Bowel perforation is seen in 12 to 31% of neonates

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1 Use of Ultrasound in the Detection of Occult owel Perforation in Neonates Stephen F. Miller, MD, Joanna J. Seibert, MD, David L. Kinder, SRT, ROMS, lyson R. Wilson, SRT, ROMS Intestinal perforation is a common and serious com plication of NEC in neonates. Plain film evidence often is absent in patients with surgically proved perfora tion. Some patients with NEC develop a distended, gasless abdomen suitable for sonographic evaluation. Five neonates with gasless abdominal distention and clinical decline were studied with ultrasonogra phy. Four patients demonstrated intraperitoneal flu- id-debris levels and ascites; all had surgical proof of perforation. The fifth patient did not demonstrate these findings and subsequently recovered. The sonographic findings of ascites and intraperitoneal fluid-debris levels in patients with NEC are suggestive of perforation. KEY WORDS: Necrotizing enterocolitis; Perforation, intestinal; Enterocolitis; Intestinal perforation; Ultrasound. owel perforation is seen in 12 to 31% of neonates suffering from NEC.1.2 Oassically, the diagnosis of perforation requires detection of pneumoperitoneum or frank ascites on plain radiographs. However, these findings occasionally are difficult to appreciate and may be absent. s many as 16% of neonates with NEC and documented perforation may not demonstrate pneumoperitoneum or ascites, and a similar number of patients may develop ascites without pneumoperitoneum.t These patients may develop a gasless, distended abdomen that is easily examined with ultrasonography. 3 The sonographic findings in four patients with NEC and radiographically occult bowel perforation are presented. Each of these patients demonstrated frank ascites and an intraperitoneal fluid-debris level. fifth patient with NEC and clinical decline was followed with ultrasonography and failed to show these findings; subsequently, clinical improvement occurred. Sonography may be useful in the detection of occult bowel perforation in patients with NEC who do not respond to conservative medical management. REVITIONS NEC, Necrotizing enterocolitis Received November 10, 1992, from the Department of Radiol ogy, rkansas Children's Hospital, University of rkansas for Medical Sciences, Uttle Rock, rkansas. Revised manuscript accepted for publication pril 6, ddress correspondence and reprint requests to Stephen F. Miller, MD, Radiology Department, Naval Medical Center, Portsmouth, Virginia Presented at the 35th nnual lum Convention, tlanta, Georgia, February 23-27, MTERILS ND METHODS Five patients with NEC and gasless abdominal distention suggestive of bowel perforation were seen at our institution over a 12 month period. Plain films were available on all patients and were reviewed by one author a.j.s.). ll patients were examined with cuson 128 ultrasound units (cuson, Mountain View, C), using 3.5 and 5.0 MHz sector or linear array transducers. NEC was diagnosed prospectively in four patients, \C 1993 by the merican Institute of Ultrasound in Medicine J Ultrasound Med 12: , /93/$3.50

