like India, ultrasound findings of hepatomegaly, splenomegaly, ileal and cecal thickening, mesenteric lymphadenopathy and thick-walled gallbladder are diagnostic features of typhoid. Ultrasound can be a non-invasive, economical and a reasonably sensitive tool for diagnosing typhoid when serology is equivocal and cultures are negative.
Keywords: Bowel ultrasound; Typhoid fever; Enteric fever
Enteric fever is caused by Salmonella More Details typhi and paratyphi bacilli and is endemic in many parts of the third world. In India, it is the fifth most common infectious disease with a high rate of complications. Atypical clinical findings make an early diagnosis difficult.[1] Definitive diagnosis of typhoid fever is made by hemoculture and serological tests, namely Widal test, both requiring from some days to over a week to show positive results.[2] Improper and inadequate use of antibiotics leads to sterile cultures adding to the difficulty in diagnosis. Imaging techniques have not generally been used in the diagnostic approach to typhoid fever. The present study was aimed at determining the usefulness of US in the early diagnosis of typhoid fever.
Material and methods
This study was conducted between July 1995 and July 2005 on eighty patients (M-52, F-28) clinically suspected to be having typhoid fever. Age of the patients ranged from 4 years to 58 years. All the eighty patients were subsequently found to be widal positive. Salmonella culture was positive in 32 patients. 26 of these patients were less than 20 years of age. These 26 patients (M-16, F-10) formed the study group. The age of the patients in the study group ranged from 4 years to 20 years.
Abdominal US examination was performed within one to three days of hospital admission. We used a convex transducer with frequency of 3.5 to 5 MHz and a linear transducer with a frequency of 7 to 12 MHz on the US machine (Logic 400, GE; Logic 500, GE; Sonolayer, Toshiba; Voluson 730 Pro, GE)
All ultrasound examinations were started with the examination of the liver wherein the size and echotexture were noted. The gall bladder was next examined concentrating on its size, luminal contents, mucosal surface, wall thickness, U/S Murphy's sign, pericholecystic edema and fluid collection. The spleen was examined concentrating on the size and echotexture. After examining the upper abdomen, the lower abdomen was examined according to the graded compression method described by Puyleart.[3] This started with the study of lower right abdominal quadrant where the ileocecal region Figure1 and the ascending colon were recognized. From this point the probe was moved upwards along the right flank unto the right hypochondrium, then transversely along the epigastrium to the left hypochondrium and then downwards along the left flank to the hypogastrium and pelvis thus studying the entire colon from cecum to the rectum. Multiple transverse & longitudinal scans of the abdomen and pelvis were then performed for the study of the small bowel to identify any areas of wall thickening. Measurement of the thickness of the bowel wall was performed by positioning the calipers between the outer margin of the inner hyperechoic layer & the outer hyperechoic layer Figure2. The thickness was considered abnormal when it measured more than 3mm.[3] Using a similar technique, enlarged mesenteric lymph nodes were visualized Figure3. Following the initial scan, the ultrasound was repeated in all patients on the fifth, tenth and fifteenth day.
Results
All 26 patients could be successfully studied by ultrasound. No patient required analgesia to achieve the adequate bowel compression. The average duration of the US examination was 20 minutes.
All 26 cases showed diffuse enlargement of the spleen. In 22 cases the spleen showed a normal echotexture Figure4. 4 cases had abscess formation in the spleen. In one eight-year-old, child the abscess was 12 × 10 cm and the patient required laparotomy and drainage as it was not responding to repeated aspirations with percutaneous drainage. Splenomegaly persisted in all 26 patients even at the follow up scan done on the 15th day. However, there was a significant decrease in the size of the spleen.
