Research Article
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The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery

Year 2023, Volume: 76 Issue: 4, 340 - 347, 05.04.2024

Abstract

Objectives: Iron deficiency anemia is quite common due to impaired iron metabolism and increased blood losses inherent in colorectal cancer. The primary objective of this retrospective research; is to investigate the effect of preoperative iron treatment on the incidence of postoperative anemia in colorectal cancer patients whose anemia was detected in the preoperative anesthesia evaluation and who were undergoing to surgery shortly after intravenous iron treatment.

Materials and Methods: Data of 40 patients who underwent colorectal cancer surgery between January 1 and August 31, 2023 were included in the study. Demographic characteristics of the patients, preoperative hemoglobin and ferritin levels, administered intravenous iron dose, amount of intraoperative bleeding, and hemoglobin levels measured in the early postoperative period, at discharge, and at the 1st and 3rd months after discharge were recorded retrospectively. Numerical variables were presented as mean ± SD, and categorical variables were presented as number and Data were analyzed with Student’s t-test and Mann-Whitney U test. Pearson’s r and Spearman’s rho test were used for correlation analysis. Alpha error level was accepted as 5% for statistical significance.

Results: Preoperative hemoglobin and ferritin levels were 11.9 g/dL and 42.9 ng/mL, respectively. Preoperative anemia prevalence was found to be 80%. When the patients’ postoperative and discharge hemoglobin levels were compared with their preoperative hemoglobin levels, about an average of 1 and 1.8 g/dL decrease was detected, respectively. The incidence of postoperative anemia was found to be 54.5%. It was observed that there was a positive correlation between postoperative hemoglobin level and intravenous iron dose. Pre - Postoperative hemoglobin difference showed positive correlation with ClassIntra scores, Clavien-Dindo scores and the amount of fluid administered intraoperatively. It was observed that patients who were found to be anemic in the third month needed more erythrocyte suspension throughout their hospitalization.

Conclusion: Anemia should be treated at any stage of the perioperative period in colorectal cancer surgery patients. It is necessary to investigate
the multifactorial etiology and pathophysiology underlying anemia for each patient.

Ethical Statement

Etik Kurul Onayı: Ankara Üniversitesi Tıp Fakültesi Klinik Araştırmaları Etik Kurulu’ndan onay (AUTFKAEK no: 2023/570, Prof. Dr. Ergün) alındı. Hasta Onayı: Retrospektif çalışmadır. Hakem Değerlendirmesi: Editörler kurulunun dışından olan kişiler tarafından değerlendirilmiştir.