2 OCCULT OWEL PERFORTION IN NEONTES 532 J Ultrasound Med 12: , 1993 Table 1: Data on Five Patients with NEC Patient Number ge, Sex Clinical Course 1 6 weeks; 2 3 weeks, Premature with bilateral ICH; NEC ensued, failed to respond to medical therapy; died Premature with failure to pass meconium; sepsis and abdomi nal distension developed; died 3 weeks, male 4 2 weeks, 5 6 weeks, male Premature with NEC; necrotic right colon and terminal ileum resected; developed recurrent NEC, failed to respond to medical therapy; recovered after re peat surgery Premature with jejunal atresia; atretic segments resected; devel oped NEC, failed to respond to medical therapy; recovered after repeat surgery Premature with NEC; necrotic right colon and terminal ileum resected; developed recurrent NEC, initially failed to respond to medical therapy; subsequently recovered Plain Film Findings at Time of Sonography Sonographic Findings Suggestive of Perforation Distended, largely gasless abdomen; no free air or ascites no free air or ascites; con trast enema showed perforation in RLQ and micro~ colon no free air or ascites Large amount of asdtes with fluid/debris levels Large amount of ascites with fluid/debris lev els in RLQ questionable free air, no ascites Pneumoperitoneum with fluid/debris lev els and ascites no free air or ascites Normal Loculated fluid collec tion LUQ with fluid/ debris levels LLQ and ascites NEC, Necrotizing mtetocolltis; ICH, intracranial hemorrhage; LUQ, left upper quadrant; LLQ, left lower quadrant; RLQ, right lower quadrant. on the basis of clinical and radiographic findings. Pneumoperitoneum or pneumatosis intestinalis was seen on plain films in these four patients with NEC at the time of initial presentation. Two of these patients underwent surgical intervention early in their hospital courses; one patient was operated on for NEC after developing pneumoperitoneum (patient 3) and the other (patient 4) underwent resection of a segment of atretic jejunum. oth patients subsequently developed clinical signs of NEC, failed to respond to medical therapy, and had nondiagnostic plain films. Two patients (patients 1, 5) with NEC were followed clinically but failed to respond to appropriate medical therapy. The fifth patient (patient 2) had NEC diagnosed retrospectively at surgery, after perforation was proved on ultrasonography and contrast enema (Table 1). Plain films from these latter patients also were nondiagnostic. scites and intraperitoneal fluid-debris levels were seen on sonography in four patients, all of whom were proved at surgery to have suffered bowel necrosis and perforation. Ultrasonography suggested perforation in two neonates prior to surgery (patients 1, 2); perforation was confirmed on contrast enema in one (Figs. 1, 2). These patients died shortly after ward. Two neonates (patients 3, 4) developed occult perforation after surgical resection of necrotic bowel. Ultrasonography suggested perforation in these patients (Fig. 3) but failed to document perforation in one neonate (patient 5) with NEC and clinical decline in whom the plain films also were nondiagnostic. This patient subsequently recovered. The clinical, radiographic, and sonographic data for all patients are summarized in Table 1. DISCUSSION Necrotizing enterocolitis (NEC) is a multifactorially caused and not infrequent complication of prematurity. NEC occurs in 5 to 15% of neonates with a birth weight of less than 1,500 g, but occasionally it is seen in larger infants, including those of full-term gestations. NEC carries a mortality rate of 10 to 30%, and is associated with significant morbidity for survivors, including hepatic failure and short-gut syndrome. 4

3 Figure 1, nteroposterior view of abdomen demonstrates distention with small amounts of gas in stomach and right lower quadrant. telectasis is present in right lung base. Orogastric catheter is present (arrow)., Transverse view of left lower quadrant shows free fluid (asterisk), dependent debris (arrow), and thickened small bowel loops (arrowheads). MILLER ET L 533 The diagnosis of NEC in the neonate is based on a combination of clinical and radiographic findings. The clinical manifestations of NEC include hypotension, abdominal distention, bloody stools, thrombocytopenia, metabolic acidosis, and protracted vomiting.5 6 The classic radiographic findings in this disorder consist of small bowel dilation, decreased bowel gas, focal ileus, pneumatosis intestinalis, and portal venous gas. Pneumoperitoneum and free intraperitoneal fluid suggest bowel perforation. 7 Serial abdominal plain films are obtained on neonates with NEC to document progress or deterioration, and the development of radiographic abnormalities often precedes clinical decline. 7 Patients with NEC usually are managed conservatively unless evidence of bowel necrosis or perforation is present. owel perforation ultimately occurs in 12 to 31% of NEC patients, and plain film evidence of such is present in most cases. 1 2 However, as many as 16% of neonates with NEC and documented perforation never demonstrate pneumoperitoneum or measurable free intraperitoneal fluid on plain films. n additional 21% of patients with NEC and surgically proved bowel perforation may develop ascites without pneumoperitoneum. 1 8 Such neonates may present a diagnostic and therapeutic dilemma, as the patient with NEC and radiographically occult bowel perforation usually fails to respond to appropriate medical management. It is well established that the mortality rate in patients with NEC rises appreciably after necrotic bowel has perforated. 9 We have found ultrasonography to be of benefit in following this subset of patients, as they may develop a distended, gasless abdomen that is particularly suited to sonographic exarnination.3 On occasion, ultrasonography has been reported to be of use in the detection of perforated ulcers in adults. Nirapathpongpom and associates reported three patients with perforated gastric ulcers in whom pneumoperitoneum was diagnosed on ultrasonography as an extraluminal, shifting echo pattern with interference artifact.to Similar findings were reported in a much larger series by Chang-Chien and coworkers in which two patients developed pneumoperitoneum that was seen on sonograms but not on plain radiographs. 11 Ultrasonography also has gained acceptance as an imaging medium in patients with NEC. Kodroff and colleagues described the sonographic appearance of necrotic bowel in NEC as being abnormally thickened with a hypoechoic periphery and termed this the "pseudokidney sign." 9 Seibert and associates have documented the utility of ultrasonography in the diagnostic evaluation of the child or neonate with a gasless, distended abdomen, in cluding an infant with NEC.3 s sonography can be

