Have a personal or library account? Click to login
Iron Deficiency Anaemia and Anaemia of Inflammation in Enteropathies Caused by Commonest Small Intestine Disorders: Current Evidence Cover

Iron Deficiency Anaemia and Anaemia of Inflammation in Enteropathies Caused by Commonest Small Intestine Disorders: Current Evidence

Open Access
|Dec 2022

References

  1. Akhuemonkhan, E., Parian, A., Miller, K., Hanauer, S., Hutfless, S. (2017). Prevalence and screening for anaemia in mild to moderate Crohn’s disease and ulcerative colitis in the United States, 2010–2014. BMJ Open Gastro, 4, e000155. DOI: 10.1136/bmjgast-2017-000155.10.1136/bmjgast-2017-000155560908228944071
  2. Akkelle, B. S., Tutar, E., Sengul, O. K., Celikel, C.A., Ertem, D. (2018). A rare complication of giardiasis in children: Protein-losing enteropathy. Pediatr. Infect. Dis. J., 37 (12), e345–e347.10.1097/INF.000000000000202530408010
  3. Bager, P., Befrits, R., Wikman, O., Lindgren, S., Moum, B., Hjortswang, H., Dahlerup, J. F. (2013). High burden of iron deficiency and different types of anemia in inflammatory bowel disease outpatients in Scandinavia: A longitudinal 2-year follow-up study. Scand. J. Gastroenterol., 48, 1286–1293. DOI: 10.3109/00365521.2013.838605.10.3109/00365521.2013.83860524073709
  4. Barisani, D., Parafioriti, A., Bardella, M. T., Zoller, H., Conte, D., Armiraglio, E., Trovato, C., Koch, R. O., Weiss, G. (2004). Adaptive changes of duodenal iron transport proteins in celiac disease. Physiol. Genom.,. 17, 316–325.10.1152/physiolgenomics.00211.200315054143
  5. Batey, R. G., Gallagher, N. D. (1977). Role of the placenta in intestinal absorption of iron in pregnant rats. Gastroenterology, 72, 255–259.10.1016/S0016-5085(77)80082-6
  6. Bengi, G., Keyvan, H., Durmaz, S. B., Akpinar, H. (2018). Frequency, types, and treatment of anemia in Turkish patients with inflammatory bowel disease. World J. Gastroenterol., 24 (36), 4186–4196. DOI: 10.3748/wjg.v24.i36.4186.10.3748/wjg.v24.i36.4186615848430271083
  7. Berry, N., Basha, J., Varma, N., Varma, S., Prasad, K. K., Vaiphei, K., Dhaka, N., Sinha, S. K., Kochhar, R. (2018). Anemia in celiac disease is multifactorial in etiology: A prospective study from India: Anemia in celiac disease. JGH Open, 2, 196–200.10.1002/jgh3.12073620701330483589
  8. Brasse-Lagnel C., Karim Z., Letteron P., Bekri S., Bado A., Beaumont C. (2011). Intestinal DMT1 cotransporter is down-regulated by hepcidin via proteasome internalization and degradation. Gastroenterology, 140, 1261–1271.10.1053/j.gastro.2010.12.03721199652
  9. Camaschella, C. (2019). Iron deficiency. Blood, 133, 30–39.10.1182/blood-2018-05-81594430401704
  10. Collins, J. F., Anderson, G. J. (2012). Molecular mechanisms of intestinal iron transport. In: Physiology of the Gastrointestinal Tract (5th edn.). Elsevier, New York, NY. 2308 pp.