Bowel wall thickening was noted in 22 cases. 12 cases showed increased wall thickness of the terminal ileum and cecum Figure5. 7 cases showed only ileal thickening, the maximum thickness noted was 9 mm. In three cases there were thickening of the whole colon from the cecum to the rectum. The increase in the bowel wall thickness was due to edema of the mucosa and submucosa. But the five layer intestinal wall structure was maintained in all cases. In one case there was an ileal perforation and pelvic abscess formation which responded to conservative management and percutaneous drainage. The bowel wall thickening resolved by 10 days in 70% of cases and by 15 days in the rest.
Enlarged mesenteric lymph nodes ranging in diameter from 8 to 34 mm (mean 18 mm) was noted in 20 cases. The lymph nodes were oval or rounded, hypoechoic structures with well defined margins seen in groups of 5 to 10. Mesenteric lymphadenopathy resolved in 60% of cases in 15 days. In the remaining 40 %, the size and number of lymph nodes decreased significantly.
The gall bladder was distended and thick walled Figure6 in 16 cases. Dense biliary sludge Figure7 was noted in 6 cases. US Murphy's sign was positive in 7 cases. Pericholecystic edema was seen in 6 cases. Color Doppler revealed increase in vascularity in thickened wall Figure8. Pericholecystic fluid collection was seen in 2 cases. One case showed an ulcer crater in the gall bladder Figure9. This case was closely monitored by ultrasound and a subsequent scan performed 15 days later showed complete healing of the ulcerated GB wall and normal mucosa. The signs of acute acalculus cholecystitis resolved by 15 days in 12 cases. In the remaining 4 cases cholecystectomy had to be performed as signs and symptoms were persistent in spite of adequate therapy.
The liver was enlarged with no change in the parenchymal echotexture in 8 cases. The liver size returned to normal by 10 days in all 8 patients.
Ascitis was noted in three cases. Bilateral renomegaly was noted in one case. Pleural effusion was noted in one case. table1table2table3
Discussion
Salmonella typhi, introduced by the oral route, multiplies in the intestinal lymphoid tissue, mainly in the ileocecal area and then disseminates systemically by either lymphatic or hematogenous route to localize in the liver, spleen or other organs.[2] The clinical features of Typhoid fever, while characteristic and suggestive of the diagnosis are, however, not pathognomonic. Inappropriate and inadequate administration of antibiotics, which is a common occurrence in our country, diminishes the possibility of culturing Salmonella from the blood and stool. The serological test, Widal, is the only diagnostic test widely available. Widal test is usually positive only in the second week and rising widal titres are required to make a definitive diagnosis. Therefore, clinically atypical cases are difficult to diagnose early. US examination of the abdomen is helpful in the diagnosis of Typhoid fever in the first week. The common US findings are hepatosplenomegaly, thickening of the walls of the terminal ileum, cecum and ascending colon, mesenteric lymphadenopathy and acute acalculus cholecystitis.
We found similar US findings of splenomegaly, bowel wall thickening, mesenteric lymphadenopathy, acute acalculus cholecystitis and hepatomegaly even in the 6 patients in the adult age group who were subsequently hemoculture positive for Widal.
The most interesting finding we noted was the mucosal ulceration in the wall of the GB in one child. We closely monitored the case and performed US examinations at frequent intervals. The ulceration completely resolved and the mucosa returned to normal after two weeks. This finding has not been previously reported in literature to the best of our knowledge.
The advent of high resolution and high frequency transducers has helped in measuring the bowel wall thickness in healthy subjects and in intestinal disorders. Increase in thickness of the walls of terminal ileum and enlargement of the regional nodes in Typhoid fever was first reported by Puyleart in 1989.[4] In 1997 Terantino et al reported similar findings in 95 patients of confirmed Typhoid.[5] These findings were also reported in Yersinia More Details and Campylobactor jejuni enterocolitis by Puyleart in 1988,[6] in tuberculous enteritis by Lee et al in 1993[7] and in inflammatory bowel diseases, Ulcerative colitis and Crohn's disease by Lim et al in 1994[8]. The findings of thickened terminal ileum associated with enlarged mesenteric nodes, although not specific for any one organism, appear to be specific for bacterial enteritis of the ileocecal region. The sensitivity and specificity for diagnosis of Typhoid in patients admitted with fever as described by Tarantino was 68.4 % and 81.4% respectively and accuracy of 77.4%.[5]
In tuberculosis enteritis, the 5 layered structure of the bowel wall is lost and narrowing of the bowel lumen and strictures are common.[7] This distinguishes it from Typhoid enteritis where the 5 layered bowel wall structure is maintained. Inflammatory bowel diseases, Ulcerative colitis and Crohn's disease are differentiated from Typhoid enteritis based on the extent and location of the thickened bowel wall.
