Adult intestinal failure
Article Outline
- Abstract
- Introduction
- Role of radiology
- Radiological techniques
- Individual diseases
- Complications arising in the IF patient
- Conclusion
- References
- Copyright
Intestinal failure (IF) is the inability of the alimentary tract to digest and absorb sufficient nutrition to maintain normal fluid balance, growth, and health. It commonly arises from disease affecting the mesenteric root. Although severe IF is usually managed in specialized units, it lies at the end of a spectrum with degrees of nutritional compromise being widely encountered, but commonly under-recognized. Furthermore, in the majority of cases, the initial enteric insult occurs in non-specialist IF centres. The aim of this article is to review the common causes of IF, general principles of its management, some commoner complications, and the role of radiology in the approach to a patient with severe IF. The radiologist has a crucial role in helping provide access for feeding solutions (both enteral and parenteral) and controlling sepsis (via drainage of collections) in an initial restorative phase of treatment, whilst simultaneously mapping bowel anatomy and quality, and searching for disease complications to assist the clinicians in planning a later, restorative phase of therapy.
Introduction
Intestinal failure (IF) is the inability of the alimentary tract to digest and absorb sufficient nutrition to maintain normal fluid balance, growth, and health.1 It occurs in both children and adults, although the spectrum of disease is rather different in the two groups. This review will deal solely with adult patients. There are two dedicated IF units in Great Britain designated by the National Commissioning Group for highly specialized services (Salford and St Mark's, Harrow), receiving tertiary and quaternary referrals for the most complex cases of severe IF.2 Nevertheless, the condition is of relevance to the general radiologist, as less severe cases along the same spectrum are common.
Annually, approximately 18 patients per million population require prolonged management of IF in hospital, with 14.6 patients per million having continuous intravenous feeding at home.2 At our unit, over a 4-year period, a slight female preponderance was noted (female 57%, male 43%) over a wide age range (16–80 years). The causes of IF in patients referred include primary small bowel disease, vascular compromise, malignancy, motility disorders, and trauma; with the first two accounting for over 50% of cases. Although this is clearly subject to selection and referral bias, these aetiologies are similar to those cited elsewhere,3 with the common thread being disease affecting the mesenteric root. A frequent goal of treatment is to halt the decline in the patient's nutritional state, replenishing deficiencies and allowing the patient to recover sufficiently such that reconstructive surgery can be contemplated with a good chance of healing. To this end, several months of patient stabilization and evaluation are often undertaken after initial referral, with assessment of bowel length, configuration and quality, control of sepsis and concurrent nutritional support the three key initial steps prior to any attempt at restorative treatment.
Role of radiology
Radiology provides the clinician with key information about the quantity and quality of remaining bowel,4 which aids them in assessing the bowel for nutritional use. The non-invasive nature of diagnostic radiology permits a thorough assessment of a complex abdomen allowing guidance of the surgeon on how to avoid adhesions and also on prognosis and in planning laparotomies to avoid inadvertent enterotomies.5 Knowledge of enterocutaneous and internal fistula anatomy is also important for planning reconstructive surgery.6 Using a variety of techniques, the following aims are met: map the bowel anatomy, including enterocutaneous fistulae; make an assessment of bowel quality and suitability for enteral feeding; establish whether surgical reconstruction may be possible; diagnose and treat complications, often involving the control of sepsis via drainage; and assist with feeding options [total parenteral nutrition (TPN) via venous routes, placement of enteral feeding tubes].
Radiological techniques
Contrast studies
Contrast studies provide the mainstay of investigations performed when patients are referred, as often the length and quality of remaining bowel is unknown. Almost all referrals have some history of prior surgery with bowel resection, even if this is not itself the primary cause of IF. Often, the precise details of surgery are unavailable, or the procedure was so complex that exact bowel anatomy was unrecognized. Therefore, initial disease management from a radiological perspective is to establish the current enteral anatomy and length. Previous studies have demonstrated reasonable correlation (0.72) between fluoroscopic and surgical measurements of bowel length.7 The critical threshold is often taken to be a length less than 100
cm; although this is an oversimplification, as the character of the remaining bowel is also relevant. For example, if colon is present, then water absorption can occur here and adequate nutrition with only 50
cm of healthy jejunum. Conversely, even with a normal length of bowel, clinical and nutritional criteria for IF can be met in the presence of a generalized disease process, for example, diffuse fold infiltration or certain motility disorders.
For highest accuracy, each surgically separated segment of bowel should be measured individually, either by oral studies or injection of contrast medium into surgically created stomas. This is best achieved when the length measured is less than 150
cm, there are no overlapping loops, and the entire length can be seen on one image.
Barium follow-through examinations have been shown to be accurate, compared to intra-operative measurement of small bowel length. Magnification can be reduced by examining the patient prone, use of overcouch films, and minimizing tube-film distance.8 Figure 1, Figure 2, Figure 3, Figure 4 illustrate a typical diagram from the referring clinicians (often drawn on the back of the request card), with corresponding contrast studies defining the anatomy.

