Pediatr Radiol (1992) 22:120-122
Pediatric Radiology 9 Springer-Verlag 1992
Recurrent pneumatosis intestinalis in young infants V. H. Chabot 1, Th. L. Slovis 1, and M. Cullen 2 1Department of Radiology 2Department of Surgery, Children's Hospital of Michigan, Wayne State University School of Medicine, Detroit, Michigan, USA Received: 7 November 1991; accepted: 5 December 1991
Abstract. In 67 infants with necrotizing enterocolitis (NEC) at Children's Hospital of Michigan from 19871990, three had recurrent pneumatosis intestinalis (PI) after the neonatal period and after hospital discharge. All three infants were p r e m a t u r e (26-34 weeks), and one had an additional risk factor of gastroschisis. All three had their initial episode of N E C within the first month of life. Two had bowel resections, and one was treated medically. 15 h to seven months after discharge from the hospital, all three infants developed recurrent PI at ages ranging from 2.5 to 9 months. Two of the infants had free intraperitoneal air. Though all three infants had PI, only one had true recurrent N E C with ischemic bowel and died. This baby was the only one with rotazyme positive stools. The second infant, who had surgery for gastroschisis, had incomplete obstruction secondary to adhesions resulting in PI. Since surgery this infant has thrived. The third infant had extensive PI of the colon with free air. At surgery there was no evidence of bowel perforation. The free air was attributed to rupture of one of the m a n y colonic cysts of PI. Subsequently, the child has done well. Recurrent PI in infants who have had N E C is unusual and the causes are varied. Because m o r e neonates are surviving NEC, the pediatric radiologist needs to be aware of this delayed complication.
Pneumatosis intestinalis (PI) is defined as intestinal emphysema and is characterized by gas cysts in the intestinal wall [1]. In the neonate, pneumatosis intestinalis has almost become pathognomonic for necrotizing enterocolitis (NEC) [2]. N E C effects 1 - 2 % of admission to neonatal intensive care facilities and is most often associated with p r e m a t u r e or low birth weight infants who have experienced some form of perinatal stress [3]. It is usually diagnosed within the first month of life [4-6]. The patient presents with abdominal distention (85-98 %) and tenderness (61-76%), blood in the stool (48-53%), peritonitis, and retention of feeding associated with bowel distention and occasionally perforation [3]. Radiographic confirmation of clinical N E C requires the presence of bowel distention and pneumatosis intestinalis (67-86 %) [3]. There may also be associated portal venous gas (2235 % ) and free intraperitoneal air (41-46 %) [3]. The etiology of N E C is multifactorial and such causes as early formula feeding, mesenteric ischemia and bowel pathogens (bacterial and viral) have been discussed in the literature. Other reported etiologies include intestinal
mucosal immaturity, decreased humoral maturity with diminished I g A in the lamina propria, and in association with maternal cocaine addiction [7]. Once injury to the bowel mucosa has taken place, release of cytotoxic free radical anions, cytokines, and platelel-activating factor may all potentiate the mucosal insult [8, 9]. N E C in term and older infants is unusual and is most often secondary to persistent diarrhea or diminished blood flow to the gastrointestinal tract secondary to cardiac disease [10,11]. Recently an association of N E C following repair of gastroschisis has been reported (18.5 % of gastroschisis) [5, 11]. The gastrochisis group was distinctive because N E C developed significantly later than expected. In both p r e m a t u r e and full term infants, the prognosis of N E C has improved since 1970 (from 58 % to 82 % survival) because of earlier recognition, changes in feeding regimens, hyperalimentation, and improved antibiotic therapy [3]. Since m o r e children are surviving N E C and leaving the hospital, recurrent pneumatosis intestinalis m a y occur more often in the older infant. At Children's Hospital of Michigan (CHM), 3 cases of recurrent delayed PI have been recorded over the last 3 years.
