Pediatric Protein-Losing Enteropathy 

  • Author: Simon S Rabinowitz, MD, PhD, FAAP; Chief Editor: Carmen Cuffari, MD   more...
 
Updated: Dec 5, 2011
 

Background

Protein-losing enteropathy (PLE) is not a single disease but a symptom. While it occurs in multiple conditions through various pathophysiologic processes, the end result is the loss of serum proteins into the GI tract. Although enteropathy is defined as an intestinal disease, and is commonly associated with the small bowel, protein-losing enteropathy includes loss of protein from the colon, stomach, and, rarely, the esophagus. Some authors have used the term protein-losing gastroenteropathy. While there is nothing unique about protein-losing enteropathy in children, the prevalence of various etiologies is different in children from that in adults.

Protein-losing enteropathy can be either a primary manifestation or a subclinical component of various diseases. Historically, patients with hypoalbuminemia of unknown cause were referred to as having idiopathic hypoproteinemia, edema disease, or nephrosis without nephrosis. These patients had neither a decrease in the production of albumin (ie, no signs of malnutrition or hepatic disease) nor an increase in albumin losses from the respiratory tract, kidneys, or skin.

In 1949, Albright et al demonstrated an increase in protein turnover in patients with protein-losing enteropathy. In 1958, Citrin et al were the first to use radiolabeled tracers to demonstrate the actual loss of a protein-containing fluid into the GI tract. Several additional diagnostic techniques using radiolabeled substrates were developed, but a major advance was made when Crossley and Elliot demonstrated that measurement of alpha1-antitrypsin (A1-AT) levels in the stool was a reliable and simple test for protein-losing enteropathy. This approach has identified various conditions that have subclinical protein-losing enteropathy as a component of the disease process.

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Pathophysiology

No single explanation accounts for the loss of protein into the GI tract seen in various clinical conditions. Recent experimental work has focused on how the loss of heparan sulfate proteoglycans from the basolateral surface of the intestinal epithelial cell results in increased protein permeability. Although not yet conclusive, damage to this epithelial matrix component, either by increased pressure in lymphatics or by inflammation, offers an intriguing and unifying hypothesis for the many causes of protein-losing enteropathy.

In vitro analyses have demonstrated that loss of this proteoglycan not only directly causes protein-losing enteropathy but also potentiates the effects of other reputed factors such as inflammatory cytokines and increased pressure.[1] In addition, infants and children with various forms of congenital glycosylation defects, another potential mechanism for loss of heparin sulfate proteoglycans, also have protein-losing enteropathy secondary to increased intestinal permeability.[2]

Protein-losing enteropathy must always be distinguished from the loss of protein through other organs, most commonly the kidney and skin. One potential clue is that renal losses of protein are usually limited to smaller proteins such as albumin where as the GI tract and skin losses are less discriminating. In addition, hypoalbuminemia may be secondary to synthetic dysfunction or excessive catabolism rather than the result of increased losses. Synthetic dysfunction itself can be seen in liver disease or as a result of inadequate precursors (ie, malnutrition or malabsorption)

For practical purposes, the disease processes that cause protein-losing enteropathy can be grouped into the following 3 major categories: (1) lymphatic obstruction (2) mucosal erosion or ulceration, and (3) epithelial cell dysfunction in the absence of macroscopic compromise.

Obstruction of lymphatics from any cause can produce increased pressure throughout the lymphatic system of the GI tract. This results in the stasis of lymph and, if the pressure is high enough, the loss of lymphatic fluid rich in albumin and other proteins from the lacteals in intestinal microvilli into the lumen of the GI tract. If the loss of albumin exceeds the rate of synthesis, hypoalbuminemia and, eventually, edema develop. In addition to the loss of albumin, other important components of lymph are also lost into the bowel, including lymphocytes, immunoglobulins, and hydrophobic molecules such as cholesterol, lipids, and fat-soluble vitamins.