  11. Corazza, G. R., Andreani, M. L., Biagi, F. (1997). The smaller size of the ‘coeliac iceberg’ in adults. Scand. J. Gastroenterol., 32, 917–919. DOI: 10.3109/00365529709011202.10.3109/003655297090112029299671
  12. Craven, M. D., Washabau, R. J. (2019). Comparative pathophysiology and management of protein-losing enteropathy. J. Vet. Intern. Med., 33 (2), 383–402.10.1111/jvim.15406643087930762910
  13. Cronin, C. C, Shanahan, F. (2001). Anemia in patients with chronic inflammatory bowel disease. Amer. J. Gastroenterol., 96, 2296.10.1111/j.1572-0241.2001.04032.x11513165
  14. Darshan, D., Wilkins, S. J., Frazer, D. M., Anderson, G. J. (2011). Reduced expression of ferroportin-1 mediates hyporesponsiveness of suckling rats to stimuli that reduce iron absorption. Gastroenterology, 141, 300–309.10.1053/j.gastro.2011.04.01221570398
  15. De Domenico, I., Ward, D. M., Langelier, C., Vaughn, M. B., Nemeth, E., Sundquist, W. I., Ganz, T., Musci, G., Kaplan, J. (2007). The molecular mechanism of hepcidin-mediated ferroportin down-regulation. Mol. Biol. Cell., 18, 2569–2578.10.1091/mbc.e07-01-0060192480717475779
  16. De Falco, L., Tortora, R., Imperatore, N., Bruno, M., Capasso, M., Girelli, D., Castagna, A., Caporaso, N., Iolascon, A., Rispo, A. (2018). The role of TMPRSS6 and HFE variants in iron deficiency anemia in celiac disease. Amer. J. Hematol., 93, 383–393.10.1002/ajh.2499129194702
  17. De Franceschi, L., Iolascon, A., Taherd, A., Cappellini, M. D. (2017). Clinical management of iron deficiency anemia in adults: Systemic review on advances in diagnosis and treatment. Eur. J. Intern. Med., 42, 16–23.10.1016/j.ejim.2017.04.01828528999
  18. Donovan, A., Lima, C. A., Pinkus, J. L., Pinkus, G. S., Zon, L. I., Robine, S., Andrews, N. C. (2005). The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab., 1, 191–200.10.1016/j.cmet.2005.01.00316054062
  19. Eastham, E. J., Walker, W. A. (1977). Effect of cow’s milk on the gastrointestinal tract: A persistent dilemma for the pediatrician. Pediatrics, 60, 477–481.10.1542/peds.60.4.477
  20. Erlandson, M. E., Walden, B., Stern, G., Hilgartner, M. W., Wehman, J., Smith C. H. (1962). Studies on congenital hemolytic syndromes, IV. Gastrointestinal absorption of iron. Blood, 19, 359–378.10.1182/blood.V19.3.359.359
  21. Evstatiev, R., Gasche, C. (2012). Iron sensing and signalling. Gut, 61, 933–952.10.1136/gut.2010.21431222016365
  22. Filmann, N., Rey J., Schneeweiss, S., Ardizzone, S., Bager, P., Bergamaschi, G., Koutroubakis, I., Lindgren, S., Morena, F. L., Moum, B., et al. (2014). Prevalence of anemia in inflammatory bowel diseases in European countries: A systematic review and individual patient data meta-analysis. Inflamm. Bowel Dis., 20, 936–945. DOI: 10.1097/01.MIB.0000442728.74340.fd.10.1097/01.MIB.0000442728.74340.fd24572205
  23. Finch, C. (1994). Regulators of iron balance in humans. Blood, 84, 1697–1702.10.1182/blood.V84.6.1697.1697
  24. Frazer, D. M., Wilkins, S. J., Anderson, G. J. (2007). Elevated iron absorption in the neonatal rat reflects high expression of iron transport genes in the distal alimentary tract. Amer. J. Physiol. Gastrointest. Liver Physiol., 293, G525–G531.10.1152/ajpgi.00579.200617627967
  25. Frazer, D. M., Wilkins, S. J., Becker, E. M., Vulpe, C. D., McKie, A. T., Trinder, D., Anderson, G. J. (2002). Hepcidin expression inversely correlates with the expression of duodenal iron transporters and iron absorption in rats. Gastroenterology, 123, 835–844.10.1053/gast.2002.3535312198710
