DOI:10.2214/AJR.06.1309
AJR 2007; 188:1604-1613
© American Roentgen Ray Society
Pneumatosis Intestinalis in the Adult: Benign to Life-Threatening Causes
Lisa M. Ho1,
Erik K. Paulson and
William M. Thompson
1 All authors: Department of Radiology, Duke University Medical Center, Box 3808
DUMC, Durham, NC 27710.
Received October 5, 2006;
accepted after revision December 29, 2006.
Address correspondence to L. M. Ho
(lisa.ho{at}duke.edu).
Abstract
OBJECTIVE. The frequency of detection of pneumatosis intestinalis
(PI) appears to be increasing. This increase may be the result of increased CT
use. New medications and surgical procedures 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 also the imaging appearance on CT.
Keywords: colon • CT • gastrointestinal radiology • ischemia • small bowel
Introduction
Pneumatosis intestinalis (PI) is defined as the presence of gas in the
bowel wall
[1–4].
This imaging finding is associated with numerous conditions, ranging from
benign to life threatening
[1–5].
The overall incidence of PI in the general population has been reported to be
0.03% based on an autopsy series
[4]. Although PI can be seen on
abdominal radiographs, CT is the most sensitive imaging test for
identification of PI [6]. The
CT detection of PI appears to be increasing, likely as a consequence of
increased use of CT technology
[7]. Increased imaging
detection of PI could also be due to an increased incidence of PI. Relatively
new surgical procedures and medications associated with PI may be contributing
to an increase in incidence of PI. The aim of this article is to describe the
imaging appearance and clinical findings of PI in the adult population.
Classification System
In 1754, Duvernoy wrote the first report of PI, which appeared in the
French literature [8]. Since
then, numerous case reports and reviews have appeared in the world literature.
In 1998, Pear [5] undertook the
most recent comprehensive review in the U.S. radiology literature. His
classification scheme was based on the current evidence and theories regarding
the cause and clinical significance of PI. In his review, PI was classified
pathogenically into four categories: bowel necrosis, mucosal disruption,
increased mucosal permeability, and pulmonary disease.
In this article, we divided PI into two categories: benign causes and
life-threatening causes (Appendix 1). It is important to understand that PI is
a sign not a disease, and it must be interpreted relative to the patient's
overall clinical condition. Therefore, clinical symptoms and laboratory data
provide the most important clues in determining whether PI is due to benign or
life-threatening causes.
Pathogenesis
Although the cause of PI appears to be multifactorial, the exact cause is
not known. Two main theories have been proposed in the medical literature. A
mechanical theory hypothesizes that gas dissects into the bowel wall from
either the intestinal lumen or the lungs via the mediastinum
[1] due to some mechanism
causing increased pressure (i.e., bowel obstruction or emphysema). A bacterial
theory proposes that gas-forming bacilli enter the submucosa through mucosal
rents or increased mucosal permeability and produce gas within the bowel wall
[1].
Studies have shown that gas collections in the bowel wall can have a
hydrogen content of up to 50%. Hydrogen is a product of bacterial metabolism
and is not produced by human cells
[1]. The major argument against
the bacterial theory is that long-standing pneumoperitoneum can occur with PI
and rarely is it associated with peritonitis
[8]. A combination of both
theories is also plausible. Bacterial overgrowth in the gastrointestinal tract
from a variety of causes can lead to excessive hydrogen gas production, bowel
distention, and subsequently, dissection of intraluminal hydrogen gas into the
bowel wall.
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Fig. 1A —Examples of linear and bubbly pneumatosis intestinalis (PI).
Abdominal CT image in 54-year-old woman shows extraluminal gas tracking along
small bowel mesentery (black arrowhead) and linear PI
(arrows) in this case of PI associated with jejunostomy tube
(white arrowhead).
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Fig. 1B —Examples of linear and bubbly pneumatosis intestinalis (PI).
Abdominal CT image in 56-year-old man shows bubbly PI (arrows) and
free air (arrowheads) in this case of PI in patient on chemotherapy
for colon cancer.
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Fig. 2A —69-year-old woman with guaiac-positive stool—benign
cause of pneumatosis intestinalis (PI). Scout radiograph from air-contrast
barium enema shows cystic PI (arrow) consistent with pneumatosis
cystoides intestinalis.
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Fig. 2B —69-year-old woman with guaiac-positive stool—benign
cause of pneumatosis intestinalis (PI). Spot film images from air-contrast
barium enema show polypoid filling defects (arrows) due to gas in
bowel wall (arrowheads) from pneumatosis cystoides intestinalis.
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Clinical Features
In cases of PI due to benign causes, especially PI associated with
pulmonary disease, the patients are usually asymptomatic
[1–4].