Methods, materials, results A chart review was conducted at CHM of cases of NEC between 1987 to 1990. Sixty-seven cases of NEC were evaluated in children less than one year of age. Of the 67 children, six were full term and the remaining 61 were premature. Among the 67 cases, 54 survived (80 %) and of these children, three were determined to have recurrent PI beyond the neonatal period and after hospital discharge. Case I (Fig. 1). A 34-week-gestation female neonate was transferred to CHM 11 days after birth because of abdominal distention, acidosis and decreased urine output. The patient's blood pressure was 65 systolic by palpation on admission. Radiographically the patient presented with pneumatosis intestinalis, portal venous gas and pn eumoperitoneum. Upon admission the patient was taken to surgery and an ileocolectomy and ileostomy were performed. Over the next two months the patient appeared septic and had multiple septic workups, but only one stool culture was positive for rotavirus. After closure of the ileostomy the patient began tolerating feedings and had normal stools, leading to discharge at three months of age. Fifteen hours after discharge the patient returned to the hospital with severe diarrhea, vomiting and peritonitis. Abdominal x-rays revealed diffuse pneumatosis intestinalis and portal venous air (Fig. 1). Exploratory laparotomy revealed an almost totally ischemic bowel and adhesions. Lysis of adhesions was performed and although bowel perfusion improved, five days after exploratory laparotomy, the patient again decompensated and expired. Case 2 (Fig. 2). A 31-week-gestation male infant was transferred to
CHM at one day of age with a history of meconium stained amniotic
Fig.la-e. Case 1. Initial episode a Frontal radiograph of the abdomen at 11 days of age reveal distention without obstruction and pneumatosis intestinalis
(arrow) b The lateral decubitus film shows the portal venous gas (arrow) c Frontal film at almost 3 months of age and 15 h after discharge shows distension and pneumatosis intestinalis (arrow) Fig.2a-c. Case 2 a Supine radiograph at 3 weeks of age reveals pneumatosis intestinalis as well as free air b Supine radiograph at 2z/2 months of age reveals distension with pneumatosis. This pattern suggests obstruction c Erect lateral chest radiograph shows small amount of free air anteriorly (arrow) Fig.3a, b. Case 3 a At 9 months of age this erect abdominal film reveals multiple areas of pneumatosis intestinalis and free air below the left hemidiaphragm b On the supine film the extensive colonic pneumatosis is seen as encircling the bowel
122 fluid and gastroschisis. The infant became apneic and was intubated. At six days of age, the first stage of abdominal wall closure was performed. Six days later, the procedure was completed. Post operatively the patient developed bloody stools and abdominal bloating. Clinical assessment suggested NEC, however, PI was never documented radiologically. The patient was discharged at five weeks of age after tolerating feedings well and gaining weight. Five days after discharge the patient was readmitted with vomiting, and marked PI, free air, and small bowel obstruction was suggested on abdominal radiographs. After antibiotic therapy the patient improved and was discharged. At 21/2months of age, approximately one week after discharge, the patient was readmitted with bright red blood per rectum. X-rays revealed the small bowel to be slightly dilated and the presence of PI (Fig. 2). He was treated for three weeks without improvement. Subsequent surgery revealed adhesions with one loop of bowel twisted 180 ~ and fixed to the abdominal wall. Following surgery the patient recovered nicely and remains healthy. Case 3 (Fig. 3). A 27-week-premature male infant was transferred to CHM at 25 days of age because of abdominal distention, jaundice and an episode of apnea. On admission to CHM the patient had a distended abdomen and diffuse peritonitis. Radiographically there was PI, portal venous gas and free intraperitoneal air (Fig. 3). On the day of admission the patient was taken to surgery and the distal half of the small bowel was removed. A jejunostomy was performed. The pathologic specimens revealed pneumatosis intestinalis. A stoma closure was performed at one month, 20 days. The patient was discharged at two months of age. He was admitted for 4 days for viral croup at 6 months of age. He again returned to CHM at 9 months of age with persistent vomiting, watery diarrhea and lethargy. The abdominal radiographs demonstrated pneumatosis intestinalis and pneumoperitoneum (Fig.3). Exploratory laparotomy revealed extensive colonic pneumatosis intestinalis with no evidence of perforation. All cultures were negative and the etiology of the patient's recurrent PI was never discovered, although it was hypothesized that one of the larger cysts perforated, leading to free intraperitoneal air.
