Research Article
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Can plasma fibrinogen level predict bone marrow fibrosis?

Year 2023, Volume: 36 Issue: 1, 80 - 86, 31.01.2023
https://doi.org/10.5472/marumj.1244611

Abstract

Objective: We aimed to assess the possible relationship between plasma fibrinogen level and bone marrow fibrosis (BMF) grades in
patients who had undergone bone marrow (BM) biopsy for any reason.
Patients and Method: This retrospective cohort study included 106 participants aged 18 years and over who had undergone
simultaneous BM biopsy and circulatory fibrinogen level measurement during 2020 and 2021 at our center. BMF grade was measured
by the modified Bauermeister grading system (MBGS). Participants were divided into two groups according to MBGS as those without
BMF and those with BMF.
Results: Fifty-eight male were included in our study, and the median age of the patients was 63 (range: 19-97) years. Fibrinogen
(p=0.004) and lactate dehydrogenase (LDH) (p=0.030) levels were significantly higher in the fibrosis group. Multiple regression
revealed that high fibrinogen (≥359) and high LDH (≥238) were independently associated with a higher likelihood of fibrosis presence
(adjusted for age and sex); however, diagnostic analyses revealed low accuracy.
Conclusion: High plasma fibrinogen and LDH levels were found to be independently associated with the presence of BMF. However,
it was also evident that neither of these parameters could be used for diagnostic purposes.

