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Open Access 01-12-2024 | Sideroblastic Anemia | Review

Blood cytopenias as manifestations of inherited metabolic diseases: a narrative review

Authors: Yannick Moutapam-Ngamby—Adriaansen, François Maillot, François Labarthe, Bertrand Lioger

Published in: Orphanet Journal of Rare Diseases | Issue 1/2024

Abstract

Inherited Metabolic Diseases (IMD) encompass a diverse group of rare genetic conditions that, despite their individual rarity, collectively affect a substantial proportion, estimated at as much as 1 in 784 live births. Among their wide-ranging clinical manifestations, cytopenia stands out as a prominent feature. Consequently, IMD should be considered a potential diagnosis when evaluating patients presenting with cytopenia. However, it is essential to note that the existing scientific literature pertaining to the link between IMD and cytopenia is limited, primarily comprising case reports and case series. This paucity of data may contribute to the inadequate recognition of the association between IMD and cytopenia, potentially leading to underdiagnosis. In this review, we synthesize our findings from a literature analysis along with our clinical expertise to offer a comprehensive insight into the clinical presentation of IMD cases associated with cytopenia. Furthermore, we introduce a structured diagnostic approach underpinned by decision-making algorithms, with the aim of enhancing the early identification and management of IMD-related cytopenia.

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Ferreira CR, Rahman S, Keller M, Zschocke J. An international classification of inherited metabolic disorders (ICIMD). J Inherit Metab Dis. 2021;44(1):164–77.PubMedPubMedCentralCrossRef

Revel-Vilk S, Szer J, Zimran A. Hematological manifestations and complications of Gaucher disease. Expert Rev Hematol. 2021;14(4):347–54. https://doi.org/10.1080/17474086.2021.1908120.CrossRefPubMed

Applegarth DA, Toone JR, Lowry RB. Incidence of inborn errors of metabolism in British Columbia, 1969–1996. Pediatrics. 2000;105(1): e10.PubMedCrossRef

Sanderson S, Green A, Preece MA, Burton H. The incidence of inherited metabolic disorders in the West Midlands UK. Arch Dis Child. 2006;91(11):896–9.PubMedPubMedCentralCrossRef

Luzzatto L, Ally M, Notaro R. Glucose-6-phosphate dehydrogenase deficiency. Blood. 2020;136(11):1225–1140.PubMedCrossRef

Grace RF, Mark Layton D, Barcellini W. How we manage patients with pyruvate kinase deficiency. Br J Haematol. 2019;184(5):721–34. https://doi.org/10.1111/bjh.15758.CrossRefPubMed

Mistry PK, Sadan S, Yang R, Yee J, Yang M. Consequences of diagnostic delays in type 1 Gaucher disease: the need for greater awareness among hematologists-oncologists and an opportunity for early diagnosis and intervention. Am J Hematol. 2007;82(8):697–701. https://doi.org/10.1002/ajh.20908.CrossRefPubMed

Castillon G, Chang SC, Moride Y. Global Incidence and prevalence of Gaucher disease: a targeted literature review. J Clin Med. 2022;12(1):85.PubMedPubMedCentralCrossRef

Lee P. Role of matriptase-2 (TMPRSS6) in iron metabolism. Acta Haematol. 2009;122(2–3):87–96.PubMedPubMedCentralCrossRef

10.

Donker AE, Schaap CCM, Novotny VMJ, Smeets R, Peters TMA, van den Heuvel BLP, et al. Iron refractory iron deficiency anemia: a heterogeneous disease that is not always iron refractory. Am J Hematol. 2016;91(12):E482–90.PubMedPubMedCentralCrossRef

11.