Discussion It is i m p o r t a n t to separate PI (a radiographic description of air in the bowel wall) f r o m N E C - a full-blown disease with signs, s y m p t o m s and radiographic manifestations. These three cases all d e m o n s t r a t e P I f r o m varied causes N E C , obstruction, and an idiopathic etiology. It appears that the unifying factors of these three cases are the presence of PI, the older age of the patients, and their outpatient status. In fact, several factors present in our patients m a y have predisposed t h e m to the delayed onset of PI. O n e of our patients had r o t a z y m e positive stools. Capitanio and G r e e n b e r g recently r e p o r t e d two full t e r m infants (4 and 6 m o n t h s of age) with r o t a z y m e positive stools w h o p r e s e n t e d with an acute onset of vomiting and diarrhea [12-14]. B o t h of these patients were treated conservatively with medical support and recovered. West et al. had eight patients with r o t a z y m e positive stools w h o p r e s e n t e d with P I b e y o n d the n e o n a t a l period [4]. T h e s e eight patients all had the short bowel s y n d r o m e and three had gastroschisis. O u r second patient had b e e n o p e r a t e d on for gastroschisis. A m o u r y et al. and O l d h a m et al. have recently rep o r t e d a series of patients with gastroschisis w h o had delayed onset of PI [5,11]. In fact in Oldham's series, 18.5 % of his patients had PI and all of these infants had full-blown N E C . T h e reason for P I and N E C in these patients is unclear a n d p r o b a b l y m u l t i f a c t o r i a l , b u t stasis and obstruction must play a role. In our patient, an element of obstruction (incomplete) was clearly a predisposing factor.
Radiologic evaluation of these children with delayed PI does not provide significant differentiation from those patients w h o had PI at the usual time. All patients had PI, portal venous gas, and free air at their first episode. T h e second time patient 1 had PI and portal venous gas without free air, while patient 2 and 3 had PI and free air. Distention was present during all these episodes in each patient, and w h e n c o m p a r e d to a group of children with the classic description of P I - N E C , there was no radiologic differentiation. T h e r e seems to be m o r e and m o r e predisposing factors to PI - gastroschisis, rotavirus, and p r o l o n g e d survival. With better survival of infants with N E C the incidence of recurrent P I will be increasing. In addition, children w h o have rotavirus (some without prior N E C ) m a y have a significantly increased incidence of PI. In contrast to n e o n a t e s with PI, the older infant with recurrent P I needs to be evaluated for multiple s e c o n d a r y causes and N E C is only one of these etiologies.
