Intussusception in Adults with Cystic Fibrosis: A Case Series with Review of the Literature
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1 Dig Dis Sci (2011) 56: DOI /s z CASE REPORT Intussusception in Adults with Cystic Fibrosis: A Case Series with Review of the Literature Edward F. Nash Anne Stephenson Emma J. Helm Terence Ho Chandra M. Thippanna Asad Ali Joanna L. Whitehouse David Honeybourne Elizabeth Tullis Peter R. Durie Received: 22 November 2010 / Accepted: 6 June 2011 / Published online: 16 June 2011 Ó Springer Science+Business Media, LLC 2011 Keywords Cystic fibrosis Adult Intussusception Ileocolic Abdominal pain Introduction Intussusception occurs when a proximal segment of bowel (intussusceptum) telescopes into the lumen of the adjacent distal segment (intussuscepiens). It is a relatively common cause of an acute abdomen in the first two years of life, but is uncommon in older children [1]. The diagnosis is rare in adult life, with presentations in adulthood comprising 5% of all intussusceptions and 1% of bowel obstructions [2]. In children it is most commonly idiopathic, in contrast with adults, for most of whom an underlying etiology is found. E. F. Nash (&) C. M. Thippanna A. Ali J. L. Whitehouse D. Honeybourne West Midlands Adult Cystic Fibrosis Centre, Birmingham Heartlands Hospital, Bordesley Green East, Birmingham B9 5SS, UK edward.nash@heartofengland.nhs.uk A. Stephenson T. Ho E. Tullis Toronto Adult CF Program, St. Michael s Hospital, University of Toronto, Toronto, ON, Canada E. J. Helm Department of Radiology, University Hospitals Coventry and Warwickshire NHS Trust, Coventry, UK E. Tullis Li Ka Shing Knowledge Institute, Toronto, ON, Canada P. R. Durie The Research Institute, The Hospital for Sick Children, University of Toronto, Toronto, ON, Canada Cystic fibrosis (CF) is the most common fatal inherited condition in Caucasians [3]. It is caused by abnormal function of the cystic fibrosis transmembrane conductance regulator (CFTR), an epithelial chloride channel. This primary defect causes epithelial secretions to be abnormally dehydrated and viscous, affecting several organs including the lungs, pancreas, intestines, and liver. CF is a well-recognized risk factor for childhood intussusception, with an incidence of 1% reported in the largest case series [4]. The peak age of presentation in this case series was between 9 and 12 years of age, much older than in the non- CF population. Although the clinical presentation and management of intussusception in children with CF is well described, that of adults is less well characterized. We therefore present a case series of CF adults diagnosed with symptomatic intussusception at our centers and perform a systematic review of the literature in order to identify previously described cases. Our aim is to examine the clinical and imaging findings of intussusception in CF adults in order to identify features of the presentation that should suggest this diagnosis. Case 1 A 37-year old CF female presented with a 24-h history of colicky central abdominal pain associated with nausea. She was nine-years post-heart lung transplant with a forced expiratory volume in 1 s (FEV 1 ) of 3.2 l (119% predicted). CF-related co-morbidities included pancreatic insufficiency and CF-related diabetes (CFRD). Bowel habit was normal, with no mucus or blood in the stool. Her presenting symptoms included anorexia associated with a 3 kg weight loss. On examination she had a soft abdomen with right iliac fossa tenderness, a palpable right-sided abdominal
2 3696 Dig Dis Sci (2011) 56: tubulovillous adenomatous ileal polyp with low-grade dysplasia at the lead point of the intussusceptum. Case 2 Fig. 1 Bulls eye ultrasound appearance of ileocolic intussusception in patient 1 A 21-year pancreatic insufficient CF male presented, while on vacation, with severe colicky abdominal pain localized to the right lower quadrant, vomiting and lack of bowel motions. Lung function was previously well maintained (FEV l, 85% predicted) and CF-related comorbidities included mild CF-associated liver disease. Abdominal examination revealed a soft abdomen and palpable periumbilical mass and ultrasound scan demonstrated features in keeping with ileocolic intussusception. Ileocolic intussusception was confirmed by laparotomy and reduced manually. Appendectomy was performed, because the appendix appeared macroscopically inflamed. On returning to the UK he complained of intermittent colicky abdominal pain for the next few months. Eight months after his first surgery he was admitted to a local hospital with further severe colicky abdominal pain, vomiting, and lack of bowel motions. Recurrent ileocolic intussusception was diagnosed by laparotomy and he underwent right hemicolectomy. Histology showed an ileal tubular adenoma with intussusception and ileal infarction. Case 3 Fig. 2 CT appearance of ileocolic intussusception in patient 1 mass, and active bowel sounds. Plain abdominal film showed colonic fecal loading. She was initially treated for presumed distal intestinal obstruction syndrome (DIOS) with intravenous