References

  • 1. Calleja JL, Delgado S, del Val A, et al. Ferric carboxymaltose reduces transfusions and hospital stay in patients with colon cancer and anemia. Int J Colorectal Dis. 2016;31:543-551.
  • 2. Chardalias L, Papaconstantinou I, Gklavas A, et al. Iron Deficiency Anemia in Colorectal Cancer Patients: Is Preoperative Intravenous Iron Infusion Indicated? A Narrative Review of the Literature. Cancer Diagn Progn. 2023;3:163-168.
  • 3. Leichtle SW, Mouawad NJ, Lampman R, et al. Does preoperative anemia adversely affect colon and rectal surgery outcomes? J Am Coll Surg. 2011;212:187-194.
  • 4. Acheson AG, Brookes MJ, Spahn DR. Effects of allogeneic red blood cell transfusions on clinical outcomes in patients undergoing colorectal cancer surgery: a systematic review and meta-analysis. Ann Surg. 2012;256:235- 244.
  • 5. Amin MB, Greene FL, Edge SB, et al. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67:93-99.
  • 6. Warner MA, Shore-Lesserson L, Shander A, et al. Perioperative Anemia: Prevention, Diagnosis, and Management Throughout the Spectrum of Perioperative Care. Anesth Analg. 2020;130:1364-1380.
  • 7. Muñoz M, Acheson AG, Auerbach M, et al. International consensus statement on the peri-operative management of anaemia and iron deficiency. Anaesthesia. 2017;72:233-247.
  • 8. Laso-Morales M, Jericó C, Gómez-Ramírez S, et al. Preoperative management of colorectal cancer-induced iron deficiency anemia in clinical practice: data from a large observational cohort. Transfusion. 2017;57:3040-3048.
  • 9. Unal D, Senayli Y, Polat R, et al. Peri-operative blood transfusion in elective major surgery: incidence, indications and outcome - an observational multicentre study. Blood Transfus. 2020;18:261-279.
  • 10. Dell-Kuster S, Gomes NV, Gawria L, et al. Prospective validation of classification of intraoperative adverse events (ClassIntra): international, multicentre cohort study. BMJ. 2020;370:m2917.
  • 11. Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187- 196.
  • 12. Wilson MJ, Dekker JW, Bruns E, et al. Short-term effect of preoperative intravenous iron therapy in colorectal cancer patients with anemia: results of a cohort study. Transfusion. 2018;58:795-803.
  • 13. Ploug M, Kroijer R, Qvist N, et al. Iron deficiency in colorectal cancer patients: a cohort study on prevalence and associations. Colorectal Dis. 2021;23:853-859.
  • 14. Spahn DR, Muñoz M, Klein AA, et al. Patient Blood Management: Effectiveness and Future Potential. Anesthesiology. 2020;133:212-222.
  • 15. Althoff FC, Neb H, Herrmann E, et al. Multimodal Patient Blood Management Program Based on a Three-pillar Strategy: A Systematic Review and Metaanalysis. Ann Surg. 2019;269:794-804.
  • 16. Mueller MM, Van Remoortel H, Meybohm P, et al. Patient Blood Management: Recommendations From the 2018 Frankfurt Consensus Conference. JAMA. 2019;321:983-997.
  • 17. Pang QY, An R, Liu HL. Perioperative transfusion and the prognosis of colorectal cancer surgery: a systematic review and meta-analysis. World J Surg Oncol. 2019;17:7.
  • 18. Väyrynen JP, Tuomisto A, Väyrynen SA, et al. Preoperative anemia in colorectal cancer: relationships with tumor characteristics, systemic inflammation, and survival. Sci Rep. 2018;8:1126.
  • 19. Aapro M, Beguin Y, Bokemeyer C, et al. Management of anaemia and iron deficiency in patients with cancer: ESMO Clinical Practice Guidelines. Ann Oncol. 2018;29(Suppl 4):iv271.
  • 20. Tartter PI. The association of perioperative blood transfusion with colorectal cancer recurrence. Ann Surg. 1992;216:633-638.
  • 21. Aguilar-Nascimento JE, Zampieri-Filho JP, Bordin JO. Implications of perioperative allogeneic red blood cell transfusion on the immuneinflammatory response. Hematol Transfus Cell Ther. 2021;43:58-64.
  • 22. Pasricha SR, Tye-Din J, Muckenthaler MU, et al. Iron deficiency. Lancet. 2021;397:233-248.
  • 23. Kotzé A, Harris A, Baker C, et al. British Committee for Standards in Haematology Guidelines on the Identification and Management of PreOperative Anaemia. Br J Haematol. 2015;171:322-331.
  • 24. Neef V, Baumgarten P, Noone S, et al. The impact of timing of intravenous iron supplementation on preoperative haemoglobin in patients scheduled for major surgery. Blood Transfus. 2022;20:188-197.
  • 25. Ng O, Keeler BD, Mishra A, et al. Iron therapy for pre-operative anaemia. Cochrane Database Syst Rev. 2015;22:CD011588.
  • 26. Keeler BD, Simpson JA, Ng O, et al. Randomized clinical trial of preoperative oral versus intravenous iron in anaemic patients with colorectal cancer. Br J Surg. 2017;104:214-221.
  • 27. Benson CS, Shah A, Stanworth SJ, et al. The effect of iron deficiency and anaemia on women’s health. Anaesthesia. 2021;76 Suppl 4:84-95.
  • 28. Keeler BD, Dickson EA, Simpson JA, et al. The impact of pre-operative intravenous iron on quality of life after colorectal cancer surgery: outcomes from the intravenous iron in colorectal cancer-associated anaemia (IVICA) trial. Anaesthesia. 2019;74:714-725.
  • 29. Dickson EA, Keeler BD, Ng O, et al. Preoperative intravenous iron therapy and survival after colorectal cancer surgery: long-term results from the IVICA randomised controlled trial. Colorectal Dis. 2020;22:2018-2027.
  • 30. Quinn EM, Meland E, McGinn S, et al. Correction of iron-deficiency anaemia in colorectal surgery reduces perioperative transfusion rates: A before and after study. Int J Surg. 2017;38:1-8.
  • 31. Richards T, Baikady RR, Clevenger B, et al. Preoperative intravenous iron for anaemia in elective major open abdominal surgery: the PREVENTT RCT. Health Technol Assess. 2021;25:1-58.
  • 32. Talboom K, Borstlap WAA, Roodbeen SX, et al. Ferric carboxymaltose infusion versus oral iron supplementation for preoperative iron deficiency anaemia in patients with colorectal cancer (FIT): a multicentre, open-label, randomised, controlled trial. Lancet Haematol. 2023;10:e250-e260.
  • 33. Richards T, Baikady RR, Clevenger B, et al. Preoperative intravenous iron to treat anaemia before major abdominal surgery (PREVENTT): a randomised, double-blind, controlled trial. Lancet. 2020;396:1353-1361.
  • 34. Ploug M, Kroijer R, Qvist N, et al. Preoperative Intravenous Iron Treatment in Colorectal Cancer: Experience From Clinical Practice. J Surg Res. 2022;277:37-43.
  • 35. Goodnough LT, Maniatis A, Earnshaw P, et al. Detection, evaluation, and management of preoperative anaemia in the elective orthopaedic surgical patient: NATA guidelines. Br J Anaesth. 2011;106:13-22.
  • 36. Kozek-Langenecker SA, Afshari A, Albaladejo P, et al. Management of severe perioperative bleeding: guidelines from the European Society of Anaesthesiology. Eur J Anaesthesiol. 2013;30:270-382.
  • 37. Cacoub P, Choukroun G, Cohen-Solal A, et al. Towards a Common Definition for the Diagnosis of Iron Deficiency in Chronic Inflammatory Diseases. Nutrients. 2022;14:1039
  • 38. Corwin HL, Gettinger A, Pearl RG, et al. The CRIT Study: Anemia and blood transfusion in the critically ill--current clinical practice in the United States. Crit Care Med. 2004;32:39-52.
  • 39. Girelli D, Nemeth E, Swinkels DW. Hepcidin in the diagnosis of iron disorders. Blood. 2016;127:2809-2813.
  • 40. Lasocki S, Lefebvre T, Mayeur C, et al. Iron deficiency diagnosed using hepcidin on critical care discharge is an independent risk factor for death and poor quality of life at one year: an observational prospective study on 1161 patients. Crit Care. 2018;22:314.

