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ANEMIA PREVALENCE, CAUSES AND RELATED FACTORS AMONG ULCERATIVE COLITIS PATIENTS IN CLINICAL REMISSION

Year 2020, , 131 - 139, 31.08.2020
https://doi.org/10.5505/deutfd.2020.26213

Abstract

Objective: Ulcerative colitis (UC) is a subtype of inflammatory bowel disease. Anemia is the most common extraintestinal finding in UC. The aim of this study is to determine the frequency, causes and related factors of anemia in UC patients with clinical remission.
Materials and Methods: This is a cross-sectional study. Total 265 UC patients followed up in Gastroenterology Unit between January-July 2019 were included. Clinical remission was defined as partial Mayo scores less than 2. Ulcerative colitis extention was grouped as E1, E2 and E3 according to Montreal. New diagnose, less than 18 years, clinical activity, pregnancy were excluded. According to WHO; Hb less than 13 g/dL in men and less than 12 g/dL in women were accepted as anemia. According to ECCO guidelines, anemia was categorized as follows; serum ferritin less than 30 μg/L iron deficiency anemia (IDA), ferritin greater than 100 μg/L and transferrin less than 20% chronic disease anemia (CDA), ferritin 30-100 μg/L IDA+CDA, MCV greater than 100 fL with B12/folate deficiency megaloblastic anemia. Serum iron, B12, folate deficiencies were defined as levels under the lower limit of normal without anemia.
Results: Mean age was 48.2±15.2, mean disease duration was 11.4±7 years, 154(58%) were male. Total 98 (37%) patients had anemia, 76(28.7%) had iron, B12 or folate deficiency. Total 63 (23.8%) patients had IDA, 4 (1.5%) CDA, 12 (4.5%) IDA+CDA, 19 (7.2%) IDA+megaloblastic anemia. Deficiencies of iron, B12 and folate without anemia were defined in 67(25.2%), 7 (2.6%) and 2 (0.75%) patients consecutively. There were significant differences between anemic and non-anemic groups according to gender, disease duration, extention, treatment, CRP and albumin levels (p less than 0.05).
Conclusion: These study results show that anemia is frequent among UC patients even in clinical remission. Anemia should be screened according to guidelines.

