Clinical Significance of Pneumatosis of the Bowel WaIF PeterJ. Feczko, MD Duane G. Mezwa, MD Michael C. Farab, MD Brian D. White, MD
The presence ofgas within the bowel wall is an uncommon condition that is typically first diagnosed by the radiologist. Although it is often seen on abdominal radiographs, computed tomography is more sensitive in demonstrating pneumatosis and its complications. There is a spectrum of disease states that produce this abnormality, ranging from the innocuous to the fatal. Its radiographic appearance is vanable, particularly the location, extent, severity, and presence of pneumopenitoneum or portal venous gas. None of these imaging characteristics can be considered pathognomonic for the underlying cause of the pneumatosis. The radiologist must be aware of the different conditions associated with this entity, as well as their variable appearances. U INTRODUCTION Although the presence ofgas within the bowel wall has been recognized since the 1700s, a better understanding of the mechanisms behind this phenomenon has been achieved relatively recently (1-7). Pneumatosis is seen in a wide variety of dinical
conditions,
which
nomenon, including lymphopneumatosis,
matosis
is used
is reflected
in the
numerous
pneumatosis cystoides and emphysematous
to indicate
the
presence
terms
used
to refer
intestinalis, pneumatosis gastnitis. In this article, of gas
within
the
bowel
to this
coli, the term wall,
phe-
cystic pneu-
regardless
of
cause or location. Generally speaking, pneumatosis has been divided into two groups: primary (or idiopathic) and secondary. Secondary pneumatosis can be attributable to any of a variety of clinical conditions (Table) Some authors indicate that secondary pneumatosis accounts for approximately 85% ofcases (1,4), but, as our appreciation of the causes of pneumatosis increases, this percentage will probably be greater. It is relatively rare nowadays to encounter a patient with primary pneumatosis, for which no underlying cause can be discerned. The list of causes that are considered to be most common has gradually changed. Studies from several decades ago indicate that pylonc obstruction or ulcer disease was one ofthe most frequent causes (1,5). Today, .
Index
terms:
RadioGraphics I
From
Intestines, 1992;
the Department
Recipient
ofa
revision
requested
: RSNA,
1992
cysts,
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CT.
70.121
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#{149} Pneumoperitoneum,
70.71
#{149} Portal
vein,
gas.
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12:1069-1078 of Diagnostic
Certificate
#{149} Intestines,
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Radiology, for a scientific
received
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1991
Hospital, RSNA
10. Address
3601 scientific reprint
W 13 Mile
Rd.
assembly.
Received
Royal
requests
to P.J.F.
Oak. March
MI 48073. 27,
1992;
1069
Conditions
Associated
with Pneumatosis Malignancies Gastrointestinal
Obstruction
Pylonic obstruction Bowel obstruction Volvulus Peptic
ulcer
or stenosis
Leukemia Extraintestinal
enterocolitis
Inflammation Crohn disease Ulcerative Infectious condition
malignancies
Trauma Surgery, anastomosis or bypass Endoscopy Penetrating or blunt injury Enema studies, barium or other
disease
Necrotizing
cancer
or lymphoma
colitis or parasitic
Pseudomembranous
Drugs (particularly
AIDS-related)
Steroids
Chemotherapy Other
colitis
Diverticulitis
Caustic
Vascular
Pulmonary
ingestion
Asthma Chronic
condition
Ischemia
Cystic
or infarction
disease
obstructive
pulmonary
disease
fibrosis
Diabetes Idiopathic
Collagen
vascular
Scleroderma Systemic lupus Dermatomyositis
Note-AIDS
=
disease Other Whipple disease Amyloidosis Complication of transplantation
erythematosus
acquired
immunodeficiency
syndrome.
pneumatosis is more likely to be encountered in patients undergoing transplantation or chemotherapy. Because of this shift, there has been further investigation into pneumatosis over the past decade, with an emphasis on a better understanding of its development, prognosis, and treatment. In this article, we describe
the
histopathologic
characteristics
of
pneumatosis, review the theories about its development, and discuss the usefulness of specific radiologic appearances of pneumatosis
in the
diagnosis
of pathologic
conditions.
