Morphological alterations of the bone marrow in patients with COVID-19. Systematic review and meta-analysis

Authors

  • Rafael Pichardo-Rodriguez Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.
  • Liz Cordova-Cueva Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.
  • Willy Peña-Oscuvilca Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.
  • Juan Jesús Bracamonte-Hernández Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.
  • Carlos Carrasco-Vergaray Facultad de Medicina, Universidad Nacional Mayor de San Marcos, Lima, Perú.
  • Marcos Saavedra-Velasco Centro de enfermedades Infecciosas (CEI), Lima, Perú
  • Oscar Ruiz-Franco Facultad de Medicina, Universidad Nacional Mayor de San Marcos, Lima, Perú

DOI:

https://doi.org/10.35434/rcmhnaaa.2022.15Supl.%201.1479

Keywords:

Bone Marrow, Hematopoiesis, COVID-19, SARS-CoV-2, Meta-Analysis, Systematic Review

Abstract

Introduction: Despite the fact that hematological alterations at the peripheral level are widely known, little is known about the alterations caused by COVID-19 at the bone marrow level. Objective: To determine the morphological alterations of the bone marrow caused by COVID-19. Material and methods: Systematic review and meta-analysis. Observational studies and reports and case series were included and editorials, reviews, letters to the editor were excluded. A search was performed in Pubmed, ScienceDirect and Scielo. The risk of bias was assessed using the NewCatell-Ottawa and Hassan Murad scales for case reports and series. The outcomes were the morphological parameters of the bone marrow. For the quantitative synthesis of the information, a proportion meta-analysis was performed using random effects in RStudio. Results: Hypercellularity occurred in 65% (95% CI: 51%-78%), maturation arrest of the myeloid series occurred in 57% (95% CI: 29%-83%). and the alteration of the M/E ratio occurred in 60% (95% CI: 46%-74%). Conclusion: The most frequent morphological alterations in the bone marrow were hypercellularity, arrest in myeloid maturation and alteration of the M/E ratio in patients with COVID-19.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Author Biographies

Rafael Pichardo-Rodriguez, Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.

Médico Residente de Hematología

Liz Cordova-Cueva, Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.

Médico Residente de Nefrología

Willy Peña-Oscuvilca, Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.

Médico especialista en Hematología

Juan Jesús Bracamonte-Hernández, Instituto de Investigaciones en Ciencias Biomédicas (INICIB), Universidad Ricardo Palma, Lima, Perú.

Estudiante de Medicina

Carlos Carrasco-Vergaray, Facultad de Medicina, Universidad Nacional Mayor de San Marcos, Lima, Perú.

Médico especialista en Hematología

Marcos Saavedra-Velasco, Centro de enfermedades Infecciosas (CEI), Lima, Perú

Médico especialista en Enfermedades infecciosas y Tropicales.

Oscar Ruiz-Franco, Facultad de Medicina, Universidad Nacional Mayor de San Marcos, Lima, Perú

Médico especialista en Hematología

References

Harris CK, Hung YP, Nielsen GP, Stone JR, Ferry JA. Bone Marrow and Peripheral Blood Findings in Patients Infected by SARS-CoV-2. Am J Clin Pathol. 2021;155(5):627–37. doi:10.1093/ajcp/aqaa274

Xu Z, Shi L, Wang Y, Zhang J, Huang L, Zhang C, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8(4):420–2. doi:10.1016/S2213-2600(20)30076-X

Rahman A, Niloofa R, Jayarajah U, Mel SD, Abeysuriya V, Seneviratne SL. Hematological Abnormalities in COVID-19: A Narrative Review. The American Journal of Tropical Medicine and Hygiene. 2021;104(4):1188–201. doi:10.4269/ajtmh.20-1536

Terpos E, Ntanasis-Stathopoulos I, Elalamy I, Kastritis E, Sergentanis TN, Politou M, et al. Hematological findings and complications of COVID-19. Am J Hematol. 2020;95(7):834–47. doi:10.1002/ajh.25829