References

  • Kulnigg S, Gasche C. Systematic review: managing anaemia in Crohn's disease. Aliment Pharmacol Ther. 2006;24:1507–23.
  • De la Morena, F, Gisbert, JP. Anemia and inflammatory bowel disease. Rev Esp Enferm Dig. 2008;100:285–93.
  • Gasche, C. Anemia in IBD: the overlooked villain. Inflamm Bowel Dis. 2000;6:142–50.
  • Gisbert, Javier P, Gomollón F. Common misconceptions in the diagnosis and management of anemia in inflammatory bowel disease. Am J Gastroenterol. 2008;103:1299–307.
  • WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva, World Health Organization, 2011. p.3-4 (WHO/NMH/NHD/MNM/11.1) (http://www.who.int/vmnis/indicators/haemoglobin.pdf, [erişim tarihi: 15.02.2020]).
  • Danese S, Hoffman C, Vel S, Greco M, Szabo H, Wilson B, et al. Anaemia from a patient perspective in inflammatory bowel disease: results from the European Federation of Crohn’s and Ulcerative Colitis Association’s online survey. Eur J Gastroenterol Hepatol. 2014;26:1385–91.
  • Stein J, Bager P, Befrits R, Gasche C, Gudehus M, Lerebours E, et al. Anaemia management in patients with inflammatory bowel disease: routine practice across nine European countries. Eur J Gastroenterol Hepatol. 2013;25:1456–63.
  • Blumenstein I, Dignass A, Vollmer S, Klemm W, Weber-Mangal S, Stein J. Current practice in the diagnosis and management of IBD-associated anaemia and iron deficiency in Germany: the German AnaemIBD Study. J Crohn's Colitis. 2014;8:1308–14.
  • Bager P, Befrits R, Wikman O, Lindgren S, Moum B, Hjortswong H, et al. The prevalence of anemia and iron deficiency in IBD outpatients in Scandinavia. Scand J Gastroenterol.2011;46:304–9.
  • Voegtlin M, Vavricka SR, Schoepfer AM, Straumann A, Voegtlin J, Regler G, et al. Prevalence of anaemia in inflammatory bowel disease in Switzerland: a cross-sectional study in patients from private practices and university hospitals. J Crohn's Colitis. 2010;4:642–8.
  • Bager P, Befrits R, Wikman O, Lindgren S, Moum B, Hjortswong H, et al. 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. 2013;48:1286–93.
  • Wilson A, Reyes, E, Ofman J. Prevalence and outcomes of anemia in inflammatory bowel disease: a systematic review of the literature. Am J Med. 2004;116:44-9.
  • Stein J, Hartmann F, Dignass AU. Diagnosis and management of iron deficiency anemia in patients with IBD. Nat Rev Gastroenterol Hepatol. 2010;7:599–610.
  • Gomollon F, Gisbert JP. Anemia and inflammatory bowel diseases. World J Gastroenterol. 2009;15:4659–65.
  • Murawska N, Fabisiak A, Fichna J. Anemia of chronic disease and iron deficiency anemia in inflammatory bowel diseases: pathophysiology, diagnosis, and treatment. Inflamm Bowel Dis. 2016;22:1198–208.
  • Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med. 2005;352:1011–23.
  • Battat R, Kopylov U, Szilagyi A, Saxena A, Rosenblatt DS, Warner M, et al. Vitamin B12 deficiency in inflammatory bowel disease: prevalence, risk factors, evaluation, and management. Inflamm Bowel Dis. 2014;20:1120–8.
  • M’Koma AE, Wise PE, Schwartz DA, Muldoon RL, Herline AJ. Prevalence and outcome of anemia after restorative proctocolectomy: a clinical literature review. Dis Colon Rectum. 2009;52:726–39.
  • Devalia V, Hamilton MS, Molloy AM, British Committee for Standards in Hematology. Guidelines for the diagnosis and treatment of cobalamin and folate disorders. Br J Haematol. 2014;166:496–513.
  • Ott C, Liebold A, Takses A, Strauch UG, Obermeier F. High prevalence but insufficient treatment of iron-deficiency anemia in patients with inflammatory bowel disease: results of a population-based cohort. Gastroenterol Res Pract. 2012;2012:595970.
  • Evstatiev R, Marteau P, Iqbal T, Khalif IL, Stein J, Bokemeyer B, et al. FERGIcor, a randomized controlled trial on ferric carboxymaltose for iron deficiency anemia in inflammatory bowel disease. Gastroenterology. 2011;141:846–53. e841–42.
  • Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalcylic acid therapy for mildly to moderately active ulcerative colitis. N Eng J Med. 1987; 317: 1625-29.