References 1. DuVernoi JK (1783) Anatomische Beobachtungen der unter der ~iusseren und Haut der Gedaerme eingeschlossenen Luft. Phys Med Abhandl Acad Wissensch Petersb 2:182 2. Touloukian RJ, Berdon WE, Amoury RA, Santulli TV (1967) Surgical experience with necrotizing enterocolitis in the infant. J Pediatr Surg 2:389 3. Grosfeld JL, Cheu H, Schlatter M, West KW, Rescorla FJ (1991) Changing trends in necortizing enterocolitis. Ann Surg 214:300 4. West KW, Rescorla F J, Grosfeld JL, Vane DW (1989) Pneumatosis intestinalis in children beyond the neonatal period. J Pediatr Surg 24:818 5. Amoury RA, Godwin CD, McGill CW, Smith TH, Aschcraft KW, Holder TM (1980) Necrotizing enterocolitis following operation in the neonatal period. J Pediatr Surg 15:1 6. Kliegman RM, Fanaroff AA (1984) Necrotizing enterocolitis. N Engl J Med 310:1093 7. Kliegman RM (1990) Neonatal necrotizing enterocolitis: bridging the basic science with the clinical disease. J Pediatr 117:833 8. Sun XM, Hsueh W (1988) Bowel necrosis induced by tumor necrosis factor in rats is mediated by platelet activating factor. J Clin Invest 81:1328 9. Caplan MS, Sun XM, Hsueh W, Hageman JR (1990) Role of platelet activating factor and tumor necrosis factor-alpha in neonatal necrotizing enterocolitis. J Pediatr 116:960 10. Polin RA, Pollack R Barlow B, Wigger HJ, Slovis TL, Santulli TV, Heird WC (1976) Necrotizing enterocolitis in term infants. J Pediatr 89:460 11. Moss TJ, Adler R (1982) Necrotizing enterocolitis in older infants, children and adolescents. J Pediatr 100:764 12. Oldham KT, Coran AG, Drongowski RA, Baker P J, Wesley JR, Polley TZ Jr (1988) The development of necrotizing enterocolitis following repair of gastroschisis: a surprisingly high incidence. J Pediatr Surg 23:945 13. Capitanio MA, Greenberg SB (1991) Pneumatosis intestinalis in two infants with rotavirus gastroenteritis. Pediatr Radio121: 361 14. Rotbart HA, Nelson WL, Golde MR Triffon TC, Kogut SJH, Yolken RH, Hernandez JA, Levin MJ (1988) Neonatal rotavirus-associated necrotizing enterocolitis: case control study and prospective surveillance during an outbreak. J Pediatr 112:87 15. Mogilner B (1983) Necrotizing enterocolitis associated with rotavirus infection. Israel J Med Sci 19:894
T. L. Slovis, MD Department of Radiology Children's Hospital of Michigan 3901 Beaubien Boulevard Detroit, Michigan 48201, USA
Pediatric Radiology 9 Springer-Verlag 1992
Recurrent pneumatosis intestinalis in young infants V. H. Chabot 1, Th. L. Slovis 1, and M. Cullen 2 1Department of Radiology 2Department of Surgery, Children's Hospital of Michigan, Wayne State University School of Medicine, Detroit, Michigan, USA Received: 7 November 1991; accepted: 5 December 1991
Abstract. In 67 infants with necrotizing enterocolitis (NEC) at Children's Hospital of Michigan from 19871990, three had recurrent pneumatosis intestinalis (PI) after the neonatal period and after hospital discharge. All three infants were p r e m a t u r e (26-34 weeks), and one had an additional risk factor of gastroschisis. All three had their initial episode of N E C within the first month of life. Two had bowel resections, and one was treated medically. 15 h to seven months after discharge from the hospital, all three infants developed recurrent PI at ages ranging from 2.5 to 9 months. Two of the infants had free intraperitoneal air. Though all three infants had PI, only one had true recurrent N E C with ischemic bowel and died. This baby was the only one with rotazyme positive stools. The second infant, who had surgery for gastroschisis, had incomplete obstruction secondary to adhesions resulting in PI. Since surgery this infant has thrived. The third infant had extensive PI of the colon with free air. At surgery there was no evidence of bowel perforation. The free air was attributed to rupture of one of the m a n y colonic cysts of PI. Subsequently, the child has done well. Recurrent PI in infants who have had N E C is unusual and the causes are varied. Because m o r e neonates are surviving NEC, the pediatric radiologist needs to be aware of this delayed complication.
