Clin J Gastroenterol (2010) 3:233–236 DOI 10.1007/s12328-010-0169-6
CASE REPORT
Pneumatosis coli with ulcerative colitis as a rare complication of colonoscopy Shigeki Bamba • Tomoyuki Tsujikawa • Takao Saotome Takafumi Okuno • Yasuharu Saito • Masaya Sasaki • Akira Andoh • Yoshihide Fujiyama
•
Received: 1 May 2010 / Accepted: 30 July 2010 / Published online: 17 August 2010 Ó Springer 2010
Abstract Pneumatosis coli is a relatively rare condition characterized by the presence of gas in the submucosa or subserosa involving mainly the large intestine and, occasionally, the mesenteric attachments. We experienced two cases of pneumatosis coli with ulcerative colitis after colonoscopy that had different clinical courses. Case 1 showed submucosal pneumatosis coli and portal venous air. The air was resolved 30 h later. Case 2 showed subserosal pneumatosis coli and retropneumoperitoneum. The air was eliminated after 3 weeks. The clinical features of pneumatosis coli may depend on the intramural region of the air. Cases 1 and 2 had different air localization, that is, submucosal and subserosal air, and this seems to reflect the differences in the complications. In Case 1 the air expanded to the portal vein, and took only a short time to resolve. In Case 2, however, the air leaked to the retroperitoneal
S. Bamba (&) T. Tsujikawa T. Okuno Y. Fujiyama Division of Gastroenterology, Shiga University of Medical Science, Seta-Tsukinowa, Ohtsu, Shiga 520-2192, Japan e-mail: [email protected] T. Saotome Intensive and Critical Medicine, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan Y. Saito Division of Endoscopy, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan M. Sasaki Division of Clinical Nutrition, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan A. Andoh Division of Mucosal Immunology, Graduate School of Medicine, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan
space and took a long time to resolve. In summary, pneumatosis coli as a complication of colonoscopy presented different features depending on the air location. To our knowledge, this is the first report to reveal the difference of air localization and the complications associated with pneumatosis coli after colonoscopy. Keywords Ulcerative colitis Pneumatosis coli Colonoscopy Pneumoperitoneum Portal venous air
Introduction The description of gas-containing cysts in the intestinal wall was first made in 1730 by Du Vernoi [1] and the term was coined by Mayer [2] in 1925. Usually, pneumatosis cystoides is asymptomatic or minimally symptomatic and follows a benign course. Pneumatosis can be classified as primary (idiopathic) or secondary. The latter is associated with chronic obstructive pulmonary disease [3], intestinal obstruction [4], collagen vascular disease [5], diverticula [6], ascites [7], organ transplantation [8], volvolus [9], iatrogenic conditions (after surgery [10] or colonoscopy [11, 12]), steroid therapy [5, 13], chloral hydrate treatment [14], and inflammatory bowel disease [13, 15]. Pneumatosis coli after total colonoscopy can be followed by polypectomy biopsy, forceful examination, or massive distention of the colon [11, 12]. Our patients with ulcerative colitis had been taking steroids, and had undergone a colonoscopy. There have been a few reports of patients with ulcerative colitis who were receiving steroids and who experienced complications with pneumatosis coli after colonoscopy. We describe 2 cases of pneumatosis coli, which occurred concomitantly with ulcerative colitis after total colonoscopy. The cases had different clinical courses
123
234
and we report them here together with a review of the literature.
Case presentation Case 1 A 54-year-old male with a 2.5-year history of ulcerative colitis was admitted to our hospital because of the exacerbation of diarrhea and bloody stools. Physical examination on admission revealed no abnormal findings such as anemia or abdominal tenderness. Laboratory findings were as follows: positive fecal occult blood, elevated C-reactive protein (0.5 mg/ml), and increased erythrocyte sedimentation rate (21 mm/h). Clinical severity of the colitis was moderate according to Seo’s complex integrated disease activity index [16]. We performed a colonoscopy immediately on the day of admission after enema preparation for bowel cleansing. The colonoscopy revealed an intact cecum and ascending colon, and marked mucosal granularity with spontaneous bleeding and purulent exudates from the transverse colon to the rectum (Matts’ grade 3). He was completely asymptomatic after colonoscopy; however, a plain abdominal X-ray revealed intraluminal air at the splenic flexure of the transverse colon and portal venous air in the liver (Fig. 1). A plain abdominal computed tomography (CT) scan detected portal venous air with the gas mainly in the submucosa of the transverse colon (Fig. 2a, b). The air dissipated 30 h later with only food deprivation.