References

  • Inagawa Y, Komeno Y, Saito S, et al. Prolonged myelosuppression due to progressive bone marrow fibrosis in a patient with acute promyelocytic leukemia. Case Reports in Hematol 2019; 2019: 1616237. doi: 10.1155/2019/1616237.
  • Leiva O, Leon C, Kah Ng S, Mangin P, Gachet C, Ravid K. The role of extracellular matrix stiffness in megakaryocyte and platelet development and function. Am J Hematol 2018; 93: 430-41. doi: 10.1002/ajh.25008.
  • Rizvi H, Butler T, Calaminici M, et al. United Kingdom immune thrombocytopenia registry: retrospective evaluation of bone marrow fibrosis in adult patients with primary immune thrombocytopenia and correlation with clinical findings. Br J Haematol 2015; 169: 590-4. doi: 10.1111/bjh.13330.
  • Narang NC, Rusia U, Sikka M, Kotru M. Morphological changes in bone marrow post imatinib therapy in chronic phase CML: a follow up study on sequential bone marrow aspirates and biopsies. J Clin Diagn Res 2017; 11: EC25-9. doi: 10.7860/JCDR/2017/25173.9650.
  • Della Porta MG, Malcovati L, Boveri E, et al. Clinical relevance of bone marrow fibrosis and CD34-positive cell clusters in primary myelodysplastic syndromes. J Clin Oncol 2009; 27: 754-62. doi: 10.1200/JCO.2008.18.2246.
  • Tu M, Hu S, Lou Z. A high value of fibrinogen in immunoglobulin A nephropathy patients is associated with a worse renal tubular atrophy/interstitial fibrosis score. J Clin Lab Anal 2022; 36: e24120. doi: 10.1002/jcla.24120.
  • Sörensen I, Susnik N, Inhester T, et al. Fibrinogen, acting as a mitogen for tubulointerstitial fibroblasts, promotes renal fibrosis. Kidney Int 2011; 80: 1035-44. doi: 10.1038/ ki.2011.214.
  • De Giorgio-Miller A, Bottoms S, Laurent G, Carmeliet P, Herrick S. Fibrin-induced skin fibrosis in mice deficient in tissue plasminogen activator. Am J Pathol 2005; 167: 721-32. doi: 10.1016/s0002-9440(10)62046-9.
  • Ahmed HH, Amer MS, Salem NA, Abou El-Fadl HM. Therapeutic implications of bone marrow mesenchymal stem cells in experimental liver fibrosis. World J Pharm Res 2013; 2: 1971-98.
  • Masamune A, Kikuta K, Watanabe T, et al. Fibrinogen induces cytokine and collagen production in pancreatic stellate cells. Gut 2009; 58: 550-9. doi: 10.1136/gut.2008.154401.
  • Vidal B, Serrano AL, Tjwa M, et al. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev 2008; 22: 1747- 52. doi: 10.1101/gad.465908.
  • Li FJ, Surolia R, Singh P, et al. Fibrinogen mediates cadmiuminduced macrophage activation and serves as a predictor of cadmium exposure in chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 2022; 322: L593-l606. doi: 10.1152/ajplung.00475.2021.
  • Reshma VJ, Anwar AS, Mufeed A, Roshni A. Estimation of plasma fibrinogen degradation products in oral submucous fibrosis: A clinico-pathological study. J Int Soc Prev Community Dent 2015; 5: 309-13. doi: 10.4103/2231- 0762.161760.
  • Zhang Y, Xin Q, Wu Z, et al. Application of isobaric tags for relative and absolute quantification (iTRAQ) coupled with two-dimensional liquid chromatography/tandem mass spectrometry in quantitative proteomic analysis for discovery of serum biomarkers for idiopathic pulmonary fibrosis. Med Sci Monit 2018; 24: 4146-53. doi: 10.12659/MSM.908702.
  • Sogawa K, Noda K, Umemura H, et al. Serum fibrinogen alpha C‐chain 5.9 k D a fragment as a biomarker for early detection of hepatic fibrosis related to hepatitis C virus. Proteomics Clin Appl 2013; 7: 424-31. doi: 10.1002/prca.201200094.
  • Yu X, Hu F, Yao Q, Li C, Zhang H, Xue Y. Serum fibrinogen levels are positively correlated with advanced tumor stage and poor survival in patients with gastric cancer undergoing gastrectomy: a large cohort retrospective study. BMC Cancer 2016; 16: 480. doi: 10.1186/s12885.016.2510-z.
  • Bauermeister DE. Quantitation of bone marrow reticulin—a normal range. Am J Clin Pathol 1971; 56: 24-31. doi: 10.1093/ ajcp/56.1.24.
  • Kuter DJ, Bain B, Mufti G, Bagg A, Hasserjian RP. Bone marrow fibrosis: pathophysiology and clinical significance of increased bone marrow stromal fibres. Br J Haematol 2007; 139: 351-62. doi: 10.1111/j.1365-2141.2007.06807.x.
  • Thiele J, Grashof K, Fisher R. Follow-up study on bone marrow reticulin fibrosis in AML. Anal Cell Pathol 1991; 3: 225-31. PMID: 1883746
  • Thiele J, Kvasnicka HM, Facchetti F, Franco V, Van Der Walt J, Orazi A. European consensus on grading bone marrow fibrosis and assessment of cellularity. Haematologica 2005; 90: 1128-32. PMID: 16079113