Pneumatosis intestinalis (PI) is defined as intestinal emphysema and is characterized by gas cysts in the intestinal wall [1]. In the neonate, pneumatosis intestinalis has almost become pathognomonic for necrotizing enterocolitis (NEC) [2]. N E C effects 1 - 2 % of admission to neonatal intensive care facilities and is most often associated with p r e m a t u r e or low birth weight infants who have experienced some form of perinatal stress [3]. It is usually diagnosed within the first month of life [4-6]. The patient presents with abdominal distention (85-98 %) and tenderness (61-76%), blood in the stool (48-53%), peritonitis, and retention of feeding associated with bowel distention and occasionally perforation [3]. Radiographic confirmation of clinical N E C requires the presence of bowel distention and pneumatosis intestinalis (67-86 %) [3]. There may also be associated portal venous gas (2235 % ) and free intraperitoneal air (41-46 %) [3]. The etiology of N E C is multifactorial and such causes as early formula feeding, mesenteric ischemia and bowel pathogens (bacterial and viral) have been discussed in the literature. Other reported etiologies include intestinal
mucosal immaturity, decreased humoral maturity with diminished I g A in the lamina propria, and in association with maternal cocaine addiction [7]. Once injury to the bowel mucosa has taken place, release of cytotoxic free radical anions, cytokines, and platelel-activating factor may all potentiate the mucosal insult [8, 9]. N E C in term and older infants is unusual and is most often secondary to persistent diarrhea or diminished blood flow to the gastrointestinal tract secondary to cardiac disease [10,11]. Recently an association of N E C following repair of gastroschisis has been reported (18.5 % of gastroschisis) [5, 11]. The gastrochisis group was distinctive because N E C developed significantly later than expected. In both p r e m a t u r e and full term infants, the prognosis of N E C has improved since 1970 (from 58 % to 82 % survival) because of earlier recognition, changes in feeding regimens, hyperalimentation, and improved antibiotic therapy [3]. Since m o r e children are surviving N E C and leaving the hospital, recurrent pneumatosis intestinalis m a y occur more often in the older infant. At Children's Hospital of Michigan (CHM), 3 cases of recurrent delayed PI have been recorded over the last 3 years.
Methods, materials, results A chart review was conducted at CHM of cases of NEC between 1987 to 1990. Sixty-seven cases of NEC were evaluated in children less than one year of age. Of the 67 children, six were full term and the remaining 61 were premature. Among the 67 cases, 54 survived (80 %) and of these children, three were determined to have recurrent PI beyond the neonatal period and after hospital discharge. Case I (Fig. 1). A 34-week-gestation female neonate was transferred to CHM 11 days after birth because of abdominal distention, acidosis and decreased urine output. The patient's blood pressure was 65 systolic by palpation on admission. Radiographically the patient presented with pneumatosis intestinalis, portal venous gas and pn eumoperitoneum. Upon admission the patient was taken to surgery and an ileocolectomy and ileostomy were performed. Over the next two months the patient appeared septic and had multiple septic workups, but only one stool culture was positive for rotavirus. After closure of the ileostomy the patient began tolerating feedings and had normal stools, leading to discharge at three months of age. Fifteen hours after discharge the patient returned to the hospital with severe diarrhea, vomiting and peritonitis. Abdominal x-rays revealed diffuse pneumatosis intestinalis and portal venous air (Fig. 1). Exploratory laparotomy revealed an almost totally ischemic bowel and adhesions. Lysis of adhesions was performed and although bowel perfusion improved, five days after exploratory laparotomy, the patient again decompensated and expired. Case 2 (Fig. 2). A 31-week-gestation male infant was transferred to
CHM at one day of age with a history of meconium stained amniotic
Fig.la-e. Case 1. Initial episode a Frontal radiograph of the abdomen at 11 days of age reveal distention without obstruction and pneumatosis intestinalis
