Pneumotosis Intestinalis

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AJR 2007; 188:16041613

0361803X/07/18861604

American Roentgen Ray Society

.atosis Intestinalis inult

A bd om in al I ma gi ng R ev ie w

Pneumatosis Intestinalis in the Adult:Benign to Life-Threatening Causes

Lisa M. Ho1

Erik K. PaulsonWilliam M. Thompson

Ho LM, Paulson EK, Thompson WM

Keywords: colon, CT, gastrointestinal radiology, ischemia,small bowel

DOI:10.2214/AJR.06.1309

Received October 5, 2006; accepted after revisionDecember 29, 2006.

1All authors: Department of Radiology, Duke UniversityMedical Center, Box 3808 DUMC, Durham, NC 27710.Address correspondence to L. M. Ho (li [email protected]).

OBJECTIVE. The frequency of detection of pneumatosis intestinalis (PI) appears to be in-creasing. This increase may be the result of increased CT use. New medications and surgical pro-cedures have been reported to be associated with an increase in the incidence of PI. The purpose of this review is to provide an update on the imaging features and clinical conditions associated with PI.

CONCLUSION. This article illustrates the imaging findings of PI due to benign and life-threatening causes, with emphasis placed on describing newly associated conditions and alsothe imaging appearance on CT.

neumatosis intestinalis (PI) is de-fined as the presence of gas in thebowel wall [14]. This imagingfinding is associated with numer-

ous conditions, ranging from benign to lifethreatening [15]. The overall incidence of PI in the general population has been re-ported to be 0.03% based on an autopsy se-ries [4]. Although PI can be seen on abdom-inal radiographs, CT is the most sensitiveimaging test for identification of PI [6]. TheCT detection of PI appears to be increasing,

likely as a consequence of increased use of CT technology [7]. Increased imaging detec-tion of PI could also be due to an increasedincidence of PI. Relatively new surgical pro-cedures and medications associated with PImay be contributing to an increase in inci-dence of PI. The aim of this article is to de-scribe the imaging appearance and clinicalfindings of PI in the adult population.

Classification SystemIn 1754, Duvernoy wrote the first report of

PI, which appeared in the French literature[8]. Since then, numerous case reports and re-

views have appeared in the world literature. In1998, Pear [5] undertook the most recentcomprehensive review in the U.S. radiologyliterature. His classification scheme wasbased on the current evidence and theories re-garding the cause and clinical significance of PI. In his review, PI was classified pathogen-ically into four categories: bowel necrosis,mucosal disruption, increased mucosal per-meability, and pulmonary disease.

In this article, we divided PI into two cat-egories: benign causes and life-threateningcauses (Appendix 1). It is important to un-derstand that PI is a sign not a disease, andit must be interpreted relative to the pa-tients overall clinical condition. Therefore,clinical symptoms and laboratory data pro-vide the most important clues in determin-ing whether PI is due to benign or life-threatening causes.

Pathogenesis

Although the cause of PI appears to bemultifactorial, the exact cause is not known.Two main theories have been proposed inthe medical literature. A mechanical theoryhypothesizes that gas dissects into the bowelwall from either the intestinal lumen or thelungs via the mediastinum [1] due to somemechanism causing increased pressure (i.e.,bowel obstruction or emphysema). A bacte-rial theory proposes that gas-forming bacillienter the submucosa through mucosal rentsor increased mucosal permeability and pro-duce gas within the bowel wall [1].

Studies have shown that gas collections in

the bowel wall can have a hydrogen contentof up to 50%. Hydrogen is a product of bac-terial metabolism and is not produced by hu-man cells [1]. The major argument againstthe bacterial theory is that long-standingpneumoperitoneum can occur with PI andrarely is it associated with peritonitis [8]. Acombination of both theories is also plausi-ble. Bacterial overgrowth in the gastrointes-tinal tract from a variety of causes can lead

P


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to excessive hydrogen gas production,bowel distention, and subsequently, dissec-tion of intraluminal hydrogen gas into thebowel wall.

