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- Original Article The prevalence and clinical characteristics of anemia in Korean patients with inflammatory bowel disease
- Dae Sung Lee, Ki Bae Bang, Ji Yeon Kim, Yoon Suk Jung, Jung Ho Park, Hong Joo Kim, Yong Kyun Cho, Chong Il Sohn, Woo Kyu Jeon, Byung Ik Kim, Kyu Young Choi, Dong Il Park
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Intestinal Research 2016;14(1):43-49.
DOI: https://doi.org/10.5217/ir.2016.14.1.43
Published online: January 26, 2016
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- Correspondence to: Dong Il Park, Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, 29 Saemunan-ro, Jongno-gu, Seoul 03181, Korea. Tel: +82-2-2001-8555, Fax: +82-2-2001-8360, diksmc.park@samsung.com
• Received: December 3, 2014 • Revised: May 11, 2015 • Accepted: May 29, 2015
© Copyright 2016. Korean Association for the Study of Intestinal Diseases. All rights reserved.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
-
Background/Aims
- Quality of life is closely related to anemia in patients with inflammatory bowel disease (IBD). Several studies have reported on anemia in patients with IBD in Western countries. This study investigated the prevalence and clinical characteristics of anemia in Korean patients with IBD.
-
Methods
- We reviewed the medical records of 92 patients with ulcerative colitis (UC) and 76 patients with Crohn's disease (CD) who were followed regularly at a single tertiary medical center in Korea between January 2003 and December 2012. Hemoglobin (Hb) thresholds used to define anemia were <13.0 g/dL in men and <12.0 g/dL in women according to the World Health Organization criteria. We chose the lowest Hb level in each year as a representative value because Hb levels changed at each examination and anemia was associated with disease deterioration. The relationship between clinical variables and lowest Hb level was assessed.
-
Results
- The prevalence of anemia was 36.3% in patients with UC and 41.6% in patients with CD. Anemia in patients with CD was associated with hospital admission, 5-aminosalicylate (5-ASA) and infliximab treatment in men. Anemia in patients with UC was associated with hospital admission, oral steroid use, thiopurine and infliximab treatment in men.
-
Conclusions
- The prevalence of anemia in Korean patients with IBD was comparable to that of patients in Western countries. Anemia was associated with male patients with CD who were admitted to the hospital and received medications including 5-ASA and infliximab, and men with UC who were admitted to the hospital and received medications including oral steroids, thiopurine and infliximab.
INTRODUCTION
METHODS
RESULTS
DISCUSSION
- 1. Høivik ML, Reinisch W, Cvancarova M, Moum B. IBSEN study group. Anaemia in inflammatory bowel disease: a populationbased 10-year follow-up. Aliment Pharmacol Ther 2014;39:69–76.PMID: 24172277.ArticlePubMed
- 2. Pizzi LT, Weston CM, Goldfarb NI, et al. Impact of chronic conditions on quality of life in patients with inflammatory bowel disease. Inflamm Bowel Dis 2006;12:47–52.PMID: 16374258.ArticlePubMed
- 3. Kim YJ. Intravenous iron and oral iron treatment in anemia of inflammatory bowel disease. Intest Res 2013;11:227–228.Article
- 4. Wells CW, Lewis S, Barton JR, Corbett S. Effects of changes in hemoglobin level on quality of life and cognitive function in inflammatory bowel disease patients. Inflamm Bowel Dis 2006;12:123–130.PMID: 16432377.ArticlePubMed
- 5. Evans RW, Rader B, Manninen DL. The quality of life of hemodialysis recipients treated with recombinant human erythropoietin. Cooperative Multicenter EPO Clinical Trial Group. JAMA 1990;263:825–830.PMID: 2404150.ArticlePubMed
- 6. Gasché C, Dejaco C, Waldhoer T, et al. Intravenous iron and erythropoietin for anemia associated with Crohn disease. A randomized, controlled trial. Ann Intern Med 1997;126:782–787.PMID: 9148651.ArticlePubMed