Figure 1
Typical request card, usually with “? Anatomy.” Numbers on the request card are used in radiological reports to help communicate with the clinicians. The arrows indicate anterior abdominal wall stomata or enterocutaneous fistulae.

Figure 2
Jejunostogram (catheter arrowed) connects opening 3 on the request card to a short segment of small bowel and colon (arrowheads).

Figure 3
Subsequent fistulogram (catheter arrowed) via fistula 5 fills the same loop of small bowel and colon shown at jejunostogram (arrowheads). Fistula 4 showed similar findings.

Figure 4
Interval fistulography via fistula 6 (catheter balloon arrowed) leads to small bowel and distal colon of the same loop. Thus, the anatomy of openings 3, 4, 5, and 6 are now defined in relation to the bowel, the length and quality of which have been partly assessed by their imaging characteristics.
Computed tomography (CT) and CT tistulography (CTF)
CT is used for assessing mesenteric pathology, particularly disease affecting the root, which is a key anatomical site where a focal disease process can lead to IF. Multiplanar reformats are often useful for assessing the mesentery. Fig. 5 demonstrates a soft-tissue mass at the mesenteric root in a patient with lymphoma. Although the overall burden of disease was relatively small in this patient, the location at this critical point, the mesenteric vascular pedicle, led to substantial nutritional compromise.

Figure 5
Axial, portal venous-phase CT image showing a soft-tissue mass at the mesenteric root in a patient with lymphoma (arrow).
CT is also crucial in assessing for intra-abdominal collections, which in the chronic setting may not manifest in the typical manner with a systemic inflammatory response; instead, a generalized malaise, hypoalbuminaemia, and cachexia are commoner. It is important to demonstrate foci of sepsis prior to intervention, as surgery in the setting of sepsis is associated with an extremely poor outcome.4 CT-guided drainage is a highly valuable technique, even more so in the IF population because of the complexity of open surgery.
CTF is a further addition to delineate fistula tracks in three dimensions and indicate why they persist (often due to downstream obstruction or persisting abscess cavities). Iodinated contrast medium (300
mg iodine/ml) should be used diluted 1 in 10, with the volume instilled dependent on a “best guess” of the length of bowel or volume of the cavity under evaluation. Oral contrast medium should be avoided to avoid doubt as to the route of origin of any intraluminal contrast. Intravenous contrast medium is of benefit. In the critically ill patient, CTF is particularly useful for problem solving, where performing prolonged contrast studies would not be feasible. Figure 6, Figure 7, Figure 8 demonstrate the advantage of CTF over standard fluoroscopic evaluations.

Figure 6
There was a tiny surface fistula to the abdominal wall in this patient, only large enough to admit a 16 G cannula for fistulography (arrowed). Although communication to bowel was demonstrated (arrowheads), exact anatomy is unclear.

Figure 7
CT fistulography shows the fistula site on the abdominal wall (arrow) leading to a loop of small bowel in the left iliac fossa (arrowhead).