Ultrasound findings are diagnostic in areas endemic for Typhoid fever. In cases with atypical clinical findings, abdominal ultrasound provides a rapid and effective tool in differentiating from conditions like appendicitis, abscesses and diverticulitis. In endemic areas of typhoid fever where yersinia and campylobactor enteritis is almost unknown, the clinical picture and ultrasound findings are almost diagnostic even when widal test is inconclusive and blood cultures are sterile or not available.[5]
Conclusion
In endemic areas ultrasound findings of splenomegaly, thickening of the ileum and cecum and multiple mesenteric nodes, with or without dilated thick walled gall bladder is diagnostic of typhoid fever particularly when serology is equivocal and cultures are negative or not available. US is a non-invasive, easily available, economical, well-acceptable and fairly sensitive investigation for the early diagnosis of typhoid fever.
Acknowledgements
Staff of Princess Durru Shehvar Children's hospital, Yashoda hospital, Asian Institute of Gastroenterology and Nitya Diagnostic Center and typist Shiva.
References
1. Gerald T. Keusch. Salmonellosis. In Fauci AS, Braunwald E, Isselbacher KJ et al eds. Harrison's Principles of Internal Medicine, 14th ed. New York: McGraw Hill, 1998;950-956
2. Hook EW. Guerrant RL. Salmonella infections. In Braunwald E, Isselbacher KJ et al, eds. Harrison's Principles of Internal Medicine, 11th ed. New York: McGraw Hill, 1987;592-596
3. Puyleart JBMC. Mesenteric adenitis and acute terminal ileitis: US evaluation using graded compression. Radiology 1986; 161 : 691-695.
4. Puyleart JBMC, Kristjansdottir S, Golterman KL, Gerard MJ, Nelly MK. Typhoid fever: Diagnosis by using Sonography. Am J Radiol 1989; 153 : 745-746.
5. Tarantino L, Giorgio A. Value of bowel ultrasonography in the diagnosis of typhoid fever. Eur J Ultrasound 1997; 5 : 77-83.
6. Puyleart JBMC, Lalisang RI, Van der werf SDJ et al. Campylobacter ileocolitis mimicking acute appendicitis: differentiation with graded compression US. Radiology 1988; 166 : 737-740.