  26. Gasche, C., Lomer, M. C., Cavill, I., Weiss, G. (2004). Iron, anaemia, and inflammatory bowel diseases. Gut, 53, 1190–1197. DOI: 10.1136/gut.2003.035758.10.1136/gut.2003.035758177413115247190
  27. Gisbert, J. P., Gomollon, F. (2008). Common misconceptions in the diagnosis and management of anemia in inflammatory bowel disease. Amer. J. Gastroenterol., 103, 1299–1307. DOI: 10.1111/j.1572-0241.2008.01846.x.10.1111/j.1572-0241.2008.01846.x18477354
  28. Goldstein, J. L., Cryer, B. (2015). Gastrointestinal injury associated with NSAID use: A case study and review of risk factors and preventative strategies. Drug Healthc. Patient Saf., 7, 31–41. DOI: 10.2147/DHPS.S71976.10.2147/DHPS.S71976431034625653559
  29. Gulec, S., Anderson, G. J., Collins J. F. (2014). Mechanistic and regulatory aspects of intestinal iron absorption. Amer. J. Physiol. Gastrointest. Liver Physiol., 307 (4), G397–G409. DOI: 10.1152/ajpgi.00348.2013.10.1152/ajpgi.00348.2013413711524994858
  30. Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L., Hediger, M. A. (1997). Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature, 388, 482–488.10.1038/413439242408
  31. Hamrick, H. J. (1994). Whole cow’s milk, iron deficiency anemia, and hypoproteinemia: A old problem revisited. Arch. Pediatr. Adolesc. Med., 148, 1351–1352.10.1001/archpedi.1994.021701201130257951824
  32. Harper, J. W., Holleran, S. F., Ramakrishnan, R., Bhagat, G., Green, P. H. (2007). Anemia in celiac disease is multifactorial in etiology. Amer. J. Hematol., 82, 996–1000.10.1002/ajh.2099617636474
  33. Hathorn, M. K. (1971). The influence of hypoxia on iron absorption in the rat. Gastroenterology, 60, 76–81.10.1016/S0016-5085(71)80009-4
  34. Hooda, J., Shah, A., Zhang, L. (2014). Heme, an essential nutrient from dietary proteins, critically impacts diverse physiological and pathological processes. Nutrients, 6 (3), 1080–1102. https://doi.org/10.3390/nu6031080.10.3390/nu6031080396717924633395
  35. Jimenez, K. M., Gasche, C. (2019). Management of iron deficency anemia in inflammatory bowel disease. Acta Haematol., 142, 30–36. https://doi.org/10.1159/000496728.10.1159/00049672830970351
  36. Koutroubakis, I. E., Ramos-Rivers, C., Regueiro, M., Koutroumpakis, E., Click, B., Schwartz, M., Swoger, J., Baidoo, L., Hashash, J. G., Barrie, A., et al. (2016). Five-year period prevalence and characteristics of anemia in a large US inflammatory bowel disease cohort. J. Clin. Gastroenterol., 50 (8), 638–643. DOI: 10.1097/MCG.0000000000000417.10.1097/MCG.0000000000000417483427726485103
  37. Le Blanc, S., Garrick, M. D., Arredondo, M. (2012). Haem carrier protein 1 transports haem and is involved in haem-Fe metabolism. Amer. J. Physiol. Cell Physiol., 302 (12), C1780–1785.
  38. Leidgens, S., Bullough, K. Z., Shi, H., Li, F., Shakoury-Elizeh, M., Yabe, T., Subramanian, P., Hsu, E., Natarajan, N., Nandal, A., et al. (2013). Each member of the poly-r(C)-binding protein 1 (PCBP) family exhibits iron chaperone activity toward ferritin. J. Biol. Chem., 288, 17791–17802.10.1074/jbc.M113.460253368257823640898
  39. Lerner, N. B., Sills, R. (2016). Iron deficiency anemia. In: Kliegman, R. M., Stanton, B. F., Schor, N. F., St. Gemelli, G. V., Behrman, R. E. (eds.). Nelson Text of Pediatrics. 20th edn. Elsevier, Amsterdam, pp. 2322–2326.