Clinical FeaturesIn cases of PI due to benign causes, espe-

cially PI associated with pulmonary disease,the patients are usually asymptomatic [14].Some patients may have mild abdominal

discomfort, which is usually related to theunderlying associated medical condition.Physical examination is rarely abnormal un-less there are peritoneal signs from intesti-nal perforation in cases of PI due to life-threatening causes. Laboratory values in thepresence of intestinal ischemia may revealacidosis with a blood pH of < 7.3, a hyper-amylasemia of > 200 IU/L, a serum bicar-bonate level of < 20 mmol/L, and an ele-

vated serum lactic acid of > 2 mmol/L [3].A recent study found that the combinationof PI and a serum lactic acid level of > 2mmol/L was associated with a greater than80% mortality rate [9].

Imaging Methods and FindingsAbdominal radiography and CT are the

most frequently used techniques for diagno-sis of PI. CT has been shown to be more sen-

A B

Fig. 1Examples oflinear and bubblypneumatosis intestinalis(PI).A,Abdominal CT image in54-year-old womanshows extraluminal gas tracking along small

bowel mesentery ( black arrowhead ) and linear PI(arrows ) in this case of PIassociated withjejunostomy tube ( white arrowhead ).B,Abdominal CT image in56-year-old man showsbubbly PI (arrows ) andfree air ( arrowheads ) in this case of PI in patienton chemotherapy forcolon cancer.

A B

Fig. 269-year-oldwoman with guaiac-positive stoolbenigncause of pneumatosisintestinalis (PI).A,Scout radiograph fromair-contrast bariumenema shows cystic PI(arrow ) consistent withpneumatosis cystoidesintestinalis.B, Spot film images fromair-contrast bariumenema show polypoidfilling defects (arrows )due to gas in bowel wall(arrowheads ) frompneumatosis cystoidesintestinalis.


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sitive than radiography at detecting PI[1014]. CT has also been shown to be moresensitive than radiography at detection of hepatic portal and portomesenteric venousgas [12, 15, 16], the presence of which in-creases the possibility of PI due to life-threatening causes. Advances in CT may

further improve the detection of PI and he-patic portal and portomesenteric venousgas; 16- and 64-MDCT scanners are capableof generating isotropic data sets that allowmultiplanar reformations with a spatial res-olution similar to or even greater than theaxial plane. The ability to study the bowel

Fig. 369-year-old manon chemotherapy forheadneck cancer withmild abdominal painbenign cause ofpneumatosis intestinalis(PI).A,Abdominal CT image

using soft-tissue windowsetting shows PI ofcecum and ascendingcolon (arrows ).B, Abdominal CT imageshows PI of cecum andascending colon(arrows ) is much betterseen using lung windowsetting. Patient improvedwithout any special therapy.

A

B

wall in the coronal, sagittal, and axial planesmay allow a more confident diagnosis of PIand portal venous gas.

On both radiographs and CT, PI usuallyappears as a low-density linear or bubblypattern of gas in the bowel wall (Fig. 1). It

can be a combination of both linear and bub-bly bowel-wall gas. There also may be cir-cular collections of gas in the bowel wall(Fig. 2). Occasionally, bowel contentsmixed with air or air trapped between mu-cosal folds can mimic PI. Viewing CT im-ages with lung windows may accentuate thedetection of PI, especially in the colon [11](Fig. 3). Because CT is more sensitive thanradiography in detecting PI, CT can be usedto clarify ambiguous radiographic findingsand also to search for potential causes [11].

