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Endoscopic features of long-standing primary intestinal lymphangiectasia
3. 4. 5. 6.
port on the complications of 5000 diagnostic or therapeutic colonoscopies. Gut 1983;24:376-83. Wu T. Occult injuries during colonoscopy. Measurement of the forces required to injure the colon and report of the cases. Gastrointest Endosc 1978;24:236-8. Ghazi A, Grossman M. Complications of colonoscopy and polypectomy. Surg Clin North Am 1982;62:889-96. Smith L. Fiberoptic colonoscopy: complications of colonoscopy and polypectomy. Dis Colon Rectum 1976;19:407-12. Houghton A, Aston N. Appendicitis complicating colonoscopy [Letter]. Gastrointest Endosc 1988;34:489.
Endoscopic features of long-standing primary intestinal lymphangiectasia Howard A. Salomons, Phillip Kramer, Sigfus Nikulasson, Paul C. Schroy,
MD MD MD MD
P r i m a r y intestinal l y m p h a n g i e c t a s i a (PIL) is a rare congenital disorder characterized by dilated a n d tort u o u s intestinal lacteals resulting f r o m i m p a i r e d lymphatic drainage. Despite its name, the condition is often generalized a n d can affect l y m p h a t i c drainage anywhere in the body. P r o m i n e n t clinical features include protein-losing e n t e r o p a t h y , l y m p h o c y t o p e n i a , steatorrhea, p e r i p h e r a l edema, and chylous effusions as originally described by W a l d m a n n et al. 1 T h e natural history of this rare disorder is not well k n o w n as only a few cases have been r e p o r t e d in the literature. We p r e s e n t herein the l o n g - t e r m follow-up of a p a t i e n t with P I L a n d the associated endoscopic, radiographic, a n d histologic features of the disorder.
CASE REPORT A 40-year-old woman initially presented to our institution at age 14 with progressive edema of the lower extremities, diarrhea, and chylothorax. Results of laboratory studies indicated lymphocytopenia, hypogammagtobulinemia, and hypoalbuminemia. An upper gastrointestinal series with small bowel follow-through (UGI/SBFT) revealed coarse mucosal folds and dilatation of the duodenum and jejunum. Small bowel biopsy with the Crosby capsule demonstrated markedly dilated and distended lymphatics within the villi and marked edema of the lamina propria, consistent with intestinal lymphangiectasia. She was subsequently placed on a low-fat diet supplemented with medium-chain triglycerides (MCT). All symptoms gradually resolved except for occasional bouts of lower extremity edema.
From the Departments of Gastroenterology and Pathology, Boston University Medical Center, Boston, Massachusetts. Reprint requests: Paul C. Schroy, MD, Boston University Medical Center, University Hospital, Division of Gastroenterology, E201, 88 East Newton St. Boston, MA, 02118 0016-5107/95/4105-051653.00 + 0 GASTROINTESTINAL ENDOSCOPY Copyright | 1995 by the American Society for Gastrointestinal Endoscopy 37/4/58483
516
GASTROINTESTINAL ENDOSCOPY
7. Brandt T, Naess A. Acute appendicitis following endoscopic polypectomy. Endoscopy 1989;21:44. 8. Barnett T, McGeehin W, Chen C, Brennan E. Acute tension pneumoperitoneum following colonoscopy. Gastrointest Endosc 1992;38:99-100. 9. Razzak I, Millan J, Schuster M. Pneumatic ileal perforation: an unusual complication of colonoscopy. Gastroenterology t976; 70:268-71. 10. Freeman S, McNally P. Diverticulitis. In: Chohan N, Wong R, eds. Med Clin North Am 1993;77:1149-67.
