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Risk Factors for Intestinal Gangrene in Children With Small-bowel Volvulus

Lin, Yu-Pi*; Lee, Jung*; Chao, Hsun-Chin*; Kong, Man-Shan*; Lai, Ming-Wei*; Chen, Chien-Chang*; Chen, Shih-Yen*; Luo, Chih-Cheng

Journal of Pediatric Gastroenterology & Nutrition: October 2011 - Volume 53 - Issue 4 - p 417–422
doi: 10.1097/MPG.0b013e3182201a7c
Original Articles: Gastroenterology

Objectives: Pediatric small-bowel volvulus (SBV) is a surgical emergency, and early diagnosis is difficult. We analyzed the clinical manifestations, imaging findings, and laboratory parameters in children with SBV and attempted to determine the risk factors for bowel gangrene.

Patients and Methods: Forty-nine children (35 boys and 14 girls) with SBV who were admitted to the hospital for a period of 13 years were enrolled. Clinical and laboratory parameters and evaluation measures included fever, abdominal pain, vomiting, bloody stool, peritoneal signs, severe dehydration, disease duration, white blood cell counts, sugar, C-reactive protein (CRP), sodium, potassium, metabolic acidosis, blood urea nitrogen, and creatinine. These parameters were statistically compared between patients with and without bowel gangrene.

Results: Thirty-six patients (73.5%) were 5 years old or younger, and nearly half were younger than 1 year old. Abdominal pain and vomiting were 2 major symptoms. Malrotation was the most common cause of SBV. In univariate analysis, nonbilious vomiting, peritoneal signs, severe dehydration, leukocytosis (WBC count >18,000 cells/mm3), elevated CRP (>50 mg/dL), and hyponatremia (<130 mmol/L) were significantly associated with bowel gangrene (P < 0.05). In multivariate analysis, nonbilious vomiting, leukocytosis, and elevated CRP were significantly (P < 0.05) associated with bowel gangrene. The resection rate for bowel gangrene was 44.9%, and no mortality was found. Seven (14.3%) patients had postoperative complications, including short-bowel syndrome (n = 2), adhesion ileus (n = 3), and intraabdominal abscess (n = 3). Seven experienced failure to thrive in later follow-up.

Conclusions: Specific clinical manifestations and laboratory parameters are helpful in the identification of bowel gangrene in children with SBV.

*Department of Pediatric Gastroenterology

Department of Pediatrics, Chang Gung Children's Medical Center, Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Taoyuan, Taiwan.

Address correspondence and reprint requests to Hsun-Chin Chao, MD, Division of Gastroenterology, Department of Pediatrics, Chang Gung Children's Medical Center, 5 Fu-Hsing St, Kuei-Shan, 33305, Taoyuan, Taiwan (e-mail:

Received 12 December, 2010

Accepted 17 April, 2011

The authors report no conflicts of interest.

Small-bowel volvulus (SBV) is a surgical emergency because of the risk of mesoaxial twisting of small-bowel loops, which results in bowel infarction from a compromised blood supply (1–3). SBV is the most common type of intestinal volvulus in children (4).

Pediatric SBV occurs rapidly and is difficult to diagnose. The morbidity and mortality rates rise in parallel with delays in diagnosis and treatment (5). Early diagnosis and treatment are necessary to avoid life-threatening complications and to achieve good outcomes (4,6). Despite the nature of this emergency, few studies have discussed the risk factors for bowel gangrene in children with SBV. Therefore, we retrospectively evaluated the clinical manifestations, image findings, and laboratory parameters in these children and attempted to determine the risk factors for bowel gangrene among patients, because understanding these may prevent further morbidity and mortality.

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Children younger than 15 years old with SBV who were admitted to Chang Gung Children's Hospital for a period of 13 years (September 1996–September 2009) were enrolled in the present study. The definitions of SBV and bowel gangrene were based on operative and pathological findings. The resources of patients and their personal details were evaluated from chart reviews. Clinical symptoms including fever, abdominal pain, vomiting (bilious or nonbilious), bloody stool, peritoneal signs, severe dehydration, and disease duration were reviewed. Laboratory parameters in the initial blood sampling including white blood cell (WBC) counts, sugar, C-reactive protein (CRP), sodium, potassium, metabolic acidosis, blood urea nitrogen (BUN), and creatinine also were evaluated. Radiological investigations consisted of plain abdomen x-ray, abdominal ultrasonography (US), upper gastrointestinal (UGI) series, lower gastrointestinal (LGI) series, and abdominal contrast-enhanced tomography (CT); these were conducted before patients agreed to the operation. Surgical findings, outcomes, complications, and mortality also were evaluated.