  • O’malley DP, Sen J, Juliar BE, Orazi A. Evaluation of stroma in human immunodeficiency virus/acquired immunodeficiency syndrome–affected bone marrows and correlation with CD4 counts. Arch Pathol Lab Med 2005; 129: 1137-40. doi: 10.5858/2005.129.1137-EOSIHI.
  • Bain BJ, Clark DM, Wilkins BS. Bone marrow pathology: John Wiley & Sons, 2019.
  • Tefferi A. Pathogenesis of myelofibrosis with myeloid metaplasia. J Clin Oncol 2005; 23: 8520-30. doi: 10.1200/ JCO.2004.00.9316.
  • Buesche G, Ganser A, Schlegelberger B, et al. Marrow fibrosis and its relevance during imatinib treatment of chronic myeloid leukemia. Leukemia 2007; 21: 2420-7. doi: 10.1038/ sj.leu.2404917.
  • Tadmor T, Shvidel L, Aviv A, et al. Significance of bone marrow reticulin fibrosis in chronic lymphocytic leukemia at diagnosis: a study of 176 patients with prognostic implications. Cancer 2013; 119: 1853-9. doi: 10.1002/cncr.27930.
  • Liu B, Limback J, Kendall M, et al. Safety of CT-Guided Bone Marrow Biopsy in Thrombocytopenic Patients: A Retrospective Review. J Vasc Interv Radiol 2017; 28: 1727-31. doi: 10.1016/j.jvir.2017.08.009.
  • Lowenthal RM, Taylor BV, Jones R, Beasley A. Severe persistent sciatic pain and weakness due to a gluteal artery pseudoaneurysm as a complication of bone marrow biopsy. J Clin Neurosci 2006; 13: 384-5. doi: 10.1016/j.jocn.2005.03.027.
  • Shehata M, Schwarzmeier JD, Hilgarth M, Hubmann R, Duechler M, Gisslinger H. TGF-β1 induces bone marrow reticulin fibrosis in hairy cell leukemia. J Clin Invest 2004; 113: 676-85. doi: 10.1172/JCI19540.
  • Hasselbalch H, Junker P, Lisse I, Bentsen KD. Serum procollagen III peptide in chronic myeloproliferative disorders. Scand J Haematol 1985; 35: 550-7. doi: 10.1111/ j.1600-0609.1985.tb02827.x.
  • Abou Zahr A, Salama ME, Carreau N, et al. Bone marrow fibrosis in myelofibrosis: pathogenesis, prognosis and targeted strategies. Haematologica 2016; 101: 660-71. doi: 10.3324/ haematol.2015.141283.
  • Cattoretti G, Schiró R, Orazi A, Soligo D, Colombo MP. Bone marrow stroma in humans: anti-nerve growth factor receptor antibodies selectively stain reticular cells in vivo and in vitro. Blood 1993; 81: 1726-38. PMID: 7681701
  • Hasselbalch HC. The role of cytokines in the initiation and progression of myelofibrosis. Cytokine Growth Factor Rev 2013; 24: 133-45. doi: 10.1016/j.cytogfr.2013.01.004.
  • Castro-Malaspina H, Rabellino EM, Yen A, Nachman RL, Moore M. Human megakaryocyte stimulation of proliferation of bone marrow fibroblasts 1981; 57: 781-7. PMID: 7470627
  • Breton-Gorius J, Bizet M, Reyes F, et al. Myelofibrosis and acute megakaryoblastic leukemia in a child: topographic relationship between fibroblasts and megakaryocytes with an α-granule defect. Leuk Res 1982; 6: 97-110. doi: 10.1016/0145- 2126(82)90048-0.
  • Schmitt A, Jouault H, Guichard J, Wendling F, Drouin A, Cramer EM. Pathologic interaction between megakaryocytes and polymorphonuclear leukocytes in myelofibrosis. Blood 2000; 96: 1342-7. PMID: 10942376
  • Schepers K, Pietras EM, Reynaud D, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 2013; 13: 285- 99. doi: 10.1016/j.stem.2013.06.009.
  • Kikuchi T, Shimizu T, Toyama T, Abe R, Okamoto S. Successful treatment of TAFRO syndrome with tocilizumab, prednisone, and cyclophosphamide. Intern Med 2017: 8522-16.
  • Herrick S, Blanc-Brude O, Gray A, Laurent G. Fibrinogen. Int J Biochem Cell Biol 1999; 31: 741-6. doi: 10.1016/s1357- 2725(99)00032-1.
  • Greiling D, Clark RA. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci 1997; 110 ( Pt 7): 861-70. doi: 10.1242/jcs.110.7.861.
  • Héron A, Lévesque JP, Hatzfeld A, et al. Mitogenic effect of fibrinogen on hematopoietic cells: involvement of two distinct specific receptors, MFR and ICAM-1. Biochem Biophys Res Commun 1998; 246: 231-7. doi: 10.1006/bbrc.1998.8583.
  • Wilberding JA, Ploplis VA, Mclennan L, et al. Development of pulmonary fibrosis in fibrinogen-deficient mice. Ann N Y Acad Sci 2001; 936: 542-8. doi: 10.1111/j.1749-6632.2001. tb03542.x.
  • Ploplis VA, Wilberding J, Mclennan L, et al. A total fibrinogen deficiency is compatible with the development of pulmonary fibrosis in mice. Am J Pathol 2000; 157: 703-8. doi: 10.1016/ s0002-9440(10)64582-8.
Year 2023, Volume: 36 Issue: 1, 80 - 86, 31.01.2023
https://doi.org/10.5472/marumj.1244611