Clin J Gastroenterol (2010) 3:233–236
refractory to high-dose (60 mg) intravenous prednisone for 10 days. In our hospital, weekly leukocytapheresis was started. Laboratory data on admission were as follows: hemoglobin, 10.8 g/dl; hematocrit, 33.4%; WBC, 10,800/ll; C-reactive protein, 2.5 mg/dl; erythrocyte sedimentation rate, 30 mm/h. Her symptoms gradually improved. The clinical severity of the colitis was mild according to Seo’s complex integrated disease activity index [16]. After the 5th session of leukocytapheresis, a colonoscopy was performed with a preparation of peroral colonic lavage solution on the 35th day of hospital admission. It showed an intact cecum and ascending colon, and multiple inflammatory polyps from the transverse colon to the rectum with the disappearance of ulceration and scar formation (Matts’ grade 3) (Fig. 3a, b). Biopsies were taken from the bottom of the cecum, ascending colon, transverse colon, descending colon, sigmoid colon and rectum. Immediately after the colonoscopy, the patient was asymptomatic; however, 9 h later the patient complained of vague right lower abdominal pain which was still there 2 days later. A plain abdominal X-ray showed subserosal air from the cecum to the ascending colon (Fig. 4). A plain abdominal
Case 2 A 33-year-old female with a 10-year history of ulcerative colitis was transferred to our hospital because she was
Fig. 1 A plain abdominal X-ray reveals submucosal air (arrowheads) at the splenic flexure and intrahepatic air (arrows)
123
Fig. 2 a An abdominal CT scan shows portal venous air (arrows). b An abdominal CT scan reveals submucosal air (arrowheads) at the splenic flexure
Clin J Gastroenterol (2010) 3:233–236
235
Fig. 3 a A biopsy sample was taken from the bottom of the intact cecum. b Multiple inflammatory polyps were observed at the transverse colon
Fig. 4 A plain abdominal X-ray reveals subserosal air (arrowheads) from the cecum to the ascending colon
CT scan also detected subserosal gas, which had reached the anterior space of the kidney through the mesentery (Fig. 5a, b). We started oxygen-breathing therapy using a nasal cannula (5 l/min) over the next 5 days but the subserosal air did not disappear; however after a 3-week follow-up period, both the air and the symptoms had completely disappeared.
Discussion Our cases displayed two different clinical features and courses. The difference in resolution times between the two patients arises from the difference in the locations of the air pockets. In Case 1, the air was in the submucosal space and portal vein where blood flow is abundant. In Case 2, however, the air leaked into the subserosal space where
Fig. 5 a A plain abdominal CT scan shows retropneumoperitoneum (arrowheads). b A plain abdominal CT scan shows that subserosal air had reached the anterior space of the kidney through the mesentery (arrowheads)
there is less blood flow. Because the cyst was a complication of colonoscopy, the composition of gas was thought to be the same as that of room air. Hydrogen gas clearance was used to evaluate the blood flow [17], although the gas composition of the cyst was different from the hydrogen gas in these two cases. Carbon dioxide insufflation which
123
236
Clin J Gastroenterol (2010) 3:233–236
has been reported to reduce patient abdominal pain and discomfort during and after colonoscopies due to the rapid absorption rate of carbon dioxide into the surrounding tissue [18] should have been used for our patients. The pain of the pneumatosis coli is also thought to result from extension of the serous membrane, which is richer in C fibers than the submucosal space. Therefore, subserosal air is expected to be more symptomatic than submucosal air. Treatment may be attempted for symptomatic lesions. High-flow oxygen breathing using 55–75% oxygen to achieve a partial pressure of oxygen of between 200 and 350 mmHg for 4–10 days is recommended to resolve pneumatosis [19]. To avoid oxygen toxicity in the pulmonary and central nervous systems, hyperbaric oxygen at 1900 mmHg for 2.5 h on 2 or 3 consecutive days has also been successful [20]; however, oxygen breathing was not effective for our second case.