Some patients may have mild abdominal discomfort, which is usually related to
the underlying associated medical condition. Physical examination is rarely
abnormal unless there are peritoneal signs from intestinal perforation in
cases of PI due to life-threatening causes. Laboratory values in the presence
of intestinal ischemia may reveal acidosis with a blood pH of < 7.3, a
hyperamylasemia of > 200 IU/L, a serum bicarbonate level of < 20 mmol/L,
and an elevated serum lactic acid of > 2 mmol/L
[3]. A recent study found that
the combination of PI and a serum lactic acid level of > 2 mmol/L was
associated with a greater than 80% mortality rate
[9].
Imaging Methods and Findings
Abdominal radiography and CT are the most frequently used techniques for
diagnosis of PI. CT has been shown to be more sensitive than radiography at
detecting PI
[10–14].
CT has also been shown to be more sensitive than radiography at detection of
hepatic portal and portomesenteric venous gas
[12,
15,
16], the presence of which
increases the possibility of PI due to life-threatening causes. Advances in CT
may further improve the detection of PI and hepatic portal and portomesenteric
venous gas; 16- and 64-MDCT scanners are capable of generating isotropic data
sets that allow multiplanar reformations with a spatial resolution similar to
or even greater than the axial plane. The ability to study the bowel wall in
the coronal, sagittal, and axial planes may allow a more confident diagnosis
of PI and portal venous gas.
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Fig. 3A —69-year-old man on chemotherapy for head–neck cancer
with mild abdominal pain—benign cause of pneumatosis intestinalis (PI).
Abdominal CT image using soft-tissue window setting shows PI of cecum and
ascending colon (arrows).
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Fig. 3B —69-year-old man on chemotherapy for head–neck cancer
with mild abdominal pain—benign cause of pneumatosis intestinalis (PI).
Abdominal CT image shows PI of cecum and ascending colon (arrows) is
much better seen using lung window setting. Patient improved without any
special therapy.
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On both radiographs and CT, PI usually appears as a low-density linear or
bubbly pattern of gas in the bowel wall (Fig.
1A,
1B). It can be a combination of
both linear and bubbly bowel-wall gas. There also may be circular collections
of gas in the bowel wall (Fig.
2A,
2B). Occasionally, bowel
contents mixed with air or air trapped between mucosal folds can mimic PI.
Viewing CT images with lung windows may accentuate the detection of PI,
especially in the colon [11]
(Fig. 3A,
3B). Because CT is more
sensitive than radiography in detecting PI, CT can be used to clarify
ambiguous radiographic findings and also to search for potential causes
[11].
The circular form of PI is usually benign and most often seen with
pneumatosis cystoides intestinalis (PCI). Linear or bubble-like PI can be due
to both benign and life-threatening causes, and its radiographic or CT
appearance alone does not allow differentiation between them. In PI due to
benign causes, the bowel wall is usually normal. The presence of additional
findings such as bowel wall thickening, absent or intense mucosal enhancement,
dilated bowel, arterial or venous occlusion, ascites, and hepatic portal or
portomesenteric venous gas increases the possibility of PI due to a
life-threatening cause [15,
17] (Fig.
4A,
4B,
4C). PI that is confined to a
portion of the small or large bowel within a specific vascular distribution
also increases the likelihood that ischemia is the cause of PI.
Intraperitoneal or retroperitoneal free air can be seen with PI due to
life-threatening or benign causes
[6,
18–20].
The association of spontaneous pneumoperitoneum with PI has been attributed to
the rupture of serosal and subserosal cysts in the bowel wall
[8].
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Fig. 4A —79-year-old woman after recent surgery for gastric cancer.
Patient developed abdominal pain and blood pH, 7.24; lactic acid, 8.1 mmol/L;
and plasma bicarbonate (HCO3), 18 mmol/L—life-threatening
cause of pneumatosis intestinalis (PI). Supine digital abdominal radiograph
shows free air (arrows), small-bowel distention, and small-bowel PI
(arrowheads).
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Fig. 4B —79-year-old woman after recent surgery for gastric cancer.
Patient developed abdominal pain and blood pH, 7.24; lactic acid, 8.1 mmol/L;
and plasma bicarbonate (HCO3), 18 mmol/L—life-threatening
cause of pneumatosis intestinalis (PI). 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 on
radiograph. At surgery, diffuse ischemia of small bowel was found. Patient
died 1 week later.
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Fig. 4C —79-year-old woman after recent surgery for gastric cancer.
Patient developed abdominal pain and blood pH, 7.24; lactic acid, 8.1 mmol/L;
and plasma bicarbonate (HCO3), 18 mmol/L—life-threatening
cause of pneumatosis intestinalis (PI). 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 on
radiograph. At surgery, diffuse ischemia of small bowel was found. Patient
died 1 week later.
