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:

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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

Volume

12

Number

6

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

RadioGraphics

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

1072

U

RadioGraphics

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

RadioGraphics

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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Feczko

et a!

Volume

12

Number

6

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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1077

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

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of pneumatosis 145:51-52.

AM, Rice RP.

surgical

management

Pneumaand

Ann Surg

1990;

212:160-

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12

Number

165.

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Clinical significance of pneumatosis of the bowel wall.

The presence of gas within the bowel wall is an uncommon condition that is typically first diagnosed by the radiologist. Although it is often seen on ...
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