fluids, analgesia, antiemetics, laxatives, oral gastrografin, and phosphate enemas. Over the next seven days she did not open her bowels and continued to experience abdominal pain and nausea. Because her symptoms failed to resolve, abdominal ultrasound was performed, which demonstrated the characteristic bull s eye appearance of intussusception on the right side of the abdomen (Fig. 1). CT imaging confirmed ileocolic intussusception involving approximately 20 cm of the terminal ileum, with thickening and edema of the ascending and proximal transverse colon (Fig. 2). The ileocolic intussusception could not be reduced by laparotomy and she underwent right hemicolectomy with primary anastomosis. She recovered well and was discharged home on the 8th post-operative day. Histology revealed a A 27-year-old pancreatic insufficient CF female with mildly impaired lung function (FEV l, 73% predicted) and normal weight (BMI 20 kg/m 2 ) presented to a local hospital with a one-day history of severe colicky epigastric pain, nausea, and vomiting. In addition she had a five-day history of failure to pass feces or flatus. Of note, she had delivered a healthy child by caesarean section six-weeks previously. On examination she was noted to be tender in the epigastrium. Blood tests including white cell count and C-reactive protein were normal. Plain abdominal X-ray was unremarkable and abdominal ultrasound was nondiagnostic. She was initially thought to have peptic ulcer disease but upper gastrointestinal endoscopy was normal. Subsequently, CT abdomen showed probable ileocolic intussusception extending up to the transverse colon. Air contrast enema could not pass beyond the splenic flexure, and there was noted to be a soft tissue intraluminal abnormality at this level. She was transferred to the specialist CF center three days after her initial presentation, at which stage her abdominal pain had improved but nausea persisted. She was passing flatus but still had not opened her bowels. Ileocolic intussusception was confirmed by laparoscopy but
3 Dig Dis Sci (2011) 56: the intussusception could not be reduced laparoscopically. The patient underwent ileocecectomy with ileo-ascending colon anastomosis by laparotomy; 8.5 cm of ileum and 7.5 cm of colon were resected. Histology showed evidence of hemorrhagic infarction within the intussusceptum with an inflamed appendix forming the lead point. Case 4 A 28-year old pancreatic insufficient CF male presented with a three-month history of vomiting after almost every meal. A sequential bilateral lung transplant had been performed 12 months previously and he was maintained on cyclosporine, azathioprine, and prednisone. Lung function was normal with FEV l (106% predicted). In addition to vomiting he also complained of infrequent bowel movements and colicky right lower quadrant pain a few hours after eating. He had lost 4.7 kg since his last clinic visit. On abdominal examination no abnormalities were noted. CT scanning revealed prominent mural thickening of the distal ileum, cecum, ascending colon, and proximal transverse colon. He was managed conservatively and his symptoms settled sufficiently for him to be discharged. However, over the next two years he continued to complain of intermittent episodes of colicky abdominal pain and vomiting. He was re-admitted with further vomiting after eating and a CT scan showed that mural thickening had extended to involve the distal transverse colon. There was also noted to be an ileocolic intussusception with dilated loops of small bowel consistent with partial small bowel obstruction. Chronic ileocolic intussusception was confirmed by laparotomy and right hemicolectomy was performed. Histology demonstrated marked bowel wall thickening, because of thickening of the muscularis propria, with chronic eosinophilic inflammation. There was noted to be thick fecal material and mucin adherent to the bowel wall. The appendix was inflamed with evidence of perforation and abscess formation and this was thought to have formed the lead point for the intussusception. Case 5 A 24-year old pancreatic insufficient CF male with chronic airway infection with Burkholderia cenocepacia had previously presented at nine years of age with colicky abdominal pain and vomiting. Air contrast enema diagnosed ileocolic intussusception, which was reduced by laparotomy without bowel resection. At 19 years of age he again complained of a two-week history of lack of bowel motions and right-sided abdominal pain. Plain abdominal films showed right-sided fecal loading and gastrografin enema showed no evidence of intussusception. He was treated for DIOS with enemas and oral polyethylene glycol solution. At the age of 24 he presented with a ten-day history of colicky abdominal pain and a two-day history of failure to pass feces or flatus. Abdomen was distended but soft with a palpable right-sided mass. Gastrografin enema and CT scan demonstrated ileocolic intussusception. This diagnosis was confirmed by laparotomy and was treated by right hemicolectomy from which he recovered well. Histology showed edema and congestion of the resected bowel