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Portal venous gas is differentiated from biliary gas by its characteristic
tubular branching lucencies that extend to the periphery of the liver, whereas
biliary air is more central (Fig.
5A,
5B). The use of coronal
reformatted images with MDCT may improve detection of portomesenteric gas
owing to the oblique vertical orientation of the mesenteric vessels
[15,
21].
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Fig. 5A —Comparison of hepatic portal venous gas and biliary gas in
two different patients. 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).
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Fig. 5B —Comparison of hepatic portal venous gas and biliary gas in
two different patients. 60-year-old man after Whipple procedure for pancreatic
cancer. Abdominal CT image shows gas in bile ducts in central part of liver
(arrowheads).
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Several reports in the literature have addressed the capability of CT of
distinguishing early and nontransmural mesenteric ischemia from full-thickness
and irreversible transmural infarction
[17,
22,
23]. Both Kernagis et al.
[23] and Weisner et al.
[22] found that linear PI was
seen more frequently than bubbly PI in patients with transmural bowel
infarction. Furthermore, both research studies found that the detection of PI
in association with portomesenteric venous gas correlated strongly with
transmural bowel infarction, whereas PI without evidence of portomesenteric
venous gas was frequently seen in cases of nontransmural intestinal ischemia.
The overall survival rate was higher in patients with nontransmural intestinal
ischemia compared with those patients with transmural intestinal
infarction.
Although the discovery of hepatic portal or portomesenteric venous gas
helps to distinguish between benign and life-threatening causes of PI, it may
also occur with or without PI as a result of nonischemic conditions.
Mesenteric abscess formation, portomesenteric thrombophlebitis, sepsis,
abdominal trauma, severe enteritis, cholangitis, chronic cholecystitis,
pancreatitis, inflammatory bowel disease, and diverticulitis and after
gastrointestinal surgery or liver transplantation are some of the various
nonischemic clinical conditions that have been associated with hepatic portal
and portomesenteric venous gas
[15,
21,
22,
24–27].
Sonography can also be used to detect PI
[28,
29]. This technique is more
commonly applied to the pediatric patient in whom avoidance of ionizing
radiation is preferred [30].
PI seen on sonography has been described as linear or focal echogenic areas
within the bowel wall [31]. It
can also appear as a continuous echogenic ring in the bowel wall
[32].
Rarely, PI can also be seen on MRI. Rabushka and Kuhlman
[33] described two cases of PI
seen with MR. They found circumferential collections of air adherent to or
within the bowel wall that became more apparent on gradient-echo images due to
blooming artifact associated with magnetic field inhomogeneities at
air–tissue interfaces.
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Fig. 6A —51-year-old man after lung transplant for cystic fibrosis.
Patient had free air on routine chest radiograph and no abdominal symptoms and
normal laboratory results—benign cause of pneumatosis intestinalis (PI).
Digital abdominal radiograph (A) and abdominal CT images (B and
C) show free air (arrows, A and B) and diffuse
linear PI of colon (arrowheads). Patient was observed and
discharged.
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Benign Causes of PI
Appendix 1 lists benign causes of PI in the adult. The number of benign
conditions associated with PI appears to be increasing. This observation may
be the effect of increased use of cross-sectional imaging. In most cases, the
natural history of PI due to benign causes is not known because there is often
no imaging follow-up. Spontaneous resolution and recurrent episodes have been
described in the literature [4,
8,
34]. PCI is one subset of PI
that is invariably benign. PCI is characterized by circular collections of gas
in the bowel wall and its mesentery
[11,
34] (Fig.
2A,
2B). It almost always occurs in
the colon. On barium enema studies, it can mimic 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 benign and range from congenital to
acquired. Cystic fibrosis, asthma, and chronic obstructive pulmonary disease
have a well-known association with PI
[35,
36]. PI has been reported in
patients who have undergone organ transplantation
[37,
38]. We have encountered a
number of cases (Fig. 6A,
6B,
6C) after lung transplantation
[18,
39–41].
Although steroid therapy is one possible cause of PI in the post–lung
transplantation 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 lung transplant recipients, which can manifest as
gastrointestinal disease [18].
In our experience, these patients respond well to conservative therapy that
includes bowel rest and empiric antiviral medication.
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Fig. 6B —51-year-old man after lung transplant for cystic fibrosis.
Patient had free air on routine chest radiograph and no abdominal symptoms and
normal laboratory results—benign cause of pneumatosis intestinalis (PI).
Digital abdominal radiograph (A) and abdominal CT images (B and
C) show free air (arrows, A and B) and diffuse
linear PI of colon (arrowheads). Patient was observed and
discharged.
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Fig. 6C —51-year-old man after lung transplant for cystic fibrosis.
Patient had free air on routine chest radiograph and no abdominal symptoms and
normal laboratory results—benign cause of pneumatosis intestinalis (PI).