Figure 8
This small bowel loop is traced across the abdomen to the right flank (arrowheads), corresponding to the loop seen in Fig. 6. The volumetric dataset of CT allowed excellent three-dimensional mapping of these bowel loops where fluoroscopy had failed.
Despite this example showing CTF to be superior, in many cases it is either not necessary or the greater spatial and temporal resolution of conventional fistulography is more helpful. One substantial advantage of fluoroscopic fistulography is the dynamic element with multiple time points of imaging being feasible, whereas with CTF, once the contrast medium is instilled, repeated or dynamic acquisitions carry a very high dose penalty.
Magnetic resonance imaging (MRI)
MR enteroclysis is a useful adjunct to barium studies in assessing the quality and quantity of bowel, although severely ill patients are often better served by CT. The other main roles of MRI include hepatobiliary assessment, mapping fistulas (particularly in the pelvis), assessing for intra-abdominal adhesions with cine MRI to look for the absence of visceral slide (loss of the free movement of bowel within the peritoneum,5 and non-invasive venography.
Ultrasound
In the acute setting, this has a limited role, as access to the patients' abdomen can be difficult from multiple dressings, stomas, and fistulas. It can be useful for assessing complications of Crohn's disease (abscess, fistulae, obstruction),9 particularly in young patients when attempting to limit radiation exposure. However, in reality CT tends to be used more frequently due to its advantages in reproducibility and evaluation of the mesentery.
Interventional techniques
These techniques are used as part of the management strategy, including placement of lines for feeding (either enteral/parenteral) and drainage of collections (see above). Enteral options include gastrostomy, either sited at endoscopy or fluoroscopically and distal enteral feeding (DEF), in which a fistula or stoma site is cannulated and the downstream bowel to which it leads is used for nutritional support. This technique may be enough to render a previously TPN-dependent patient capable of adequate enteral nutrition, thus avoiding the complications of indwelling vascular catheters.10
Venous lines can last for decades if looked after carefully, but may generate a prothrombotic tendency. Vascular access for patients dependent on parenteral nutrition is life-preserving, and two-thirds of patients require at least some parenteral nutrition long term. Scrupulous technique in insertion and care of these lines is mandatory, as loss of vascular access is a potentially life-threatening situation (analogous to the haemodialysis-dependent patient).
Individual diseases
The following section covers the individual causes of IF, dealing with the commonest causes in sequence. In general, the radiological findings are no different from those seen in cases of the disease process that have not caused IF. The primary difference is usually the severity of the disease or the number or complexity of complications. This section does not attempt to review all the general findings of these diseases, but rather to bring out the relevant features as they relate to IF.
Crohn's disease
In the UK, Crohn's disease is the most common cause of adult IF11; 40% of patients who require TPN in the UK have Crohn's disease. IF is generally seen in those patients with the advanced and uncommon end of the spectrum, usually with years of disease. Uncomplicated Crohn's resection has a low incidence of IF (0.5–2.2%). In the patients with IF, it generally results from multiple laparotomies for sepsis with associated small bowel resections. The areas of diseased bowel predict which nutrient deficiencies the patient is likely to have, which is important in management. If proximal disease predominates, calorie deficiency is most likely. Distal ileal disease leads to bile salt and vitamin B12 deficiency, and colonic disease causes difficulties with water balance.
Barium studies are key in the initial diagnostic studies and in investigating acute episodes, as in Fig. 9, showing severe distal Crohn's disease, with the corresponding MRI image in Fig. 10. Many CT radiological signs in the acute setting, including bowel wall thickening, ulceration, increased mesenteric vascularity (“comb sign”), increased mural enhancement, mural stratification, and submucosal oedema, are well reviewed elsewhere.12

Figure 9
Severe distal Crohn's disease. Note marked loop separation, mesenteric shortening, and anti-mesenteric sacculation, with sharp “rose-thorn” ulceration on the more cranial loop and upstream dilatation.

Figure 10
Coronal half-Fourier axial single-shot fast spin-echo MRI image in the same patient as Fig. 9 demonstrating a similar contour to the lumen of the distal ileal loops with florid wall thickening (the patient had refused naso-jejunal intubation for formal MRI enteroclysis).
Multiple operations
A history of prior bowel resection is present in over 90% of patients referred to our unit. The initial procedure is often unexpectedly complex or (in retrospect) was ill advised. There is often a past history of multiple laparotomies, increasingly complicated and each with their own associated complications, such as collections and inadvertent enterotomies (Fig. 11).