Conclusion In summary, pneumatosis coli as a complication of colonoscopy presented different features depending on the air location. In our 2 cases it seems that the location of air reflects the developed symptoms. Furthermore, the submucosal air seemed to take a relatively short time to resolve, although the air expanded into a portal vein. The subserosal air, however, seemed to take a long time to resolve and showed pneumoperitoneum or retropneumoperitoneum as a complication of pneumatosis. In conclusion, careful examination is needed for patients with longstanding ulcerative colitis and a long clinical course of steroid therapy, because they are at risk of pneumatosis coli. Conflict of interest peting interests.
The authors declare that they have no com-
References 1. Mac KE. Pneumatosis intestinalis. Review of the literature with report of 13 cases. Pediatrics. 1951;7:537–49. 2. Matthews FJ. Enteric pneumatosis. Br Med J. 1954;1:851–2.
123
3. Gagliardi G, Thompson IW, Hershman MJ, Forbes A, Hawley PR, Talbot IC. Pneumatosis coli: a proposed pathogenesis based on study of 25 cases and review of the literature. Int J Colorectal Dis. 1996;11:111–8. 4. Kleinman PL, King DR. Ischemic jejunitis and pneumatosis intestinalis secondary to anastomotic obstruction following jejunal atresia repair. Gastrointest Radiol. 1977;2:113–5. 5. Sequeira W. Pneumatosis cystoides intestinalis in systemic sclerosis and other diseases. Semin Arthritis Rheum. 1990;19:269–77. 6. Jorgensen A, Wille-Jorgensen P. Pneumatosis intestinalis and pneumoperitoneum due to a solitary sigmoid diverticulum. Acta Chir Scand. 1982;148:625–6. 7. Tsega E. Pneumatosis cystoides intestinalis with unexplained ascites in Ethiopian patients. Br J Surg. 1975;62:379–82. 8. Andorsky RI. Pneumatosis cystoides intestinalis after organ transplantation. Am J Gastroenterol. 1990;85:189–94. 9. Gillon J, Holt S, Sircus W. Pneumatosis coli and sigmoid volvulus: a report of 4 cases. Br J Surg. 1979;66:802–5. 10. Horiuchi A, Akamatsu T, Mukawa K, Ochi Y, Arakura N, Kiyosawa K. Case report: Pneumatosis cystoides intestinalis associated with post-surgical bowel anastomosis: a report of three cases and review of the Japanese literature. J Gastroenterol Hepatol. 1998;13:534–7. 11. Heer M, Altorfer J, Pirovino M, Schmid M. Pneumatosis cystoides coli: a rare complication of colonoscopy. Endoscopy. 1983; 15:119–20. 12. McCollister DL, Hammerman HJ. Air, air, everywhere: pneumatosis cystoides coli after colonoscopy. Gastrointest Endosc. 1990;36:75–6. 13. John A, Dickey K, Fenwick J, Sussman B, Beeken W. Pneumatosis intestinalis in patients with Crohn’s disease. Dig Dis Sci. 1992;37:813–7. 14. Florin TH. Alkyl halides, super hydrogen production and the pathogenesis of pneumatosis cystoides coli. Gut. 1997;41:778–84. 15. Galandiuk S, Fazio VW, Petras RE. Pneumatosis cystoides intestinalis in Crohn’s disease. Report of two cases. Dis Colon Rectum. 1985;28:951–6. 16. Seo M, Okada M, Yao T, Ueki M, Arima S, Okumura M. An index of disease activity in patients with ulcerative colitis. Am J Gastroenterol. 1992;87:971–6. 17. Oohata Y, Mibu R, Hotokezaka M, Ikeda S, Nakahara S, Itoh H. Comparison of blood flow assessment between laser Doppler velocimetry and the hydrogen gas clearance method in ischemic intestine in dogs. Am J Surg. 1990;160:511–4. 18. Bretthauer M, Thiis-Evensen E, Huppertz-Hauss G, Gisselsson L, Grotmol T, Skovlund E, et al. NORCCAP (Norwegian colorectal cancer prevention): a randomised trial to assess the safety and efficacy of carbon dioxide versus air insufflation in colonoscopy. Gut. 2002;50:604–7. 19. Miralbes M, Hinojosa J, Alonso J, Berenguer J. Oxygen therapy in pneumatosis coli. What is the minimum oxygen requirement? Dis Colon Rectum. 1983;26:458–60. 20. van der Linden W. Letter: reappearance of intestinal gas cysts after oxygen treatment. Lancet. 1974;2:1388–9.