Pichardo-Rodriguez R, Peña-Oscuvilca W, Diaz-Robles D, Mendoza-Sanchez D, Carrasco-Vergaray C, Garcia-Perdomo HA, et al. Características morfológicas de las médulas óseas en pacientes con infección por SARS-Cov2 del Hospital 2 de Mayo, Perú. Revista del Cuerpo Médico Hospital Nacional Almanzor Aguinaga Asenjo. 2021;14(3):352–6. doi:10.35434/rcmhnaaa.2021.143.1256

Swoboda J, Wittschieber D, Sanft J, Kleemann S, Elschner S, Ihle H, et al. Bone marrow haemophagocytosis indicates severe infection with severe acute respiratory syndrome coronavirus 2. Histopathology. 2021;78(5):727–37. doi:10.1111/his.14281

Duarte-Neto AN, Caldini EG, Gomes-Gouvêa MS, Kanamura CT, Monteiro RA de A, Ferranti JF, et al. An autopsy study of the spectrum of severe COVID-19 in children: From SARS to different phenotypes of MIS-C. eClinicalMedicine. 2021;35: 100850. doi:10.1016/j.eclinm.2021.100850

Ihlow J, Michaelis E, Greuel S, Heynol V, Lehmann A, Radbruch H, et al. B cell depletion and signs of sepsis-acquired immunodeficiency in bone marrow and spleen of COVID-19 deceased. International Journal of Infectious Diseases. 2021;103:628–35. doi:10.1016/j.ijid.2020.12.078

Roncati L, Ligabue G, Nasillo V, Lusenti B, Gennari W, Fabbiani L, et al. A proof of evidence supporting abnormal immunothrombosis in severe COVID-19: naked megakaryocyte nuclei increase in the bone marrow and lungs of critically ill patients. Platelets. 2020;31(8):1085–9. doi:10.1080/09537104.2020.1810224

Yepes-Nuñez JJ, Urrútia G, Romero-García M, Alonso-Fernández S. Declaración PRISMA 2020: una guía actualizada para la publicación de revisiones sistemáticas. Revista Española de Cardiología [Internet]. 2021 [citado el 6 de agosto de 2021];74 (9): 790-9. Doi:10.1016/j.recesp.2021.06.016

Norris JM, Simpson BS, Ball R, Freeman A, Kirkham A, Parry MA, et al. A Modified Newcastle-Ottawa Scale for Assessment of Study Quality in Genetic Urological Research. Eur Urol. 2021;79(3):325–6. doi:10.1016/j.eururo.2020.12.017

Modesti PA, Reboldi G, Cappuccio FP, Agyemang C, Remuzzi G, Rapi S, et al. Panethnic Differences in Blood Pressure in Europe: A Systematic Review and Meta-Analysis. PLOS ONE. 2016;11(1):e0147601. doi:10.1371/journal.pone.0147601

Murad MH, Sultan S, Haffar S, Bazerbachi F. Methodological quality and synthesis of case series and case reports. BMJ Evidence-Based Medicine. 2018;23(2):60–3. doi:10.1136/bmjebm-2017-110853

Issa N, Lacassin F, Camou F. First case of persistent pancytopenia associated with SARS-CoV-2 bone marrow infiltration in an immunocompromised patient. Ann Oncol. 2020;31(10):1418–9. doi:10.1016/j.annonc.2020.06.016

Hernandez JM, Quarles R, Lakshmi S, Casanas B, Eatrides J, McCoy E, et al. Pancytopenia and Profound Neutropenia as a Sequela of Severe SARS-CoV-2 Infection (COVID-19) With Concern for Bone Marrow Involvement. Open Forum Infectious Diseases. 2021;8(2):ofab017. doi:10.1093/ofid/ofab017

Velier M, Priet S, Appay R, Atieh T, Lepidi H, Kaplanski G, et al. Severe and Irreversible Pancytopenia Associated With SARS-CoV-2 Bone Marrow Infection in a Patient With Waldenstrom Macroglobulinemia. Clin Lymphoma Myeloma Leuk. 2021;21(6):e503–5. doi:10.1016/j.clml.2021.01.005