HISTOPATHOLOGIC CHARACTERISTICS U
Pneumatosis is seen grossly as bubbles ring in the wall of the involved segment bowel (Fig 1) (i-3). The bubbles range from a few millimeters to greater than timeter. Typically, these gas collections found
in the
submucosa, They are
1070
U
RadioGrapbics
subserosa,
less
commonly
occurof in size
a cenare in the
and rarely in the muscularis layer. found more often along the mesen-
U
Feczko
et a!
From
references
2, 4, 5, and
8.
tenc side of the bowel but can be seen along the antimesenteric side and even within the mesentery itself. When cyst formation occurs, the cysts are usually thin walled, do not communicate with the bowel lumen, and contain gas that may be under pressure. Analysis of the gas within the cysts indicates that it consists of approximately 50% hydrogen, compared with 14% hydrogen in normal intestinal gas (1,8). This high level of hydrogen is strong evidence for a bacterial origin of the gas, since hydrogen is produced by bacterial metabolism and not by that ofmammalian cells (i). It is unlikely that the gas comes from the lungs because the concentration of hydrogen in the pulmonary gases is normally not that high. Histologically, these cysts have a poorly defined lining that includes multinucleated giant cells (Fig 2). At one time, these cysts were thought to be distended lymphatic yessels, but this concept is no longer accepted (3,5-9). Some authors have observed an associated mild inflammatory reaction in the adjacent mucosa (1-3). These inflammatory changes include infiltration with leukocytes and macrophages, both around the cysts and
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Figures bowel, stain)
tains
1, 2. (1) Endoscopic with overlying normal of a focus
some
view ofpneumatosis shows mucosa. (2) Photomicrograph
of pneumatosis
multinucleated
in the
giant
submucosa
shows
the polypoid protrusions (original magnification, the
poorly
formed
lining
into the lumen of the x 10; hematoxylin-eosin of the
‘
‘cyst,
‘ ‘
which
con-
cells.
with computed tomography indicates that CT is more ography in the detection well as in the evaluation
(CT), however, sensitive than radiof this condition, as of its extent and pos-
sible complications (Fig 3) (10-12). In many cases, pneumatosis was evident at CT but not at abdominal radiography (1 1 12). Detection of pneumatosis by means of ultrasound (US) has also been reported (13). Because US is frequently used as the initial screening examination for someone with abdominal pain, radiologists should be alert for the signs of pneumatosis (13). ,
Figure 3. CT scan of a patient with small bowel pneumatosis demonstrates tions
on the
dependent
sides
of the
extensive gas collecbowel.
in the submucosa. Granulomas, as well as fibrosis, may form in chronic cases (3,5). Earher studies suggested that the overlying mucosa was normal, but more recent reports indicate that there is a high frequency of subtie inflammatory changes in the mucosa (1,3,8). U
IMAGING
OF
PNEUMATOSIS
U
DISCUSSION
.
Etiologic
Theories
Numerous ideas have been proposed concerning the development ofgas within the bowel wall. Given the multitude of conditions that can produce pneumatosis, the cause will vary depending on the clinical condition (Table) In the vast majority of cases, pneumato.
sis
develops
secondary
to
a disruption
of the
mucosal integrity, often with an associated mechanical abnormality and resultant entry of bacteria into the bowel wall (Fig 4) (3,5,8). The following sections discuss several etiologic theories and how they may interact to cause
pneumatosis.
Conventional abdominal radiography has been the preferred imaging modality for the detection of pneumatosis. Recent experience
November
1992
Feczko
et a!
U
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U
1071
Figure 4. Diagram illustrates the proposed mechanism for the development of pneumatosis in a large majority of cases. Mucosal damage along with mechanical factors force anaerobic bacteria into the wall with subsequent cyst formation. Air = gas. (Adapted from reference 3.)
Bacterial cal and produced gin.
Theory.-There is growing experimental evidence that the in pneumatosis is of bacterial
Interestingly,
some
studies
from
clinigas on-
the
early
origin
(8).