Lymphopenia is a common finding associated with protein-losing enteropathy due to primary intestinal lymphangiectasia, Whipple disease, or constrictive pericarditis. In cases of protein-losing enteropathy associated with lymphatic obstruction, alleviating the obstruction corrects the lymphopenia. A decrease in the circulating levels of immunoglobulins is also a feature of lymphatic obstruction, but because the synthetic machinery remains intact, response to antigenic challenge is usually good.

In patients with lymphatic obstruction, fat malabsorption may also develop secondary to damage produced to the lymphatics. In these patients, deficiencies in the fat-soluble vitamins (ie, A, D, E, K) can occur. A wide variety of infectious diseases and noninfectious diseases can produce inflammation and ulceration of the GI mucosa resulting in protein-losing enteropathy, and each of these processes has its own unique pathophysiology. However, because lymphatic obstruction does not play a role in these conditions, lymphopenia and loss of immunoglobulins are not seen.

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Epidemiology

Frequency

United States

No published data have reported an accurate incidence or prevalence of protein-losing enteropathy in any parts of the United States.

International

No published have reported an accurate incidence or prevalence. The incidence is highest in areas with significant infectious enterocolitis. A recent multicenter European review of over 3000 patients with Fontan procedure describes a prevalence of 3.9%.[3] These authors used stringent criteria; three fourths of the patients had effusions and edema. Other studies have reported an even higher prevalence after this surgery.

Mortality/Morbidity

Morbidity and mortality is dependent on the diseases that are the cause of the protein-losing enteropathy and the availability of prompt recognition and treatment. In the European cohort of Fontan patients described above, medical treatment was ineffective in 75%, with a mortality of 46%, and surgical treatment was ineffective in 81%, with a mortality of 62%.

Race

There is no known racial predilection. For some entities, especially infections of the GI tract, the prevalence is higher in the developing world and in those races more commonly found there.

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Contributor Information and Disclosures
Author

Simon S Rabinowitz, MD, PhD, FAAP  Professor of Clinical Pediatrics, Vice Chairman, Clinical Practice Development, Pediatric Gastroenterology, Hepatology, and Nutrition, State University of New York Downstate College of Medicine, The Children's Hospital at Downstate

Simon S Rabinowitz, MD, PhD, FAAP is a member of the following medical societies: American Academy of Pediatrics, American Association for the Advancement of Science, American College of Gastroenterology, American Gastroenterological Association, American Medical Association, New York Academy of Sciences, North American Society for Pediatric Gastroenterology and Nutrition, Phi Beta Kappa, and Sigma Xi

Disclosure: Abbott nutrition Honoraria Speaking and teaching

Coauthor(s)

Esther N Prince, MD  Pediatric Gastroenterology Fellow, State University of New York Downstate Medical Center

Disclosure: Nothing to disclose.

Specialty Editor Board

Robert Baldassano, MD  Director, Center for Pediatric Inflammatory Bowel Disease, Children's Hospital of Philadelphia; Professor, Department of Pediatrics, Division of Gastroenterology and Nutrition, University of Pennsylvania School of Medicine

Robert Baldassano, MD is a member of the following medical societies: Alpha Omega Alpha, American Academy of Pediatrics, American Gastroenterological Association, and North American Society for Pediatric Gastroenterology and Nutrition

Disclosure: Abbott, Inc Consulting fee Consulting

Mary L Windle, PharmD  Adjunct Associate Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Nothing to disclose.

David A Piccoli, MD  Chief of Pediatric Gastroenterology, Hepatology and Nutrition, The Children's Hospital of Philadelphia; Professor, University of Pennsylvania School of Medicine

David A Piccoli, MD is a member of the following medical societies: American Association for the Study of Liver Diseases, American Gastroenterological Association, and North American Society for Pediatric Gastroenterology and Nutrition

Disclosure: Nothing to disclose.