with adherent fecal material. The appendix appeared normal and no other specific cause of intussusception was identified. Case 6 A 28-year old pancreatic insufficient CF male complained of a several-year history of intermittent colicky abdominal pain and vomiting. He presented acutely with a further episode of abdominal pain and vomiting after eating. Sequential bilateral lung transplantation had been performed two years previously and FEV 1 was 106% predicted. On examination, tenderness and a palpable mass were noted in the right iliac fossa. He was initially treated for DIOS but, because of failure of the symptoms to resolve over the next two weeks, an abdominal CT scan was performed. This showed chronic ileocolic intussusception, with thickened terminal ileum and colon up to the splenic flexure and dilated loops of small bowel. Ileocolic intussusception was confirmed by laparotomy and right hemicolectomy was performed. Histopathology showed the colonic muscularis propria was severely thickened and the appendix was perforated with abscess formation. Systematic Review We identified 133 published articles, reporting a total of 791 cases of symptomatic adult intussusception (Table 1). Of these, however, only four were previously reported cases in CF adults. Three of these cases were individual case reports [5 7] and one was a single CF adult included in a case series. Because no clinical details were provided for the patient included in the case series, we are only able to summarize the three individual case reports. McIntosh et al. [5] reported the case of an 18-year old CF female with moderately severe CF lung disease (FEV1 44% predicted). She presented with a three-day history of melena followed by two days of bright red rectal bleeding. She denied vomiting but did report an episode of abdominal pain two weeks previously. Colonoscopy revealed a 4 cm 9 4 cm multilobulated pedunculated polypoid mass
4 3698 Dig Dis Sci (2011) 56: Table 1 Etiology of intussusception in the cases identified by the systematic literature review Etiology n (%) Neoplastic Malignant 286 (36) Benign 252 (32) Idiopathic 104 (13) Non-neoplastic Post-operative complications 48 (6) Meckel s diverticulum 36 (5) Peutz-Jegher s syndrome 19 (2) Celiac disease 7 (1) Miscellaneous 7 (1) Intestinal tuberculosis 6 (0.8) Local inflammation 6 (0.8) Cystic fibrosis 4 (0.5) Lymphoid hyperplasia 3 (0.4) Appendicitis 3 (0.4) Crohn s disease 2 (0.3) Aberrant pancreatic tissue 2 (0.3) Abdominal trauma 2 (0.3) Endometriosis 2 (0.3) Scleroderma 1 (0.1) Hyperglycemia 1 (0.1) Blue rubber bleb naevus sy. 1 (0.1) Round worm 1 (0.1) in the cecum. It was then decided to proceed to laparotomy, which that revealed post-inflammatory adhesions around the cecum, and a cecal mass that was resected. Histological examination revealed a 9 cm cm intussusception and microscopic examination revealed distension of the appendiceal glands with inspissated eosinophilic material and marked inflammatory infiltration of the appendix. Webb et al. [6] reported an 18-year old pancreatic insufficient CF male with normal lung function (FEV1 100% predicted) presenting with acute abdominal pain, vomiting, and lack of bowel motions. Plain abdominal radiographs showed no evidence of intestinal obstruction and initial treatment was conservative, with intravenous fluids and enemas. He was subsequently transferred to the CF center, where his intermittent abdominal pain did not settle despite treatment with gastrografin. An abdominal ultrasound examination revealed an epigastric mass with a bull s eye pattern, but the correct diagnosis was not made despite several further ultrasound examinations and an abdominal CT scan. He was discharged home still complaining of intermittent abdominal pain, but was re-admitted one month after his initial symptoms with severe abdominal pain and vomiting. An ileocolic intussusception was diagnosed by laparotomy and 6 cm of small bowel and 15 cm of large bowel were resected. Histological findings were not reported in this case. Khera et al. [7] reported the case of an 18-year old CF male presenting with a five-hour history of acute onset colicky right iliac fossa pain and nausea. These symptoms had been preceded by a two-day history of influenza-like symptoms. Physical examination revealed right iliac fossa tenderness and localized guarding. On the basis of these findings he underwent laparotomy for a presumed diagnosis of acute appendicitis. Ileocolic intussusception was found, requiring extension of the initial incision, and limited right hemicolectomy was performed with primary anastomosis. A grossly distended enlarged appendix was found and was felt to have formed the lead point of the intussusception. Post-operative recovery was uncomplicated, but the authors commented that pre-operative imaging would probably have reduced anesthetic time and altered the choice of extended transverse incision to a midline laparotomy. Discussion In children with CF, the underlying cause of intussusception seems to be related to intestinal abnormalities that are unique to the CF phenotype [4]. Intestinal contents