7. Lee DH.Sonongraphic findings of intestinal tuberculosis. J Ultrasound Med 1993; 12 : 537-540.
8. Lim JH, Ku YT, Lee DH et al. Sonography of inflammatory bowel diseases. Am J Radiol 1994; 163 : 343-347.(Mateen MA, Saleem Sheena,)
2 Department of Radiodiagnosis, Nitya Diagnostic Centre, Hyderabad, India
3 Department of Radiodiagnosis, Gandhi Hospital, Hyderabad, India
4 Department of Radiodiagnosis, Asian Institute of Gastroenterology, Hyderabad, India
Abstract
Objectives. To establish the efficacy of ultrasound (US) of the abdomen as a diagnostic test in Typhoid. To determine the ultrasound diagnostic criteria in cases of Typhoid. Methods. The Widal test is the most commonly used method of detecting Typhoid fever, but does not provide results until a week after onset of fever due to the need for enough antibodies to develop to render a positive result. Abdominal Ultrasound was performed within three days of the onset of fever in 80 cases suspected to be having Typhoid fever. Subsequent follow -up scans were performed at five days, ten days and fifteen days. Subsequently, all 80 cases were found to be Widal positive and Salmonella culture was positive in 32 cases. We present our findings in 26 patients in the age group between 4 to 20 years in whom both Widal test and Salmonella culture was subsequently positive. Results. The US findings were as follows: splenomegaly (n-26, 100%); Bowel wall thickening (n-22, 85%); mesenteric lymphadenopathy(n-20,77%); hepatomegaly with normal parenchymal echotexture (n-8, 31%); thickened gall bladder (n-16, 62%); biliary sludge (n-6, 23%); positive US Murphy's sign (n-7, 27%); pericholecystic edema with increased vascularity (n-6, 23%); mucosal ulceration in the wall of the gall bladder (n-1, 3.8%). Conclusion. In endemic areas like India, ultrasound findings of hepatomegaly, splenomegaly, ileal and cecal thickening, mesenteric lymphadenopathy and thick-walled gallbladder are diagnostic features of typhoid. Ultrasound can be a non-invasive, economical and a reasonably sensitive tool for diagnosing typhoid when serology is equivocal and cultures are negative.
Keywords: Bowel ultrasound; Typhoid fever; Enteric fever
Enteric fever is caused by Salmonella More Details typhi and paratyphi bacilli and is endemic in many parts of the third world. In India, it is the fifth most common infectious disease with a high rate of complications. Atypical clinical findings make an early diagnosis difficult.[1] Definitive diagnosis of typhoid fever is made by hemoculture and serological tests, namely Widal test, both requiring from some days to over a week to show positive results.[2] Improper and inadequate use of antibiotics leads to sterile cultures adding to the difficulty in diagnosis. Imaging techniques have not generally been used in the diagnostic approach to typhoid fever. The present study was aimed at determining the usefulness of US in the early diagnosis of typhoid fever.
Material and methods
This study was conducted between July 1995 and July 2005 on eighty patients (M-52, F-28) clinically suspected to be having typhoid fever. Age of the patients ranged from 4 years to 58 years. All the eighty patients were subsequently found to be widal positive. Salmonella culture was positive in 32 patients. 26 of these patients were less than 20 years of age. These 26 patients (M-16, F-10) formed the study group. The age of the patients in the study group ranged from 4 years to 20 years.
Abdominal US examination was performed within one to three days of hospital admission. We used a convex transducer with frequency of 3.5 to 5 MHz and a linear transducer with a frequency of 7 to 12 MHz on the US machine (Logic 400, GE; Logic 500, GE; Sonolayer, Toshiba; Voluson 730 Pro, GE)
All ultrasound examinations were started with the examination of the liver wherein the size and echotexture were noted. The gall bladder was next examined concentrating on its size, luminal contents, mucosal surface, wall thickness, U/S Murphy's sign, pericholecystic edema and fluid collection. The spleen was examined concentrating on the size and echotexture. After examining the upper abdomen, the lower abdomen was examined according to the graded compression method described by Puyleart.[3] This started with the study of lower right abdominal quadrant where the ileocecal region Figure1 and the ascending colon were recognized. From this point the probe was moved upwards along the right flank unto the right hypochondrium, then transversely along the epigastrium to the left hypochondrium and then downwards along the left flank to the hypogastrium and pelvis thus studying the entire colon from cecum to the rectum. Multiple transverse & longitudinal scans of the abdomen and pelvis were then performed for the study of the small bowel to identify any areas of wall thickening. Measurement of the thickness of the bowel wall was performed by positioning the calipers between the outer margin of the inner hyperechoic layer & the outer hyperechoic layer Figure2. The thickness was considered abnormal when it measured more than 3mm.[3] Using a similar technique, enlarged mesenteric lymph nodes were visualized Figure3. Following the initial scan, the ultrasound was repeated in all patients on the fifth, tenth and fifteenth day.
Results
All 26 patients could be successfully studied by ultrasound. No patient required analgesia to achieve the adequate bowel compression. The average duration of the US examination was 20 minutes.