- 7. Auerbach M. Oral or IV iron in inflammatory bowel disease. Am J Gastroenterol 2012;107:950author reply 950-951. PMID: 22664849.ArticlePubMedPDF
- 8. Gomollón F, Gisbert JP. Current management of iron deficiency anemia in inflammatory bowel diseases: a practical guide. Drugs 2013;73:1761–1770.PMID: 24114623.ArticlePubMed
- 9. Cronin CC, Shanahan F. Anemia in patients with chronic inflammatory bowel disease. Am J Gastroenterol 2001;96:2296–2298.PMID: 11513165.ArticlePubMed
- 10. 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(Suppl 7A): 44S–49S.PMID: 15050885.ArticlePubMed
- 11. Lennard-Jones JE. Classification of inflammatory bowel disease. Scand J Gastroenterol Suppl 1989;170:2–6.discussion 16-19PMID: 2617184.ArticlePubMed
- 12. Dignass A, Lindsay JO, Sturm A, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 2: current management. J Crohns Colitis 2012;6:991–1030.PMID: 23040451.ArticlePubMedPDF
- 13. Dignass A, Van Assche G, Lindsay JO, et al. The second European evidence-based Consensus on the diagnosis and management of Crohn's disease: Current management. J Crohns Colitis 2010;4:28–62.PMID: 21122489.ArticlePubMedPDF
- 14. Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut 2006;55:749–753.PMID: 16698746.ArticlePubMed
- 15. Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 2005;19(Suppl A): 5A–36A.ArticlePubMedPDF
- 16. Koller O. The clinical significance of hemodilution during pregnancy. Obstet Gynecol Surv 1982;37:649–652.PMID: 7145246.ArticlePubMed
- 17. McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr 2009;12:444–454.PMID: 18498676.ArticlePubMed
- 18. Harries AD, Fitzsimons E, Dew MJ, Heatley RV, Rhodes J. Association between iron deficiency anaemia and mid-arm circumference in Crohn's disease. Hum Nutr Clin Nutr 1984;38:47–53.PMID: 6693295.PubMed
- 19. Schreiber S, Howaldt S, Schnoor M, et al. Recombinant erythropoietin for the treatment of anemia in inflammatory bowel disease. N Engl J Med 1996;334:619–623.PMID: 8592524.ArticlePubMed
- 20. Solberg IC, Lygren I, Jahnsen J, et al. Clinical course during the first 10 years of ulcerative colitis: results from a populationbased inception cohort (IBSEN Study). Scand J Gastroenterol 2009;44:431–440.PMID: 19101844.ArticlePubMed
- 21. Solberg IC, Vatn MH, Høie O, et al. Clinical course in Crohn's disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol 2007;5:1430–1438.PMID: 18054751.ArticlePubMed
- 22. Spivak JL. Iron and the anemia of chronic disease: vindication for the non-essential role of iron supplementation. Oncology (Williston Park) 2011;25:421–423.PMID: 21710838.PubMed
- 23. Gearry RB, Barclay ML. Azathioprine and 6-mercaptopurine pharmacogenetics and metabolite monitoring in inflammatory bowel disease. J Gastroenterol Hepatol 2005;20:1149–1157.PMID: 16048561.ArticlePubMed
- 24. Avni T, Bieber A, Steinmetz T, Leibovici L, Gafter-Gvili A. Treatment of anemia in inflammatory bowel disease-systematic review and meta-analysis. PLoS One 2013;8:e75540PMID: 24312441.ArticlePubMedPMC
- 25. Lugg S, Beal F, Nightingale P, Bhala N, Iqbal T. Iron treatment and inflammatory bowel disease: what happens in real practice? J Crohns Colitis 2014;8:876–880.PMID: 24486177.ArticlePubMedPDF
REFERENCES
Fig. 1
Prevalence of anemia in patients with IBD. Mean prevalence of anemia in patients with IBD is higher than that of the general population. Anemia is more common in patients with CD than those with UC. There was a larger variation in the prevalence of anemia in patients with CD than those with UC. (A) The prevalence of anemia is higher in women with UC than in men with UC (41.4% in women and 33.1% in men). (B) The prevalence of anemia is higher in women with CD than in men with CD (56.6% in women and 39.4% in men).