  40. Levitt, D. G., Levitt, M. D. (2017). Protein losing enteropathy: Comprehensive review of the mechanistic association with clinical and subclinical disease states. Clin. Exp. Gastroenterol., 10, 147–168.10.2147/CEG.S136803552266828761367
  41. Lim, Y. J., Yang, C.-H. (2012). Non-steroidal anti-inflammatory drug-induced enteropathy. Clin. Endosc., 45 (2), 138–144. DOI: 10.5946/ce.2012.45.2.138.10.5946/ce.2012.45.2.138340161722866254
  42. Luo, X., Hill, M., Johnson, A., Latunde-Dada, G. O. (2014). Modulation of Dcytb (Cybrd 1) expression and function by iron, dehydroascorbate and Hif-2alpha in cultured cells. Biochim. Biophys. Acta, 1840, 106–112.10.1016/j.bbagen.2013.08.01223981688
  43. Mackenzie, B., Garrick, M. D. (2005). Iron imports. II. Iron uptake at the apical membrane in the intestine. Amer. J. Physiol. Gastrointest. Liver Physiol., 289, G981–G986.
  44. Madanchi, M., Fagagnini, S., Fournier, N., Biedermann, L., Zeitz, J., Battegay, E., Zimmerli, L., Vavricka, S. R., Rogler, G., Scharl, M., Swiss IBD Cohort Study Group. (2018). The relevance of vitamin and iron deficiency in patients with inflammatory bowel diseases in patients of the Swiss IBD Cohort. Inflamm. Bowel Dis., 24 (8), 1768–1779. DOI: 10.1093/ibd/izy054.10.1093/ibd/izy05429669023
  45. Mahadev, S., Laszkowska, M., Sundström, J., Björkholm, M., Lebwohl, B., Green, P. H. R., Ludvigsson, J. F. (2018). Prevalence of celiac disease in patients with iron deficiency anemia-A systematic review with meta-analysis. Arq Gastroenterol., 55 (1), 86–93. DOI: 10.1590/S0004-2803.201800000-17.10.1590/s0004-2803.201800000-17
  46. Marcil, V., Levy, E., Amre, D., Bitton, A., de Araújo Sant'Anna, A.M.G., Szilagy, A., Sinnett, D., Seidman E.G. (2019). A cross-sectional study on malnutrition in inflammatory bowel disease: Is there a difference based on pediatric or adult age grouping? Inflamm. Bowel Dis., 25 (8), 1428–1441. DOI: 10.1093/ibd/izy403.10.1093/ibd/izy403663581830793155
  47. Martín-Masot, R., Nestares, M. T., Diaz-Castro, J., López-Aliaga, I., Muñoz-Alférez, M. J., Moreno-Fernandez, J., Maldonado, J. (2019). Multifactorial etiology of anemia in celiac disease and effect of gluten-free diet: A comprehensive review. Nutrients, 11, 2557.10.3390/nu11112557689353731652803
  48. McKie, A. T., Barrow, D., Latunde-Dada, G. O., Rolfs, A., Sager, G., Mudaly, E., Mudaly, M., Richardson, C., Barlow, D., Bomford, A., et al. (2001). An iron-regulated ferric reductase associated with the absorption of dietary iron. Science, 291, 1755–1759.10.1126/science.105720611230685
  49. McKie, A. T., Marciani, P., Rolfs, A., Brennan, K., Wehr, K., Barrow, D., Miret, S., Bomford, A., Peters, T. J., Farzaneh, F., et al. (2000). A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell, 5, 299–309.10.1016/S1097-2765(00)80425-610882071