All 26 cases showed diffuse enlargement of the spleen. In 22 cases the spleen showed a normal echotexture Figure4. 4 cases had abscess formation in the spleen. In one eight-year-old, child the abscess was 12 × 10 cm and the patient required laparotomy and drainage as it was not responding to repeated aspirations with percutaneous drainage. Splenomegaly persisted in all 26 patients even at the follow up scan done on the 15th day. However, there was a significant decrease in the size of the spleen.
Bowel wall thickening was noted in 22 cases. 12 cases showed increased wall thickness of the terminal ileum and cecum Figure5. 7 cases showed only ileal thickening, the maximum thickness noted was 9 mm. In three cases there were thickening of the whole colon from the cecum to the rectum. The increase in the bowel wall thickness was due to edema of the mucosa and submucosa. But the five layer intestinal wall structure was maintained in all cases. In one case there was an ileal perforation and pelvic abscess formation which responded to conservative management and percutaneous drainage. The bowel wall thickening resolved by 10 days in 70% of cases and by 15 days in the rest.
Enlarged mesenteric lymph nodes ranging in diameter from 8 to 34 mm (mean 18 mm) was noted in 20 cases. The lymph nodes were oval or rounded, hypoechoic structures with well defined margins seen in groups of 5 to 10. Mesenteric lymphadenopathy resolved in 60% of cases in 15 days. In the remaining 40 %, the size and number of lymph nodes decreased significantly.
The gall bladder was distended and thick walled Figure6 in 16 cases. Dense biliary sludge Figure7 was noted in 6 cases. US Murphy's sign was positive in 7 cases. Pericholecystic edema was seen in 6 cases. Color Doppler revealed increase in vascularity in thickened wall Figure8. Pericholecystic fluid collection was seen in 2 cases. One case showed an ulcer crater in the gall bladder Figure9. This case was closely monitored by ultrasound and a subsequent scan performed 15 days later showed complete healing of the ulcerated GB wall and normal mucosa. The signs of acute acalculus cholecystitis resolved by 15 days in 12 cases. In the remaining 4 cases cholecystectomy had to be performed as signs and symptoms were persistent in spite of adequate therapy.
The liver was enlarged with no change in the parenchymal echotexture in 8 cases. The liver size returned to normal by 10 days in all 8 patients.
Ascitis was noted in three cases. Bilateral renomegaly was noted in one case. Pleural effusion was noted in one case. table1table2table3
Discussion
Salmonella typhi, introduced by the oral route, multiplies in the intestinal lymphoid tissue, mainly in the ileocecal area and then disseminates systemically by either lymphatic or hematogenous route to localize in the liver, spleen or other organs.[2] The clinical features of Typhoid fever, while characteristic and suggestive of the diagnosis are, however, not pathognomonic. Inappropriate and inadequate administration of antibiotics, which is a common occurrence in our country, diminishes the possibility of culturing Salmonella from the blood and stool. The serological test, Widal, is the only diagnostic test widely available. Widal test is usually positive only in the second week and rising widal titres are required to make a definitive diagnosis. Therefore, clinically atypical cases are difficult to diagnose early. US examination of the abdomen is helpful in the diagnosis of Typhoid fever in the first week. The common US findings are hepatosplenomegaly, thickening of the walls of the terminal ileum, cecum and ascending colon, mesenteric lymphadenopathy and acute acalculus cholecystitis.
We found similar US findings of splenomegaly, bowel wall thickening, mesenteric lymphadenopathy, acute acalculus cholecystitis and hepatomegaly even in the 6 patients in the adult age group who were subsequently hemoculture positive for Widal.
The most interesting finding we noted was the mucosal ulceration in the wall of the GB in one child. We closely monitored the case and performed US examinations at frequent intervals. The ulceration completely resolved and the mucosa returned to normal after two weeks. This finding has not been previously reported in literature to the best of our knowledge.