  • Rutgeerts P, Sandborn WJ, Feagan BG. Reinnisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353:2462-76.
  • Lewis JD, Chuai S, Nessel L, Lichtenstein GR, Aberra FN, Ellenberg JH. Use of the noninvasive components of the Mayo score to assess clinical response in ulcerative colitis. Inflamm Bowel Dis. 2008;14:1660-6.
  • Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut. 2006;55:749-53.
  • Dignass AU, Gasche C, Bettenworth D, Birgegård G, Danese S, Gisbert JP, et al. European consensus on the diagnosis and management of iron deficiency and anaemia in inflammatory bowel diseases. J Crohns Colitis. 2015;9:211–22.
  • Alkhouri RH, Hashmi H, Baker RD, Gelfond D, Baker SS. Vitamin and mineral status in patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2013;56:89–92.
  • Green R. Indicators for assessing folate and vitamin B-12 status and for monitoring the efficacy of intervention strategies. Am J Clin Nutr. 2011;94:666S–72S
  • Filmann N, Rey J, Schneeweiss S, Ardizzone S, Bager P,Bergamaschi G, Koutroubakis J, et al. Prevalence of anemia in inflammatory bowel diseases in European countries: a systematic review and individual patient data meta-analysis. Inflamm Bowel Dis.2014;20:936-45.
  • Burisch J, Vegh Z, Katsanos K.H, Christodoulou DK, Lazar D, Goldis A, et al. Occurrence of anaemia in the first year of inflammatory bowel disease in a European population-based inception cohort—an ECCO-EpiCom study. J Crohn's Colitis. 2017; 11:1213–22.
  • Akhuemonkhan E, Parian A, Miller K, Hanauer S, Hutflesc S. Prevalence and screening for anaemia in mild to moderate Crohn's disease and ulcerative colitis in the United States, 2010–2014. BMJ Open Gastroenterol. 2017;4.1:e000155.
  • Chaubal A, Pandey V, Choksi D, Poddar P, Ingle M, Phadke A, et al. Anemia in patients with ulcerative colitis in remission: A study from western India. Indian J Gastroenterol. 2017;36:361–5.
  • Atuğ Ö, Kani HT, Banzragch M, İmeryüz N, Akın H. Incidence rate of anemia in inflammatory bowel diseases. Turk J Gastroenterol. 2006;27:143–8.
  • Gasche C, Lomer E, Cavill I, Weiss G. Iron, anaemia, and inflammatory bowel diseases. Gut. 2004;53:1190-7.
  • Oldenburg B, Koningsberger JC, Van Berge Henegouwen GP, Van Asbeck BS, Marx JJ. Iron and inflammatory bowel disease. Aliment Pharmacol Ther. 2001;15:429-38.
  • Woźniak M, Barańska M, Małecka-Panas E, Talar-Wojnarowska R. The prevalence, characteristics, and determinants of anaemia in newly diagnosed patients with inflammatory bowel disease. Prz Gastroenterol.2019;14: 39–47.
  • Lucendo A. J, Arias Á, Roncero Ó, Hervías D, Verdejo C, Naveas Polo J, et al. Anemia at the time of diagnosis of inflammatory bowel disease: Prevalence and associated factors in adolescent and adult patients. Dig Liver Dis.2017;49:405–11.
  • Høivik L, Reinisch W, Cvancarova M, Boum M, IBSEN Study Group. Anaemia in inflammatory bowel disease: A population-based 10-year follow-up. Aliment Pharmacol Ther.2014;39:69–76.
  • Bengi G, Keyvan H, Durmaz SB, Akpınar H. Frequency, types, and treatment of anemia in Turkish patients with inflammatory bowel disease. World J Gastroenterol. 2018;24: 4186–96.
  • Koutroubakis IE, Ramos–Rivers C, Regueiro M, Koutroumpakis E, Click B, Schoen RE, et al. Persistent or recurrent anemia is associated with severe and disabling inflammatory bowel disease. Clin Gastroenterol and Hepatol. 2015;13:1760-6.
  • Koutroubakis IE, Ramos–Rivers C, Regueiro M, Koutroumpakis E, Click B, Schwartz M, et al. Five-year period prevalence and characteristics of anemia in a large us inflammatory bowel disease cohort. J Clin Gastroenterol. 2016;50:638–43.
  • Dilek İ, Altun S, Tuncer İ, Uygan İ, Topal C, Aksoy H. Demir eksikliği anemisinde hemoglobin, hematokrit değerleri, eritrosit indeksleri ve etiyolojik nedenlerin değerlendirilmesi. Van Tıp Fak Derg.2000;7:51-6.
  • Testa A, Rispo A, Romano M, Riegler G, Selvaggi F, Botiglieri E, et al. The burden of anaemia in patients with inflammatory bowel diseases. Dig Liver Dis.2016; 48:267–70.

