SRU TOSHIBA RESIDENT TEACHING CASE
Abdominal Sonography in the Evaluation of Necrotizing Enterocolitis Audrey McCarron, MD CLINICAL HISTORY A 2-week-old, former full-term male infant born via spontaneous vaginal delivery presented with upper respiratory symptoms and neonatal fever of 100.5-F. The patient had been transferred from an outside hospital, where a plain film of the abdomen was unrevealing. An abdomen ultrasound (US) was ordered to investigate the source of suspected sepsis.
DIAGNOSIS Necrotizing enterocolitis (NEC) was diagnosed.
DISCUSSION Necrotizing enterocolitis is the most significant gastrointestinal medical and/or surgical condition afflicting neonates. Premature infants are most vulnerable, with 90% of cases occurring in this population, because incidence is inversely proportional to gestational age. Term infants constitute a small minority. Predisposing factors for term infants include congenital heart disease primarily, in addition to perinatal asphyxia, patent ductus arteriosus, indomethacin therapy, and decreased umbilical flow in utero.1 The overall incidence of NEC is reported to be approximately 1 (0.1%) in 1000 births and as high as 20% in low birth infants weighing less than 1500 g.2 Necrotizing enterocolitis most commonly manifests within the first or second week of life, although time of presentation varies with the gestational age. For example, very premature neonates may manifest later, in the second or third week of life. Term infants ostensibly manifest earlier, in the first week of life.2 Clinical presentation is nonspecific and can include poor feeding, abdominal distention, ileus or decreased bowel sounds, bilious vomiting, diarrhea, respiratory distress with acidosis, and features of generalized sepsis.2,3 The pathophysiology remains incompletely understood. Necrotizing enterocolitis has been postulated to be ischemic or infectious in etiology, with immature immunity as a contributing factor. Whatever the cause, vasodilatation of the affected bowel loop combined with inflammatory cytokines and
Received for publication June 23, 2014; accepted June 25, 2014. Children’s National Medical Center, Washington, DC. The author declares no conflict of interest. Reprints: Audrey McCarron, MD, Children’s National Medical Center, 111 Michigan Ave NW 200, Washington, DC 20010 (e-mail: audrey_pichair@ yahoo.com). Copyright * 2014 by Lippincott Williams & Wilkins
202
www.ultrasound-quarterly.com
activated pathways results in loss of mucosal integrity and an inflammatory cascade culminating in ischemic compromise of the tissue. Poorly perfused bowel wall may necrose, slough, thin, and eventually perforate. The most commonly affected location is the terminal ileum, although the cecum and right colon are other common sites.3 The mortality rate in NEC is between 20% and 40% and higher in neonates of very low birth rate, climbing to 64% for the very low birth weight infant once perforation has occurred.1 Early identification of severely ischemic or necrotic loops of bowel can impact morbidity and mortality. Thus, imaging can play an important role in the successful treatment of this disease entity. Identification of free intraperitoneal air is a universally agreed indication for surgical intervention.2 The standard modality for evaluation of neonates suspected of having NEC is plain abdominal radiography. Findings include dilated bowel loops, loss of the normal mosaic or polygonal gas pattern, bowel wall edema evidenced by thumbprinting, pneumatosis intestinalis, portal venous gas, and pneumoperitoneum.3 Bowel dilatation is the most common sign, present in more than 90% of patients, and is an early finding. Pneumatosis is not present in all cases, with reported incidence ranging widely from 19% to 98%, but presence confirms the diagnosis of NEC. Portal venous gas has been reported in up to 30% of neonates with NEC1 and is a later finding than pneumatosis and usually seen in more severe cases. Abdominal sonography should be considered a valuable modality for evaluation of NEC because it allows direct observation of the bowel loops in real time. There are major advantages for plain abdominal radiography: US is able to depict abdominal