Abstract

References

  • Inagawa Y, Komeno Y, Saito S, et al. Prolonged myelosuppression due to progressive bone marrow fibrosis in a patient with acute promyelocytic leukemia. Case Reports in Hematol 2019; 2019: 1616237. doi: 10.1155/2019/1616237.
  • Leiva O, Leon C, Kah Ng S, Mangin P, Gachet C, Ravid K. The role of extracellular matrix stiffness in megakaryocyte and platelet development and function. Am J Hematol 2018; 93: 430-41. doi: 10.1002/ajh.25008.
  • Rizvi H, Butler T, Calaminici M, et al. United Kingdom immune thrombocytopenia registry: retrospective evaluation of bone marrow fibrosis in adult patients with primary immune thrombocytopenia and correlation with clinical findings. Br J Haematol 2015; 169: 590-4. doi: 10.1111/bjh.13330.
  • Narang NC, Rusia U, Sikka M, Kotru M. Morphological changes in bone marrow post imatinib therapy in chronic phase CML: a follow up study on sequential bone marrow aspirates and biopsies. J Clin Diagn Res 2017; 11: EC25-9. doi: 10.7860/JCDR/2017/25173.9650.
  • Della Porta MG, Malcovati L, Boveri E, et al. Clinical relevance of bone marrow fibrosis and CD34-positive cell clusters in primary myelodysplastic syndromes. J Clin Oncol 2009; 27: 754-62. doi: 10.1200/JCO.2008.18.2246.
  • Tu M, Hu S, Lou Z. A high value of fibrinogen in immunoglobulin A nephropathy patients is associated with a worse renal tubular atrophy/interstitial fibrosis score. J Clin Lab Anal 2022; 36: e24120. doi: 10.1002/jcla.24120.
  • Sörensen I, Susnik N, Inhester T, et al. Fibrinogen, acting as a mitogen for tubulointerstitial fibroblasts, promotes renal fibrosis. Kidney Int 2011; 80: 1035-44. doi: 10.1038/ ki.2011.214.
  • De Giorgio-Miller A, Bottoms S, Laurent G, Carmeliet P, Herrick S. Fibrin-induced skin fibrosis in mice deficient in tissue plasminogen activator. Am J Pathol 2005; 167: 721-32. doi: 10.1016/s0002-9440(10)62046-9.
  • Ahmed HH, Amer MS, Salem NA, Abou El-Fadl HM. Therapeutic implications of bone marrow mesenchymal stem cells in experimental liver fibrosis. World J Pharm Res 2013; 2: 1971-98.
  • Masamune A, Kikuta K, Watanabe T, et al. Fibrinogen induces cytokine and collagen production in pancreatic stellate cells. Gut 2009; 58: 550-9. doi: 10.1136/gut.2008.154401.
  • Vidal B, Serrano AL, Tjwa M, et al. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev 2008; 22: 1747- 52. doi: 10.1101/gad.465908.
  • Li FJ, Surolia R, Singh P, et al. Fibrinogen mediates cadmiuminduced macrophage activation and serves as a predictor of cadmium exposure in chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 2022; 322: L593-l606. doi: 10.1152/ajplung.00475.2021.
  • Reshma VJ, Anwar AS, Mufeed A, Roshni A. Estimation of plasma fibrinogen degradation products in oral submucous fibrosis: A clinico-pathological study. J Int Soc Prev Community Dent 2015; 5: 309-13. doi: 10.4103/2231- 0762.161760.
  • Zhang Y, Xin Q, Wu Z, et al. Application of isobaric tags for relative and absolute quantification (iTRAQ) coupled with two-dimensional liquid chromatography/tandem mass spectrometry in quantitative proteomic analysis for discovery of serum biomarkers for idiopathic pulmonary fibrosis. Med Sci Monit 2018; 24: 4146-53. doi: 10.12659/MSM.908702.
  • Sogawa K, Noda K, Umemura H, et al. Serum fibrinogen alpha C‐chain 5.9 k D a fragment as a biomarker for early detection of hepatic fibrosis related to hepatitis C virus. Proteomics Clin Appl 2013; 7: 424-31. doi: 10.1002/prca.201200094.
  • Yu X, Hu F, Yao Q, Li C, Zhang H, Xue Y. Serum fibrinogen levels are positively correlated with advanced tumor stage and poor survival in patients with gastric cancer undergoing gastrectomy: a large cohort retrospective study. BMC Cancer 2016; 16: 480. doi: 10.1186/s12885.016.2510-z.
  • Bauermeister DE. Quantitation of bone marrow reticulin—a normal range. Am J Clin Pathol 1971; 56: 24-31. doi: 10.1093/ ajcp/56.1.24.
  • Kuter DJ, Bain B, Mufti G, Bagg A, Hasserjian RP. Bone marrow fibrosis: pathophysiology and clinical significance of increased bone marrow stromal fibres. Br J Haematol 2007; 139: 351-62. doi: 10.1111/j.1365-2141.2007.06807.x.
  • Thiele J, Grashof K, Fisher R. Follow-up study on bone marrow reticulin fibrosis in AML. Anal Cell Pathol 1991; 3: 225-31. PMID: 1883746
  • Thiele J, Kvasnicka HM, Facchetti F, Franco V, Van Der Walt J, Orazi A. European consensus on grading bone marrow fibrosis and assessment of cellularity. Haematologica 2005; 90: 1128-32. PMID: 16079113