To determine the risk factors for bowel gangrene in SBV, the clinical records of these patients were carefully reviewed. For vital signs, fever was defined as a body temperature >38°C according to an ear thermometer; severe dehydration was defined as palpitation or hypotension according to the advanced paediatric life support guidelines and accepted fluid challenge. In laboratory studies, leukocytosis was recognized to be a WBC count of >18,000 cells per cubic millimetre; glucose elevation was defined as a blood sugar level >150 mg/dL; elevated CRP was recognized to be a value >50 mg/dL; and hyponatremia and hyperkalemia were defined as a blood sodium level of <130 mEq/L and a blood potassium level of >5.5 mEq/L, respectively. Metabolic acidosis also was evaluated when blood gas examination was performed.

For univariate analysis, χ2 test with Fisher exact test and Student t test were used to test the significance of categorical and numerical variables, respectively. For the assessment of risk factors of bowel gangrene in SBV, a multivariate logistic regression analysis was performed. Variables were kept in the final model if the P value was <0.05. We used a retrospective review to find reliable differences between gangrenous and viable small bowel. The study was approved by the institutional review board of the local institute (CGMH 99–2647B).

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A total of 49 children with SBV were reviewed for the present study, including 35 boys and 14 girls, with an average age of 22 months (range 1 day–14 years). Thirty-six (73.5%) were 5 years of age or younger, and 23 (46.9%) were <1 year of age. The etiologies of SBV were classified into 4 groups based on surgical findings: malrotation, adhesions or bands, idiopathic, and Meckel diverticulum with umbilicus connection. Boys predominated (71.4%) in our patients, with the exception of the Meckel diverticulum group. Malrotation (n = 22, 44.9%) was the most common cause of SBV, and adhesions or bands (n = 15, 30.6%) were the second most common causes (Table 1). Among the 22 malrotation patients, 15 (68.2%) were newborns (age 1 month or younger), and the incidence decreased with age; however, adhesions or bands occurred mostly in older children. Most adhesions followed previous abdominal surgery, but 4 of these cases were not associated with abdominal surgery. Idiopathic volvulus (n = 6) and Meckel diverticulum with umbilicus connection (n = 6) were the next most common causes of volvulus.

Most patients (n = 43, 87.8%) experienced emergency admission with various clinical presentations. Abdominal pain was a complaint in all of the patients older than 2 years (n = 22, 100%), followed by vomiting (n = 48, 98%), peritoneal signs (n = 21, 42.9%), and fever (n = 13, 26.5%) (Table 2). For vomiting, bilious and nonbilious types were each present in half of the patients.

All of the patients underwent plain abdominal radiography and most (n = 41, 83.7%) showed nonspecific features of small bowel obstruction, with either distended bowel loops or vanished distal bowel air. Five patients with previous operation histories accepted operations based on the ileus on abdominal radiography. Thirty-seven abdominal USs were arranged, which revealed bowel obstruction with ascites in 21 patients. Among the 22 malrotation patients, 18 underwent abdominal US. Thirteen showed typical sonographic features of malrotation, that is, reversal of the normal superior mesenteric artery and superior mesenteric vein relation, and all of the diagnoses were proven surgically. Five patients who were not diagnosed as having malrotation by US had bowel obstruction on US; 2 were newborns (younger than 1 week old), and 3 were older children (7, 8, and 12 years old).

Thirteen UGI series were arranged to evaluate the cause of ileus and 11 showed a typical corkscrew appearance of malrotation. The 2 negative examinations included 1 surgically proven malrotation and 1 vascular band. Eight LGI series detected 5 malrotations. Nine abdominal contrast-enhanced CTs revealed 7 bowel obstructions, 1 abdominal mass, and 1 pelvis abscess.