Brissot P, Kunz J, Brissot E, Troadec MB, Loréal O, Ropert M. Une anémie ferriprive génétique rare: le syndrome IRIDA. Bull Académie Natl Médecine. 2022;206(3):317–22.CrossRef

12.

van der Staaij H, Donker AE, Bakkeren DL, Salemans JMJI, Mignot-Evers LAA, Bongers MY, et al. Transferrin saturation/hepcidin ratio discriminates TMPRSS6-related iron refractory iron deficiency anemia from patients with multi-causal iron deficiency anemia. Int J Mol Sci. 2022;23(3):1917.PubMedPubMedCentralCrossRef

13.

Mims MP, Guan Y, Pospisilova D, Priwitzerova M, Indrak K, Ponka P, et al. Identification of a human mutation of DMT1 in a patient with microcytic anemia and iron overload. Blood. 2005;105(3):1337–42. https://doi.org/10.1182/blood-2004-07-2966.CrossRefPubMed

14.

Iolascon A, De Falco L. Mutations in the Gene Encoding DMT1: Clinical Presentation and Treatment. Semin Hematol. 2009;46(4):358–70.PubMedCrossRef

15.

Piperno A, Pelucchi S, Mariani R. Inherited iron overload disorders. Transl Gastroenterol Hepatol. 2020;5:25.PubMedPubMedCentralCrossRef

16.

Fujiwara T, Harigae H. Molecular pathophysiology and genetic mutations in congenital sideroblastic anemia. Free Radic Biol Med. 2019;133:179–85.PubMedCrossRef

17.

Aceruloplasminemia KS. Aceruloplasminemia. Curr Drug Targets. 2012;13(9):1190–9.CrossRef

18.

Bruno M, De Falco L, Iolascon A. How I diagnose non-thalassemic microcytic anemias. Semin Hematol. 2015;52(4):270–8.PubMedCrossRef

19.

Vroegindeweij LHP, Langendonk JG, Langeveld M, Hoogendoorn M, Kievit AJA, Di Raimondo D, et al. New insights in the neurological phenotype of aceruloplasminemia in Caucasian patients. Parkinsonism Relat Disord. 2017;36:33–40.PubMedCrossRef

20.

Zoller H, Henninger B. Pathogenesis, diagnosis and treatment of hemochromatosis. Dig Dis. 2016;34(4):364–73.PubMedCrossRef

21.

Dabboubi R, Amri Y, Yahyaoui S, Mahjoub R, Sahli CA, Sahli C, et al. A new case of congenital atransferrinemia with a novel splice site mutation: c.293–63del. Eur J Med Genet. 2020;63(5):103874.PubMedCrossRef

22.

Chiabrando D, Mercurio S, Tolosano E. Heme and erythropoieis: more than a structural role. Haematologica. 2014;99(6):973–83.PubMedPubMedCentralCrossRef

23.

Bergmann AK, Campagna DR, McLoughlin EM, Agarwal S, Fleming MD, Bottomley SS, et al. Systematic molecular genetic analysis of congenital sideroblastic anemia: Evidence for genetic heterogeneity and identification of novel mutations. Pediatr Blood Cancer. 2010;54(2):273–8. https://doi.org/10.1002/pbc.22244.CrossRefPubMedPubMedCentral

24.

Bottomley SS, Fleming MD. Sideroblastic Anemia. Hematol Oncol Clin North Am. 2014;28(4):653–70.PubMedCrossRef

25.

Donker AE, Raymakers RA, Nieuwenhuis HK, Coenen MJH, Janssen MC, MacKenzie MA, et al. X-linked sideroblastic anaemia due to ALAS2 mutations in the Netherlands: a disease in disguise. 2014;72(4).

26.

Daher R, Mansouri A, Martelli A, Bayart S, Manceau H, Callebaut I, et al. GLRX5 mutations impair heme biosynthetic enzymes ALA synthase 2 and ferrochelatase in human congenital sideroblastic anemia. Mol Genet Metab. 2019;128(3):342–51.PubMedCrossRef

27.

Kumar A, Jazieh AR. Case report of sideroblastic anemia caused by ingestion of coins. Am J Hematol. 2001;66(2):126–9.PubMedCrossRef

28.