Steven M Schwarz, MD, FAAP, FACN, AGAF  Professor of Pediatrics, Children's Hospital at Downstate, State University of New York Downstate Medical Center

Steven M Schwarz, MD, FAAP, FACN, AGAF is a member of the following medical societies: American Academy of Pediatrics, American College of Nutrition, American College of Physician Executives, American Gastroenterological Association, American Pediatric Society, Gastroenterology Research Group, New York Academy of Medicine, North American Society for Pediatric Gastroenterology and Nutrition, and Society for Pediatric Research

Disclosure: Curemark, LLC Consulting fee Board membership; Centocor, Inc. Grant/research funds Independent contractor; Johnson & Johnson, Inc. Grant/research funds Independent contractor

Chief Editor

Carmen Cuffari, MD  Associate Professor, Department of Pediatrics, Division of Gastroenterology/Nutrition, Johns Hopkins University School of Medicine

Carmen Cuffari, MD is a member of the following medical societies: American College of Gastroenterology, American Gastroenterological Association, North American Society for Pediatric Gastroenterology, Hepatology and Nutrition, and Royal College of Physicians and Surgeons of Canada

Disclosure: Nothing to disclose.

Additional Contributors

The authors and editors of Medscape Reference gratefully acknowledge the contributions of previous author Barry K Wershil, MD, to the original writing and development of this article.

References
  1. Damen G, de Klerk H, Huijmans J, den Hollander J, Sinaasappel M. Gastrointestinal and other clinical manifestations in 17 children with congenital disorders of glycosylation type Ia, Ib, and Ic. J Pediatr Gastroenterol Nutr. Mar 2004;38(3):282-7. [Medline].

  2. Bode L, Freeze HH. Applied glycoproteomics--approaches to study genetic-environmental collisions causing protein-losing enteropathy. Biochim Biophys Acta. Apr 2006;1760(4):547-59. [Medline].

  3. Mertens L, Hagler DJ, Sauer U, Somerville J, Gewillig M. Protein-losing enteropathy after the Fontan operation: an international multicenter study. PLE study group. J Thorac Cardiovasc Surg. May 1998;115(5):1063-73. [Medline].

  4. Weng MT, Wong JM, Shin SR, Yao M, Wei SC. Papillary thyroid cancer associated with light-chain amyloidosis initially presenting with small-bowel bleeding and protein-losing enteropathy. J Clin Oncol. Oct 10 2010;28(29):e557-9. [Medline].

  5. Hwang YY, Leung AY, Ng IO, Chan GS, Chan KW, Tse E, et al. Protein-losing enteropathy due to T-cell large granular lymphocyte leukemia. J Clin Oncol. Apr 20 2009;27(12):2097-8. [Medline].

  6. Burrow TA, Cohen MB, Bokulic R, et al. Gaucher disease: progressive mesenteric and mediastinal lymphadenopathy despite enzyme therapy. J Pediatr. Feb 2007;150(2):202-6. [Medline].

  7. Damry N, Hottat N, Azzi N, Ferster A, Avni F. Unusual findings in two cases of Langerhans' cell histiocytosis. Pediatr Radiol. Mar 2000;30(3):196-9. [Medline].

  8. Yamashita K, Saito M, Itoh M, et al. Juvenile polyposis complicated with protein losing gastropathy. Intern Med. 2009;48(5):335-8. [Medline].

  9. Kok J, Chen SC, Anderson L, et al. Protein-losing enteropathy and hypogammaglobulinaemia as first manifestations of disseminated histoplasmosis coincident with Nocardia infection. J Med Microbiol. May 2010;59:610-3. [Medline].

  10. Ogawa E, Murata M, Unno M, et al. Protein-losing enteropathy during highly active antiretroviral therapy in a patient with AIDS-related disseminated Mycobacterial avium complex infection. J Infect Chemother. Aug 2009;15(4):252-6. [Medline].

  11. Berni AD, Elias Júnior E, Arão Filho A, Paniago AM. Protein-losing enteropathy in paracoccidioidomycosis identified by scintigraphy: report of three cases. Braz J Infect Dis. Sep-Oct 2010;14(5):540-3. [Medline].

  12. Yamamoto M, Nishibuchi I, Matsuyama A, et al. Gastric carcinoma with protein-losing gastroenteropathy: report of a case. Surg Today. Jan 2011;41(1):125-9. [Medline].