The patient remained well until age 40, when she presented with a 6-month history of fevers to 102 ~F, chills, night sweats, shortness of breath, progressive lower extremity edema, and intermittent diarrhea described as white in appearance. Physical examination revealed an afebrile woman in no distress. She had decreased breath sounds with dullness to percussion at the right lung base, 2/6 systolic ejection murmur, mild right upper quadrant tenderness without hepatosplenomegaly, and 3+ pitting edema of both lower extremities extending proximally to the midthighs. Laboratory findings included white blood cell count 7000/mm 3 with no lymphocytes, total protein 4.0 g/dL, albumin 1.4 g/dL, gamma globulin 0.8 g/dL (normal, 0.6 to 1.6 g/dL), erythrocyte sedimentation rate 62 ram/h, vitamin A 15 #g/dL (norreal, 30 to 95 #g/dL), 25-hydroxycholecalciferol 6 ng/mL (normal, 10 to 55 ng/mL). Blood, urine, and sputum bacterial cultures were negative, as were tests for antinuclear antibody and rheumatoid factor. Chest films demonstrated a small right pleural effusion, which was subsequently tapped and found to be chylous in nature with a triglyceride level of 364 mg/dL. CT of the abdomen was remarkable for mediastinal, retrocrural, and retroperitoneal lymphadenopathy; thickening of the proximal small bowel in the region of the jejunum, and a 1.5-cm cyst in the lower part of the spleen. A UGI/SBFT demonstrated multiple round filling defects within the mucosa of the proximal and middle segments of the small bowel, particularly in the region of the duodenal sweep; the terminal ileum appeared normal (Fig. 1). Because of the findings on UGI/SBFT, an enteroscopy was performed with the Olympus PCF-100 pediatric video colonoscope (Olympus America Inc., Lake Success, N.Y.) to the proximal jejunum. Multiple submucosal nodules and well-circumscribed xanthomatous plaques of varying sizes were noted throughout the duodenum and jejunum (Fig. 2A-D). The mucosa was remarkable for a prominent whitetipped villous pattern. A 3-cm multilobulated cystic mass observed within the duodenal sweep had an erythematous and friable overlying mucosa (Fig. 2). Biopsy of this cystic mass resulted in an exudation of white, chylous material. Histologic examination revealed dilatation of lacteals within the villi, consistent with the diagnosis of intestinal lymphangiectasia; no evidence of lymphoma was noted (Fig. 3). The patient was again placed on a low-fat, MCT-supptemented diet. She was also started on vitamin supplements because of the decreased levels of vitamins A and D. Her condition rapidly improved, and at a 3-month follow-up visit she was essentially asymptomatic with significantly less peripheral edema, a serum albumin of 2.9 g/dL, and normal levels of vitamins A and D.
VOLUME 41, NO. 5, 1995
Figure 2. Endoscopic features of PIL. A, Large, multilobulated cystic mass with an erythematous and friable mucosa located in the duodenal sweep. B, Proximal jejunum with cystic submucosal nodules and well-circumscribed xanthomatous plaques. C and D, Mucosa with white-tipped villous appearance.
DISCUSSION
Figure 1. Upper gastrointestinal series. A, Multiple large mucosal filling defects (arrow) and B, smaller nodular defects (arrow) within the lumen of the duodenum and proximal jejunum.
V O L U M E 41, NO. 5, 1995
PIL, a rare congenital disorder, is often not limited to the intestine but rather is associated with a generalized lymphatic disturbance. It is a diagnosis of exclusion as secondary forms of the disease have been described in association with tuberculosis, sarcoidosis, Crohn's disease, Budd-Chiari syndrome, lymphoma, constrictive pericarditis, chronic congestive heart failure, Whipple's disease, retroperitoneal malignancies and fibrosis, and systemic lupus erythematosus. 2 Patients with PIL usually present before age 30. Peripheral edema, the most common presenting symptom, may be caused by impaired lymphatic drainage, bypoalbuminemia, or both. Patients may also present with manifestations of protein-losing enteropathy, steatorrhea, or chylous effusions. Hypoalbuminemia, lymphocytopenia, hypogammaglobulinemia, and fatsoluble vitamin deficiencies are common laboratory findings. Iron deficiency anemia secondary to chronic blood loss has also been reported in patients in whom resected segments of small bowel revealed ulcers, scarring, and granulation tissue over areas of dilated lymphatic vessels/ Histologic appearance includes dilated lymphatics located within the lamina propria, often associated with broadening of the villi and stromal edema. Dilated lymphatics may also be found in the submucosa and on occasion within the serosal layer and meGASTROINTESTINAL ENDOSCOPY
517
Figure 3. Duodenal biopsy specimen demonstrating dilated lacteals within the lamina propria of the villi (H&E, original magnification • 125).