Breath
hydrogen
levels,
which
re-
flect bacterial activity vated in patients with that indicates increased
in the intestine, are elepneumatosis, a finding activity of anaerobic, gas-producing organisms (1,5). Expenimentally, Clostridium species have been injected into the submucosa of animals and have induced pneumatosis (8). Interestingly, hyperbaric oxygen has been used to treat both pneumatosis and clostnidial infections (1,3,5,8); the high oxygen levels are thought to diminish anaerobic activity. In some cases, pneumatosis has been shown to respond to treatment with antibiotics (metronidazole or ampicillin), a finding that supports a bacterial cause (3,5). A bacterial origin of pneumatosis would account for the inflammatory reaction evident about the cysts. Of course, the bacterial theory also depends on other factors, such as a loss
of mucosal
the mucosa
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U
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integrity
for
bacteria
and
possible
mechanical
U
Feczko
et a!
to enter forces.
Mechanical Theory.-This that gas enters the bowel rect trauma or increased sis).
Mechanical
is the
1900s suggested a bacterial cause (1). The high hydrogen content within the cysts is strong circumstantial evidence of a bacterial
---
main
theory suggests wall because of dipressure (jeristal-
disruption cause
of the
of pneumatosis
bowel
wall
in cases
of
trauma, surgery, on endoscopy (Fig 5) and is the predisposing cause in pneumatosis associated with obstruction (1,5). It is also known that pneumatosis may occur in instances of vomiting or diarrhea. Although this concept seems logical, one must recognize that gas does not track readily through the bowel wall and consider other factors as well. MucosalDamage mucosal disruption ing factor in virtually so that
bacteria
Theory.-Some type of must occur as an undenlyall cases of pneumatosis,
or gas
become
forced
into
the
bowel wall. Mucosal disruption is the primary causative factor of pneumatosis associated with inflammation or ischemia and is also considered a major factor in pneumatosis associated with Crohn disease when use of steroids depletes Peyer patches in the bowel wall (Fig 6). Many early descriptions of pneumatosis emphasize the integrity of overlying mucosa and how no communication between the bowel lumen and the cysts could be demonstrated. More recent pathologic studies show subtle mucosal inflammatory abnormalities, with the development of tiny cysts in the lamma propria (3).
Volume
12
Number
6
I
I
5-
Figures 5-7. (5) Postoperative pneumatosis. Abdominal radiograph of a patient who had undergone sigmoid resection for diventiculitis reveals pneumatosis on the right side of the colon. Angiography was performed, with normal results. (6) Crohn disease. Abdominal radiograph of a patient with Crohn disease who was receiving stenoids for active inflammation in the colon. (7) Chemotherapy.
shows linear Abdominal
pneumatosis radiograph
of a patient who was undergoing chemotherapy for testicular cancer shows right colonic pneumatosis and gas in the retroperitoneum from ruptured cysts. The patient was asymptomatic, and a barium enema study showed no abnormality.
Beaumont
of Carol
Bosanko,
MD,
William
For patients with asthma or emphysema who develop pneumatosis, it is thought that a low oxygen pressure exists within the bowel wall that leads to overgrowth of anaerobes in the bowel. When small mucosal breaks occur, with entry of these anaerobes into the bowel wall, pneumatosis results (3,5,8).
7-
Pulmonary Disease Theory.-On the basis of animal experiments performed several decades ago, it was proposed that disruption of alveoli causes gas to dissect down the mediastinum along tissue planes and into the bowel wall (6,7). Indeed, many patients with pneumatosis are known to have chronic pulmonary disease. These researchers injected air into the mediastinum of animals, which resulted in the development of pneumatosis (7). It was theorized that air dissected along lymphatic channels by means of peristalsis. However, the hypothesis could not be substantiated in humans, and there was no associated pneumomediastinum or other abnormalities to support it. Today, it is not regarded as a plausible theory (1,5,8).
November
(Courtesy
Hospital, Royal Oak, Mich.)
1992
Other Theories.-Chemical, nutritional, neoplastic, and other theories have also been proposed. There are isolated cases of dietary conditions producing pneumatosis, and this theory may be plausible if they produce a change in bacterial flora or fermentation (1). Patients with neoplasms can occasionally develop pneumatosis, but this may be related more to ischemic complications or to the effect of chemotherapeutic agents on mucosal integrity and bacterial growth (Fig 7).
Feczko
et a!
U
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U
1073
8b.
8a.