Waldron HA. The anaemia of lead poisoning: a review. Br J Ind Med. 1966;23(2):83–100.PubMedPubMedCentral

29.

Piso RJ, Kriz K, Desax MC. Severe isoniazid related sideroblastic anemia. Hematol Rep. 2011;3(1):e2.PubMedPubMedCentralCrossRef

30.

Xiong S, Jia Y, Li S, Huang P, Xiong J, Mao D, et al. The first case report of X-linked sideroblastic anemia with ataxia of Chinese origin and literature review. Front Pediatr. 2021. https://doi.org/10.3389/fped.2021.692459.CrossRefPubMedPubMedCentral

31.

Mendonca LO, Prado AI, Costa IMC, Bandeira M, Dyer R, Barros SF, et al. Case report: expanding clinical, immunological and genetic findings in sideroblastic anemia with immunodeficiency, fevers and development delay (SIFD) syndrome. Front Immunol. 2021. https://doi.org/10.3389/fimmu.2021.586320.CrossRefPubMedPubMedCentral

32.

Liskova A, Samec M, Koklesova L, Kudela E, Kubatka P, Golubnitschaja O. Mitochondriopathies as a clue to systemic disorders—analytical tools and mitigating measures in context of predictive, preventive, and personalized (3P) medicine. Int J Mol Sci. 2021;22(4):2007.PubMedPubMedCentralCrossRef

33.

Topyildiz E, Edeer Karaca N, Bas I, Aykut A, Durmaz A, Guven Bilgin RB, et al. A novel homozygous TRNT1 mutation in a child with an early diagnosis of common variable immunodeficiency leading to mild hypogammaglobulinemia and hemolytic anemia. J Pediatr Hematol Oncol. 2021;43(6):e780.PubMedCrossRef

34.

Karim Z, Lyoumi S, Nicolas G, Deybach JC, Gouya L, Puy H. Porphyrias: A 2015 update. Clin Res Hepatol Gastroenterol. 2015;39(4):412–25.PubMedCrossRef

35.

Erwin AL, Desnick RJ. Congenital erythropoietic porphyria: recent advances. Mol Genet Metab. 2019;128(3):288–97.PubMedCrossRef

36.

Di Pierro E, Russo R, Karakas Z, Brancaleoni V, Gambale A, Kurt I, et al. Congenital erythropoietic porphyria linked to GATA1-R216W mutation: challenges for diagnosis. Eur J Haematol. 2015;94(6):491–7. https://doi.org/10.1111/ejh.12452.CrossRefPubMed

37.

Lecha M, Puy H, Deybach JC. Erythropoietic protoporphyria. Orphanet J Rare Dis. 2009;4(1):19. https://doi.org/10.1186/1750-1172-4-19.CrossRefPubMedPubMedCentral

38.

Hill A, Hill QA. Autoimmune hemolytic anemia. Hematology. 2018;2018(1):382–9. https://doi.org/10.1182/asheducation-2018.1.382.CrossRefPubMedPubMedCentral

39.

Fattizzo B, Giannotta JA, Cecchi N, Barcellini W. Confounding factors in the diagnosis and clinical course of rare congenital hemolytic anemias. Orphanet J Rare Dis. 2021;16(1):415. https://doi.org/10.1186/s13023-021-02036-4.CrossRefPubMedPubMedCentral

40.

Thiagarajan P, Parker CJ, Prchal JT. How do red blood cells die? Front Physiol. 2021. https://doi.org/10.3389/fphys.2021.655393/full.CrossRefPubMedPubMedCentral

41.

Diegues A, Simões P, Ceriz T, Lopes AR, Tomé E. Favism: a case report. Cureus. 2023;14(3):23269.

42.

Veldhuijzen N, Kamphuis S, van den Bergh F, Spronk P, Braber A. Madam, why are you so sour? Eur J Anaesthesiol EJA. 2021;29(8):398.CrossRef

43.