  13. Liu NF, Lu Q, Wang CG, Zhou JG. Magnetic resonance imaging as a new method to diagnose protein losing enteropathy. Lymphology. Sep 2008;41(3):111-5. [Medline].

  14. Kinsell L, Margen S, Tarver H. J Clin Invest. 1950;29:238.

  15. Gordon RS. J Polym Sci. 1957;31:191.

  16. Martinez-Sanchis B, Cortés-Vizcaíno V, Frontado-Morales L, Sopena-Novales P. Intestinal uptake of (99m)Tc-MDP: a case report of protein-losing enteropathy correlated with pathology findings from autopsy. Ann Nucl Med. Feb 2011;25(2):139-41. [Medline].

  17. Liu M, Liu L, Zhou HM. [Reversal of protein-losing enteropathy with heparin therapy in a patient after Fontan operation]. Zhonghua Er Ke Za Zhi. Jan 2009;47(1):76-7. [Medline].

  18. Schumacher KR, Cools M, Goldstein BH, Ioffe-Dahan V, King K, Gaffney D, et al. Oral budesonide treatment for protein-losing enteropathy in Fontan-palliated patients. Pediatr Cardiol. Oct 2011;32(7):966-71. [Medline].

  19. Connor FL, Angelides S, Gibson M, et al. Successful resection of localized intestinal lymphangiectasia post-Fontan: role of (99m)technetium-dextran scintigraphy. Pediatrics. Sep 2003;112(3 Pt 1):e242-7. [Medline]. [Full Text].

  20. Bac DJ, Van Hagen PM, Postema PT, et al. Octreotide for protein-losing enteropathy with intestinal lymphangiectasia. Lancet. Jun 24 1995;345(8965):1639. [Medline].

  21. Bai JC, Sambuelli A, Niveloni S, et al. Alpha 1-antitrypsin clearance as an aid in the management of patients with celiac disease. Am J Gastroenterol. Aug 1991;86(8):986-91. [Medline].

  22. Belamarich PF, Ortiz A, Mones RL. Severe hypoproteinemia and edema in association with varicella infection. Clin Pediatr (Phila). Jan 1991;30(1):56-8. [Medline].

  23. Boccon-Gibod LA, Krichen HA, Carlier-Mercier LM, et al. Digestive tract involvement with exudative enteropathy in Langerhans cell histiocytosis. Pediatr Pathol. Jul-Aug 1992;12(4):515-24. [Medline].

  24. Bode L, Murch S, Freeze HH. Heparan sulfate plays a central role in a dynamic in vitro model of protein-losing enteropathy. J Biol Chem. Mar 24 2006;281(12):7809-15. [Medline].

  25. Bouhnik Y, Chaussade S, Robin P, Gobert JG, Couturier D, Guerre J. [Protein-losing enteropathy syndrome caused by a localization of Kaposi's sarcoma in AIDS]. Gastroenterol Clin Biol. Oct 1989;13(10):838-40. [Medline].

  26. Bryan RL, Newman J, Alexander-Williams J. Giant inflammatory polyposis in ulcerative colitis presenting with protein losing enteropathy. J Clin Pathol. Apr 1990;43(4):346-7. [Medline]. [Full Text].

  27. Chiu NT, Lee BF, Hwang SL, et al. Protein-losing enteropathy: diagnosis with 99mTc-labeled human serum albumin scintigraphy. Radiol. Apr 2001;219(1):86-90.

  28. Cho CS, Min JK, Park SH, et al. Protein losing enteropathy associated with Henoch-Schonlein purpura in a patient with rheumatoid arthritis. Scand J Rheumatol. 1996;25(5):334-6. [Medline].

  29. Cohen HA, Shapiro RP, Frydman M, Varsano I. Childhood protein-losing enteropathy associated with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr. Aug 1991;13(2):201-3. [Medline].