9a. 9b. Figures 8, 9. Radiographic appearance ofpneumatosis does not help (8a) Bowel infarction. Abdominal radiograph shows bubbly pneumatosis;
in distinguishing
however,
the
rather
cause.
than
being
an in-
nocuous sign, gangrenous bowel was found at surgery. (8b) Idiopathic pneumatosis. Abdominal radiograph demonstrates linear pneumatosis; however, rather than being indicative of a more serious pathogenesis, the patient’s condition proved to be benign. (9a) Idiopathic pneumatosis. Abdominal radiograph shows bubbly pneumatosis in the left colon in a patient with no known abnormality. (9b) Ischemic bowel. Abdominal radiograph shows a similar appearing bubbly bowel in a patient who proved to have ischemia.
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a.
b.
10. Location ofpneumatosis does tnic pneumatosis from vomiting. Abdominal Figure
not
always
radiograph
help
in determining
of a 12-year-old
its clinical
boy who
significance.
had been
(a)
vomiting
strates pneumatosis that proved to be transient. (b) Diabetic gastric pneumatosis. Abdominal radiograph an elderly man with diabetes shows gastric pneumatosis. He developed emphysematous gastritis with crosis, which has a high associated mortality.
. Significance of Pneumatosis Numerous statements have been cerning the ability of the radiologist
made conto distin-
the
guish
the
of pneuma-
matosis
tosis
seen
causes
on imaging
criteria
include
ity,
location
and
and the
significance
studies. appearance,
of pneumatosis
Radiologic extent, and
severthe
pres-
ence of pneumoperitoneum or portal venous gas. Although there may be some merit to some of the radiologic observations, there are many exceptions to these “rules,” and it is difficult to predict cause or clinical outcome on the basis of radiologic appearances. Some authors have suggested that pneumatosis with a cystic or bubbly appearance is more typical of an innocuous pneumatosis, whereas linear gas collections have a more severe connotation (10). This does not always hold true, however, and the radiologic appearance is not a predictor of the severity of disease (Figs 8, 9). Radiologic appearances probably depend on the layer of the bowel wall involved.
November
1992
Others colon
(5,14).
Gas-
demonof ne-
have indicated that pneumatosis of is probably clinically insignificant Although this may be true, even pneuof the
small
bowel
and
of the
stomach
can have location
relatively benign causes. Thus, the of the pneumatosis may have no bearing on its clinical significance (Fig 10) (1,2, 14). Another general perception is that the greater the extent of pneumatosis, the more serious the disease. However, often, the extent of the pneumatosis is actually inversely related to the severity of the disease (14). That is, life-threatening conditions such as ischemia do not have a chance to form extensive
pneumatosis
compared
with
that
associ-
ated with less serious conditions (Fig 1 1). Free intraperitoneal air (gas) develops in pneumatosis whenever one of the subserosal collections of gas ruptures. This can occur with
pneumatosis
from
Feczko
any
condition
et a!
U
and
is
RadioGraphics
U
1075
F
a. Figure
1 1.
Abdominal
bowel
Extent
of pneumatosis
radiograph
shows
was infarcted,
asymptomatic
only
1076
U
RadioGraphics
demonstrates
free intrapenitoneal
U
a slight
and she subsequently
outpatient
Figure 12. Free intraperitoneal rupture of the cysts. (a) Abdominal scleroderma who presented with demonstrates
does
Feczko
et a!
not correlate amount
died. prominent
with
b. severity
of pneumatosis.
(b) Idiopathic small
bowel
b. air (gas) may be encountered radiograph shows extensive vague air.
abdominal
complaints
.
or clinical However,
pneumatosis.
cause. most
(a) Intestinal of the
Abdominal
patient’s
radiograph
ischemia. small
of an
pneumatosis.
with pneumatosis of any cause, secondary pneumatosis in an elderly woman with to the
emergency
room.
Volume
(b)
Chest
12
to
radiograph
Number
6
13L
13b.
14a.
14b.