  • O’malley DP, Sen J, Juliar BE, Orazi A. Evaluation of stroma in human immunodeficiency virus/acquired immunodeficiency syndrome–affected bone marrows and correlation with CD4 counts. Arch Pathol Lab Med 2005; 129: 1137-40. doi: 10.5858/2005.129.1137-EOSIHI.
  • Bain BJ, Clark DM, Wilkins BS. Bone marrow pathology: John Wiley & Sons, 2019.
  • Tefferi A. Pathogenesis of myelofibrosis with myeloid metaplasia. J Clin Oncol 2005; 23: 8520-30. doi: 10.1200/ JCO.2004.00.9316.
  • Buesche G, Ganser A, Schlegelberger B, et al. Marrow fibrosis and its relevance during imatinib treatment of chronic myeloid leukemia. Leukemia 2007; 21: 2420-7. doi: 10.1038/ sj.leu.2404917.
  • Tadmor T, Shvidel L, Aviv A, et al. Significance of bone marrow reticulin fibrosis in chronic lymphocytic leukemia at diagnosis: a study of 176 patients with prognostic implications. Cancer 2013; 119: 1853-9. doi: 10.1002/cncr.27930.
  • Liu B, Limback J, Kendall M, et al. Safety of CT-Guided Bone Marrow Biopsy in Thrombocytopenic Patients: A Retrospective Review. J Vasc Interv Radiol 2017; 28: 1727-31. doi: 10.1016/j.jvir.2017.08.009.
  • Lowenthal RM, Taylor BV, Jones R, Beasley A. Severe persistent sciatic pain and weakness due to a gluteal artery pseudoaneurysm as a complication of bone marrow biopsy. J Clin Neurosci 2006; 13: 384-5. doi: 10.1016/j.jocn.2005.03.027.
  • Shehata M, Schwarzmeier JD, Hilgarth M, Hubmann R, Duechler M, Gisslinger H. TGF-β1 induces bone marrow reticulin fibrosis in hairy cell leukemia. J Clin Invest 2004; 113: 676-85. doi: 10.1172/JCI19540.
  • Hasselbalch H, Junker P, Lisse I, Bentsen KD. Serum procollagen III peptide in chronic myeloproliferative disorders. Scand J Haematol 1985; 35: 550-7. doi: 10.1111/ j.1600-0609.1985.tb02827.x.
  • Abou Zahr A, Salama ME, Carreau N, et al. Bone marrow fibrosis in myelofibrosis: pathogenesis, prognosis and targeted strategies. Haematologica 2016; 101: 660-71. doi: 10.3324/ haematol.2015.141283.
  • Cattoretti G, Schiró R, Orazi A, Soligo D, Colombo MP. Bone marrow stroma in humans: anti-nerve growth factor receptor antibodies selectively stain reticular cells in vivo and in vitro. Blood 1993; 81: 1726-38. PMID: 7681701
  • Hasselbalch HC. The role of cytokines in the initiation and progression of myelofibrosis. Cytokine Growth Factor Rev 2013; 24: 133-45. doi: 10.1016/j.cytogfr.2013.01.004.
  • Castro-Malaspina H, Rabellino EM, Yen A, Nachman RL, Moore M. Human megakaryocyte stimulation of proliferation of bone marrow fibroblasts 1981; 57: 781-7. PMID: 7470627
  • Breton-Gorius J, Bizet M, Reyes F, et al. Myelofibrosis and acute megakaryoblastic leukemia in a child: topographic relationship between fibroblasts and megakaryocytes with an α-granule defect. Leuk Res 1982; 6: 97-110. doi: 10.1016/0145- 2126(82)90048-0.
  • Schmitt A, Jouault H, Guichard J, Wendling F, Drouin A, Cramer EM. Pathologic interaction between megakaryocytes and polymorphonuclear leukocytes in myelofibrosis. Blood 2000; 96: 1342-7. PMID: 10942376
  • Schepers K, Pietras EM, Reynaud D, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 2013; 13: 285- 99. doi: 10.1016/j.stem.2013.06.009.
  • Kikuchi T, Shimizu T, Toyama T, Abe R, Okamoto S. Successful treatment of TAFRO syndrome with tocilizumab, prednisone, and cyclophosphamide. Intern Med 2017: 8522-16.
  • Herrick S, Blanc-Brude O, Gray A, Laurent G. Fibrinogen. Int J Biochem Cell Biol 1999; 31: 741-6. doi: 10.1016/s1357- 2725(99)00032-1.
  • Greiling D, Clark RA. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci 1997; 110 ( Pt 7): 861-70. doi: 10.1242/jcs.110.7.861.
  • Héron A, Lévesque JP, Hatzfeld A, et al. Mitogenic effect of fibrinogen on hematopoietic cells: involvement of two distinct specific receptors, MFR and ICAM-1. Biochem Biophys Res Commun 1998; 246: 231-7. doi: 10.1006/bbrc.1998.8583.
  • Wilberding JA, Ploplis VA, Mclennan L, et al. Development of pulmonary fibrosis in fibrinogen-deficient mice. Ann N Y Acad Sci 2001; 936: 542-8. doi: 10.1111/j.1749-6632.2001. tb03542.x.
  • Ploplis VA, Wilberding J, Mclennan L, et al. A total fibrinogen deficiency is compatible with the development of pulmonary fibrosis in mice. Am J Pathol 2000; 157: 703-8. doi: 10.1016/ s0002-9440(10)64582-8.
There are 42 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Original Research
Authors