Fig. 2
Hemoglobin (Hb) level in IBD patients. The mean Hb level is higher in patients with UC than in patients with CD. (A) Male patients with UC are not anemic during the follow up period, while female patients with UC are not anemic during the second half of a 10-years follow up period. (B) CD patients are anemic during most time of follow period. This anemia is more severe in females with CD than in males with CD.
Table 1
![ir-14-43-i001.jpg]()
Baseline Characteristics of Ulcerative Colitis Patients
Table 2
![ir-14-43-i002.jpg]()
Baseline Characteristics in Crohn's disease Patients
Table 3
![ir-14-43-i003.jpg]()
Classification of Anemia Type by Mean Cell Volume and Mean Concentration of Hemoglobin per Volume of Red Cells
| Type | Hypochromic | Normochromic | Hyperchromic |
|---|---|---|---|
| Microcytic | 1 | 2 | 3 |
| Normochromic | 4 | 5 | 6 |
| Macrocytic | 7 | 8 | 9 |
Table 4
![ir-14-43-i004.jpg]()
Type of Anemia by Red Cell Indices
Figure & Data
REFERENCES
Citations
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The prevalence and clinical characteristics of anemia in Korean patients with inflammatory bowel disease
Fig. 1 Prevalence of anemia in patients with IBD. Mean prevalence of anemia in patients with IBD is higher than that of the general population. Anemia is more common in patients with CD than those with UC. There was a larger variation in the prevalence of anemia in patients with CD than those with UC. (A) The prevalence of anemia is higher in women with UC than in men with UC (41.4% in women and 33.1% in men). (B) The prevalence of anemia is higher in women with CD than in men with CD (56.6% in women and 39.4% in men).
Fig. 2 Hemoglobin (Hb) level in IBD patients. The mean Hb level is higher in patients with UC than in patients with CD. (A) Male patients with UC are not anemic during the follow up period, while female patients with UC are not anemic during the second half of a 10-years follow up period. (B) CD patients are anemic during most time of follow period. This anemia is more severe in females with CD than in males with CD.
Fig. 1
Fig. 2
The prevalence and clinical characteristics of anemia in Korean patients with inflammatory bowel disease
Baseline Characteristics of Ulcerative Colitis Patients
| Variable | Female (n=37) | Male (n=55) | ||||
|---|---|---|---|---|---|---|
| Anemic | Non anemic | P-value | Anemic | Non anemic | P-value | |
| Hospitalization | 10 (27.0) | 6 (16.2) | 0.269 | 13 (23.6) | 15 (27.2) | 0.017 |
| Total bowel resection | 4 (10.8) | 3 (8.1) | 0.669 | 8 (14.5) | 13 (23.6) | 0.056 |
| 5-ASA | 20 (54.0) | 12 (32.4) | 1.000 | 19 (34.5) | 30 (54.5) | 0.674 |
| Oral steroid | 9 (24.3) | 5 (13.5) | 1.000 | 10 (18.1) | 3 (5.4) | 0.003 |
| IV steroid | 2 (5.4) | 1 (2.7) | 1.000 | 2 (3.6) | 0 | 0.156 |
| Thiopurine | 8 (21.6) | 1 (2.7) | 0.112 | 10 (18.1) | 3 (5.4) | 0.003 |
| Infliximab | 0 | 0 | 5 (9.0) | 0 | 0.008 | |
| Disease extent | 0.075 | 0.544 | ||||
| Proctitis | 14 (37.8) | 13 (35.1) | 16 (29.0) | 25 (45.4) | ||
| Left-sided | 4 (10.8) | 1 (2.7) | 2 (3.6) | 5 (9.0) | ||
| Extensive disease | 5 (13.5) | 0 | 4 (7.2) | 3 (5.4) | ||
Values are presented as n (%).
5-ASA, 5-aminosalicylate; IV, intravenous.