Kolorektal Kanser Cerrahisi Geçiren Anemik Hastalarda Preoperatif İntravenöz Demir Tedavisinin Taburculuk Sonrası Anemi İnsidansına Etkisi

Year 2023, Volume: 76 Issue: 4, 340 - 347, 05.04.2024

Abstract

Amaç: Kolorektal kanserin doğasında olan bozulmuş demir metabolizması ve artan kan kayıpları nedeniyle demir eksikliği anemisi oldukça sık görülmektedir. Bu araştırmanın primer amacı; preoperatif anestezi değerlendirmesinde anemisi tespit edilen ve intravenöz demir tedavisi uygulandıktan kısa süre sonra cerrahiye alınan kolorektal kanserli hastalarda cerrahi öncesinde uygulanan demir tedavisinin postoperatif anemi insidansına yarattığı etkiyi ortaya koymaktır.

Gereç ve Yöntem: Araştırmaya 01 Ocak-31 Ağustos 2023 tarihleri arasında kolorektal kanser cerrahisi geçiren 40 hastanın verisi dahil edildi. Hastaların demografik özellikleri, preoperatif hemoglobin ve ferritin düzeyleri, uygulanan intravenöz demir dozu, intraoperatif kanama miktarı, postoperatif erken dönemde, taburculukta ve taburculuktan sonraki 1. ve 3. ay ölçülen hemoglobin düzeyleri retrospektif olarak kaydedildi. Sayısal değişkenler ortalama ± SS, kategorik değişkenler sayı ve % ile sunuldu. Veriler Student’s t-testi ve Mann-Whitney U testi ile analiz edildi. Korelasyon analizi için Pearson’s r ve Spearman’s rho testi kullanıldı. İstatistiksel anlamlılık için alfa hata düzeyi %5 kabul edildi.