  50. Melenovsky, V., Kubanek, M., Kacer, P. (2018). Protein-losing enteropathy in an adult with non-ischaemic cardiomyopathy: Complete reversal by heart transplantation. ESC Heart Fail, 5 (5), 842–845.10.1002/ehf2.12342616593730051970
  51. Millard, K. N., Frazer, D. M., Wilkins, S. J., Anderson, G. J. (2004). Changes in the expression of intestinal iron transport and hepatic regulatory molecules explain the enhanced iron absorption associated with pregnancy in the rat. Gut, 53, 655–660.10.1136/gut.2003.031153177405715082582
  52. Miller, S. D., Cuffari, C., Akhuemonkhan, E., Guerrerio, A. L., Lehmann, H., Hutfless, S. (2019). Anemia screening, prevalence, and treatment in pediatric inflammatory bowel disease in the United States, 2010–2014. Pediatr. Gastroenterol. Hepatol. Nutr., 22 (2), 152–161. DOI: 10.5223/pghn.2019.22.2.15210.5223/pghn.2019.22.2.152641638930899691
  53. Miranda, W. R., Borlaug, B. A., Hagler, D. J., Connolly, H. M., Egbe, A. C. (2019). Haemodynamic profiles in adult Fontan patients: Associated haemodynamics and prognosis. Eur. J. Heart Fail., 21 (6), 803–809.10.1002/ejhf.136530672076
  54. MohanKumar, K., Namachivayam, K., Sivakumar, N. (2020). Severe neonatal anemia increases intestinal permeability by disrupting epithelial adherens junctions. Amer. J. Physiol. Gastrointest. Liver Physiol., 318, G705–G716.10.1152/ajpgi.00324.2019719146532090604
  55. Nagra, N., Dang, S. (2021). Protein Losing Enteropathy. StatPearls Publishing, Treasure Island, FL.
  56. Nemeth, E., Tuttle, M. S., Powelson, J., Vaughn, M. B., Donovan, A., Ward, D. M., Ganz, T., Kaplan, J. (2004). Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science, 306, 2090–2093.10.1126/science.110474215514116
  57. Nickerson, H. J., Silberman, T., Park, R. W., DeVries, E. O., Broste, S. K. (2000). Treatment of iron deficiency anemia and associated protein-losing enteropathy in children. J. Pediatr. Hematol. Oncol., 22, 50–54.10.1097/00043426-200001000-0001010695822
  58. Nicolas, G., Bennoun, M., Devaux, I., Beaumont, C., Grandchamp, B., Kahn, A., Vaulont, S. (2001). Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc. Natl. Acad. Sci USA, 98, 8780–8785.10.1073/pnas.1511794983751211447267
  59. Nicolas, G., Bennoun, M., Porteu, A., Mativet, S., Beaumont, C., Grandchamp, B., Sirito, M., Sawadogo, M., Kahn, A., Vaulont, S. (2002). Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc. Natl. Acad. Sci USA, 99, 4596–4601.10.1073/pnas.07263249912369311930010
  60. Nicolas, G., Chauvet, C., Viatte, L., Danan, J. L., Bigard, X., Devaux, I., Beaumont, C., Kahn, A., Vaulont, S. (2002). The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J. Clin. Invest., 110,1037–1044.10.1172/JCI0215686
  61. Nielsen, O. H., Soendergaard, C., Vikner, M. E., Weiss, G. (2018). Rational management of iron-deficiency anaemia in inflammatory bowel disease. Nutrients, 10 (1), 82. DOI: 10.3390/nu1001008210.3390/nu10010082579331029342861