The advent of high resolution and high frequency transducers has helped in measuring the bowel wall thickness in healthy subjects and in intestinal disorders. Increase in thickness of the walls of terminal ileum and enlargement of the regional nodes in Typhoid fever was first reported by Puyleart in 1989.[4] In 1997 Terantino et al reported similar findings in 95 patients of confirmed Typhoid.[5] These findings were also reported in Yersinia More Details and Campylobactor jejuni enterocolitis by Puyleart in 1988,[6] in tuberculous enteritis by Lee et al in 1993[7] and in inflammatory bowel diseases, Ulcerative colitis and Crohn's disease by Lim et al in 1994[8]. The findings of thickened terminal ileum associated with enlarged mesenteric nodes, although not specific for any one organism, appear to be specific for bacterial enteritis of the ileocecal region. The sensitivity and specificity for diagnosis of Typhoid in patients admitted with fever as described by Tarantino was 68.4 % and 81.4% respectively and accuracy of 77.4%.[5]
In tuberculosis enteritis, the 5 layered structure of the bowel wall is lost and narrowing of the bowel lumen and strictures are common.[7] This distinguishes it from Typhoid enteritis where the 5 layered bowel wall structure is maintained. Inflammatory bowel diseases, Ulcerative colitis and Crohn's disease are differentiated from Typhoid enteritis based on the extent and location of the thickened bowel wall.
Ultrasound findings are diagnostic in areas endemic for Typhoid fever. In cases with atypical clinical findings, abdominal ultrasound provides a rapid and effective tool in differentiating from conditions like appendicitis, abscesses and diverticulitis. In endemic areas of typhoid fever where yersinia and campylobactor enteritis is almost unknown, the clinical picture and ultrasound findings are almost diagnostic even when widal test is inconclusive and blood cultures are sterile or not available.[5]
Conclusion
In endemic areas ultrasound findings of splenomegaly, thickening of the ileum and cecum and multiple mesenteric nodes, with or without dilated thick walled gall bladder is diagnostic of typhoid fever particularly when serology is equivocal and cultures are negative or not available. US is a non-invasive, easily available, economical, well-acceptable and fairly sensitive investigation for the early diagnosis of typhoid fever.
Acknowledgements
Staff of Princess Durru Shehvar Children's hospital, Yashoda hospital, Asian Institute of Gastroenterology and Nitya Diagnostic Center and typist Shiva.
References
1. Gerald T. Keusch. Salmonellosis. In Fauci AS, Braunwald E, Isselbacher KJ et al eds. Harrison's Principles of Internal Medicine, 14th ed. New York: McGraw Hill, 1998;950-956
2. Hook EW. Guerrant RL. Salmonella infections. In Braunwald E, Isselbacher KJ et al, eds. Harrison's Principles of Internal Medicine, 11th ed. New York: McGraw Hill, 1987;592-596
3. Puyleart JBMC. Mesenteric adenitis and acute terminal ileitis: US evaluation using graded compression. Radiology 1986; 161 : 691-695.
4. Puyleart JBMC, Kristjansdottir S, Golterman KL, Gerard MJ, Nelly MK. Typhoid fever: Diagnosis by using Sonography. Am J Radiol 1989; 153 : 745-746.
5. Tarantino L, Giorgio A. Value of bowel ultrasonography in the diagnosis of typhoid fever. Eur J Ultrasound 1997; 5 : 77-83.
6. Puyleart JBMC, Lalisang RI, Van der werf SDJ et al. Campylobacter ileocolitis mimicking acute appendicitis: differentiation with graded compression US. Radiology 1988; 166 : 737-740.
7. Lee DH.Sonongraphic findings of intestinal tuberculosis. J Ultrasound Med 1993; 12 : 537-540.
8. Lim JH, Ku YT, Lee DH et al. Sonography of inflammatory bowel diseases. Am J Radiol 1994; 163 : 343-347.(Mateen MA, Saleem Sheena,)