Bulgular: Preoperatif hemoglobin ve ferritin düzeyleri sırasıyla 11,9 g/dL ve 42,9 ng/mL idi. Preoperatif anemi prevelansı %80 bulundu. Hastaların postoperatif ve taburculuk hemoglobin düzeyleri, preoperatif hemoglobin düzeyleri karşılaştırıldığında sırasıyla yaklaşık ortalama 1 ve 1,8 g/dL’lik azalma tespit edildi. Postoperatif anemi insidansı %54,5 bulundu. Postoperatif hemoglobin düzeyi ile intravenöz demir dozunun pozitif korelasyonunun olduğu görüldü. Pre - Postoperatif hemoglobin farkı; ClassIntra, Clavien-Dindo skorları ve intraoperatif uygulanan sıvı miktarı ile pozitif korelasyon gösterdi. Üçüncü ayda anemik saptanan hastaların hastane yatışları boyunca daha fazla eritrosit süspansiyonuna ihtiyacı olduğu görüldü.

Sonuç: Kolorektal kanser cerrahisi hastalarında perioperatif dönemin herhangi bir aşamasında anemi tedavi edilmelidir. Her hasta için aneminin altında yatan çok faktörlü etiyolojinin ve patofizyolojinin araştırılması gereklidir.

References

  • 1. Calleja JL, Delgado S, del Val A, et al. Ferric carboxymaltose reduces transfusions and hospital stay in patients with colon cancer and anemia. Int J Colorectal Dis. 2016;31:543-551.
  • 2. Chardalias L, Papaconstantinou I, Gklavas A, et al. Iron Deficiency Anemia in Colorectal Cancer Patients: Is Preoperative Intravenous Iron Infusion Indicated? A Narrative Review of the Literature. Cancer Diagn Progn. 2023;3:163-168.
  • 3. Leichtle SW, Mouawad NJ, Lampman R, et al. Does preoperative anemia adversely affect colon and rectal surgery outcomes? J Am Coll Surg. 2011;212:187-194.
  • 4. Acheson AG, Brookes MJ, Spahn DR. Effects of allogeneic red blood cell transfusions on clinical outcomes in patients undergoing colorectal cancer surgery: a systematic review and meta-analysis. Ann Surg. 2012;256:235- 244.
  • 5. Amin MB, Greene FL, Edge SB, et al. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67:93-99.
  • 6. Warner MA, Shore-Lesserson L, Shander A, et al. Perioperative Anemia: Prevention, Diagnosis, and Management Throughout the Spectrum of Perioperative Care. Anesth Analg. 2020;130:1364-1380.
  • 7. Muñoz M, Acheson AG, Auerbach M, et al. International consensus statement on the peri-operative management of anaemia and iron deficiency. Anaesthesia. 2017;72:233-247.
  • 8. Laso-Morales M, Jericó C, Gómez-Ramírez S, et al. Preoperative management of colorectal cancer-induced iron deficiency anemia in clinical practice: data from a large observational cohort. Transfusion. 2017;57:3040-3048.
  • 9. Unal D, Senayli Y, Polat R, et al. Peri-operative blood transfusion in elective major surgery: incidence, indications and outcome - an observational multicentre study. Blood Transfus. 2020;18:261-279.
  • 10. Dell-Kuster S, Gomes NV, Gawria L, et al. Prospective validation of classification of intraoperative adverse events (ClassIntra): international, multicentre cohort study. BMJ. 2020;370:m2917.
  • 11. Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187- 196.
  • 12. Wilson MJ, Dekker JW, Bruns E, et al. Short-term effect of preoperative intravenous iron therapy in colorectal cancer patients with anemia: results of a cohort study. Transfusion. 2018;58:795-803.
  • 13. Ploug M, Kroijer R, Qvist N, et al. Iron deficiency in colorectal cancer patients: a cohort study on prevalence and associations. Colorectal Dis. 2021;23:853-859.
  • 14. Spahn DR, Muñoz M, Klein AA, et al. Patient Blood Management: Effectiveness and Future Potential. Anesthesiology. 2020;133:212-222.
  • 15. Althoff FC, Neb H, Herrmann E, et al. Multimodal Patient Blood Management Program Based on a Three-pillar Strategy: A Systematic Review and Metaanalysis. Ann Surg. 2019;269:794-804.
  • 16. Mueller MM, Van Remoortel H, Meybohm P, et al. Patient Blood Management: Recommendations From the 2018 Frankfurt Consensus Conference. JAMA. 2019;321:983-997.
  • 17. Pang QY, An R, Liu HL. Perioperative transfusion and the prognosis of colorectal cancer surgery: a systematic review and meta-analysis. World J Surg Oncol. 2019;17:7.
  • 18. Väyrynen JP, Tuomisto A, Väyrynen SA, et al. Preoperative anemia in colorectal cancer: relationships with tumor characteristics, systemic inflammation, and survival. Sci Rep. 2018;8:1126.