Digital abdominal radiograph (A) and abdominal CT images (B and
C) show free air (arrows, A and B) and diffuse
linear PI of colon (arrowheads). Patient was observed and
discharged.
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Fig. 7A —27-year-old woman with history of scleroderma who presented
with abdominal distention. Physical examination and laboratory results were
normal—benign cause of pneumatosis intestinalis (PI). Supine abdominal
radiograph shows PI (arrows) of small bowel.
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Fig. 7B —27-year-old woman with history of scleroderma who presented
with abdominal distention. Physical examination and laboratory results were
normal—benign cause of pneumatosis intestinalis (PI). Upright abdominal
radiograph shows pneumoperitoneum (arrows).
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Fig. 8B —Patients with sudden onset of abdominal
pain—life-threatening cause of pneumatosis intestinalis (PI). Superior
mesenteric arteriogram of same patient as A shows acute thrombosis
(arrows) resulting in small-bowel ischemia and infarction. Patient
died.
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Fig. 8C —Patients with sudden onset of abdominal
pain—life-threatening cause of pneumatosis intestinalis (PI). Abdominal
CT in 65-year-old woman shows acute thrombus (arrows) in superior
mesenteric artery.
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Systemic diseases and intestinal disorders make up a large number of causes
of PI. These include collagen vascular disease such as scleroderma
[42,
43] (Fig.
7A,
7B) and inflammatory bowel
disease [19,
44,
45]. John et al.
[45] reported that CT evidence
of PI in patients with Crohn's disease usually correlated with a higher
severity of disease. However, the presence of PI in these patients did not
dictate a specific course of treatment, and therapy was based on the overall
clinical picture.
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Fig. 9A —19-year-old man with toxic megacolon due to Crohn's
disease—life-threatening cause of pneumatosis intestinalis (PI).
Emergency colectomy was performed. Supine (A) and upright (B)
abdominal radiographs show diffuse PI of colon (arrows).
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Fig. 9B —19-year-old man with toxic megacolon due to Crohn's
disease—life-threatening cause of pneumatosis intestinalis (PI).
Emergency colectomy was performed. Supine (A) and upright (B)
abdominal radiographs show diffuse PI of colon (arrows).
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The association of PI with AIDS was frequently reported in the early days
of the HIV epidemic [20,
46,
47]. However, this finding
appears to have become less common, presumably due to the effectiveness of new
medications and treatments for patients with HIV.
Iatrogenic causes can also be encountered. PI has been seen as a sequela of
double-contrast barium enema
[48]. There have been numerous
reports of patients with PI associated with jejunostomy tubes
[3,
49,
50].
Medication side effects can be an overlooked cause of unexplained PI.
Corticosteroid administration is the most common cause of medication-induced
PI [4]. Steroids have been
shown to cause atrophy of lymphoid aggregates (Peyer patches) in the
gastrointestinal tract, which can in turn lead to loss of submucosal
structural integrity and allow dissection of intraluminal air into the
intestinal wall. PI has been associated with medications that cause bowel
distention or diarrhea. The development of PI in cancer patients has also been
attributed to several chemotherapeutic agents
[4,
51]. Sorbitol, lactulose, and
voglibose have also been reported to cause PI. In most of these cases, PI
resolved with discontinuation of the medication
[4,
52–55].
Life-Threatening Causes of PI
Mesenteric ischemia (Fig.
4A,
4B,
4C) is the most common
life-threatening cause of PI (Appendix 1). Occasionally, thromboembolization
is proven as a cause of the ischemia
[6] (Fig.
8A,
8B,
8C), but often the exact cause
is never established. Other life-threatening causes of PI include bowel
obstruction, cecal ileus, toxic megacolon (Fig.
9A,
9B), and collagen vascular
diseases (which may also produce PI due to benign causes). As described, PI in
the setting of organ transplantation is often benign, but it can also be life
threatening, especially after bone marrow transplantation
[56–58].
Acute graft-versus-host disease as a life-threatening complication of bone
marrow transplantation can also lead to PI
[59].
Conclusion
There are many benign and life-threatening causes of PI. The imaging
appearance of both may look very similar. Therefore, correlation with clinical
history, physical examination, and laboratory test results is the best
indicator of whether PI is due to a benign or life-threatening cause. PCI is
one subset of PI that is almost always benign. In cases of PI associated with
suspected bowel ischemia, the additional detection of hepatic portal or
portomesenteric venous gas increases the likelihood of transmural bowel
infarction.
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 |
| • Crohn's disease |
| • Leukemia |
| • Perforated jejunal diverticulum |
| • Whipple's 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
|
|
Note—A number of causes and associations occur under both benign and
life-threatening categories.
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Abstract
Introduction