Figures 13, 14. tion. Abdominal
Gas
in the
radiograph
portal
system
of an 84-year-old
does
not
woman
always
indicate
shows
marked
a grave
portal
prognosis.
venous
(13a)
gas and
Bowel
small
infarc-
bowel
The patient proved to have an infarcted bowel and subsequently died. (13b) Portal venous gas from vomiting. Abdominal radiograph of a patient with persistent vomiting shows gastric pneumatosis and portal venous gas. This spontaneously resolved in 1 day. (14) Postoperative pneumatosis and portal venous gas. (a) CT scan of an elderly man who developed abdominal distention several days after surgery shows marked pneumatosis of the small bowel. (b) CT scan through the liver demonstrates portal venous gas. The patient underwent exploratory laparotomy, with negative results. The pneumatosis resolved spontaneously, and the patient was discharged several days later. (Courtesy of Robert Halpert, MD, University of South Florida, Tampa.) pneumatosis.
often an ongoing process. These patients will have a persistent or ‘balanced’ pneumoperitoneum or perhaps some associated bloating, cramps, or pain. It is important for the radiologist to realize that pneumoperitoneum associated with pneumatosis does not indicate severe disease, even in the presence of some abdominal symptoms (Fig 12). Gas in the portal system can frequently be seen in necrotizing enterocolitis in infants or in bowel infarction in adults. Thus, this finding tends to carry a severe connotation to ‘
November
1992
‘
both the radiologist and clinician. In these diseases, it is associated with a high mortality. Over the past few years, there have been several reports ofgas in the portal vein in conditions with a benign pneumatosis (1 1 14). Although the surgical literature suggests that gas in the portal system is an indication for operation, this is not necessarily true (Figs 13, ,
14)(14).
Feczko
et a!
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5.
U CONCLUSION Although it is an infrequent finding, ologist will be the first to diagnose sis on ditions
the the
an
imaging
that
produce
innocuous radiologist
ditions
that
can
of specificity
ties
encountered.
1
.
Meyers Goodman trointest
3.
spectrum
pneumatosis
of conranges
from
produce
of the
pneumatosis
radiologic
and
7.
9.
nalis in systemic Semin Arthritis
10.
CaudillJL, tomography intestinalis. 226.
11
.
of pneumatoPathol 1985; 12.
16:683-688.
4.
6.
8.
Rectum 1986; 29:358-363. MA, Ghahremani GG, ClementsJL, K. Pneumatosis intestinalis. GasRadiol 1977; 2:91-105. AS, Leong AS, Rowland R. The mu-
Pieterse cosal changes and pathogenesis siscystoides intestinalis.Hum
\W, Madewell JE. Pneumatosis cystoides intestinalis: a pathophysiologic planation of the roentgenographic signs. trointestRadiol 1976; 1:177-181.
RJ, Goldstein intestinalis.
F. Pneumatosis In: BerkJE, ed,
cysBockus’
gastroenterology. 4th ed. Philadelphia: Saunders, 1985; 2474-2483. Doub HP, SheaJJ. Pneumatosis cystoides intestinalis. JAMA 1960; 172:1238-1242. Keyting WS, McCarver RR, KovarikJL, Daywitt AL. Pneumatosis intestinalis: a new concept. Radiology 1961; 76:733-741. Yale CE, Balish E, Wu JP. The bacterial etiology ofpneumatosis cystoides intestinalis. Arch Surg 1974; 109:89-94. Sequeira W. Pneumatosis cystoides intesti-
the
abnormali-
REFERENCES Galandiuk 5, Fazio \W. Pneumatosis cystoides intestinalis: a review of the literature. Dis Colon
2.
The
radi-
pneumato-
to the fatal. It is important that be aware of the variety of con-
lack
U
study.
the
Priest toides
Olmsted
13.
Rose BS. The role of computed in the evaluation of pneumatosis J Clin Gastroenterol 1987; 9:223-
Federle MP, Chun G, Jeffrey RB, Rayor R. Computed tomographic findings in bowel infarction. AJR 1984; 142:91-95. Lund EC, Han SY, Holley HC, Intestinal ischemia: comparison
diographic
exGas-
sclerosis and other diseases. Rheum 1990; 19:269-277.
and computed
tomographic
find-
ings. RadioGraphics 1988; 8:1083-1108. Vernacchia FS, Jeffrey RB, Laing FC, Wing
VW.
Sonographic
in-
recognition
testinalis. AJR 1985; 14.
Berland LC. of plain ra-
Knechtle
SJ, Davidoff
tosis intestinalis: clinical outcome.
of pneumatosis 145:51-52.
AM, Rice RP.
surgical
management
Pneumaand
Ann Surg
1990;
212:160-
Volume
12
Number
165.
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