sentery, which can lead to the formation of chylous ascites. As chylomicron absorption continues, the dilated lymphatics become f u r t h e r engorged and eventually either leak or r u p t u r e directly into the intestinal lumen, with the possibility of lymphoenteric fistula formation. E i t h e r process results in the progressive loss of l y m p h and its various constituents, thus explaining the c o m m o n observation of hypoalbuminemia, lymphocytopenia, and hypogammaglobulinemia. T h e presence of a protein-losing e n t e r o p a t h y has been d o c u m e n t e d with albumin 1 131, albumin Cr 51, and c h r o m i u m chloride Cr 51 serum protein. More recently, fecal clearance of a l - a n t i t r y p s i n has been used. 4 Imaging studies with C T or U G I / S B F T m a y d e m o n s t r a t e diffuse nodular thickening of the bowel wall, as in this patient, and thus aid in the diagnosis. C T is also useful in excluding secondary causes by d e m o n s t r a t i n g a normal liver and spleen and no significant aortic or mesenteric adenopathy. 5 T h e endoscopic examination in this case demonstrated a variety of lesions within the small bowel. Previous endoscopic reports of P I L have described white plaques 6 and white-tipped villi 7, s within the small bowel. B y electron microscopy, the white villous p a t t e r n of the mucosa appears to represent collections of chylomicrons within the epithelial cells, lamina propria, and interepithelial spaces. 7 In our case, however, the variably sized cystic nodules were the pred o m i n a n t lesions, p r e s u m a b l y representing dilatation of the stromal and submucosal lymphatics. T h e large, friable cystic mass, which leaked lymphatic contents into the intestinal l u m e n u p o n biopsy, d e m o n s t r a t e d
518 G A S T R O I N T E S T I N A L ENDOSCOPY
the e x t e n t to which these nodules can become engorged and potentially r u p t u r e into the lumen. We speculate t h a t the cystic nodules and cystic mass are manifestations of long-standing p r i m a r y disease, as they have not been previously reported. As in our patient, the natural course appears to be relatively constant, with occasional episodes of protein-losing e n t e r o p a t h y and worsening e d e m a during periods of dietary indiscretion. R e i n t r o d u c t i o n of a low-fat, M C T - s u p p l e m e n t e d diet, the m a i n s t a y of t r e a t m e n t for PIL, 9 caused these s y m p t o m s to abate. Exacerbations m a y also occur in relation to specific oral allergens or infective agents. P a t i e n t s with P I L do not appear to be at increased risk for opportunistic infections despite the m a r k e d l y m p h o p e n i a and hypogammaglobulinemia. T h e risk for l y m p h o m a t o u s t r a n s f o r m a t i o n is not clear as only a few cases of P I L preceding the diagnosis of l y m p h o m a have been reported. 1~ T h i s was a concern in our case and p r o m p t e d the endoscopic evaluation of the proximal small bowel, which failed to d e m o n s t r a t e evidence of lymphoma. REFERENCES 1. Waldmann TA, Steinfeld JL, Dutcher TF, Davidson JD, Gordon RS. The role of the gastrointestinal system in idiopathic hypoproteinemia. Gastroenterology 1961;41:197-207. 