  30. Couper RT, Durie PR, Stafford SE, et al. Late gastrointestinal bleeding and protein loss after distal small- bowel resection in infancy. J Pediatr Gastroenterol Nutr. Nov 1989;9(4):454-60. [Medline].

  31. Dansinger ML, Johnson S, Jansen PC, et al. Protein-losing enteropathy is associated with Clostridium difficile diarrhea but not with asymptomatic colonization: a prospective, case- control study. Clin Infect Dis. Jun 1996;22(6):932-7. [Medline].

  32. Desmazures C, Giraudeaux V, Florent C, L'Hirondel C, Bernier JJ. [Intestinal clearance of alpha 1 anti-trypsin: a simple technique for diagnosis of protein losing enteropathy (author's transl)]. Nouv Presse Med. May 31 1980;9(24):1691-4. [Medline].

  33. Donnelly JP, Rosenthal A, Castle VP, Holmes RD. Reversal of protein-losing enteropathy with heparin therapy in three patients with univentricular hearts and Fontan palliation. J Pediatr. Mar 1997;130(3):474-8. [Medline].

  34. Ehringhaus C, Dominick HC, Schuller M. Protein-losing enteropathy associated with Clostridium perfringens infection [letter]. Lancet. Jul 29 1989;2(8657):268-9. [Medline].

  35. Florent C, L'Hirondel C, Desmazures C, Aymes C, Bernier JJ. Intestinal clearance of alpha 1-antitrypsin. A sensitive method for the detection of protein-losing enteropathy. Gastroenterology. Oct 1981;81(4):777-80. [Medline].

  36. Ghilain JM, Martiat P, Fiasse R, et al. Exudative enteropathy caused by an acute graft-vs-host reaction. Apropos of a case report [in French]. Acta Gastroenterol Belg. Sep-Dec 1990;53(5-6):488-98. [Medline].

  37. Grill BB, Hillemeier AC, Gryboski JD. Fecal alpha 1-antitrypsin clearance in patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 1984;3(1):56-61. [Medline].

  38. Groisman GM, George J, Berman D, Harpaz N. Resolution of protein-losing hypertrophic lymphocytic gastritis with therapeutic eradication of Helicobacter pylori. Am J Gastroenterol. Sep 1994;89(9):1548-51. [Medline].

  39. Hardikar W, Smith AL, Chow CW. Neonatal protein-losing enteropathy caused by intestinal lymphatic hypoplasia in siblings. J Pediatr Gastroenterol Nutr. Aug 1997;25(2):217-21. [Medline].

  40. Henley JD, Kratzer SS, Seo IS, Davis T. Endometriosis of the small intestine presenting as a protein-losing enteropathy. Am J Gastroenterol. Jan 1993;88(1):130-3. [Medline].

  41. Inoue Y, Ohtake T, Koga H, et al. Tc-99m albumin scintigraphy in protein-losing gastroenteropathy caused by gastric polyposis. Clin Nucl Med. May 1998;23(5):322-3. [Medline].

  42. Jacobs ML, Rychik J, Byrum CJ, Norwood WI Jr. Protein-losing enteropathy after Fontan operation: resolution after baffle fenestration. Ann Thorac Surg. Jan 1996;61(1):206-8. [Medline].

  43. Jain A, Reif S, O'Neil K, Gandhi A, Rossi T. Small intestinal bacterial overgrowth and protein-losing enteropathy in an infant with AIDS. J Pediatr Gastroenterol Nutr. Nov 1992;15(4):452-4. [Medline].

  44. Jarnum S, Westergaard H, Yssing M, Jensen H. Quantitation of gastrointestinal protein loss by means of FE59-labeled iron dextran. Gastroenterology. Aug 1968;55(2):229-41. [Medline].

  45. Karbach U, Ewe K, Bodenstein H. Alpha 1-antitrypsin, a reliable endogenous marker for intestinal protein loss and its application in patients with Crohn's disease. Gut. Aug 1983;24(8):718-23. [Medline].