  62. Niepel, D., Klag, T., Malek, N. P., Wehkamp J., (2018). Practical guidance for the management of iron deficiency in patients with inflammatory bowel disease. Therap Adv Gastroenterol., 11, 1756284818769074. DOI: 10.1177/175628481876907410.1177/1756284818769074594659029760784
  63. Peyssonnaux, C., Zinkernagel, A. S., Schuepbach, R. A., Rankin, E., Vaulont, S., Haase, V. H., Nizet, V., Johnson, R. S. (2007). Regulation of iron homeostasis by the hypoxia-inducible transcription factors (HIFs). J. Clin. Invest., 117, 1926–1932.10.1172/JCI31370188469017557118
  64. Raja, K. B., Simpson, R. J., Pippard, M. J., Peters, T. J. (1988). In vivo studies on the relationship between intestinal iron (Fe3+) absorption, hypoxia and erythropoiesis in the mouse. Brit. J. Haematol., 68, 373–378.10.1111/j.1365-2141.1988.tb04217.x3355797
  65. Reilly, N. R., Aguilar, K., Hassid, B. G. (2011). Celiac disease in normal-weight and overweight children: Clinical features and growth outcomes following a gluten-free diet. J. Pediatr. Gastroenterol. Nutr., 53, 528–531.10.1097/MPG.0b013e3182276d5e21670710
  66. Repo, M., Hannula, M., Taavela, J., Hyttinen, J., Isola, J., Hiltunen, P., Popp, A., Kaukinen, K., Kurppa, K., Lindfors, K. (2021). Iron transporter protein expressions in children with celiac disease. Nutrients, 13, 776.10.3390/nu13030776799728833673530
  67. Rivera, S., Nemeth, E., Gabayan, V., Lopez, M. A., Farshidi, D., Ganz, T. (2005). Synthetic hepcidin causes rapid dose-dependent hypoferremia and is concentrated in ferroportin-containing organs. Blood, 106, 2196–2199.10.1182/blood-2005-04-1766189513715933050
  68. Roetto, A., Papanikolaou, G., Politou, M., Alberti, F., Girelli, D., Christakis, J., Loukopoulos, D., Camaschella, C. (2003). Mutant antimicrobial peptide hepcidin is associated with severe juvenile hemochromatosis. Nat. Genet., 33, 21–22.10.1038/ng105312469120
  69. Schumacher, K. R., Yu, S., Butts, R., Castleberry, C., Chen, S., Edens, E., Godown, J., Johnson, J., Kemna, M., Lin, K., et al. (2019). Fontan-associated protein-losing enteropathy and post‒heart transplant outcomes: A multicenter study. J. Heart Lung Transplant., 38 (1), 17–25.10.1016/j.healun.2018.09.02430391195
  70. Sharma, M., Singh, P., Agnihotri, A., Das, P., Mishra, A., Verma, A. K., Ahuja, A., Sreenivas, V., Khadgawat, R., Gupta, S. D., et al. (2013). Celiac disease: A disease with varied manifestations in adults and adolescents. J. Dig. Dis., 14, 518–525.10.1111/1751-2980.1207823906112
  71. Shawki, A., Knight, P. B., Maliken, B. D., Niespodzany, E. J., Mackenzie, B. (2012). H(+)-coupled divalent metal-ion transporter-1: Functional properties, physiological roles and therapeutics. Curr. Top Membr., 70, 169–214.10.1016/B978-0-12-394316-3.00005-3702739723177986
  72. Shayeghi, M., Latunde-Dada, G. O., Oakhill, J. S., Laftah, A. H., Takeuchi, K., Halliday, N., Khan, Y., Warley, A., McCann, F. E., Hider, R. C. et al. (2005). Identification of an intestinal haem transporter. Cell, 122 (5), 789–801.