Figure 11
Flowchart illustrating the cycle of complex surgery followed by multiple complications and nutritional decline.
Vascular causes
Small bowel vascular compromise leads to IF both via the direct bowel insult and via surgical resection, which itself often leads to complications (see prior section). In our centre, there is approximately a 2:1 ratio of venous disease to arterial disease as a cause of IF, exemplified in Fig. 12. There is a disparity between a 5% incidence of venous thrombosis as a cause of mesenteric ischaemia13 and a 60–70% rate of venous thrombosis as a cause of IF. This is largely due to the extremely poor survival rates of those sustaining severe arterial infarction. In 70% of our patients who had sustained a venous insult, an underlying pro-coagulable state is found. This figure concurs with other studies, the underlying prothrombotic tendencies including Factor V Leiden deficiency, protein S or C deficiency, and antithrombin III deficiency.14 Therefore, these should be actively sought out should this diagnosis be made, a fact, which should be highlighted to the clinicians. Another less common vascular cause is radiotherapy injury, causing microvasculitis or diffuse obliterative endarteritis (Fig. 13).

Figure 12
Portal venous-phase CT image demonstrates a filling defect in the superior mesenteric vein (arrow), with a thickened and abnormal adjacent bowel loop (arrowhead).

Figure 13
Contrast angiography shows a diffuse field change with hypervascularity in radiotherapy-damaged bowel.
Motility disorders
These are usually associated with a structural malabsorptive process as well as dysmotility, the prototype being scleroderma. Severe dysmotility leads to bacterial overgrowth, which compounds nutritional deficiencies, which contribute to a gut-derived chronic inflammatory state.15 Underlying disease processes include scleroderma, severe diabetes-associated dysmotility, coeliac disease, and idiopathic dysmotility disorders. Fig. 14 shows a case of idiopathic small bowel dysmotility.

Figure 14
This patient had extremely abnormal gut motility, with severely delayed small bowel transit clinically, radiologically, and by nuclear medicine. The coronal reformat from multidetector CT demonstrates significantly dilated small bowel loops with no mechanical obstruction or point of transition. There is abnormal “slurry-like” small bowel content, suggestive of stasis and bacterial overgrowth, confirmed on breath testing.
Trauma
Both penetrating and blunt trauma can lead to IF. Although early studies with axial CT in blunt trauma suggested its performance was disappointing in demonstrating bowel and mesenteric injury,16 helical CT has been shown to be highly accurate in both types of injury when read by experienced staff.17 Commonly, surgery with subsequent complications is the mode of presentation, especially if the peritoneum is soiled by enteric content following bowel rupture. Fig. 15 illustrates a case of post-blunt abdominal trauma, with fairly subtle CT abnormalities but extensive injury detected at laparotomy.

Figure 15
CT following blunt trauma from a car accident shows a triangular fluid pocket close to thick-walled, briskly enhancing loops of small bowel (arrowhead). Several tiny pockets of free gas are visible anteriorly (arrows). The patient underwent laparotomy, where perforation and mesenteric tear with haemorrhage was confirmed.
Complications arising in the IF patient
Sepsis is the commonest complication encountered, which may relate both to the primary disease and its treatment. Crohn's disease, in particular, leads to sepsis as a part of the intrinsic disease process, where structures adjacent to inflamed bowel become injured, and a local inflammatory process occurs. In motility disorders, bacterial overgrowth and translocation may contribute to septic foci in the liver and spleen.
Iatrogenic complications depend on the treatment modality used, but again sepsis is a recurring theme. After surgery, inadvertent enterotomies and anastomotic breakdown commonly lead to infected collections. Steroid use in Crohn's disease and chemotherapy in those with a malignant cause for IF are further predispositions to infection in a population whose nutritional compromise already puts them at increased risk.
Critical loss of venous access is defined as when more than two veins suitable for a feeding catheter are occluded, or where positioning of a feeding catheter can only be achieved with the aid of complex interventional radiological or surgical techniques.1 MR venography is an excellent technique for gaining an overview of venous anatomy and defining alternative sites for potential vascular access (Fig. 16). Line-related sepsis is a constant concern for these patients, and careful handling of lines is required and should be avoided if at all possible. Line occlusion (thrombosis) is another potential complication, for which fluoroscopic contrast linograms are the reference standard.