in pancreatic insufficient individuals are dehydrated and viscous, readily adhering to the bowel wall. This putty-like consistency of inspissated distal small bowel and cecal contents is proposed to cause a reduced capacity for intestinal forward propulsion [4]. The adherent small bowel contents may themselves act as a lead-point for intussusception; otherwise an underlying focal abnormality, for example an inflamed dilated appendix or ileal adenomatous polyp, may be implicated. Intestinal motility can be impaired in CF [8] and small bowel and colonic wall thickness is significantly greater in CF subjects than in healthy controls [9]. These factors may also contribute to reduced bowel forward propulsion and increase the chances of intussusception. In five out of the six patients in this case series, an underlying bowel abnormality was found in the intussusceptum on histological examination. Three patients had an inflamed appendix and two patients had a benign ileal adenomatous polyp. Whether the inflamed appendix did indeed act as a lead point or whether it was an innocent bystander in these cases is uncertain. The appendix is frequently found to be abnormal even in asymptomatic CF patients, with radiological features of increased diameter [10 12] and histological findings of goblet cell hypertrophy and inspissated eosinophilic secretions [13]. In addition, in a chronic intussusception, appendiceal inflammation could also be a consequence of, rather than the cause of, the
5 Dig Dis Sci (2011) 56: intussusception. By definition, the appendix will always be within an ileocolic intussusception and therefore the finding of the previously mentioned appendiceal abnormalities does not necessarily implicate it in causing the intussusception. Abdominal pain is a common complaint in adults with CF and as a result there is a wide differential diagnosis to consider [14]. Conditions that need consideration include gastro-esophageal reflux, constipation, gastritis, peptic ulcer disease, distal intestinal obstruction syndrome (DIOS), acute appendicitis, appendiceal abscess, cholelithiasis, and splenic infarction (in patients with splenomegaly because of portal hypertension). In pancreatic sufficient patients, acute or chronic pancreatitis should also be considered [15]. The six cases identified in this series and the three additional previously reported cases enable analysis of the clinical presentation of symptomatic intussusception in CF adults. All nine patients presented with colicky abdominal pain, which was commonly either central or located in the right lower quadrant. Nausea and vomiting were frequent and most patients reported altered bowel habit. In particular, several patients complained of lack of bowel motions and two patients reported failure to pass either feces or flatus. In five patients an abdominal mass was palpable. The main differential diagnoses in a CF adult presenting with central or right-sided colicky abdominal pain, with or without a palpable mass are DIOS and appendiceal inflammation. Four patients were initially misdiagnosed as DIOS but investigation for another etiology was prompted when symptoms failed to resolve after therapy. One of the nine patients was initially misdiagnosed with acute appendicitis and for a further three patients an abnormal appendix was thought to have formed the lead point of the intussusception. The difficulty in diagnosing appendicitis in individuals with CF and the potential adverse consequences as a result of delayed diagnosis are well reported [16]. Despite the limitations of small numbers of cases reported to date, combined analysis of all cases reported in this series and in the literature suggests that the clinical manifestations of intussusception adults and children with CF are somewhat different. Childhood-onset intussusception almost always has an acute presentation, with severe symptoms of complete bowel obstruction (abdominal distention, vomiting and often passage of bright red blood per rectum) [4]. The diagnosis is usually established within a short time and urgent investigation is required to minimize the chances of bowel infarction and perforation. In contrast, CF adults seem to present with chronic (or intermittent) intussusception, with a time delay between onset of symptoms and diagnosis ranging from one week to several months. This is likely to be because of several issues, including the lack of suspicion of this complication in CF adults and the fact that other more common conditions (for example DIOS and appendiceal abscess) may occur with similar symptoms in CF adults. In our series intussusception was diagnosed after abdominal ultrasound or CT scanning. Intussusception has characteristic appearances on these imaging modalities [11, 17]. Alternative diagnoses, for example acute appendicitis with appendiceal abscess or cholecystitis can also be diagnosed by use of these techniques. In children, ultrasonography is the diagnostic modality of choice (over CT), the bull s eye appearance being pathognomonic of this diagnosis. We suggest that ultrasonography also has an important role to