Postoperative pneumatosis intestinalis (PI) and portal venous gas (PVG) may indicate bowel necrosis: a 52-case study

PI is the presence of gas within the submucosa or subserosa of the intestine. A previous study found that the mean age of PI patients is 56.6 ± 19.4 years and that 57 % of patients were male [8]. PI is a rare disease and is still poorly understood. Four main theories exist, positing that PI is caused by: (1) increased intraluminal pressure derived from intestinal obstruction, colonoscopy, or gastroenteric tumor (mechanical theory); (2) pulmonary alveolar rupture resulting from pulmonary diseases, such as chronic obstructive pulmonary disease or asthma (pulmonary theory); (3) gas produced by gas-forming bacteria that enter the mucosal barrier (bacterial theory); or (4) α-glucosidase inhibitors (chemical theory) [9]. However, each theory alone also fails to account for the cause of PI [2, 3].

PVG is the presence of air in the portal venous system. The mechanism for the appearance of gas in the portal vein is also not well understood. There are two major theories: (1) gas dissects into the intestinal wall from the intestinal lumen, or lung and intestinal mucosal damage allows intraluminal gas to enter the venous system (Mechanical theory); and (2) gas-forming bacteria enter the mucosal barrier and produce gas within the intestinal wall, which then enters into the portal vein system (bacterial theory) [4, 10].

Previous reports have suggested that PI and PVG usually originate from bowel necrosis, via similar mechanisms, and are often detected concomitantly in clinical situations. However, PI and PVG have been studied and treated as independent symptoms in many publications. In the current report, we treated patients with PI and/or PVG as having one condition [5].

PI was previously thought to predict poor outcomes due to the development of bowel necrosis, but DuBose et al. evaluated 500 patients with PI and reported that it was not necessarily associated with bowel necrosis [8]. Similarly, PVG was also thought to be indicative of a poor prognosis due to the development of bowel necrosis. This is supported by the findings of Kinoshita et al., who reported that the overall mortality rate for patients with PVG was 39 %, increasing to 75 % in patients with bowel necrosis and only 11.7 % in patients without necrosis [4]. Furthermore, 97 % of PVG cases were reported to be related to bowel necrosis [11]. In recent years, the widespread use of CT has enabled increased detection of PI/PVG, showing that these clinical signs are not always predictive of a poor outcome. However, this is because bowel necrosis is not always found in some patients with PI and/or PVG. The increased sensitivity of CT scans has increased the detection of PI and PVG, increasing the difficulty of determining whether or not a patient with PI/PVG has bowel necrosis. Some authors have reported the development of therapeutic algorithms for treating PI/PVG [5, 12], but the wide variety of potential clinical features makes the development of an algorithm that is applicable to all patients with PI/PVG difficult.

Some clinical findings have also been suggested to predict bowel necrosis in patients with PI/PVG. Some reports suggested that bowel necrosis was associated with the distribution of PVG and bowel gas morphology, though conflicting reports have made this suggestion controversial [7, 13‐15]. Bowel necrosis could not be predicted from the distribution or extent of PVG/PI. The distribution of PVG was entirely unrelated to bowel necrosis, whereas linear PI had a nonsignificant association with bowel necrosis. Patient characteristics and past medical histories have been reported to influence the occurrence of PI/PVG [15, 16], but we found no such relationship. Many laboratory tests have also been reported to be useful for the diagnosis of PI/PVG. Some reports have suggested that blood lactate levels and acidosis, indicators of tissue necrosis, are predictive of outcomes [8, 17, 18]. Our univariate analysis showed that elevated levels of lactate, C-reactive protein, and creatinine were significantly associated with bowel necrosis. These laboratory parameters are related to tissue necrosis, inflammation, and dehydration, suggesting that our findings are reasonable. Furthermore, abdominal physical examination findings are important predictors of bowel necrosis. In particular, signs of peritoneal irritation have been thought to be useful for diagnosing peritonitis due to bowel necrosis [19]. Our study supported this contention, suggesting that both abdominal pain and signs of peritoneal irritation predict bowel necrosis. However, the assessment of physical findings is physician-dependent, making an objective or numerical expression of such findings difficult. Several scoring systems that evaluate patient condition severity have been put forth as useful prognostic indicators for patients with bowel necrosis [20, 21]. In this study, the SIRS, APACHE II, and SOFA scores were used to assess severity. All three scores were related to bowel necrosis, indicating that these scores can be useful for evaluating patients undergoing surgery or conservative treatment. Recently, procalcitonin and presepsin may indicate useful prognostic information for patients with severe sepsis or septic shock. These parameters are expected to be useful for evaluating the severity of patients’ condition in the future [22].

PI/PVG is more likely to indicate bowel necrosis in postoperative patients than in patients who have not had surgery. There are several reasons that postoperative PI/PVG may be an indicator of bowel necrosis. First, the proliferation of intestinal bacteria and the production of gas in the bowel increase the intraluminal pressure, particularly in patients with postoperative ileus; this may lead to bowel ischemia and PI/PVG. Second, inflammatory cytokines increase vascular permeability, and the resulting intravascular dehydration may cause bowel ischemia [23]. In our study, the decrease in intravascular fluid, secondary to severe operative stress and perioperative catecholamine use, may have caused bowel ischemia in patients who underwent highly invasive surgeries, such as esophagectomies or pancreaticoduodenectomies. Third, the intestine can be damaged during abdominal surgery, and suture failure sometimes occurs after bowel resection and anastomosis. If there is massive leakage of bowel contents into the abdominal cavity, re-operation may be required due to bowel necrosis or peritonitis. Moreover, vasoconstrictors or vasopressors (e.g., catecholamines) are used if the patient’s blood pressure is unstable. Although vasoconstrictors increase blood pressure, they may also compromise blood flow to the peripheral intestinal vessels. Excessive vasoconstriction or repeated alternation of vasoconstriction and vasodilatation may also induce mesenteric artery spasms, causing ischemic enteritis or NOMI [24, 25]. Diagnosis of PI/PVG in postoperative patients is thus a simple indicator of potential bowel necrosis and may be useful for determining treatment.

In many cases, PI or PVG occurs in patients who have not undergone surgery, and it appears to resolve spontaneously in many of these patients. This is because PI or PVG can occur due to transient and reversible intestinal ischemia under certain conditions. For example, gas-forming bacteria can enter the mucosal barrier, through mucosal rents or increased mucosal permeability, and produce gas within the bowel wall; alternatively, the intestinal wall may be injured, or increased intraluminal pressure may serve as the driving force in PI that causes the intramural gas, due to conditions such as intestinal obstruction, inflammatory bowel disease, bowel preparation, or colonoscopy.

Our study had several limitations, including being a retrospective, single-center investigation involving a small sample size. The PI/PVG and bowel ischemia diagnoses were dependent upon the subjective judgment of the attending physicians, leading to potential selection bias. Furthermore, this study did not evaluate patients with bowel necrosis who did not have PI and/or PVG, so the association between PI/PVG and bowel necrosis cannot be fully assessed. The pathogenesis and clinical significance of PI/PVG should thus be further investigated in future multicenter prospective studies.