(arrow) b The lateral decubitus film shows the portal venous gas (arrow) c Frontal film at almost 3 months of age and 15 h after discharge shows distension and pneumatosis intestinalis (arrow) Fig.2a-c. Case 2 a Supine radiograph at 3 weeks of age reveals pneumatosis intestinalis as well as free air b Supine radiograph at 2z/2 months of age reveals distension with pneumatosis. This pattern suggests obstruction c Erect lateral chest radiograph shows small amount of free air anteriorly (arrow) Fig.3a, b. Case 3 a At 9 months of age this erect abdominal film reveals multiple areas of pneumatosis intestinalis and free air below the left hemidiaphragm b On the supine film the extensive colonic pneumatosis is seen as encircling the bowel
122 fluid and gastroschisis. The infant became apneic and was intubated. At six days of age, the first stage of abdominal wall closure was performed. Six days later, the procedure was completed. Post operatively the patient developed bloody stools and abdominal bloating. Clinical assessment suggested NEC, however, PI was never documented radiologically. The patient was discharged at five weeks of age after tolerating feedings well and gaining weight. Five days after discharge the patient was readmitted with vomiting, and marked PI, free air, and small bowel obstruction was suggested on abdominal radiographs. After antibiotic therapy the patient improved and was discharged. At 21/2months of age, approximately one week after discharge, the patient was readmitted with bright red blood per rectum. X-rays revealed the small bowel to be slightly dilated and the presence of PI (Fig. 2). He was treated for three weeks without improvement. Subsequent surgery revealed adhesions with one loop of bowel twisted 180 ~ and fixed to the abdominal wall. Following surgery the patient recovered nicely and remains healthy. Case 3 (Fig. 3). A 27-week-premature male infant was transferred to CHM at 25 days of age because of abdominal distention, jaundice and an episode of apnea. On admission to CHM the patient had a distended abdomen and diffuse peritonitis. Radiographically there was PI, portal venous gas and free intraperitoneal air (Fig. 3). On the day of admission the patient was taken to surgery and the distal half of the small bowel was removed. A jejunostomy was performed. The pathologic specimens revealed pneumatosis intestinalis. A stoma closure was performed at one month, 20 days. The patient was discharged at two months of age. He was admitted for 4 days for viral croup at 6 months of age. He again returned to CHM at 9 months of age with persistent vomiting, watery diarrhea and lethargy. The abdominal radiographs demonstrated pneumatosis intestinalis and pneumoperitoneum (Fig.3). Exploratory laparotomy revealed extensive colonic pneumatosis intestinalis with no evidence of perforation. All cultures were negative and the etiology of the patient's recurrent PI was never discovered, although it was hypothesized that one of the larger cysts perforated, leading to free intraperitoneal air.
Discussion It is i m p o r t a n t to separate PI (a radiographic description of air in the bowel wall) f r o m N E C - a full-blown disease with signs, s y m p t o m s and radiographic manifestations. These three cases all d e m o n s t r a t e P I f r o m varied causes N E C , obstruction, and an idiopathic etiology. It appears that the unifying factors of these three cases are the presence of PI, the older age of the patients, and their outpatient status. In fact, several factors present in our patients m a y have predisposed t h e m to the delayed onset of PI. O n e of our patients had r o t a z y m e positive stools. Capitanio and G r e e n b e r g recently r e p o r t e d two full t e r m infants (4 and 6 m o n t h s of age) with r o t a z y m e positive stools w h o p r e s e n t e d with an acute onset of vomiting and diarrhea [12-14]. B o t h of these patients were treated conservatively with medical support and recovered. West et al. had eight patients with r o t a z y m e positive stools w h o p r e s e n t e d with P I b e y o n d the n e o n a t a l period [4]. T h e s e eight patients all had the short bowel s y n d r o m e and three had gastroschisis. O u r second patient had b e e n o p e r a t e d on for gastroschisis. A m o u r y et al. and O l d h a m et al. have recently rep o r t e d a series of patients with gastroschisis w h o had delayed onset of PI [5,11]. In fact in Oldham's series, 18.5 % of his patients had PI and all of these infants had full-blown N E C . T h e reason for P I and N E C in these patients is unclear a n d p r o b a b l y m u l t i f a c t o r i a l , b u t stasis and obstruction must play a role. In our patient, an element of obstruction (incomplete) was clearly a predisposing factor.