2. Edworthy SM, Fritzler MJ, Kelly JK, McHattie JD, Shaffer EA. Protein-losing enteropathy in systemic lupus erythematosus associated with intestinal lymphangiectasia. Am J Gastroenterol 1990;85:1398-402. 3. Iida F, Wada R, Sato A, Yamada T. Clinicopathologic consideration of protein-losing enteropathy due to lymphangiectasia of the intestine. Surg Gynecol Obstet 1980;151:391-5. 4. Hill RE, Herez A, Corey ML, Gilday DL. Fecal clearance of alpha-l-antitrypsin: a reliable measure of enteric protein loss in children. J Pediatr 1981;99:416-8. 5. Fakhri A, Fishman EK, Jones B, Kuhajda F, Siegelman SS. Primary intestinal lymphangiectasia: clinical and CT findings. J Comput Assis Tomogr 1985;9:767-70. 6. Donzelli F, Norberto L, Marigo A, et al. Primary intestinal lymphangiectasia. Comparison between endoscopic and radiologic findings. Helvetica Paediatrica Acta 1980;35:169-75. 7. Riemann JF, Schmidt H. Synopsis of endoscopic and other morphological findings in intestinal lymphangiectasia. Endoscopy 1981;13:60-3. 8. Asakura H, Miura S, Morishita T, et al. Endoscopic and histopathological study on primary and secondary intestinal lymphangiectasia. Dig Dis Sci 1981;26:312-20. 9. Holt PR. Dietary treatment of protein loss in intestinal lymphangiectasia. Pediatrics 1964;34:629-35. 10. Herait P, Gisselbrecht C, Ferme C, et ah Non-Hodgkin lymphoma arising in a case of Waldmann's intestinal lymphangiectasis. Nouv Rev Fr Hematol 1985;27:299-302. 11. Broder S, Callihan TR, Jaffe ES, et al. Resolution of longstanding protein-losing enteropathy in a patient with intestinal lymphangiectasia after treatment for malignant lymphoma. Gastroenterology 1980;80:166-8.
VOLUME 41, NO. 5, 1995
port on the complications of 5000 diagnostic or therapeutic colonoscopies. Gut 1983;24:376-83. Wu T. Occult injuries during colonoscopy. Measurement of the forces required to injure the colon and report of the cases. Gastrointest Endosc 1978;24:236-8. Ghazi A, Grossman M. Complications of colonoscopy and polypectomy. Surg Clin North Am 1982;62:889-96. Smith L. Fiberoptic colonoscopy: complications of colonoscopy and polypectomy. Dis Colon Rectum 1976;19:407-12. Houghton A, Aston N. Appendicitis complicating colonoscopy [Letter]. Gastrointest Endosc 1988;34:489.
Endoscopic features of long-standing primary intestinal lymphangiectasia Howard A. Salomons, Phillip Kramer, Sigfus Nikulasson, Paul C. Schroy,
MD MD MD MD
P r i m a r y intestinal l y m p h a n g i e c t a s i a (PIL) is a rare congenital disorder characterized by dilated a n d tort u o u s intestinal lacteals resulting f r o m i m p a i r e d lymphatic drainage. Despite its name, the condition is often generalized a n d can affect l y m p h a t i c drainage anywhere in the body. P r o m i n e n t clinical features include protein-losing e n t e r o p a t h y , l y m p h o c y t o p e n i a , steatorrhea, p e r i p h e r a l edema, and chylous effusions as originally described by W a l d m a n n et al. 1 T h e natural history of this rare disorder is not well k n o w n as only a few cases have been r e p o r t e d in the literature. We p r e s e n t herein the l o n g - t e r m follow-up of a p a t i e n t with P I L a n d the associated endoscopic, radiographic, a n d histologic features of the disorder.