Klinik remisyondaki ülseratif kolit hastalarında anemi sıklığı, sebepleri ve ilişkili faktörler

Year 2020, , 131 - 139, 31.08.2020
https://doi.org/10.5505/deutfd.2020.26213

Abstract

Amaç: Ülseratif kolit (ÜK) inflamatuar bağırsak hastalığı alt tipidir. Anemi, ÜK’de en sık görülen ekstraintestinal bulgudur. Bu çalışmada amaç klinik remisyondaki ÜK hastalarında anemi sıklığı, sebepleri ve ilişkili faktörlerin saptanmasıdır.
Gereç ve Yöntem: Bu çalışma kesitsel bir çalışmadır. Ocak-Temmuz 2019 arasında Gastroenteroloji kliniğinde ÜK tanısı ile ayaktan takip edilen ve klinik remisyonda 265 ÜK hastası çalışmaya alınmıştır. Klinik remisyon, parsiyel Mayo skoru 2'den küçük olarak kabul edilmiştir. Ülseratif kolit tutulumu Montreal’e göre E1, E2 ve E3 olarak gruplanmıştır. Yeni tanı ÜK, 18 yaş'tan küçük, klinik aktivite ve gebe olanlar çalışmadan dışlanmıştır. Demografik, klinik ve laboratuvar veriler kaydedilmiştir. Anemi tanısı, DSÖ’ye göre; hemoglobin, erkeklerde 13 g/dL'den küçük, kadınlarda 12 g/dL'den küçük olarak kabul edilmiştir. ECCO kılavuzuna göre, aktif hastalığı olmayanlarda serum ferritin 30 μg/L'den küçük demir eksikliği anemisi (DEA), ferritin 100μg/L'den büyük ve transferrin %20'den küçük kronik hastalık anemisi (KHA), ferritin 30-100 μg/L DEA+KHA, B12/folat eksikliği ile MCV 100 fL'den büyük megaloblastik anemi olarak tanımlanmıştır. Anemi olmaksızın serum demir, B12 ve folatın normalin alt sınırı altında olması eksiklik olarak tanımlanmıştır.
Bulgular: Hastaların ortalama yaşı 48,2±15,2 yıl, 154'ü (% 58) erkek, ortalama hastalık süresi 11,4±7 yıl, 98'inde (%37) anemi, 76'sında (%28,7) anemisiz demir, B12 veya folat eksikliği vardı. Hastaların 63’ü (%23,8) DEA, 4’ü (%1,5) KHA, 19’u (%7,2) DEA+megaloblastik anemi, 12’si (%4,5) DEA+KHA, 67’si (%25,2) demir eksikliği, 7’si (%2,6) B12, 2’si (%0,75) folat eksikliğidir. Anemi olan ve olmayan gruplar arasında cinsiyet, hastalık süresi, tutulum, tedavi, CRP ve albümin düzeyleri arasında anlamlı fark saptandı (p küçük 0,05).
Sonuç: Bu çalışma aneminin klinik remisyondaki ÜK hastalarında bile sık olduğunu ve kılavuzlara göre taranması gerekliliğini vurgulamıştır.