  46. Karbach U, Ewe K, Dehos H. Antiinflammatory treatment and intestinal alpha 1-antitrypsin clearance in active Crohn's disease. Dig Dis Sci. Mar 1985;30(3):229-35. [Medline].

  47. Keaney NP, Kelleher J. Faecal excretion of alpha 1-antitrypsin in protein-losing enteropathy. Lancet. Mar 29 1980;1(8170):711. [Medline].

  48. Kelly AM, Feldt RH, Driscoll DJ, Danielson GK. Use of heparin in the treatment of protein-losing enteropathy after Fontan operation for complex congenital heart disease. Mayo Clin Proc. Aug 1998;73(8):777-9. [Medline].

  49. Koga H, Iida M, Aoyagi K, et al. Generalized giant inflammatory polyposis in a patient with ulcerative colitis presenting with protein-losing enteropathy. Am J Gastroenterol. May 1995;90(5):829-31. [Medline].

  50. Konar A, Brown CB, Hancock BW, Moss S. Protein losing enteropathy as a sole manifestation of non-Hodgkin's lymphoma. Postgrad Med J. May 1986;62(727):399-400. [Medline].

  51. Korman SH, Bar-Oz B, Mandelberg A, Matoth I. Giardiasis with protein-losing enteropathy: diagnosis by fecal alpha 1- antitrypsin determination. J Pediatr Gastroenterol Nutr. Feb 1990;10(2):249-52. [Medline].

  52. Laine L, Politoske EJ, Gill P. Protein-losing enteropathy in acquired immunodeficiency syndrome due to intestinal Kaposi's sarcoma. Arch Intern Med. Jun 1987;147(6):1174-5. [Medline].

  53. Laster L, Waldmann TA, Fenster LF, Singleton JW. Albumin metabolism in patients with Whipple's disease. J Clin Invest. May 1966;45(5):637-44. [Medline].

  54. Madina EH, Soliman AT, Morsi MR. Protein losing enteropathy in the different forms of protein-energy malnutrition. J Trop Pediatr. Oct 1987;33(5):254-6. [Medline].

  55. Matoth I, Granot E, Gorenstein A, et al. Gastrointestinal protein loss in children recovering from burns. J Pediatr Surg. Oct 1991;26(10):1175-8. [Medline].

  56. Mertens L, Hagler DJ, Sauer U, et al. Protein-losing enteropathy after the Fontan operation: an international multicenter study. PLE study group. J Thorac Cardiovasc Surg. May 1998;115(5):1063-73. [Medline].

  57. Meuwissen SG, Ridwan BU, Hasper HJ, Innemee G. Hypertrophic protein-losing gastropathy. A retrospective analysis of 40 cases in The Netherlands. The Dutch Menetrier Study Group. Scand J Gastroenterol Suppl. 1992;194:1-7. [Medline].

  58. Molina JF, Brown RF, Gedalia A, Espinoza LR. Protein losing enteropathy as the initial manifestation of childhood systemic lupus erythematosus. J Rheumatol. Jul 1996;23(7):1269-71. [Medline].

  59. Nakano S, Kuramochi S, Hosoda Y, Miura S. Protein-losing enteropathy due to intestinal lymphangiectasia accompanied by mesenteric lymph node fibrosis. Pathol Int. Nov 1996;46(11):883-6. [Medline].

  60. Nakase H, Itani T, Mimura J, et al. Transient protein-losing enteropathy associated with cytomegalovirus infection in a noncompromised host: a case report. Am J Gastroenterol. Jun 1998;93(6):1005-6. [Medline].

  61. Petersen VP, Hastrup J. Protein losing enteropathy in constrictive pericarditis. Acta Med Scand. 1963;173:401.

  62. Rybolt AH, Bennett RG, Laughon BE, et al. Protein-losing enteropathy associated with Clostridium difficile infection. Lancet. Jun 17 1989;1(8651):1353-5. [Medline].

  63. Rychik J, Piccoli DA, Barber G. Usefulness of corticosteroid therapy for protein-losing enteropathy after the Fontan procedure. Am J Cardiol. Sep 15 1991;68(8):819-21. [Medline].