4 534 OCCULT OWEL PERFORTION IN NEONTES c Figure 2, nteroposterior view of abdomen shows gasless distention. Orogastric catheter is seen (arrow). telectasis is present in the right lung base., Transverse view of right lower quadrant shows intraperitoneal free fluid (asterisk) and hyperechoic dependent debris (arrow). I, Right iliac wing; V, vertebral body. Scattered echoes within the fluid pocket are artifacts. C, nteroposterior view of abdomen after contrast enema demonstrates perforation of the as cending colon with free intraperitoneal contrast medium (arrowheads). The microcolon was believed to be secondary to extreme prematurity. (From Seibert JJ, Williamson SL, GoUaday ES, Molitt DL, et al: The distended gasless abdo men: fertile field for ultrasound. J Ultrasound Med 5:301, 1986.) performed at the bedside using portable equipment, it is possible to identify cases of suggested bowel perforation in critically ill neonates without transporting the patient to the radiology department. In our series of four neonates with occult bowel perforation, findings on ultrasonographic examination that suggested perforation were ascites and solitary or multiple fluid-debris levels. In au cases, free intraperitoneal fluid was hypoechoic. When present, dependent debris was more hyperechoic than fluid and isoechoic to slightly hyperechoic with respect to liver and bowel. Pneumoperitoneum was seen on ultrasonography in one patient as extraluminal echoes with distal ring artifact that shifted to a nondependent location when the position of the patient was changed. The patient with NEC and clinical de-

5 MILLER ET L 535 findings suggestive of perforation underwent surgical exploration. owel perforation was confirmed in each case, as were the sonographic findings of intraperitoneal debris and ascites. No false-positive results were encountered. In conclusion, sonographic examination of the neonate with a history of NEC who fails to respond to appropriate medical management should be performed when findings on plain radiographs are not definitive. s many as 37% of neonates with NEC and demonstrated bowel perforation may have nondiagnostic plain film examinations. s some neonates with radiographically occult perforation have gasless abdominal distention, ultrasonographic evaluation is technically feasible and may, in fact, lead to the correct diagnosis. The survival rate of patients with NEC decreases markedly after perforation has occurred. Ideally, the sonographic identification of subtle bowel perforation should lead to more prompt surgical intervention and decreased mortality in these patients. REFERENCES Figure 3, nteroposterior view of abdomen demonstrates gasless distention. Gastrostomy catheter is present (arrow)., Longitudinal midline view shows distended bladder (arrowhead), free intraperitoneal fluid (asterisk), and dependent hyperechoic debris (arrow). cline who subsequently improved did not demonstrate ascites or fluid-debris levels. Sonographic findings consistent with NEC but not diagnostic of perforation also were encountered in our series. Loops of bowel with hypoechoic, thickened walls were seen in all five patients. Several of these patients demonstrated the pseudokidney sign of Kodroff and associates. 9 Evanescent gas within the portal venous system was seen on real-time examination in one patient with NEC as minute, mobile hyperechoic foci within the intrahepatic branches of the portal vein. This patient died and was found to have extensive bowel necrosis at autopsy. ll of the patients in our series with sonographic 1. Frey EE, Smith W, Franken E Jr, et al: nalysis of bowel perforation in necrotizing enterocolitis. Pediatr Radiol17:380, Kosloske M, Musemeche C, all WS Jr, et al: Necrotizing enterocolitis: Value of radiographic findings to predict outcome. JR 151:771, Seibert fl, Williamson SL, Golladay ES, et al: The distended gasless abdomen: fertile field for ultrasound. J Ultrasound Med 5:301, Kliegman RM: Neonatal necrotizing enterocolitis: ridging the basic science with the clinical disease. J Pediatr 117:833, Grosfeld JL, Cheu H, Schlatter M, et al: Changing trends in necrotizing enterocolitis. nn Surg 214:300, rown EG, Sweet Y: Neonatal necrotizing enterocolitis. Pediatr Clin North m 29:1149, Daneman, Woodward 5, de SUva M: The radiology of necrotizing enterocolitis (NEC). Pediatr Radio) 7:70, Virjee J, Somers S, DeSa D, et al: Changing patterns of neonatal necrotizing enterocolitis. Gastrointest Radio! 4:169, Kodroff M, Hartenburg M, Goldschmidt R: Ultrasonographic diagnosis of gangrenous bowel in neonatal necrotizing enterocolitis. Pediatr Radiol14:168, Nirapathpongpom 5, Osatavanichvong K, Udompanich 0, et al: Pneumoperitoneum detected by ultrasound. Radiology 150:831, Chang-Chien C-S, Lin H-H, Yen C-L, et al: Sonographic demonstration of free air in perforated peptic ulcers: Comparison of sonography with radiography. J Clin Ultrasound 17:95, 1989