Brooker G, Jeffery J, Nataraj T, Sair M, Ayling R. High anion gap metabolic acidosis secondary to pyroglutamic aciduria (5-oxoprolinuria): association with prescription drugs and malnutrition. Ann Clin Biochem. 2007;44(4):406–9. https://doi.org/10.1258/000456307780945769.CrossRefPubMed

44.

Kamerbeek NM, van Zwieten R, de Boer M, Morren G, Vuil H, Bannink N, et al. Molecular basis of glutathione reductase deficiency in human blood cells. Blood. 2007;109(8):3560–366.PubMedCrossRef

45.

Chiarelli LR, Fermo E, Zanella A, Valentini G. Hereditary erythrocyte pyrimidine 5′-nucleotidase deficiency: a biochemical, genetic and clinical overview. Hematology. 2006;11(1):67–72. https://doi.org/10.1080/10245330500276667.CrossRefPubMed

46.

Zanella A, Bianchi P, Fermo E, Valentini G. Hereditary pyrimidine 5′-nucleotidase deficiency: from genetics to clinical manifestations. Br J Haematol. 2006;133(2):113–23. https://doi.org/10.1111/j.1365-2141.2006.05992.x.CrossRefPubMed

47.

He S, Chen H, Guo X, Gao J. Red cell adenylate kinase deficiency in China: molecular study of 2 new mutations (413G > A, 223dupA). BMC Med Genom. 2022;15(1):102. https://doi.org/10.1186/s12920-022-01248-2.CrossRef

48.

Walshe JM. The acute haemolytic syndrome in Wilson’s disease–a review of 22 patients. QJM Mon J Assoc Phys. 2013;106(11):1003–8.

49.

Poujois A, Woimant F. Wilson’s disease: a 2017 update. Clin Res Hepatol Gastroenterol. 2018;42(6):512–20.PubMedCrossRef

50.

Członkowska A, Litwin T, Dusek P, Ferenci P, Lutsenko S, Medici V, et al. Wilson disease. Nat Rev Dis Primer. 2018;4(1):21.CrossRef

51.

Stremmel W, Merle U, Weiskirchen R. Clinical features of Wilson disease. Ann Transl Med. 2019;7(Suppl 2):S61.PubMedPubMedCentralCrossRef

52.

Fritsch C, Bolsen K, Ruzicka T, Goerz G. Congenital erythropoietic porphyria. J Am Acad Dermatol. 1997;36(4):594–610.PubMedCrossRef

53.

Sabry W, Elemary M, Burnouf T, Seghatchian J, Goubran H. Vitamin B12 deficiency and metabolism-mediated thrombotic microangiopathy (MM-TMA). Transfus Apher Sci. 2020;59(1):102717.PubMedCrossRef

54.

Bayer G, von Tokarski F, Thoreau B, Bauvois A, Barbet C, Cloarec S, et al. Etiology and Outcomes of thrombotic microangiopathies. Clin J Am Soc Nephrol. 2019;14(4):557.PubMedPubMedCentralCrossRef

55.

Lemoine M, François A, Grangé S, Rabant M, Châtelet V, Cassiman D, et al. Cobalamin C deficiency induces a typical histopathological pattern of renal arteriolar and glomerular thrombotic microangiopathy. Kidney Int Rep. 2018;3(5):1153–62.PubMedPubMedCentralCrossRef

56.

Bratosin D, Tissier JP, Lapillonne H, Hermine O, de Villemeur TB, Cotoraci C, et al. A cytometric study of the red blood cells in Gaucher disease reveals their abnormal shape that may be involved in increased erythrophagocytosis. Cytometry B Clin Cytom. 2011;80B(1):28–37. https://doi.org/10.1002/cyto.b.20539.CrossRef

57.

Hershkop E, Bergman I, Kurolap A, Dally N, Feldman HB. Non-immune hemolysis in Gaucher disease and review of the literature. Rambam Maimonides Med J. 2021;12(3):e0025.PubMedPubMedCentralCrossRef

58.