  • 19. Aapro M, Beguin Y, Bokemeyer C, et al. Management of anaemia and iron deficiency in patients with cancer: ESMO Clinical Practice Guidelines. Ann Oncol. 2018;29(Suppl 4):iv271.
  • 20. Tartter PI. The association of perioperative blood transfusion with colorectal cancer recurrence. Ann Surg. 1992;216:633-638.
  • 21. Aguilar-Nascimento JE, Zampieri-Filho JP, Bordin JO. Implications of perioperative allogeneic red blood cell transfusion on the immuneinflammatory response. Hematol Transfus Cell Ther. 2021;43:58-64.
  • 22. Pasricha SR, Tye-Din J, Muckenthaler MU, et al. Iron deficiency. Lancet. 2021;397:233-248.
  • 23. Kotzé A, Harris A, Baker C, et al. British Committee for Standards in Haematology Guidelines on the Identification and Management of PreOperative Anaemia. Br J Haematol. 2015;171:322-331.
  • 24. Neef V, Baumgarten P, Noone S, et al. The impact of timing of intravenous iron supplementation on preoperative haemoglobin in patients scheduled for major surgery. Blood Transfus. 2022;20:188-197.
  • 25. Ng O, Keeler BD, Mishra A, et al. Iron therapy for pre-operative anaemia. Cochrane Database Syst Rev. 2015;22:CD011588.
  • 26. Keeler BD, Simpson JA, Ng O, et al. Randomized clinical trial of preoperative oral versus intravenous iron in anaemic patients with colorectal cancer. Br J Surg. 2017;104:214-221.
  • 27. Benson CS, Shah A, Stanworth SJ, et al. The effect of iron deficiency and anaemia on women’s health. Anaesthesia. 2021;76 Suppl 4:84-95.
  • 28. Keeler BD, Dickson EA, Simpson JA, et al. The impact of pre-operative intravenous iron on quality of life after colorectal cancer surgery: outcomes from the intravenous iron in colorectal cancer-associated anaemia (IVICA) trial. Anaesthesia. 2019;74:714-725.
  • 29. Dickson EA, Keeler BD, Ng O, et al. Preoperative intravenous iron therapy and survival after colorectal cancer surgery: long-term results from the IVICA randomised controlled trial. Colorectal Dis. 2020;22:2018-2027.
  • 30. Quinn EM, Meland E, McGinn S, et al. Correction of iron-deficiency anaemia in colorectal surgery reduces perioperative transfusion rates: A before and after study. Int J Surg. 2017;38:1-8.
  • 31. Richards T, Baikady RR, Clevenger B, et al. Preoperative intravenous iron for anaemia in elective major open abdominal surgery: the PREVENTT RCT. Health Technol Assess. 2021;25:1-58.
  • 32. Talboom K, Borstlap WAA, Roodbeen SX, et al. Ferric carboxymaltose infusion versus oral iron supplementation for preoperative iron deficiency anaemia in patients with colorectal cancer (FIT): a multicentre, open-label, randomised, controlled trial. Lancet Haematol. 2023;10:e250-e260.
  • 33. Richards T, Baikady RR, Clevenger B, et al. Preoperative intravenous iron to treat anaemia before major abdominal surgery (PREVENTT): a randomised, double-blind, controlled trial. Lancet. 2020;396:1353-1361.
  • 34. Ploug M, Kroijer R, Qvist N, et al. Preoperative Intravenous Iron Treatment in Colorectal Cancer: Experience From Clinical Practice. J Surg Res. 2022;277:37-43.
  • 35. Goodnough LT, Maniatis A, Earnshaw P, et al. Detection, evaluation, and management of preoperative anaemia in the elective orthopaedic surgical patient: NATA guidelines. Br J Anaesth. 2011;106:13-22.
  • 36. Kozek-Langenecker SA, Afshari A, Albaladejo P, et al. Management of severe perioperative bleeding: guidelines from the European Society of Anaesthesiology. Eur J Anaesthesiol. 2013;30:270-382.
  • 37. Cacoub P, Choukroun G, Cohen-Solal A, et al. Towards a Common Definition for the Diagnosis of Iron Deficiency in Chronic Inflammatory Diseases. Nutrients. 2022;14:1039
  • 38. Corwin HL, Gettinger A, Pearl RG, et al. The CRIT Study: Anemia and blood transfusion in the critically ill--current clinical practice in the United States. Crit Care Med. 2004;32:39-52.
  • 39. Girelli D, Nemeth E, Swinkels DW. Hepcidin in the diagnosis of iron disorders. Blood. 2016;127:2809-2813.
  • 40. Lasocki S, Lefebvre T, Mayeur C, et al. Iron deficiency diagnosed using hepcidin on critical care discharge is an independent risk factor for death and poor quality of life at one year: an observational prospective study on 1161 patients. Crit Care. 2018;22:314.
There are 40 citations in total.