CASE REPORT A 40-year-old woman initially presented to our institution at age 14 with progressive edema of the lower extremities, diarrhea, and chylothorax. Results of laboratory studies indicated lymphocytopenia, hypogammagtobulinemia, and hypoalbuminemia. An upper gastrointestinal series with small bowel follow-through (UGI/SBFT) revealed coarse mucosal folds and dilatation of the duodenum and jejunum. Small bowel biopsy with the Crosby capsule demonstrated markedly dilated and distended lymphatics within the villi and marked edema of the lamina propria, consistent with intestinal lymphangiectasia. She was subsequently placed on a low-fat diet supplemented with medium-chain triglycerides (MCT). All symptoms gradually resolved except for occasional bouts of lower extremity edema.
From the Departments of Gastroenterology and Pathology, Boston University Medical Center, Boston, Massachusetts. Reprint requests: Paul C. Schroy, MD, Boston University Medical Center, University Hospital, Division of Gastroenterology, E201, 88 East Newton St. Boston, MA, 02118 0016-5107/95/4105-051653.00 + 0 GASTROINTESTINAL ENDOSCOPY Copyright | 1995 by the American Society for Gastrointestinal Endoscopy 37/4/58483
516
GASTROINTESTINAL ENDOSCOPY
7. Brandt T, Naess A. Acute appendicitis following endoscopic polypectomy. Endoscopy 1989;21:44. 8. Barnett T, McGeehin W, Chen C, Brennan E. Acute tension pneumoperitoneum following colonoscopy. Gastrointest Endosc 1992;38:99-100. 9. Razzak I, Millan J, Schuster M. Pneumatic ileal perforation: an unusual complication of colonoscopy. Gastroenterology t976; 70:268-71. 10. Freeman S, McNally P. Diverticulitis. In: Chohan N, Wong R, eds. Med Clin North Am 1993;77:1149-67.
The patient remained well until age 40, when she presented with a 6-month history of fevers to 102 ~F, chills, night sweats, shortness of breath, progressive lower extremity edema, and intermittent diarrhea described as white in appearance. Physical examination revealed an afebrile woman in no distress. She had decreased breath sounds with dullness to percussion at the right lung base, 2/6 systolic ejection murmur, mild right upper quadrant tenderness without hepatosplenomegaly, and 3+ pitting edema of both lower extremities extending proximally to the midthighs. Laboratory findings included white blood cell count 7000/mm 3 with no lymphocytes, total protein 4.0 g/dL, albumin 1.4 g/dL, gamma globulin 0.8 g/dL (normal, 0.6 to 1.6 g/dL), erythrocyte sedimentation rate 62 ram/h, vitamin A 15 #g/dL (norreal, 30 to 95 #g/dL), 25-hydroxycholecalciferol 6 ng/mL (normal, 10 to 55 ng/mL). Blood, urine, and sputum bacterial cultures were negative, as were tests for antinuclear antibody and rheumatoid factor. Chest films demonstrated a small right pleural effusion, which was subsequently tapped and found to be chylous in nature with a triglyceride level of 364 mg/dL. CT of the abdomen was remarkable for mediastinal, retrocrural, and retroperitoneal lymphadenopathy; thickening of the proximal small bowel in the region of the jejunum, and a 1.5-cm cyst in the lower part of the spleen. A UGI/SBFT demonstrated multiple round filling defects within the mucosa of the proximal and middle segments of the small bowel, particularly in the region of the duodenal sweep; the terminal ileum appeared normal (Fig. 1). Because of the findings on UGI/SBFT, an enteroscopy was performed with the Olympus PCF-100 pediatric video colonoscope (Olympus America Inc., Lake Success, N.Y.) to the proximal jejunum. Multiple submucosal nodules and well-circumscribed xanthomatous plaques of varying sizes were noted throughout the duodenum and jejunum (Fig. 2A-D). The mucosa was remarkable for a prominent whitetipped villous pattern. A 3-cm multilobulated cystic mass observed within the duodenal sweep had an erythematous and friable overlying mucosa (Fig. 2). Biopsy of this cystic mass resulted in an exudation of white, chylous material. Histologic examination revealed dilatation of lacteals within the villi, consistent with the diagnosis of intestinal lymphangiectasia; no evidence of lymphoma was noted (Fig. 3). The patient was again placed on a low-fat, MCT-supptemented diet. She was also started on vitamin supplements because of the decreased levels of vitamins A and D. Her condition rapidly improved, and at a 3-month follow-up visit she was essentially asymptomatic with significantly less peripheral edema, a serum albumin of 2.9 g/dL, and normal levels of vitamins A and D.