CASE REPORT
Pneumatosis coli with ulcerative colitis as a rare complication of colonoscopy Shigeki Bamba • Tomoyuki Tsujikawa • Takao Saotome Takafumi Okuno • Yasuharu Saito • Masaya Sasaki • Akira Andoh • Yoshihide Fujiyama
•
Received: 1 May 2010 / Accepted: 30 July 2010 / Published online: 17 August 2010 Ó Springer 2010
Abstract Pneumatosis coli is a relatively rare condition characterized by the presence of gas in the submucosa or subserosa involving mainly the large intestine and, occasionally, the mesenteric attachments. We experienced two cases of pneumatosis coli with ulcerative colitis after colonoscopy that had different clinical courses. Case 1 showed submucosal pneumatosis coli and portal venous air. The air was resolved 30 h later. Case 2 showed subserosal pneumatosis coli and retropneumoperitoneum. The air was eliminated after 3 weeks. The clinical features of pneumatosis coli may depend on the intramural region of the air. Cases 1 and 2 had different air localization, that is, submucosal and subserosal air, and this seems to reflect the differences in the complications. In Case 1 the air expanded to the portal vein, and took only a short time to resolve. In Case 2, however, the air leaked to the retroperitoneal
S. Bamba (&) T. Tsujikawa T. Okuno Y. Fujiyama Division of Gastroenterology, Shiga University of Medical Science, Seta-Tsukinowa, Ohtsu, Shiga 520-2192, Japan e-mail: [email protected] T. Saotome Intensive and Critical Medicine, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan Y. Saito Division of Endoscopy, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan M. Sasaki Division of Clinical Nutrition, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan A. Andoh Division of Mucosal Immunology, Graduate School of Medicine, Shiga University of Medical Science, Ohtsu, Shiga 520-2192, Japan
space and took a long time to resolve. In summary, pneumatosis coli as a complication of colonoscopy presented different features depending on the air location. To our knowledge, this is the first report to reveal the difference of air localization and the complications associated with pneumatosis coli after colonoscopy. Keywords Ulcerative colitis Pneumatosis coli Colonoscopy Pneumoperitoneum Portal venous air
Introduction The description of gas-containing cysts in the intestinal wall was first made in 1730 by Du Vernoi [1] and the term was coined by Mayer [2] in 1925. Usually, pneumatosis cystoides is asymptomatic or minimally symptomatic and follows a benign course. Pneumatosis can be classified as primary (idiopathic) or secondary. The latter is associated with chronic obstructive pulmonary disease [3], intestinal obstruction [4], collagen vascular disease [5], diverticula [6], ascites [7], organ transplantation [8], volvolus [9], iatrogenic conditions (after surgery [10] or colonoscopy [11, 12]), steroid therapy [5, 13], chloral hydrate treatment [14], and inflammatory bowel disease [13, 15]. Pneumatosis coli after total colonoscopy can be followed by polypectomy biopsy, forceful examination, or massive distention of the colon [11, 12]. Our patients with ulcerative colitis had been taking steroids, and had undergone a colonoscopy. There have been a few reports of patients with ulcerative colitis who were receiving steroids and who experienced complications with pneumatosis coli after colonoscopy. We describe 2 cases of pneumatosis coli, which occurred concomitantly with ulcerative colitis after total colonoscopy. The cases had different clinical courses
123
234
and we report them here together with a review of the literature.
Case presentation Case 1 A 54-year-old male with a 2.5-year history of ulcerative colitis was admitted to our hospital because of the exacerbation of diarrhea and bloody stools. Physical examination on admission revealed no abnormal findings such as anemia or abdominal tenderness. Laboratory findings were as follows: positive fecal occult blood, elevated C-reactive protein (0.5 mg/ml), and increased erythrocyte sedimentation rate (21 mm/h). Clinical severity of the colitis was moderate according to Seo’s complex integrated disease activity index [16]. We performed a colonoscopy immediately on the day of admission after enema preparation for bowel cleansing. The colonoscopy revealed an intact cecum and ascending colon, and marked mucosal granularity with spontaneous bleeding and purulent exudates from the transverse colon to the rectum (Matts’ grade 3). He was completely asymptomatic after colonoscopy; however, a plain abdominal X-ray revealed intraluminal air at the splenic flexure of the transverse colon and portal venous air in the liver (Fig. 1). A plain abdominal computed tomography (CT) scan detected portal venous air with the gas mainly in the submucosa of the transverse colon (Fig. 2a, b). The air dissipated 30 h later with only food deprivation.