  73. Shi, H., Bencze, K. Z., Stemmler, T. L., Philpott, C. C. (2008). A cytosolic iron chaperone that delivers iron to ferritin. Science, 320, 1207–1210.10.1126/science.1157643250535718511687
  74. Shin, S. J., Noh, C-K., Lim, S. G., Lee, K. M., Lee, K. J. (2017). Non-steroidal anti-inflammatory drug-induced enteropathy. Intest. Res., 15 (4), 446–455. DOI: 10.5217/ir.2017.15.4.446.10.5217/ir.2017.15.4.446568397529142512
  75. Song, H. J., Shim, K.-N. (2016). Current status and future perspectives of capsule endoscopy. Intest. Res., 14 (1), 21–29. DOI: 10.5217/ir.2016.14.1.21.10.5217/ir.2016.14.1.21475451826884731
  76. Stein, J., Hartmann, F., Dignass, A. U. (2010). Diagnosis and management of iron deficiency anemia in patients with IBD. Nat. Rev. Gastroenterol. Hepatol., 7 (11), 599–610.10.1038/nrgastro.2010.15120924367
  77. Tolone, C., Bellini, G., Punzo, F., Papparella, A., Miele, E., Vitale, A., Nobili, B., Strisciuglio, C., Rossi, F. (2017). The DMT1 IVS4+44C>A polymorphism and the risk of iron deficiency anemia in children with celiac disease. PLoS ONE, 12, e0185822.10.1371/journal.pone.0185822563826929023457
  78. Tracy, M. S., Yasuda, J. L., Rufo, P. A. (2020). Protein-losing enteropathy in the setting of iron deficiency anemia: A case series. JPGN Reports., 1 (2), e009. DOI: 10.1097/PG9.0000000000000009.10.1097/PG9.0000000000000009
  79. Vanoaica, L., Darshan, D., Richman, L., Schumann, K., Kuhn, L. C. (2010). Intestinal ferritin H is required for an accurate control of iron absorption. Cell Metab., 12, 273–282.10.1016/j.cmet.2010.08.00320816093
  80. Vivas, S., Ruiz de Morales, J. M., Fernandez, M. (2008). Age-related clinical, serological, and histopathological features of celiac disease. Amer. J. Gastroenterol., 103, 2360–2365. DOI: 10.1111/j.1572-0241.2008.01977.x.10.1111/j.1572-0241.2008.01977.x18702652
  81. Vlachodimitropoulou, E., Naftalin, R. J., Sharp, P. A. (2010). Quercetin is a substrate for the transmembrane oxidoreductase Dcytb. Free Radic. Biol. Med., 48, 1366–1369.10.1016/j.freeradbiomed.2010.02.02120184953
  82. Volta, U., Bellentani, S., Bianchi, F. B. (2001). High prevalence of celiac disease in Italian general population. Dig. Dis. Sci., 46, 1500–1505. DOI: 10.1023/A:1010648122797.10.1023/A:1010648122797
  83. West, A. R., Oates, P. S. (2008). Mechanisms of haem iron absorption: Current questions and controversies. World J. Gastroenterol., 14, 4101–4110.10.3748/wjg.14.4101272536818636652
  84. Yasuda, J. L., Rufo, P. A. (2018). Protein-losing enteropathy in the setting of severe iron deficiency anemia. J. Investig. Med. High Impact Case Rep., 6, 2324709618760078. DOI: 10.1177/2324709618760078.10.1177/2324709618760078583320529511696
  85. Zubiaga Toro, L., Ruiz-Tovar, J., Castro, M. J., Ortiz de Solórzano, F. J., Luque de León, E., Jiménez, J. M., Carbajo, M. Á. (2019). Whipple disease after bariatric surgery: From malabsorption to malnutrition status. Nutr. Hosp., 36 (1), 238–241.
DOI: https://doi.org/10.2478/prolas-2022-0088 | Journal eISSN: 2255-890X | Journal ISSN: 1407-009X
Language: English
Page range: 561 - 568
Published on: Dec 10, 2022
Published by: Latvian Academy of Sciences
In partnership with: Paradigm Publishing Services
Publication frequency: 6 issues per year

© 2022 Olesja Basina, Jelena Derova, Aleksejs Derovs, Sandra Lejniece, published by Latvian Academy of Sciences
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.