fluid, whether intraluminal or extraluminal, free in the peritoneal cavity or in a loculated fluid collection. Ultrasound is able to depict the bowel wall directly and assess bowel wall thickness, echogenicity, and peristalsis.1 Third, US allows direct assessment of arterial perfusion of the bowel wall: hypervascularity may indicate engorgement in the early state, whereas hypovascularity may indicate infarction in a later stage. Intramural gas manifests as bright echogenic foci within the bowel wall. Portal gas manifests as hyperechoic foci in sufficient volume forming a linear branching pattern that outlines the portal tree. ‘‘Doppler interrogation of the main portal vein illustrates an artifact which can be appreciated audibly as a crackle and visibly on the spectral tracing as sharp bidirectional spikes of Doppler superimposed on the portal venous waveforms.’’1 Diagnostic pitfalls in the US evaluation of NEC exist. Pneumatosis may be mimicked by pockets of intraluminal gas in the nondependent part of the gut lumen that become Ultrasound Quarterly
& Volume 30, Number 3, September 2014
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ultrasound Quarterly
& Volume 30, Number 3, September 2014
Abdominal Sonography of Necrotizing Enterocolitis
FIGURE 1. A, B, Abdominal US: loops of bowel in the right lower quadrant are dilated and demonstrate circumferential bright echogenic foci with ‘‘dirty shadowing’’ or reverberation artifacts representing gas bubbles within the bowel wall.
FIGURE 2. A, B, and C, Multiple sonographic images demonstrate echogenic foci throughout the hepatic parenchyma in the arborizing distribution of the portal vein, consistent with portal venous gas. D, Doppler interrogation of the main portal vein illustrates an artifact that can be appreciated audibly as a crackle and visibly on the spectral tracing as sharp bidirectional spikes of Doppler superimposed on the portal venous wave form.
FIGURE 3. A, B, Supine and lateral decubitus abdomen radiographs: there are mottled circular and linear lucencies in the right lower quadrant, consistent with pneumatosis intestinalis. A close look reveals juxtaposed black (radiolucent) and white (radiopaque) bands along the margin of the involved loop. The white band represents mucosa and submucosa contrasted on the peritoneal side by intramural gas and on the luminal side by intraluminal gas. The black band represents intramural gas in the serosal layer of the bowel wall. * 2014 Lippincott Williams & Wilkins
www.ultrasound-quarterly.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
203
Ultrasound Quarterly
McCarron
temporarily trapped within mucosal folds.4 In addition, bubbles of intraluminal gas may be falsely localized to the intramural compartment, termed as pseudo pneumatosis intestinalis by the authors, or may give a false impression of bowel wall thickening.4 The patient in our case was evaluated by the surgical consult team. Presentation was benign and nontoxic on physical examination, prompting the surgical team to advocate conservative management rather than operative intervention. The patient underwent serial abdominal examinations, radiographic surveillance, and medical treatment of suspected NEC. He improved with antibiotic treatment sufficiently for discharge, illustrating the common pathways of medical versus surgical treatment for NEC (Figs. 1Y3).
204
www.ultrasound-quarterly.com
& Volume 30, Number 3, September 2014
ACKNOWLEDGMENT The author would like to acknowledge Dorothy Bulas, MD, director of the Pediatric Radiology Fellowship, and Anjum Bandarkar, MD, staff radiologist. REFERENCES 1. Epelman M, Daneman A, Navarro O, et al. Necrotizing enterocolitis: review of state-of-the-art imaging findings with pathologic correlation. Radiographics. 2007;27:285Y305. 2. Necrotizing Enterocolitis (NEC). Available at: http:// www.learningradiology.com/archives05/COW%20156-NEC/neccorrect.htm. Accessed August 2013. 3. Necrotising Enterocolitis. Available at: http://radiopaedia.org/articles/ necrotising-enterocolitis-1. Accessed August 2013. 4. Wilson SR, Burns PN, Wilkinson LM, et al. Gas at abdominal US: appearance, relevance, and analysis of artifacts. Radiology. 1999;210:113Y123.