Dewaele K, Claeys R. Hemophagocytic lymphohistiocytosis in SARS-CoV-2 infection. Blood. 2020;135(25):2323. doi:10.1182/blood.2020006505

Lacinel Gurlevik S, Aksu T, Ozen S, Kesici S, Gumruk F, Ozsurekci Y. Hemophagocytosis in bone marrow aspirates in multisystem inflammatory syndrome in children. Pediatr Blood Cancer. 2021;68(6):e28931. doi:10.1002/pbc.28931

Li M-Y, Li L, Zhang Y, Wang X-S. Expression of the SARS-CoV-2 cell receptor gene ACE2 in a wide variety of human tissues. Infect Dis Poverty. 2020;9(1):45. doi:10.1186/s40249-020-00662-x

Dhurve SA, Dhurve AS. Bone Marrow Abnormalities in HIV Disease. Mediterr J Hematol Infect Dis. 2013;5(1):e2013033. doi:10.4084/MJHID.2013.033

Khalil SH, Nounou RM, Frayha H, Halim MA, Ellis M, Black FT. Bone Marrow Morphologic Findings in Patients with Human Immunodeficiency Virus (HIV) Infection. Annals of Saudi Medicine. 1996;16(1):16–9. doi:10.5144/0256-4947.1996.16

Naidoo S, Naicker VL. Retrospective comparison of cytological and histological bone marrow morphology in adult antiretroviral-naïve and antiretroviral experienced human immunodeficiency virus-infected patients with peripheral blood cytopaenias. Southern African Journal of Infectious Diseases. 2016;31(2):50–6. doi: 10.4102/sajid.v31i2.90

Wiseman D, Lin J, Routy J-P, Samoukovic G. Haemophagocytic lymphohistiocytosis in an adult with postacute COVID-19 syndrome. BMJ Case Reports CP. 2021;14(9):e245031. doi:10.1136/bcr-2021-245031

Dandu H, Yadav G, Malhotra HS, Pandey S, Sachu R, Dubey K. Hemophagocytic histiocytosis in severe SARS‐CoV‐2 infection: A bone marrow study. Int J Lab Hematol. 2021; 43(6):1291-1301. Doi:10.1111/ijlh.13619

Retamozo S, Brito-Zerón P, Sisó-Almirall A, Flores-Chávez A, Soto-Cárdenas M-J, Ramos-Casals M. Haemophagocytic syndrome and COVID-19. Clin Rheumatol. 2021;40(4):1233–44. doi:10.1007/s10067-020-05569-4

Ramos-Casals M, Brito-Zerón P, López-Guillermo A, Khamashta MA, Bosch X. Adult haemophagocytic syndrome. Lancet. 2014;383(9927):1503–16. doi:10.1016/S0140-6736(13)61048-X

Antony AC. Chapter 39 - Megaloblastic Anemias. En: Hoffman R, Benz EJ, Silberstein LE, Heslop HE, Weitz JI, Anastasi J, et al., editores. Hematology (Seventh Edition) [Internet]. Elsevier; 2018 [citado el 14 de abril de 2022]; 514-545.e7. doi:10.1016/B978-0-323-35762-3.00039-1

Randhawa J, Ondrejka SL, Setrakian S, Taylor H. What should I know before ordering a bone marrow aspiration/biopsy in patients with vitamin B12 deficiency? BMJ Case Rep. 2013;2013:bcr2013010200. doi:10.1136/bcr-2013-010200

Published

2022-10-06

How to Cite

1.
Pichardo-Rodriguez R, Cordova-Cueva L, Peña-Oscuvilca W, Bracamonte-Hernández JJ, Carrasco-Vergaray C, Saavedra-Velasco M, Ruiz-Franco O. Morphological alterations of the bone marrow in patients with COVID-19. Systematic review and meta-analysis. Rev. Cuerpo Med. HNAAA [Internet]. 2022 Oct. 6 [cited 2024 May 16];15(Supl. 1). Available from: http://www.cmhnaaa.org.pe/ojs/index.php/rcmhnaaa/article/view/1479

Recommended Articles