Clin J Gastroenterol (2010) 3:233–236
refractory to high-dose (60 mg) intravenous prednisone for 10 days. In our hospital, weekly leukocytapheresis was started. Laboratory data on admission were as follows: hemoglobin, 10.8 g/dl; hematocrit, 33.4%; WBC, 10,800/ll; C-reactive protein, 2.5 mg/dl; erythrocyte sedimentation rate, 30 mm/h. Her symptoms gradually improved. The clinical severity of the colitis was mild according to Seo’s complex integrated disease activity index [16]. After the 5th session of leukocytapheresis, a colonoscopy was performed with a preparation of peroral colonic lavage solution on the 35th day of hospital admission. It showed an intact cecum and ascending colon, and multiple inflammatory polyps from the transverse colon to the rectum with the disappearance of ulceration and scar formation (Matts’ grade 3) (Fig. 3a, b). Biopsies were taken from the bottom of the cecum, ascending colon, transverse colon, descending colon, sigmoid colon and rectum. Immediately after the colonoscopy, the patient was asymptomatic; however, 9 h later the patient complained of vague right lower abdominal pain which was still there 2 days later. A plain abdominal X-ray showed subserosal air from the cecum to the ascending colon (Fig. 4). A plain abdominal
Case 2 A 33-year-old female with a 10-year history of ulcerative colitis was transferred to our hospital because she was
Fig. 1 A plain abdominal X-ray reveals submucosal air (arrowheads) at the splenic flexure and intrahepatic air (arrows)
123
Fig. 2 a An abdominal CT scan shows portal venous air (arrows). b An abdominal CT scan reveals submucosal air (arrowheads) at the splenic flexure
Clin J Gastroenterol (2010) 3:233–236
235
Fig. 3 a A biopsy sample was taken from the bottom of the intact cecum. b Multiple inflammatory polyps were observed at the transverse colon
Fig. 4 A plain abdominal X-ray reveals subserosal air (arrowheads) from the cecum to the ascending colon
CT scan also detected subserosal gas, which had reached the anterior space of the kidney through the mesentery (Fig. 5a, b). We started oxygen-breathing therapy using a nasal cannula (5 l/min) over the next 5 days but the subserosal air did not disappear; however after a 3-week follow-up period, both the air and the symptoms had completely disappeared.
Discussion Our cases displayed two different clinical features and courses. The difference in resolution times between the two patients arises from the difference in the locations of the air pockets. In Case 1, the air was in the submucosal space and portal vein where blood flow is abundant. In Case 2, however, the air leaked into the subserosal space where
Fig. 5 a A plain abdominal CT scan shows retropneumoperitoneum (arrowheads). b A plain abdominal CT scan shows that subserosal air had reached the anterior space of the kidney through the mesentery (arrowheads)
there is less blood flow. Because the cyst was a complication of colonoscopy, the composition of gas was thought to be the same as that of room air. Hydrogen gas clearance was used to evaluate the blood flow [17], although the gas composition of the cyst was different from the hydrogen gas in these two cases. Carbon dioxide insufflation which
123
236
Clin J Gastroenterol (2010) 3:233–236
has been reported to reduce patient abdominal pain and discomfort during and after colonoscopies due to the rapid absorption rate of carbon dioxide into the surrounding tissue [18] should have been used for our patients. The pain of the pneumatosis coli is also thought to result from extension of the serous membrane, which is richer in C fibers than the submucosal space. Therefore, subserosal air is expected to be more symptomatic than submucosal air. Treatment may be attempted for symptomatic lesions. High-flow oxygen breathing using 55–75% oxygen to achieve a partial pressure of oxygen of between 200 and 350 mmHg for 4–10 days is recommended to resolve pneumatosis [19]. To avoid oxygen toxicity in the pulmonary and central nervous systems, hyperbaric oxygen at 1900 mmHg for 2.5 h on 2 or 3 consecutive days has also been successful [20]; however, oxygen breathing was not effective for our second case.