Melzak KA, Muth M, Kirschhöfer F, Brenner-Weiss G, Bieback K. Lipid ratios as a marker for red blood cell storage quality and as a possible explanation for donor gender differences in storage quality. Vox Sang. 2020;115(8):655–63. https://doi.org/10.1111/vox.12924.CrossRefPubMed

59.

Mehta R, Elías-López D, Martagón AJ, Pérez-Méndez OA, Sánchez MLO, Segura Y, et al. LCAT deficiency: a systematic review with the clinical and genetic description of Mexican kindred. Lipids Health Dis. 2021;20:70.PubMedPubMedCentralCrossRef

60.

Godin DV, Gray GR, Frohlich J. Study of erythrocytes in a hereditary hemolytic syndrome (HHS): comparison with erythrocytes in lecithin:cholesterol acyltransferase (LCAT) deficiency. Scand J Haematol. 1980;24(2):122–30.PubMedCrossRef

61.

Takahashi M, Okazaki H, Ohashi K, Ogura M, Ishibashi S, Okazaki S, et al. Current diagnosis and management of Abetalipoproteinemia. J Atheroscler Thromb. 2021;28(10):1009–19.PubMedPubMedCentralCrossRef

62.

Dali-Youcef N, Andrès E. An update on cobalamin deficiency in adults. QJM Int J Med. 2009;102(1):17–28. https://doi.org/10.1093/qjmed/hcn138.CrossRef

63.

Briani C, Dalla Torre C, Citton V, Manara R, Pompanin S, Binotto G, et al. Cobalamin deficiency: clinical picture and radiological findings. Nutrients. 2013;5(11):4521–39.PubMedPubMedCentralCrossRef

64.

Pawlak R, Lester SE, Babatunde T. The prevalence of cobalamin deficiency among vegetarians assessed by serum vitamin B12: a review of literature. Eur J Clin Nutr. 2014;68(5):541–8.PubMedCrossRef

65.

Saultier P, Loosveld M, Benoist JF, Michel G. Pancytopenia and megaloblastic erythropoiesis reveal a novel GIF mutation. Br J Haematol. 2018;181(3):304–304. https://doi.org/10.1111/bjh.15104.CrossRefPubMed

66.

Gräsbeck R. Imerslund-Gräsbeck syndrome (selective vitamin B12 malabsorption with proteinuria). Orphanet J Rare Dis. 2006;1(1):17. https://doi.org/10.1186/1750-1172-1-17.CrossRefPubMedPubMedCentral

67.

Ünal S, Karahan F, Arıkoğlu T, Akar A, Kuyucu S. Different presentations of patients with transcobalamin II deficiency: a single-center experience from Turkey. Turk J Hematol. 2019;36(1):37–42.CrossRef

68.

Chu TH, Chien YH, Lin HY, Liao HC, Ho HJ, Lai CJ, et al. Methylmalonic acidemia/propionic academia—the biochemical presentation and comparing the outcome between liver transplantation versus non-liver transplantation groups. Orphanet J Rare Dis. 2019;14(1):1–10. https://doi.org/10.1186/s13023-019-1045-1.CrossRef

69.

Zhou X, Cui Y, Han J. Methylmalonic acidemia: current status and research priorities. Intractable Rare Dis Res. 2018;7(2):73–8.PubMedPubMedCentralCrossRef

70.

Baumgartner MR, Hörster F, Dionisi-Vici C, Haliloglu G, Karall D, Chapman KA, et al. Proposed guidelines for the diagnosis and management of methylmalonic and propionic acidemia. Orphanet J Rare Dis. 2014;9(1):1–36. https://doi.org/10.1186/s13023-014-0130-8.CrossRef

71.