* 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Abdominal Sonography in the Evaluation of Necrotizing Enterocolitis Audrey McCarron, MD CLINICAL HISTORY A 2-week-old, former full-term male infant born via spontaneous vaginal delivery presented with upper respiratory symptoms and neonatal fever of 100.5-F. The patient had been transferred from an outside hospital, where a plain film of the abdomen was unrevealing. An abdomen ultrasound (US) was ordered to investigate the source of suspected sepsis.
DIAGNOSIS Necrotizing enterocolitis (NEC) was diagnosed.
DISCUSSION Necrotizing enterocolitis is the most significant gastrointestinal medical and/or surgical condition afflicting neonates. Premature infants are most vulnerable, with 90% of cases occurring in this population, because incidence is inversely proportional to gestational age. Term infants constitute a small minority. Predisposing factors for term infants include congenital heart disease primarily, in addition to perinatal asphyxia, patent ductus arteriosus, indomethacin therapy, and decreased umbilical flow in utero.1 The overall incidence of NEC is reported to be approximately 1 (0.1%) in 1000 births and as high as 20% in low birth infants weighing less than 1500 g.2 Necrotizing enterocolitis most commonly manifests within the first or second week of life, although time of presentation varies with the gestational age. For example, very premature neonates may manifest later, in the second or third week of life. Term infants ostensibly manifest earlier, in the first week of life.2 Clinical presentation is nonspecific and can include poor feeding, abdominal distention, ileus or decreased bowel sounds, bilious vomiting, diarrhea, respiratory distress with acidosis, and features of generalized sepsis.2,3 The pathophysiology remains incompletely understood. Necrotizing enterocolitis has been postulated to be ischemic or infectious in etiology, with immature immunity as a contributing factor. Whatever the cause, vasodilatation of the affected bowel loop combined with inflammatory cytokines and
Received for publication June 23, 2014; accepted June 25, 2014. Children’s National Medical Center, Washington, DC. The author declares no conflict of interest. Reprints: Audrey McCarron, MD, Children’s National Medical Center, 111 Michigan Ave NW 200, Washington, DC 20010 (e-mail: audrey_pichair@ yahoo.com). Copyright * 2014 by Lippincott Williams & Wilkins
202
www.ultrasound-quarterly.com
activated pathways results in loss of mucosal integrity and an inflammatory cascade culminating in ischemic compromise of the tissue. Poorly perfused bowel wall may necrose, slough, thin, and eventually perforate. The most commonly affected location is the terminal ileum, although the cecum and right colon are other common sites.3 The mortality rate in NEC is between 20% and 40% and higher in neonates of very low birth rate, climbing to 64% for the very low birth weight infant once perforation has occurred.1 Early identification of severely ischemic or necrotic loops of bowel can impact morbidity and mortality. Thus, imaging can play an important role in the successful treatment of this disease entity. Identification of free intraperitoneal air is a universally agreed indication for surgical intervention.2 The standard modality for evaluation of neonates suspected of having NEC is plain abdominal radiography. Findings include dilated bowel loops, loss of the normal mosaic or polygonal gas pattern, bowel wall edema evidenced by thumbprinting, pneumatosis intestinalis, portal venous gas, and pneumoperitoneum.3 Bowel dilatation is the most common sign, present in more than 90% of patients, and is an early finding. Pneumatosis is not present in all cases, with reported incidence ranging widely from 19% to 98%, but presence confirms the diagnosis of NEC. Portal venous gas has been reported in up to 30% of neonates with NEC1 and is a later finding than pneumatosis and usually seen in more severe cases. Abdominal sonography should be considered a valuable modality for evaluation of NEC because it allows direct observation of the bowel loops in real time. There are major advantages for plain abdominal radiography: US is able to depict abdominal fluid, whether