All of the patients in our study received hydration, prophylactic antibiotics, and nasogastric tube decompression as initial management. Treatment was by simple untwisting in patients with viable gut segments, enterolysis of adhesions, resection of bands, or resection of gangrenous segments and primary small-bowel anastomosis. The Ladd procedure was performed for all of the patients with malrotation. The bowel gangrene and total resection rate was 44.9% (22/49) (Table 2). Patients with bowel gangrene showed marked differences in leukocytosis, glucose, CRP, sodium, and BUN compared with the nongangrenous-bowel group (P < 0.05) (Table 3). Other biochemistry results, duration before operation, and hospital stay showed no significant differences between the 2 groups.

All of the patients in the idiopathic group (n = 6) and Meckel diverticulum group (n = 6) had bowel gangrene; both resection rates were 100% (Table 2). Only 4 patients in the malrotation group (n = 22) had bowel gangrene; the resection rate was 18.2%. In our study, 5 patients (22.7%) with bowel resection were infants, and 17 (77.3%) were older children. Eight had extensive small-bowel resection (117–267 cm), 4 had jejunum resection, and 10 had ileum resection. Only a patient had resection of ileocecal valve and proximal colon.

There was no mortality in our patients. The mean hospital stay was 17.55 ± 21.5 days. Outpatient department follow-up was noted in all of the patients, with duration ranging from 1 to 6 years. Complications included 3 patients with intraabdominal abscesses, 2 with short-bowel syndrome (1 patient, a 7-year-old, had resection of the small bowel 267 cm, 22 cm jejunum remaining; the other, a 6-year-old, had resection of small bowel 222 cm, ileocecal valve, ascending colon 27 cm, 75 cm jejunum remaining), 3 with adhesion ileus; the complication rate was 14.3% (n = 7) (Table 2). In addition, 7 patients (14.3%) had failure to thrive (weight fell to lower than the third percentile on growth charts) during the 6-month follow-up.

Risk factors were determined by comparing patients with and without bowel gangrene (Table 4). In univariate analysis, nonbilious vomiting, peritoneal signs, severe dehydration, leukocytosis (WBC count >18,000 cells/mm3), elevated CRP (>50 mg/L), and hyponatremia (Na <130 mEq/L) were significantly associated with bowel gangrene. Because nearly half of the cases of SBV were caused by malrotation and most (n = 17, 77.3%) (Table 2) presented with bilious vomiting, we further analyzed the risk of nonbilious vomiting for intestinal gangrene in patients with and without malrotation. The results showed that nonbilious vomiting tended to be associated with intestinal gangrene in patients with and without malrotation (Table 5); the association was stronger (P = 0.024) in malrotation. Six significant variables from the univariate analysis were entered into the logistic regression model. In the multivariate analysis, nonbilious vomiting, WBC count >18,000 cells/mm3, and CRP >50 mg/L were kept in the model to be significant predictors for bowel gangrene requiring resection in children with SBV (Table 6).

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Boys outnumbered girls, with an overall incidence of 71.4% in the present study, which is relatively lower than results found in Asian and African countries (75%–100%) (7–9), but is higher than those in US studies (46%–50%) (10,11). Boys especially predominated in the malrotation group (Table 1). Thirty-six patients (73.5%) were 5 years or younger, and 23 (46.9%) were infants (under 1 year old) in our series, unlike other reports, in which SBV children were commonly 1 to 5 years old (5) or were equally divided between those younger and older than 5 years old (12). The differences in age at presentation of SBV among studies are caused by differences in etiologies among different areas. In our series, SBV was classified into 4 etiologies; malrotation mainly occurred in infants, whereas other etiologies mainly occurred in other age groups.