Figure 16
This patient had required numerous indwelling central venous catheters for long-term parenteral nutrition as an adjunct to enteral feeding. The coronal minimum intensity projection images from this post-gadolinium MR venography show bilateral subclavian occlusions (arrowheads) with collateral vessel formation.
Liver disease is significant in IF patients because when hepatic impairment occurs, prognosis worsens as a second organ system is now failing.18 At this point, a transplant of either small bowel alone or in combination with a liver transplant should be considered, particularly in the presence of portal hypertension.3 MRI is useful in assessing the gastrointestinal and hepatic disease process and excluding reversible causes of hepatic failure. Chemical shift imaging is also useful in demonstrating hepatic steatosis, a complication of parenteral nutrition.
Conclusion
In our experience, IF often arises from a particularly severe form of a common disease process, which often affects the mesenteric root. This is frequently followed by a surgical procedure involving bowel resection, which is often unexpectedly complex and followed by multiple complications and re-do procedures. Imaging has a key role in characterizing and helping utilize any remaining functional bowel for nutritional support. Multiple imaging modes should be applied flexibly to characterize the disease process and assist in management. The radiologist has a crucial role in assisting in the multidisciplinary management of these patients, mapping anatomy, demonstrating complications, draining infected foci and placing feeding lines, all in the hope of controlling the disease process and rebuilding the patient's nutritional state such that reconstructive surgery can be offered at a later date once the acute inflammatory components of the disease have settled.
References
- Collaborative strategies to reduce mortality and morbidity in patients with chronic intestinal failure including those who are referred for small bowel transplantation. Transplantation. 2008;85:1378–1384
- . A strategic framework for intestinal failure and home parenteral services for adults in England. National Commissioning Group for Highly Specialised Services; April 2008;Available from: http://www.nnng.org/Links/National%20Guidence,%20Audit%20and%20Research/HIFNET%20document.pdfhttp://www.ncg.nhs.uk/ncg_services.htm#Severe%20intestinal%20failure%20(IF)%20service[Accessed 23.11.09]
- . Etiology and initial management of short bowel syndrome. Gastroenterology. 2006;130(Suppl. 1):S5–S15
- . Surgical management of intestinal failure. Proc Nutr Soc. 2003;62:711–718
- Detection and mapping of intraabdominal adhesions by using functional cine MR imaging: preliminary results. Radiology. 2000;217:421–425
- Treatment strategies in 135 consecutive patients with enterocutaneous fistulas. World J Surg. 2008;32:445–453
- . Length of residual bowel after partial resection: correlation between radiographic and surgical measurements. Gastrointest Radiol. 1991;16:305–306
- Reliability of radiographic measurement of small intestinal length. Colorectal Dis. 2003;6:327–329
- . Manifestations of Crohn disease at US. RadioGraphics. 1996;16:499–520
- Fistuloclysis can successfully replace parenteral feeding in the nutritional support of patients with enterocutaneous fistula. Br J Surg. 2004;91:625–631
- Mechanisms of intestinal failure in Crohn's disease. Dis Colon Rectum. 2001;44:1834–1837
- . CT features of jejunal pathology. Clin Radiol. 2007;62:1154–1162
- . Acute mesenteric ischaemia: classification, evaluation and therapy. Acta Gastroenterol Belg. 2002;65:220–225
- Prevalence of prothrombotic abnormalities in patients with acute mesenteric ischemia. World J Surg. 2005;29:1135–1138
- . Small intestinal bacterial overgrowth: roles of antibiotics, prebiotics and probiotics. Gastroenterology. 2006;130(2 Suppl. 1):S78–S90
- The diagnostic superiority of computerized tomography. J Trauma. 1985;25:938–946
- Surgically important bowel and/or mesenteric injury in blunt trauma: accuracy of multidetector CT for evaluation. Radiology. 2008;249:524–533
- Incidence, prognosis and etiology of end-stage liver disease in patients receiving home total parenteral nutrition. Surgery. 1999;126:28–34
PII: S0009-9260(10)00061-9
doi:10.1016/j.crad.2010.01.011
© 2010 The Royal College of Radiologists. Published by Elsevier Inc. All rights reserved.