  64. Sierra C, Calleja F, Picazo B, Martinez-Valverde A. Protein-losing enteropathy secondary to Fontan procedure resolved after cardiac transplantation. J Pediatr Gastroenterol Nutr. Feb 1997;24(2):229-30. [Medline].

  65. Strober W, Wochner RD, Carbone PP, Waldmann TA. Intestinal lymphangiectasia: a protein-losing enteropathy with hypogammaglobulinemia, lymphocytopenia and impaired homograft rejection. The Journal of Clinical Investigation. Oct 1967;46(10):1643-56. [Medline].

  66. Su J, Smith MB, Rerknimitr R, Morrow D. Small intestine bacterial overgrowth presenting as protein-losing enteropathy. Dig Dis Sci. Mar 1998;43(3):679-81. [Medline].

  67. Sunagawa T, Kinjo F, Gakiya I, et al. Successful long-term treatment with cyclosporin A in protein losing gastroenteropathy. Intern Med. May 2004;43(5):397-9. [Medline].

  68. Sunheimer RL, Finck C, Mortazavi S, et al. Primary lupus-associated protein-losing enteropathy. Ann Clin Lab Sci. May-Jun 1994;24(3):239-42. [Medline].

  69. Sutton DL, Kamath KR. Giardiasis with protein-losing enteropathy. J Pediatr Gastroenterol Nutr. Feb 1985;4(1):56-9. [Medline].

  70. Therrien J, Webb GD, Gatzoulis MA. Reversal of protein losing enteropathy with prednisone in adults with modified Fontan operations: long term palliation or bridge to cardiac transplantation?. Heart. Aug 1999;82(2):241-3. [Medline]. [Full Text].

  71. Tift WL, Lloyd JK. Intestinal lymphangiectasia. Long-term results with MCT diet. Arch Dis Child. Apr 1975;50(4):269-76. [Medline].

  72. Tsutsumi A, Sugiyama T, Matsumura R, et al. Protein losing enteropathy associated with collagen diseases. Ann Rheum Dis. Mar 1991;50(3):178-81. [Medline].

  73. Tusseau F, Beaugerie L, Cardon B, Rozenbaum W, Gendre JP, Le Quintrec Y. [Anasarca caused by exudative enteropathy due to digestive Kaposi's sarcoma]. Presse Med. Sep 16 1989;18(28):1393. [Medline].

  74. Waldmann TA. Gastrointestinal protein loss demonstrated by 51Cr-labelled albumin. Lancet. 1961;July:121-3.

  75. Wargny D, Dichy J, de Broucker F, et al. Protein-losing enteropathy caused by intestinal metastases of melanosarcoma [in French]. J Radiol. Oct 1989;70(10):577-9. [Medline].

  76. Westphal V, Murch S, Kim S, et al. Reduced heparan sulfate accumulation in enterocytes contributes to protein-losing enteropathy in a congenital disorder of glycosylation. Am J Pathol. Dec 2000;157(6):1917-25. [Medline]. [Full Text].

  77. Wing-Harkins DL, Dellinger GW, Lynch C, Mihas AA. Eosinophilic gastro-enteritis associated with protein-losing enteropathy and protein C deficiency. J Int Med Res. Jan-Feb 1996;24(1):155-63. [Medline].

  78. Yamada M, Sumazaki R, Adachi H, et al. Resolution of protein-losing hypertrophic gastropathy by eradication of Helicobacter pylori. Eur J Pediatr. Mar 1997;156(3):182-5. [Medline].

  79. Yoshikawa I, Murata I, Tamura M, et al. A case of protein-losing gastropathy caused by acute Helicobacter pylori infection. Gastrointest Endosc. Feb 1999;49(2):245-8. [Medline].

  80. Zellers TM, Brown K. Protein-losing enteropathy after the modified Fontan operation: oral prednisone treatment with biopsy and laboratory proved improvement. Pediatr Cardiol. Mar-Apr 1996;17(2):115-7. [Medline].

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