Radiologic evaluation of these children with delayed PI does not provide significant differentiation from those patients w h o had PI at the usual time. All patients had PI, portal venous gas, and free air at their first episode. T h e second time patient 1 had PI and portal venous gas without free air, while patient 2 and 3 had PI and free air. Distention was present during all these episodes in each patient, and w h e n c o m p a r e d to a group of children with the classic description of P I - N E C , there was no radiologic differentiation. T h e r e seems to be m o r e and m o r e predisposing factors to PI - gastroschisis, rotavirus, and p r o l o n g e d survival. With better survival of infants with N E C the incidence of recurrent P I will be increasing. In addition, children w h o have rotavirus (some without prior N E C ) m a y have a significantly increased incidence of PI. In contrast to n e o n a t e s with PI, the older infant with recurrent P I needs to be evaluated for multiple s e c o n d a r y causes and N E C is only one of these etiologies.
References 1. DuVernoi JK (1783) Anatomische Beobachtungen der unter der ~iusseren und Haut der Gedaerme eingeschlossenen Luft. Phys Med Abhandl Acad Wissensch Petersb 2:182 2. Touloukian RJ, Berdon WE, Amoury RA, Santulli TV (1967) Surgical experience with necrotizing enterocolitis in the infant. J Pediatr Surg 2:389 3. Grosfeld JL, Cheu H, Schlatter M, West KW, Rescorla FJ (1991) Changing trends in necortizing enterocolitis. Ann Surg 214:300 4. West KW, Rescorla F J, Grosfeld JL, Vane DW (1989) Pneumatosis intestinalis in children beyond the neonatal period. J Pediatr Surg 24:818 5. Amoury RA, Godwin CD, McGill CW, Smith TH, Aschcraft KW, Holder TM (1980) Necrotizing enterocolitis following operation in the neonatal period. J Pediatr Surg 15:1 6. Kliegman RM, Fanaroff AA (1984) Necrotizing enterocolitis. N Engl J Med 310:1093 7. Kliegman RM (1990) Neonatal necrotizing enterocolitis: bridging the basic science with the clinical disease. J Pediatr 117:833 8. Sun XM, Hsueh W (1988) Bowel necrosis induced by tumor necrosis factor in rats is mediated by platelet activating factor. J Clin Invest 81:1328 9. Caplan MS, Sun XM, Hsueh W, Hageman JR (1990) Role of platelet activating factor and tumor necrosis factor-alpha in neonatal necrotizing enterocolitis. J Pediatr 116:960 10. Polin RA, Pollack R Barlow B, Wigger HJ, Slovis TL, Santulli TV, Heird WC (1976) Necrotizing enterocolitis in term infants. J Pediatr 89:460 11. Moss TJ, Adler R (1982) Necrotizing enterocolitis in older infants, children and adolescents. J Pediatr 100:764 12. Oldham KT, Coran AG, Drongowski RA, Baker P J, Wesley JR, Polley TZ Jr (1988) The development of necrotizing enterocolitis following repair of gastroschisis: a surprisingly high incidence. J Pediatr Surg 23:945 13. Capitanio MA, Greenberg SB (1991) Pneumatosis intestinalis in two infants with rotavirus gastroenteritis. Pediatr Radio121: 361 14. Rotbart HA, Nelson WL, Golde MR Triffon TC, Kogut SJH, Yolken RH, Hernandez JA, Levin MJ (1988) Neonatal rotavirus-associated necrotizing enterocolitis: case control study and prospective surveillance during an outbreak. J Pediatr 112:87 15. Mogilner B (1983) Necrotizing enterocolitis associated with rotavirus infection. Israel J Med Sci 19:894
T. L. Slovis, MD Department of Radiology Children's Hospital of Michigan 3901 Beaubien Boulevard Detroit, Michigan 48201, USA