Conclusion In summary, pneumatosis coli as a complication of colonoscopy presented different features depending on the air location. In our 2 cases it seems that the location of air reflects the developed symptoms. Furthermore, the submucosal air seemed to take a relatively short time to resolve, although the air expanded into a portal vein. The subserosal air, however, seemed to take a long time to resolve and showed pneumoperitoneum or retropneumoperitoneum as a complication of pneumatosis. In conclusion, careful examination is needed for patients with longstanding ulcerative colitis and a long clinical course of steroid therapy, because they are at risk of pneumatosis coli. Conflict of interest peting interests.
The authors declare that they have no com-
References 1. Mac KE. Pneumatosis intestinalis. Review of the literature with report of 13 cases. Pediatrics. 1951;7:537–49. 2. Matthews FJ. Enteric pneumatosis. Br Med J. 1954;1:851–2.
123
3. Gagliardi G, Thompson IW, Hershman MJ, Forbes A, Hawley PR, Talbot IC. Pneumatosis coli: a proposed pathogenesis based on study of 25 cases and review of the literature. Int J Colorectal Dis. 1996;11:111–8. 4. Kleinman PL, King DR. Ischemic jejunitis and pneumatosis intestinalis secondary to anastomotic obstruction following jejunal atresia repair. Gastrointest Radiol. 1977;2:113–5. 5. Sequeira W. Pneumatosis cystoides intestinalis in systemic sclerosis and other diseases. Semin Arthritis Rheum. 1990;19:269–77. 6. Jorgensen A, Wille-Jorgensen P. Pneumatosis intestinalis and pneumoperitoneum due to a solitary sigmoid diverticulum. Acta Chir Scand. 1982;148:625–6. 7. Tsega E. Pneumatosis cystoides intestinalis with unexplained ascites in Ethiopian patients. Br J Surg. 1975;62:379–82. 8. Andorsky RI. Pneumatosis cystoides intestinalis after organ transplantation. Am J Gastroenterol. 1990;85:189–94. 9. Gillon J, Holt S, Sircus W. Pneumatosis coli and sigmoid volvulus: a report of 4 cases. Br J Surg. 1979;66:802–5. 10. Horiuchi A, Akamatsu T, Mukawa K, Ochi Y, Arakura N, Kiyosawa K. Case report: Pneumatosis cystoides intestinalis associated with post-surgical bowel anastomosis: a report of three cases and review of the Japanese literature. J Gastroenterol Hepatol. 1998;13:534–7. 11. Heer M, Altorfer J, Pirovino M, Schmid M. Pneumatosis cystoides coli: a rare complication of colonoscopy. Endoscopy. 1983; 15:119–20. 12. McCollister DL, Hammerman HJ. Air, air, everywhere: pneumatosis cystoides coli after colonoscopy. Gastrointest Endosc. 1990;36:75–6. 13. John A, Dickey K, Fenwick J, Sussman B, Beeken W. Pneumatosis intestinalis in patients with Crohn’s disease. Dig Dis Sci. 1992;37:813–7. 14. Florin TH. Alkyl halides, super hydrogen production and the pathogenesis of pneumatosis cystoides coli. Gut. 1997;41:778–84. 15. Galandiuk S, Fazio VW, Petras RE. Pneumatosis cystoides intestinalis in Crohn’s disease. Report of two cases. Dis Colon Rectum. 1985;28:951–6. 16. Seo M, Okada M, Yao T, Ueki M, Arima S, Okumura M. An index of disease activity in patients with ulcerative colitis. Am J Gastroenterol. 1992;87:971–6. 17. Oohata Y, Mibu R, Hotokezaka M, Ikeda S, Nakahara S, Itoh H. Comparison of blood flow assessment between laser Doppler velocimetry and the hydrogen gas clearance method in ischemic intestine in dogs. Am J Surg. 1990;160:511–4. 18. Bretthauer M, Thiis-Evensen E, Huppertz-Hauss G, Gisselsson L, Grotmol T, Skovlund E, et al. NORCCAP (Norwegian colorectal cancer prevention): a randomised trial to assess the safety and efficacy of carbon dioxide versus air insufflation in colonoscopy. Gut. 2002;50:604–7. 19. Miralbes M, Hinojosa J, Alonso J, Berenguer J. Oxygen therapy in pneumatosis coli. What is the minimum oxygen requirement? Dis Colon Rectum. 1983;26:458–60. 20. van der Linden W. Letter: reappearance of intestinal gas cysts after oxygen treatment. Lancet. 1974;2:1388–9.
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