play in the initial diagnostic work-up of CF adults with suspected intussusception and has the advantage of not exposing the patient to ionizing radiation. However, the choice of imaging modality will depend partly on local availability and radiological expertise. In children, reduction by air or contrast enema is the first choice treatment modality unless there are specific contraindications, for example evidence of bowel perforation. However, the rarity of intussusception in CF adults, combined with the lack of published evidence, makes it difficult to provide overall recommendations on optimum management. Surgical exploration and reduction of the intussusception (with or without bowel resection) was performed in all the cases in this series, whereas surgical resection is unusual in pediatric patients. It has been suggested that air or contrast enema should not be used in adults, because there is frequently a pathological lead point that may require surgical resection [2, 18]. However, such recommendations may be less relevant in young CF adults in which malignancy is less common. Rather, it is suggested that cases are managed on an individual basis, taking into account the patient s underlying disease status and acute symptoms and signs. We suggest that in young CF adults with confirmed intussusception, but without features of bowel infarction or perforation, an initial attempt at reduction by air or contrast enema should be considered. However, if this is successful, ileo-colonoscopy and imaging should be used to identify a lead point and specifically to rule out malignancy. Initial reduction by air or contrast enema also has a potential role in patients that are not considered ideal candidates for bowel resection because of severe CF lung disease. In patients with features of bowel infarction (or other causes of a surgical abdomen), prompt exploratory laparotomy is obviously mandated if the patient is regarded as a surgical candidate. A surgical approach may also be required in patients not resolving after attempted air or contrast enema. In conclusion, intussusception is an uncommon but important cause of abdominal pain and bowel obstruction in adults with CF. Because of the rarity of symptomatic intussusception in adults with CF, its diagnosis requires a
6 3700 Dig Dis Sci (2011) 56: high index of clinical suspicion. Imaging with ultrasound and CT can both be helpful in reaching a diagnosis and should be considered in any CF adult presenting with abdominal pain, lack of bowel motions and vomiting, with or without a palpable abdominal mass. Acknowledgments We would like to thank the patients and families at the institutions that contributed to this study. Conflict of interest report. References None of the authors has a conflict of interest to 1. Turner D, Richwood AMK, Brereton RJ. Intussusception in older children. Arch Dis Child. 1980;55: Azar T, Berger DL. Adult intussusception. Ann Surg. 1997;226: O Sullivan BP, Freedman SD. Cystic fibrosis. Lancet. 2009;373: Holsclaw DS, Rocmans C, Shwachman H. Intussusception in patients with cystic fibrosis. Pediatrics. 1971;48: McIntosh JC, Mroczek EC, Baldwin C, et al. Intussusception of the appendix in a patient with cystic fibrosis. J Pediatr Gastroenterol Nutr. 1990;110: Webb AK, Khan A. Chronic intussusception in a young adult with cystic fibrosis. J R Soc Med. 1989;82: Khera G, Kumarage S, Strekozov B. Adult intussusception in a cystic fibrosis patient mimicking acute appendicitis. ANZ J Surg. 2004;74:9. 8. Taylor CJ, Hilleil PG, Ghosal S, et al. Gastric emptying and intestinal transit of pancreatic enzyme supplements in cystic fibrosis. Arch Dis Child. 1999;80: Haber HP, Benda N, Fitzke G, et al. Colonic wall thickness measured by ultrasound: Striking differences in patients with cystic fibrosis versus healthy controls. Gut. 1997;40: Wilschanski M, Fisher D, Hadas-Halperin I, et al. Findings on routine abdominal ultrasonography in cystic fibrosis patients. J Ped Gastroenterol Nutr. 1999;28: Lardenoye SW, Puylaert JB, Smit MJ, et al. Appendix in children with cystic fibrosis: US features. Radiology. 2004;232: Menten R, Lebecque P, Saint-Martin C, et al. Outer diameter of the vermiform appendix: not a valid sonographic criterion for acute appendicitis in patients with cystic fibrosis. Am J Roentgenol. 2005;184: Coughlin JP, Gauderer MW, Stern RC, et al. The spectrum of appendiceal disease in cystic fibrosis. J Pediatr Surg. 1990;25: Constantine S, Au VW, Slavotinek JP. Abdominal manifestations of cystic fibrosis in adults: a review. Australas Radiol. 2004;48: Ooi CY, Dorfman R, Cipolli M, et al. Type of CFTR mutation determines risk of pancreatitis in patients with cystic fibrosis. Gastroenterology. 2011;140: Shields MD, Levison H, Reisman JJ, et al. Appendicitis in cystic fibrosis. Arch Dis Child. 1991;66: Warshauer DM, Lee JKT. Adult intussusception detected at CT or MR imaging: Clinical-imaging correlation. Radiology. 1999; 212: Begos D, Sandor A, Modlin I. The diagnosis and management of adult intussusception. Am J Surg. 1997;173:88 94.
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