Yildiz Ipek This is me 0000-0003-2952-2286

Ayse Nilgun Kul This is me 0000-0003-1806-2261

Publication Date January 31, 2023
Published in Issue Year 2023 Volume: 36 Issue: 1

Cite

APA Ipek, Y., & Kul, A. N. (2023). Can plasma fibrinogen level predict bone marrow fibrosis?. Marmara Medical Journal, 36(1), 80-86. https://doi.org/10.5472/marumj.1244611
AMA Ipek Y, Kul AN. Can plasma fibrinogen level predict bone marrow fibrosis?. Marmara Med J. January 2023;36(1):80-86. doi:10.5472/marumj.1244611
Chicago Ipek, Yildiz, and Ayse Nilgun Kul. “Can Plasma Fibrinogen Level Predict Bone Marrow Fibrosis?”. Marmara Medical Journal 36, no. 1 (January 2023): 80-86. https://doi.org/10.5472/marumj.1244611.
EndNote Ipek Y, Kul AN (January 1, 2023) Can plasma fibrinogen level predict bone marrow fibrosis?. Marmara Medical Journal 36 1 80–86.
IEEE Y. Ipek and A. N. Kul, “Can plasma fibrinogen level predict bone marrow fibrosis?”, Marmara Med J, vol. 36, no. 1, pp. 80–86, 2023, doi: 10.5472/marumj.1244611.
ISNAD Ipek, Yildiz - Kul, Ayse Nilgun. “Can Plasma Fibrinogen Level Predict Bone Marrow Fibrosis?”. Marmara Medical Journal 36/1 (January 2023), 80-86. https://doi.org/10.5472/marumj.1244611.
JAMA Ipek Y, Kul AN. Can plasma fibrinogen level predict bone marrow fibrosis?. Marmara Med J. 2023;36:80–86.
MLA Ipek, Yildiz and Ayse Nilgun Kul. “Can Plasma Fibrinogen Level Predict Bone Marrow Fibrosis?”. Marmara Medical Journal, vol. 36, no. 1, 2023, pp. 80-86, doi:10.5472/marumj.1244611.
Vancouver Ipek Y, Kul AN. Can plasma fibrinogen level predict bone marrow fibrosis?. Marmara Med J. 2023;36(1):80-6.