Baseline Characteristics in Crohn's disease Patients
| Variable | Female (n=18) | Male (n=58) | ||||
|---|---|---|---|---|---|---|
| Anemic | Non Anemic | P-value | Anemic | Non Anemic | P-value | |
| Hospitalization | 12 (66.6) | 1 (5.5) | 0.490 | 40 (68.9) | 5 (8.6) | 0.010 |
| Operation of bowel resection | 1 (5.5) | 0 | 1.000 | 13 (22.4) | 1 (1.7) | 0.265 |
| 5-ASA | 15 (83.3) | 1 (5.5) | 0.210 | 47 (81.0) | 9 (15.5) | 0.033 |
| Oral steroid | 5 (27.7) | 0 | 1.000 | 21 (36.2) | 5 (8.6) | 1.000 |
| IV steroid | 2 (11.1) | 0 | 1.000 | 6 (10.3) | 1 (1.7) | 1.000 |
| Thiopurine | 7 (38.8) | 0 | 0.497 | 33 (56.8) | 4 (6.8) | 0.077 |
| CS | 0 | 0 | 2 (3.4) | 0 | 1.000 | |
| Infliximab | 6 (33.3) | 0 | 0.529 | 21 (36.2) | 1 (1.7) | 0.039 |
| Location | 1.000 | 0.150 | ||||
| Ileal | 1 (5.5) | 0 | 1 (1.7) | 2 (3.4) | ||
| Colonic | 8 (44.4) | 2 (11.1) | 23 (39) | 5 (8.6) | ||
| Ileo-colonic | 4 (22.2) | 0 | 13 (22.4) | 1 (1.7) | ||
| Isolated upper GI disease | 3 (16.6) | 0 | 10 (17.2) | 3 (5.1) | ||
| Concomitant perianal | 6 (31.3) | 0 | 28 (58.0) | 11 (48.0) | ||
| Behavior | 0.412 | 0.067 | ||||
| Non-stricturing and non-penetrating | 9 (49.9) | 2 (11.1) | 24 (41.3) | 9 (15.4) | ||
| Stricturing | 6 (33.3) | 0 | 15 (25.8) | 1 (1.7) | ||
| Penetrating | 1 (5.5) | 0 | 8 (13.7) | 1 (1.7) | ||
Values are presented as n (%).
5-ASA, 5-aminosalicylate; IV, intravenous; CS, cycloserine; GI, gastrointestinal.
Classification of Anemia Type by Mean Cell Volume and Mean Concentration of Hemoglobin per Volume of Red Cells
| Type | Hypochromic | Normochromic | Hyperchromic |
|---|---|---|---|
| Microcytic | 1 | 2 | 3 |
| Normochromic | 4 | 5 | 6 |
| Macrocytic | 7 | 8 | 9 |
Type of Anemia by Red Cell Indices
| Type | CD | UC | ||
|---|---|---|---|---|
| Female (n=101) | Male (n=298) | Female (n=160) | Male (n=213) | |
| 1 | 9 (8.9) | 23 (7.7) | 13 (8.1) | 13 (6.1) |
| 2 | 1 (1.0) | 0 | 2 (1.3) | 4 (1.9) |
| 3 | 0 | 0 | 0 | 0 |
| 4 | 17 (16.8) | 35 (11.7) | 11 (6.8) | 7 (3.3) |
| 5 | 66 (65.3) | 192 (64.4) | 115 (71.9) | 169 (79.3) |
| 6 | 4 (4.0) | 35 (11.7) | 14 (8.8) | 12 (5.6) |
| 7 | 1 (1.0) | 1 (0.3) | 0 | 0 |
| 8 | 3 (3.0) | 10 (3.4) | 3 (1.9) | 7 (3.3) |
| 9 | 0 | 2 (0.7) | 2 (1.3) | 1 (0.5) |
Values are presented as n (%).
Table 1 Baseline Characteristics of Ulcerative Colitis Patients
Values are presented as n (%). 5-ASA, 5-aminosalicylate; IV, intravenous.
Table 2 Baseline Characteristics in Crohn's disease Patients
Values are presented as n (%). 5-ASA, 5-aminosalicylate; IV, intravenous; CS, cycloserine; GI, gastrointestinal.
Table 3 Classification of Anemia Type by Mean Cell Volume and Mean Concentration of Hemoglobin per Volume of Red Cells
Table 4 Type of Anemia by Red Cell Indices
Values are presented as n (%).