The most common etiology for SBV was malrotation in our series, whereas idiopathic etiologies (13–16) or worm mass (5) were the most common etiologies in previous studies. In our study, 50% of patients with malrotation presented within the first week of life, and 68% presented within the first month. A previous study reported an incidence of midgut volvulus in symptomatic malrotation of 42.1% in the neonatal period and 50% beyond the neonatal period (17). Although midgut malrotation was the most common cause of SBV in our patients, the incidence of bowel gangrene was relatively low (18.2%) compared with other studies. The incidence of bowel gangrene with malrotation in other reports was evaluated and was found to range from 2.9% to 48% (13,15,18,19). Adhesions and bands were the second most common causes of volvulus (n = 15, 30.6%) in our study; the present result is similar to findings of 23% to 32% in previous reports (5,12). Nearly three-quarters (11/15, 73.3%) of our patients had experienced previous intraabdominal surgery compared with other reports ranging between 0% and 50% (5,12). Our results demonstrate that idiopathic and Meckel diverticulum incidences were low (n = 6, 12.2%, individually), but all of the patients required bowel resection. The incidence of idiopathic volvulus in the present study was similar to that in Western countries (10%–20%) (10,11,20,21), although this result was lower than that reported in certain parts of Africa, Asia, and the Middle East (31%–100%) (1,7–9,21,22). Meckel diverticulum, which is connected to the umbilicus by a fiber band, was a fulcrum around which the small bowel rotated (23,24). Intestinal obstruction is an uncommon complication of Meckel diverticulum and is reported in 14% to 53% of cases (21,25).

The degree of abdominal pain increased as bowel gangrene progressed (21,25). In our series, abdominal pain and vomiting were the hallmark expressions of SBV. Bilious vomiting was present in half of the patients, especially in infants. Previous investigations have indicated that vomiting, abdominal distension, shock, dehydration, and peritonitis are common clinical features in SBV (5,12). Peritoneal signs with muscle guarding were present in 42.9% of our patients, which is much lower than the 74% found in another report (5). The incidence of severe dehydration was also lower than in other reports (22.4% vs 88%) (5).

Bowel wall edema and increasing intraluminal pressure compromise perfusion to intestine segments (26). Necrosis ensues; concomitant fever, leukocytosis, and metabolic acidosis can result if the bowel becomes ischemic owing to hypoperfusion of the gut and other tissues. The stress response to critical illness may result in hyperglycemia and tissue infarction; SBV induces severe hypoperfusion and inflammation, leading to significant leukocytosis and elevated CRP, BUN, and creatinine. In our study, leukocytosis, elevated CRP, elevated sugar, elevated BUN, and hyponatremia were associated with bowel gangrene (P < 0.05); fever (ear temperature >38°C) was nearly significant (P = 0.054) in our study, possibly because of our limited case numbers.

Only a few reports have mentioned the risk factors in children with SBV. In adults, no single diagnostic clinical sign identified the presence of infarcted bowel (27), and no single hematological test was found to reliably differentiate gangrenous from viable small bowel (28,29). A WBC level >18,000 cells/mm3 was correlated with the presence of gangrenous bowel (30,31). Mucha showed 55% hyperamylasemia and abnormal serum lactate levels in 86% of patients with gangrenous small bowel, in contrast to 5% and 4%, respectively, in those with other causes of small bowel obstruction (32). Metabolic acidosis was present in 75% of those with strangulated bowel. In adult reports, 90% of those with bowel obstruction with gangrenous small bowel had a combination of fever, tachycardia, and peritoneal irritation (33). Bowel strangulation and gangrene of the obstructed bowel segment must be considered in patients with signs and symptoms of intestinal obstruction with continuous, severe abdominal pain, peritoneal irritation, and leukocytosis (6).

Our results indicate that leukocytosis (WBC count >18,000 cells/mm3) and CRP elevation (>50 mg/L) are helpful in the identification of bowel gangrene in children with SBV. In animal studies, CRP levels increase with the severity of bacterial translocation in acute intestinal obstruction (34). CRP is also used as a marker of intestinal ischemia, although CRP levels do not permit discrimination between simple and strangulated intestinal obstruction (34). Bilious vomiting is a useful sign to detect small-bowel obstruction, but it is not a specific parameter for bowel gangrene according to our results.