The circular form of PI is usually benignand most often seen with pneumatosis cys-

toides intestinalis (PCI). Linear or bubble-like PI can be due to both benign and life-threatening causes, and its radiographic orCT appearance alone does not allow differ-entiation between them. In PI due to benigncauses, the bowel wall is usually normal.The presence of additional findings such asbowel wall thickening, absent or intensemucosal enhancement, dilated bowel, arte-rial or venous occlusion, ascites, and he-patic portal or portomesenteric venous gasincreases the possibility of PI due to a life-threatening cause [15, 17] (Fig. 4). PI that isconfined to a portion of the small or large

bowel within a specific vascular distributionalso increases the likelihood that ischemia isthe cause of PI. Intraperitoneal or retroperi-toneal free air can be seen with PI due tolife-threatening or benign causes [6, 1820].The association of spontaneous pneumo-peritoneum with PI has been attributed tothe rupture of serosal and subserosal cysts inthe bowel wall [8].

Portal venous gas is differentiated frombiliary gas by its characteristic tubularbranching lucencies that extend to the pe-riphery of the liver, whereas biliary air ismore central (Fig. 5). The use of coronal re-

formatted images with MDCT may improvedetection of portomesenteric gas owing tothe oblique vertical orientation of the mesen-teric vessels [15, 21].

Several reports in the literature have ad-dressed the capability of CT of distinguish-ing early and nontransmural mesenteric is-chemia from full-thickness and irreversibletransmural infarction [17, 22, 23]. Both Ker-nagis et al. [23] and Weisner et al. [22] found


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A

B

C

Fig. 479-year-old woman after recent surgery for gastric cancer. Patient developedabdominal pain and blood pH, 7.24; lactic acid, 8.1 mmol/L; and plasma bicarbonate(HCO3), 18 mmol/Llife-threatening cause of pneumatosis intestinalis (PI).A,Supine digital abdominal radiograph shows free air ( arrows ), small-boweldistention, and small-bowel PI ( arrowheads ).B and C,Abdominal CT images show free air ( long arrows ) and small-bowel PI ( short

arrows , C) but also hepatic portal venous gas ( arrowheads , B) not seen onradiograph. At surgery, diffuse ischemia of small bowel was found. Patient died 1week later.

that linear PI was seen more frequently thanbubbly PI in patients with transmural bowelinfarction. Furthermore, both research stud-

ies found that the detection of PI in associa-tion with portomesenteric venous gas corre-lated strongly with transmural bowelinfarction, whereas PI without evidence of portomesenteric venous gas was frequentlyseen in cases of nontransmural intestinal is-chemia. The overall survival rate was higherin patients with nontransmural intestinal is-chemia compared with those patients withtransmural intestinal infarction.

Although the discovery of hepatic portalor portomesenteric venous gas helps to dis-tinguish between benign and life-threatening

causes of PI, it may also occur with or with-out PI as a result of nonischemic conditions.Mesenteric abscess formation, portomesen-teric thrombophlebitis, sepsis, abdominaltrauma, severe enteritis, cholangitis, chroniccholecystitis, pancreatitis, inflammatorybowel disease, and diverticulitis and aftergastrointestinal surgery or liver transplanta-tion are some of the various nonischemicclinical conditions that have been associated

with hepatic portal and portomesentericvenous gas [15, 21, 22, 2427].

Sonography can also be used to detect PI

[28, 29]. This technique is more commonlyapplied to the pediatric patient in whomavoidance of ionizing radiation is preferred[30]. PI seen on sonography has been de-scribed as linear or focal echogenic areaswithin the bowel wall [31]. It can also ap-pear as a continuous echogenic ring in thebowel wall [32].

Rarely, PI can also be seen on MRI.Rabushka and Kuhlman [33] described two


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A B

Fig. 5Comparison of hepatic portal venous gas and biliary gas in two different patients.A,23-year-old woman after heart transplant admitted for mild rejection but no abdominal symptoms and normal laboratory results. Abdominal CT image shows hepatic portal

venous gas in periphery of liver ( arrows ).B, 60-year-old man after Whipple procedure for pancreatic cancer. Abdominal CT image shows gas in bile ducts in central part of liver ( arrowheads ).