VOLUME 41, NO. 5, 1995
Figure 2. Endoscopic features of PIL. A, Large, multilobulated cystic mass with an erythematous and friable mucosa located in the duodenal sweep. B, Proximal jejunum with cystic submucosal nodules and well-circumscribed xanthomatous plaques. C and D, Mucosa with white-tipped villous appearance.
DISCUSSION
Figure 1. Upper gastrointestinal series. A, Multiple large mucosal filling defects (arrow) and B, smaller nodular defects (arrow) within the lumen of the duodenum and proximal jejunum.
V O L U M E 41, NO. 5, 1995
PIL, a rare congenital disorder, is often not limited to the intestine but rather is associated with a generalized lymphatic disturbance. It is a diagnosis of exclusion as secondary forms of the disease have been described in association with tuberculosis, sarcoidosis, Crohn's disease, Budd-Chiari syndrome, lymphoma, constrictive pericarditis, chronic congestive heart failure, Whipple's disease, retroperitoneal malignancies and fibrosis, and systemic lupus erythematosus. 2 Patients with PIL usually present before age 30. Peripheral edema, the most common presenting symptom, may be caused by impaired lymphatic drainage, bypoalbuminemia, or both. Patients may also present with manifestations of protein-losing enteropathy, steatorrhea, or chylous effusions. Hypoalbuminemia, lymphocytopenia, hypogammaglobulinemia, and fatsoluble vitamin deficiencies are common laboratory findings. Iron deficiency anemia secondary to chronic blood loss has also been reported in patients in whom resected segments of small bowel revealed ulcers, scarring, and granulation tissue over areas of dilated lymphatic vessels/ Histologic appearance includes dilated lymphatics located within the lamina propria, often associated with broadening of the villi and stromal edema. Dilated lymphatics may also be found in the submucosa and on occasion within the serosal layer and meGASTROINTESTINAL ENDOSCOPY
517
Figure 3. Duodenal biopsy specimen demonstrating dilated lacteals within the lamina propria of the villi (H&E, original magnification • 125).
sentery, which can lead to the formation of chylous ascites. As chylomicron absorption continues, the dilated lymphatics become f u r t h e r engorged and eventually either leak or r u p t u r e directly into the intestinal lumen, with the possibility of lymphoenteric fistula formation. E i t h e r process results in the progressive loss of l y m p h and its various constituents, thus explaining the c o m m o n observation of hypoalbuminemia, lymphocytopenia, and hypogammaglobulinemia. T h e presence of a protein-losing e n t e r o p a t h y has been d o c u m e n t e d with albumin 1 131, albumin Cr 51, and c h r o m i u m chloride Cr 51 serum protein. More recently, fecal clearance of a l - a n t i t r y p s i n has been used. 4 Imaging studies with C T or U G I / S B F T m a y d e m o n s t r a t e diffuse nodular thickening of the bowel wall, as in this patient, and thus aid in the diagnosis. C T is also useful in excluding secondary causes by d e m o n s t r a t i n g a normal liver and spleen and no significant aortic or mesenteric adenopathy. 5 T h e endoscopic examination in this case demonstrated a variety of lesions within the small bowel. Previous endoscopic reports of P I L have described white plaques 6 and white-tipped villi 7, s within the small bowel. B y electron microscopy, the white villous p a t t e r n of the mucosa appears to represent collections of chylomicrons within the epithelial cells, lamina propria, and interepithelial spaces. 7 In our case, however, the variably sized cystic nodules were the pred o m i n a n t lesions, p r e s u m a b l y representing dilatation of the stromal and submucosal lymphatics. T h e large, friable cystic mass, which leaked lymphatic contents into the intestinal l u m e n u p o n biopsy, d e m o n s t r a t e d