Abdominal radiography is usually the initial investigation performed, and it usually shows nonspecific features of small-bowel obstruction. US was used to diagnose or screen for malrotation in the present study, and the typical whirlpool sign on US has been shown to be specific for midgut volvulus caused by malrotation; however, a normal US finding cannot exclude malrotation (35,36). Approximately 2% to 3% of patients still may have malrotation (37–40). According to a previous report, malrotation has obvious signs, and 85% of the time it can be detected on a UGI series, which remains the gold standard for diagnosing malrotation (41). In our study, the UGI series detected 11 (91.7%) of 12 malrotations. It showed malposition of the duodenal-jejunal junction to the right side of the spine, with dilatation of the proximal duodenum and corkscrew-like deformity of the duodenum. LGI series are preferred in patients with multiple dilated loops of bowel, in whom distal bowel obstruction is suspected (4). It facilitates the diagnosis of SBV if the LGI series shows LGI tract obstruction, particularly if the head of the barium column has a beaked appearance (4). In our study, the LGI series detected 5 (83.3%) of 6 malrotations.

The present study indicates that US and GI series were helpful to diagnose malrotation and bowel obstruction, but not intestinal gangrene, in SBV. The performance of GI series (especially UGI series) is not appropriate in patients with emergency status because of its potential complications, for example, aggravated abdominal symptoms, influence of vital signs, or bowel perforation. Although CT or magnetic resonance imaging scanning may show diagnostic features and highlight potential small-bowel ischemia (42,43), our study found the diagnostic value of CT studies to be limited. In our study, only 9 patients arranged CT studies, and in only 1 patient who was diagnosed as having small-bowel obstruction could we rule out volvulus with impending ischemia. Bowel wall thickening and high attenuation of the bowel wall are the most important signs of ischemia on unenhanced CT scans, whereas abnormal bowel wall enhancement and mesenteric fluid appear best on enhanced CT scans (44). CT angiography with 3-dimensional reconstruction is reportedly a diagnostic tool in acute intestinal ischemia (45). Duplex and color Doppler flow US are helpful in the differentiation between ischemia and inflammatory bowel wall thickening (46,47), but the diagnostic accuracy of duplex US is often restricted by air-filled bowels (45). In our hospital, we did not routinely use color Doppler flow US for patients; therefore, we could not confirm its diagnostic value.

In the present study, the bowel resection rate for gangrenous bowels was 44.9%, compared with previous studies reporting rates of 21% to 61% (5,12,13,15). The obvious risk of resectional surgery is the development of short-bowel syndrome, which arises from a substantial loss of small-bowel length (28). In our study, short-bowel syndrome, adhesion, intraabdominal abscess, and failure to thrive were the major complications. The rate of intraabdominal abscess (n = 3, 6.1%) was relatively lower than that in a previous report (36%) (12). Failure to thrive was the major long-term complication in our patients. In previous studies, the mortality rate ranged from a low of 2.9% to a high of 50% (18,19). There was no mortality in our series; all of our patients had preoperative corrections of volume deficiencies and electrolyte imbalances, as well as administration of broad-spectrum antibiotics. The outcome of our series is relatively good in comparison with previous experiences; we consider that such a difference is based on a large number of patients with malrotation associated with a noncomplicated midgut volvulus. Intensive preoperative corrections of volume and electrolyte deficits and administration of broad-spectrum antibiotics give patients the best chance of survival (12). Obviously, early arrival, early diagnosis, and active supportive treatment including intensive care, ventilatory support, and total parenteral nutrition followed by definitive treatment are the keys to minimizing morbidity and mortality (5). Septicemia, shock, and multiorgan failure are risk factors for mortality (5). In our series, 11 patients had severe dehydration with shock or impending shock (Table 2), but there was no mortality. Preoperative preparation decreased the mortality rate, but not the bowel resection rate (n = 22, 44.9%) in our patients.

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In conclusion, leukocytosis (WBC count >18,000 cells/mm3) and CRP elevation (>50 mg/L) are helpful in the identification of bowel gangrene in children with SBV. Bilious vomiting is a useful sign to detect small-bowel obstruction, but it is not a specific parameter for bowel gangrene. When intestinal obstruction is suspected on presentation, combined with WBC levels of >18,000 cells/mm3 and CRP levels of >50 mg/L, bowel gangrene should be considered and treated promptly.

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bowel resection; children; intestinal gangrene; small-bowel volvulus

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