Fig. 651-year-old manafter lung transplant forcystic fibrosis. Patienthad free air on routinechest radiograph and noabdominal symptomsand normal laboratoryresultsbenign cause ofpneumatosis intestinalis(PI).AC,Digital abdominalradiograph ( A) andabdominal CT images (B and C) show free air(arrows , A and B) anddiffuse linear PI of colon(arrowheads ). Patientwas observed anddischarged.(Fig. 6 continues on nextpage)

A

cases of PI seen with MR. They found cir-cumferential collections of air adherent to orwithin the bowel wall that became more ap-parent on gradient-echo images due to bloom-ing artifact associated with magnetic field in-homogeneities at airtissue interfaces.

Benign Causes of PIAppendix 1 lists benign causes of PI in

the adult. The number of benign conditionsassociated with PI appears to be increasing.

This observation may be the effect of in-creased use of cross-sectional imaging. Inmost cases, the natural history of PI due tobenign causes is not known because there isoften no imaging follow-up. Spontaneousresolution and recurrent episodes have beendescribed in the literature [4, 8, 34]. PCI isone subset of PI that is invariably benign.PCI is characterized by circular collectionsof gas in the bowel wall and its mesentery[11, 34] (Fig. 2). It almost always occurs inthe colon. On barium enema studies, it canmimic polyps when viewed en face(Fig. 2B), but in profile the gas cysts can be

clearly identified within the colon wall(Fig. 2B).

Pulmonary causes of PI are usually benignand range from congenital to acquired. Cysticfibrosis, asthma, and chronic obstructive pul-monary disease have a well-known associa-tion with PI [35, 36]. PI has been reported inpatients who have undergone organ transplan-tation [37, 38]. We have encountered a num-ber of cases (Fig. 6) after lung transplantation[18, 3941]. Although steroid therapy is one


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B C

Fig. 6 (continued)51-year-old man after lung transplant for cystic fibrosis. Patient had free air on routine chest radiograph and no abdominal symptoms and normallaboratory resultsbenign cause of pneumatosis intestinalis (PI).AC,Digital abdominal radiograph ( A) and abdominal CT images ( B and C) show free air ( arrows , Aand B) and diffuse linear PI of colon ( arrowheads ). Patient was observedand discharged.

A B

Fig. 727-year-old woman with history of scleroderma who presented with abdominal distention. Physical examination and laboratory results were normalbenign causeof pneumatosis intestinalis (PI).A,Supine abdominal radiograph shows PI ( arrows ) of small bowel.B, Upright abdominal radiograph shows pneumoperitoneum ( arrows ).


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A B

C

Fig. 8Patients with sudden onset of abdominal painlife-threatening cause ofpneumatosis intestinalis (PI).A,Supine abdominal radiograph in 60-year-old man shows PI of small bowel(arrows ).B, Superior mesenteric arteriogram of same patient as A shows acute thrombosis(arrows ) resulting in small-bowel ischemia and infarction. Patient died.C,Abdominal CT in 65-year-old woman shows acute thrombus ( arrows ) in superiormesenteric artery.

possible cause of PI in the postlung trans-plantation period, cytomegalovirus (CMV)colitis has also been implicated as a cause of PI in the lung transplant patient. CMV colitis

is a common opportunistic infection in lungtransplant recipients, which can manifest asgastrointestinal disease [18]. In our experi-ence, these patients respond well to conserva-

tive therapy that includes bowel rest and em-piric antiviral medication.

Systemic diseases and intestinal disor-ders make up a large number of causes of PI .


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These include collagen vascular diseasesuch as scleroderma [42, 43] (Fig. 7) and in-flammatory bowel disease [19, 44, 45]. Johnet al. [45] reported that CT evidence of PI in

patients with Crohns disease usually corre-lated with a higher severity of disease. How-ever, the presence of PI in these patients didnot dictate a specific course of treatment,and therapy was based on the overall clini-cal picture.