intraluminal or extraluminal, free in the peritoneal cavity or in a loculated fluid collection. Ultrasound is able to depict the bowel wall directly and assess bowel wall thickness, echogenicity, and peristalsis.1 Third, US allows direct assessment of arterial perfusion of the bowel wall: hypervascularity may indicate engorgement in the early state, whereas hypovascularity may indicate infarction in a later stage. Intramural gas manifests as bright echogenic foci within the bowel wall. Portal gas manifests as hyperechoic foci in sufficient volume forming a linear branching pattern that outlines the portal tree. ‘‘Doppler interrogation of the main portal vein illustrates an artifact which can be appreciated audibly as a crackle and visibly on the spectral tracing as sharp bidirectional spikes of Doppler superimposed on the portal venous waveforms.’’1 Diagnostic pitfalls in the US evaluation of NEC exist. Pneumatosis may be mimicked by pockets of intraluminal gas in the nondependent part of the gut lumen that become Ultrasound Quarterly
& Volume 30, Number 3, September 2014
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ultrasound Quarterly
& Volume 30, Number 3, September 2014
Abdominal Sonography of Necrotizing Enterocolitis
FIGURE 1. A, B, Abdominal US: loops of bowel in the right lower quadrant are dilated and demonstrate circumferential bright echogenic foci with ‘‘dirty shadowing’’ or reverberation artifacts representing gas bubbles within the bowel wall.
FIGURE 2. A, B, and C, Multiple sonographic images demonstrate echogenic foci throughout the hepatic parenchyma in the arborizing distribution of the portal vein, consistent with portal venous gas. D, Doppler interrogation of the main portal vein illustrates an artifact that can be appreciated audibly as a crackle and visibly on the spectral tracing as sharp bidirectional spikes of Doppler superimposed on the portal venous wave form.
FIGURE 3. A, B, Supine and lateral decubitus abdomen radiographs: there are mottled circular and linear lucencies in the right lower quadrant, consistent with pneumatosis intestinalis. A close look reveals juxtaposed black (radiolucent) and white (radiopaque) bands along the margin of the involved loop. The white band represents mucosa and submucosa contrasted on the peritoneal side by intramural gas and on the luminal side by intraluminal gas. The black band represents intramural gas in the serosal layer of the bowel wall. * 2014 Lippincott Williams & Wilkins
www.ultrasound-quarterly.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
203
Ultrasound Quarterly
McCarron
temporarily trapped within mucosal folds.4 In addition, bubbles of intraluminal gas may be falsely localized to the intramural compartment, termed as pseudo pneumatosis intestinalis by the authors, or may give a false impression of bowel wall thickening.4 The patient in our case was evaluated by the surgical consult team. Presentation was benign and nontoxic on physical examination, prompting the surgical team to advocate conservative management rather than operative intervention. The patient underwent serial abdominal examinations, radiographic surveillance, and medical treatment of suspected NEC. He improved with antibiotic treatment sufficiently for discharge, illustrating the common pathways of medical versus surgical treatment for NEC (Figs. 1Y3).
204
www.ultrasound-quarterly.com
& Volume 30, Number 3, September 2014
ACKNOWLEDGMENT The author would like to acknowledge Dorothy Bulas, MD, director of the Pediatric Radiology Fellowship, and Anjum Bandarkar, MD, staff radiologist. REFERENCES 1. Epelman M, Daneman A, Navarro O, et al. Necrotizing enterocolitis: review of state-of-the-art imaging findings with pathologic correlation. Radiographics. 2007;27:285Y305. 2. Necrotizing Enterocolitis (NEC). Available at: http:// www.learningradiology.com/archives05/COW%20156-NEC/neccorrect.htm. Accessed August 2013. 3. Necrotising Enterocolitis. Available at: http://radiopaedia.org/articles/ necrotising-enterocolitis-1. Accessed August 2013. 4. Wilson SR, Burns PN, Wilkinson LM, et al. Gas at abdominal US: appearance, relevance, and analysis of artifacts. Radiology. 1999;210:113Y123.
* 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