Details

Primary Language English
Subjects Intensive Care
Journal Section Research Article
Authors

Hakan Yılmaz

Ayşegül Güven This is me 0000-0002-7837-7655

Submission Date October 10, 2023
Acceptance Date October 17, 2023
Publication Date April 5, 2024
Published in Issue Year 2023 Volume: 76 Issue: 4

Cite

APA Yılmaz, H., & Güven, A. (2024). The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery. Ankara Üniversitesi Tıp Fakültesi Mecmuası, 76(4), 340-347. https://doi.org/10.4274/atfm.galenos.2023.42103
AMA Yılmaz H, Güven A. The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery. Ankara Üniversitesi Tıp Fakültesi Mecmuası. July 2024;76(4):340-347. doi:10.4274/atfm.galenos.2023.42103
Chicago Yılmaz, Hakan, and Ayşegül Güven. “The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery”. Ankara Üniversitesi Tıp Fakültesi Mecmuası 76, no. 4 (July 2024): 340-47. https://doi.org/10.4274/atfm.galenos.2023.42103.
EndNote Yılmaz H, Güven A (July 1, 2024) The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery. Ankara Üniversitesi Tıp Fakültesi Mecmuası 76 4 340–347.
IEEE H. Yılmaz and A. Güven, “The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery”, Ankara Üniversitesi Tıp Fakültesi Mecmuası, vol. 76, no. 4, pp. 340–347, 2024, doi: 10.4274/atfm.galenos.2023.42103.
ISNAD Yılmaz, Hakan - Güven, Ayşegül. “The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery”. Ankara Üniversitesi Tıp Fakültesi Mecmuası 76/4 (July2024), 340-347. https://doi.org/10.4274/atfm.galenos.2023.42103.
JAMA Yılmaz H, Güven A. The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery. Ankara Üniversitesi Tıp Fakültesi Mecmuası. 2024;76:340–347.
MLA Yılmaz, Hakan and Ayşegül Güven. “The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery”. Ankara Üniversitesi Tıp Fakültesi Mecmuası, vol. 76, no. 4, 2024, pp. 340-7, doi:10.4274/atfm.galenos.2023.42103.
Vancouver Yılmaz H, Güven A. The Effect of Preoperative Intravenous Iron Therapy on Postdischarge Incidence of Anemia in Anemic Patients Undergoing Colorectal Cancer Surgery. Ankara Üniversitesi Tıp Fakültesi Mecmuası. 2024;76(4):340-7.