The association of PI with AIDS was fre-quently reported in the early days of the HIVepidemic [20, 46, 47]. However, this findingappears to have become less common, pre-sumably due to the effectiveness of new med-ications and treatments for patients with HIV.

Iatrogenic causes can also be encountered.PI has been seen as a sequela of double-con-

trast barium enema [48]. There have been nu-merous reports of patients with PI associatedwith jejunostomy tubes [3, 49, 50].

Medication side effects can be an over-looked cause of unexplained PI. Corticoster-oid administration is the most common causeof medication-induced PI [4]. Steroids havebeen shown to cause atrophy of lymphoid ag-gregates (Peyer patches) in the gastrointesti-nal tract, which can in turn lead to loss of sub-

mucosal structural integrity and allowdissection of intraluminal air into the intesti-nal wall. PI has been associated with medica-tions that cause bowel distention or diarrhea.

The development of PI in cancer patients hasalso been attributed to several chemothera-peutic agents [4, 51]. Sorbitol, lactulose, andvoglibose have also been reported to cause PI.In most of these cases, PI resolved with dis-continuation of the medication [4, 5255].

Life-Threatening Causes of PIMesenteric ischemia (Fig. 4) is the most

common life-threatening cause of PI (Appen-dix 1). Occasionally, thromboembolization isproven as a cause of the ischemia [6] (Fig. 8),but often the exact cause is never established.Other life-threatening causes of PI include

bowel obstruction, cecal ileus, toxic megaco-lon (Fig. 9), and collagen vascular diseases(which may also produce PI due to benigncauses). As described, PI in the setting of or-gan transplantation is often benign, but it canalso be life threatening, especially after bonemarrow transplantation [5658]. Acute graft-versus-host disease as a life-threatening com-plication of bone marrow transplantation canalso lead to PI [59].

ConclusionThere are many benign and life-threatening

causes of PI. The imaging appearance of bothmay look very similar. Therefore, correlation

with clinical history, physical examination,and laboratory test results is the best indicatorof whether PI is due to a benign or life-threat-ening cause. PCI is one subset of PI that is al-most always benign. In cases of PI associatedwith suspected bowel ischemia, the additionaldetection of hepatic portal or portomesentericvenous gas increases the likelihood of trans-mural bowel infarction.

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APPENDIX 1. Causes of Pneumatosis Intestinalis in the Adult: Benign and Life-Threatening Causes and Associations

A. Benign causes

Pulmonary Asthma Bronchitis Emphysema Pulmonary fibrosis Positive end-expiratory pressure (PEEP) Cystic fibrosis

Systemic disease Scleroderma Systemic lupus AIDS

Intestinal causes Pyloric stenosis Intestinal pseudoobstruction Enteritis Peptic ulcers Bowel obstruction Adynamic ileus

Inflammatory bowel disease Ulcerative colitis Crohns disease Leukemia Perforated jejunal diverticulum Whipples disease Intestinal parasites Collagen vascular disease (especially scleroderma) Diverticulitis

Iatrogenic Barium enema Jejunoileal bypass Jejunostomy tubes Postsurgical anastomosis Endoscopy

Medications Corticosteroids Chemotherapeutic agents Lactulose Sorbitol Voglibose

Organ transplantation Bone marrow Kidney Liver Cardiac Lung Graft versus host

Primary pneumatosis Idiopathic (up to 15% of cases and usually involves the colon) Pneumatosis cystoides intestinalis

B. Life-threatening causes

Intestinal ischemia

Mesenteric vascular disease

Intestinal obstruction (especially strangulation)

Enteritis

Colitis

Ingestion of corrosive agents

Toxic megacolon

Trauma

Organ transplantation (especially bone marrow transplants)

Collagen vascular disease

NoteA number of causes and associations occur under both benign and life-threatening categories.

Pneumotosis Intestinalis

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