References

  • Kulnigg S, Gasche C. Systematic review: managing anaemia in Crohn's disease. Aliment Pharmacol Ther. 2006;24:1507–23.
  • De la Morena, F, Gisbert, JP. Anemia and inflammatory bowel disease. Rev Esp Enferm Dig. 2008;100:285–93.
  • Gasche, C. Anemia in IBD: the overlooked villain. Inflamm Bowel Dis. 2000;6:142–50.
  • Gisbert, Javier P, Gomollón F. Common misconceptions in the diagnosis and management of anemia in inflammatory bowel disease. Am J Gastroenterol. 2008;103:1299–307.
  • WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva, World Health Organization, 2011. p.3-4 (WHO/NMH/NHD/MNM/11.1) (http://www.who.int/vmnis/indicators/haemoglobin.pdf, [erişim tarihi: 15.02.2020]).
  • Danese S, Hoffman C, Vel S, Greco M, Szabo H, Wilson B, et al. Anaemia from a patient perspective in inflammatory bowel disease: results from the European Federation of Crohn’s and Ulcerative Colitis Association’s online survey. Eur J Gastroenterol Hepatol. 2014;26:1385–91.
  • Stein J, Bager P, Befrits R, Gasche C, Gudehus M, Lerebours E, et al. Anaemia management in patients with inflammatory bowel disease: routine practice across nine European countries. Eur J Gastroenterol Hepatol. 2013;25:1456–63.
  • Blumenstein I, Dignass A, Vollmer S, Klemm W, Weber-Mangal S, Stein J. Current practice in the diagnosis and management of IBD-associated anaemia and iron deficiency in Germany: the German AnaemIBD Study. J Crohn's Colitis. 2014;8:1308–14.
  • Bager P, Befrits R, Wikman O, Lindgren S, Moum B, Hjortswong H, et al. The prevalence of anemia and iron deficiency in IBD outpatients in Scandinavia. Scand J Gastroenterol.2011;46:304–9.
  • Voegtlin M, Vavricka SR, Schoepfer AM, Straumann A, Voegtlin J, Regler G, et al. Prevalence of anaemia in inflammatory bowel disease in Switzerland: a cross-sectional study in patients from private practices and university hospitals. J Crohn's Colitis. 2010;4:642–8.
  • Bager P, Befrits R, Wikman O, Lindgren S, Moum B, Hjortswong H, et al. 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. 2013;48:1286–93.
  • Wilson A, Reyes, E, Ofman J. Prevalence and outcomes of anemia in inflammatory bowel disease: a systematic review of the literature. Am J Med. 2004;116:44-9.
  • Stein J, Hartmann F, Dignass AU. Diagnosis and management of iron deficiency anemia in patients with IBD. Nat Rev Gastroenterol Hepatol. 2010;7:599–610.
  • Gomollon F, Gisbert JP. Anemia and inflammatory bowel diseases. World J Gastroenterol. 2009;15:4659–65.
  • Murawska N, Fabisiak A, Fichna J. Anemia of chronic disease and iron deficiency anemia in inflammatory bowel diseases: pathophysiology, diagnosis, and treatment. Inflamm Bowel Dis. 2016;22:1198–208.
  • Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med. 2005;352:1011–23.
  • Battat R, Kopylov U, Szilagyi A, Saxena A, Rosenblatt DS, Warner M, et al. Vitamin B12 deficiency in inflammatory bowel disease: prevalence, risk factors, evaluation, and management. Inflamm Bowel Dis. 2014;20:1120–8.
  • M’Koma AE, Wise PE, Schwartz DA, Muldoon RL, Herline AJ. Prevalence and outcome of anemia after restorative proctocolectomy: a clinical literature review. Dis Colon Rectum. 2009;52:726–39.
  • Devalia V, Hamilton MS, Molloy AM, British Committee for Standards in Hematology. Guidelines for the diagnosis and treatment of cobalamin and folate disorders. Br J Haematol. 2014;166:496–513.
  • Ott C, Liebold A, Takses A, Strauch UG, Obermeier F. High prevalence but insufficient treatment of iron-deficiency anemia in patients with inflammatory bowel disease: results of a population-based cohort. Gastroenterol Res Pract. 2012;2012:595970.
  • Evstatiev R, Marteau P, Iqbal T, Khalif IL, Stein J, Bokemeyer B, et al. FERGIcor, a randomized controlled trial on ferric carboxymaltose for iron deficiency anemia in inflammatory bowel disease. Gastroenterology. 2011;141:846–53. e841–42.
  • Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalcylic acid therapy for mildly to moderately active ulcerative colitis. N Eng J Med. 1987; 317: 1625-29.
  • Rutgeerts P, Sandborn WJ, Feagan BG. Reinnisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353:2462-76.
  • Lewis JD, Chuai S, Nessel L, Lichtenstein GR, Aberra FN, Ellenberg JH. Use of the noninvasive components of the Mayo score to assess clinical response in ulcerative colitis. Inflamm Bowel Dis. 2008;14:1660-6.
  • Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut. 2006;55:749-53.
  • Dignass AU, Gasche C, Bettenworth D, Birgegård G, Danese S, Gisbert JP, et al. European consensus on the diagnosis and management of iron deficiency and anaemia in inflammatory bowel diseases. J Crohns Colitis. 2015;9:211–22.
  • Alkhouri RH, Hashmi H, Baker RD, Gelfond D, Baker SS. Vitamin and mineral status in patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2013;56:89–92.
  • Green R. Indicators for assessing folate and vitamin B-12 status and for monitoring the efficacy of intervention strategies. Am J Clin Nutr. 2011;94:666S–72S
  • Filmann N, Rey J, Schneeweiss S, Ardizzone S, Bager P,Bergamaschi G, Koutroubakis J, et al. Prevalence of anemia in inflammatory bowel diseases in European countries: a systematic review and individual patient data meta-analysis. Inflamm Bowel Dis.2014;20:936-45.
  • Burisch J, Vegh Z, Katsanos K.H, Christodoulou DK, Lazar D, Goldis A, et al. Occurrence of anaemia in the first year of inflammatory bowel disease in a European population-based inception cohort—an ECCO-EpiCom study. J Crohn's Colitis. 2017; 11:1213–22.
  • Akhuemonkhan E, Parian A, Miller K, Hanauer S, Hutflesc S. Prevalence and screening for anaemia in mild to moderate Crohn's disease and ulcerative colitis in the United States, 2010–2014. BMJ Open Gastroenterol. 2017;4.1:e000155.
  • Chaubal A, Pandey V, Choksi D, Poddar P, Ingle M, Phadke A, et al. Anemia in patients with ulcerative colitis in remission: A study from western India. Indian J Gastroenterol. 2017;36:361–5.
  • Atuğ Ö, Kani HT, Banzragch M, İmeryüz N, Akın H. Incidence rate of anemia in inflammatory bowel diseases. Turk J Gastroenterol. 2006;27:143–8.
  • Gasche C, Lomer E, Cavill I, Weiss G. Iron, anaemia, and inflammatory bowel diseases. Gut. 2004;53:1190-7.
  • Oldenburg B, Koningsberger JC, Van Berge Henegouwen GP, Van Asbeck BS, Marx JJ. Iron and inflammatory bowel disease. Aliment Pharmacol Ther. 2001;15:429-38.
  • Woźniak M, Barańska M, Małecka-Panas E, Talar-Wojnarowska R. The prevalence, characteristics, and determinants of anaemia in newly diagnosed patients with inflammatory bowel disease. Prz Gastroenterol.2019;14: 39–47.
  • Lucendo A. J, Arias Á, Roncero Ó, Hervías D, Verdejo C, Naveas Polo J, et al. Anemia at the time of diagnosis of inflammatory bowel disease: Prevalence and associated factors in adolescent and adult patients. Dig Liver Dis.2017;49:405–11.
  • Høivik L, Reinisch W, Cvancarova M, Boum M, IBSEN Study Group. Anaemia in inflammatory bowel disease: A population-based 10-year follow-up. Aliment Pharmacol Ther.2014;39:69–76.
  • Bengi G, Keyvan H, Durmaz SB, Akpınar H. Frequency, types, and treatment of anemia in Turkish patients with inflammatory bowel disease. World J Gastroenterol. 2018;24: 4186–96.
  • Koutroubakis IE, Ramos–Rivers C, Regueiro M, Koutroumpakis E, Click B, Schoen RE, et al. Persistent or recurrent anemia is associated with severe and disabling inflammatory bowel disease. Clin Gastroenterol and Hepatol. 2015;13:1760-6.
  • Koutroubakis IE, Ramos–Rivers C, Regueiro M, Koutroumpakis E, Click B, Schwartz M, et al. Five-year period prevalence and characteristics of anemia in a large us inflammatory bowel disease cohort. J Clin Gastroenterol. 2016;50:638–43.
  • Dilek İ, Altun S, Tuncer İ, Uygan İ, Topal C, Aksoy H. Demir eksikliği anemisinde hemoglobin, hematokrit değerleri, eritrosit indeksleri ve etiyolojik nedenlerin değerlendirilmesi. Van Tıp Fak Derg.2000;7:51-6.
  • Testa A, Rispo A, Romano M, Riegler G, Selvaggi F, Botiglieri E, et al. The burden of anaemia in patients with inflammatory bowel diseases. Dig Liver Dis.2016; 48:267–70.
There are 43 citations in total.

Details

Primary Language Turkish
Subjects Clinical Sciences
Journal Section Research Articles
Authors

Nalan Gülşen Ünal This is me 0000-0001-8870-2450

Ali Şenkaya This is me 0000-0002-5787-3422

Ferit Çalik This is me 0000-0003-4459-7657

Seymur Aslanov This is me 0000-0001-7520-6650

Ahmet Ömer Özütemiz This is me 0000-0002-6960-4043

Publication Date August 31, 2020
Submission Date April 7, 2020
Published in Issue Year 2020

Cite

Vancouver Ünal NG, Şenkaya A, Çalik F, Aslanov S, Özütemiz AÖ. Klinik remisyondaki ülseratif kolit hastalarında anemi sıklığı, sebepleri ve ilişkili faktörler. DEU Tıp Derg. 2020;34(2):131-9.