518 G A S T R O I N T E S T I N A L ENDOSCOPY
the e x t e n t to which these nodules can become engorged and potentially r u p t u r e into the lumen. We speculate t h a t the cystic nodules and cystic mass are manifestations of long-standing p r i m a r y disease, as they have not been previously reported. As in our patient, the natural course appears to be relatively constant, with occasional episodes of protein-losing e n t e r o p a t h y and worsening e d e m a during periods of dietary indiscretion. R e i n t r o d u c t i o n of a low-fat, M C T - s u p p l e m e n t e d diet, the m a i n s t a y of t r e a t m e n t for PIL, 9 caused these s y m p t o m s to abate. Exacerbations m a y also occur in relation to specific oral allergens or infective agents. P a t i e n t s with P I L do not appear to be at increased risk for opportunistic infections despite the m a r k e d l y m p h o p e n i a and hypogammaglobulinemia. T h e risk for l y m p h o m a t o u s t r a n s f o r m a t i o n is not clear as only a few cases of P I L preceding the diagnosis of l y m p h o m a have been reported. 1~ T h i s was a concern in our case and p r o m p t e d the endoscopic evaluation of the proximal small bowel, which failed to d e m o n s t r a t e evidence of lymphoma. REFERENCES 1. Waldmann TA, Steinfeld JL, Dutcher TF, Davidson JD, Gordon RS. The role of the gastrointestinal system in idiopathic hypoproteinemia. Gastroenterology 1961;41:197-207. 2. Edworthy SM, Fritzler MJ, Kelly JK, McHattie JD, Shaffer EA. Protein-losing enteropathy in systemic lupus erythematosus associated with intestinal lymphangiectasia. Am J Gastroenterol 1990;85:1398-402. 3. Iida F, Wada R, Sato A, Yamada T. Clinicopathologic consideration of protein-losing enteropathy due to lymphangiectasia of the intestine. Surg Gynecol Obstet 1980;151:391-5. 4. Hill RE, Herez A, Corey ML, Gilday DL. Fecal clearance of alpha-l-antitrypsin: a reliable measure of enteric protein loss in children. J Pediatr 1981;99:416-8. 5. Fakhri A, Fishman EK, Jones B, Kuhajda F, Siegelman SS. Primary intestinal lymphangiectasia: clinical and CT findings. J Comput Assis Tomogr 1985;9:767-70. 6. Donzelli F, Norberto L, Marigo A, et al. Primary intestinal lymphangiectasia. Comparison between endoscopic and radiologic findings. Helvetica Paediatrica Acta 1980;35:169-75. 7. Riemann JF, Schmidt H. Synopsis of endoscopic and other morphological findings in intestinal lymphangiectasia. Endoscopy 1981;13:60-3. 8. Asakura H, Miura S, Morishita T, et al. Endoscopic and histopathological study on primary and secondary intestinal lymphangiectasia. Dig Dis Sci 1981;26:312-20. 9. Holt PR. Dietary treatment of protein loss in intestinal lymphangiectasia. Pediatrics 1964;34:629-35. 10. Herait P, Gisselbrecht C, Ferme C, et ah Non-Hodgkin lymphoma arising in a case of Waldmann's intestinal lymphangiectasis. Nouv Rev Fr Hematol 1985;27:299-302. 11. Broder S, Callihan TR, Jaffe ES, et al. Resolution of longstanding protein-losing enteropathy in a patient with intestinal lymphangiectasia after treatment for malignant lymphoma. Gastroenterology 1980;80:166-8.
VOLUME 41, NO. 5, 1995