Huemer M, Diodato D, Schwahn B, Schiff M, Bandeira A, Benoist JF, et al. Guidelines for diagnosis and management of the cobalamin-related remethylation disorders cblC, cblD, cblE, cblF, cblG, cblJ and MTHFR deficiency. J Inherit Metab Dis. 2017;40(1):21–48. https://doi.org/10.1007/s10545-016-9991-4.CrossRefPubMed

72.

Kripps KA, Sremba L, Larson AA, Van Hove JLK, Nguyen H, Wright EL, et al. Methionine synthase deficiency: variable clinical presentation and benefit of early diagnosis and treatment. J Inherit Metab Dis. 2022;45(2):157–68. https://doi.org/10.1002/jimd.12448.CrossRefPubMed

73.

Bidla G, Watkins D, Chéry C, Froese DS, Ells C, Kerachian M, et al. Biochemical analysis of patients with mutations in MTHFD1 and a diagnosis of methylenetetrahydrofolate dehydrogenase 1 deficiency. Mol Genet Metab. 2020;130(3):179–82.PubMedCrossRef

74.

Allen LH. Causes of vitamin B12 and folate deficiency. Food Nutr Bull. 2008;29(2):S20-34. https://doi.org/10.1177/15648265080292S105.CrossRefPubMed

75.

Cario H, Smith DEC, Blom H, Blau N, Bode H, Holzmann K, et al. Dihydrofolate reductase deficiency due to a homozygous DHFR mutation causes megaloblastic anemia and cerebral folate deficiency leading to severe neurologic disease. Am J Hum Genet. 2011;88(2):226–31.PubMedPubMedCentralCrossRef

76.

Cario H, Smith DEC, Blom HJ, Bode H, Blau N, Holzmann K, et al. Dihydrofolate reductase deficiency is caused by a homozygous DHFR mutation and leads to congenital megaloblastic anemia and cerebral folate deficiency. Blood. 2010;116(21):1006.CrossRef

77.

Majumdar R, Yori A, Rush PW, Raymond K, Gavrilov D, Tortorelli S, et al. Allelic spectrum of formiminotransferase-cyclodeaminase gene variants in individuals with formiminoglutamic aciduria. Mol Genet Genomic Med. 2017;5(6):795–9. https://doi.org/10.1002/mgg3.333.CrossRefPubMedPubMedCentral

78.

Hilton JF, Christensen KE, Watkins D, Raby BA, Renaud Y, de la Luna S, et al. The molecular basis of glutamate formiminotransferase deficiency. Hum Mutat. 2003;22(1):67–73. https://doi.org/10.1002/humu.10236.CrossRefPubMed

79.

Lu H, Lu H, Vaucher J, Tran C, Vollenweider P, Castioni J. L’anémie mégaloblastique thiamine dépendante ou syndrome de Rogers: une revue de la littérature. Rev Médecine Interne. 2019;40(1):20–7.CrossRef

80.

Green R. Mystery of thiamine-responsive megaloblastic anemia unlocked. Blood. 2003;102. Available from: https://www.researchgate.net/publication/245966557_Mystery_of_thiamine-responsive_megaloblastic_anemia_unlocked.

81.

Qin M, Luo P, Wen X, Li J. Misdiagnosis of sitosterolemia in a patient as Evans syndrome and familial hypercholesterolemia. J Clin Lipidol. 2022;16(1):33–9.PubMedCrossRef

82.

Xia Y, Duan Y, Zheng W, Liang L, Zhang H, Luo X, et al. Clinical, genetic profile and therapy evaluation of 55 children and 5 adults with sitosterolemia. J Clin Lipidol. 2022;16(1):40–51.PubMedCrossRef

83.

Marín-Quílez A, Di Buduo CA, Benito R, Balduini A, Rivera J, Bastida JM. GALE variants associated with syndromic manifestations, macrothrombocytopenia, bleeding, and platelet dysfunction. Platelets. 2023;34(1):2176699. https://doi.org/10.1080/09537104.2023.2176699.CrossRefPubMed

84.

Seo A, Gulsuner S, Pierce S, Ben-Harosh M, Shalev H, Walsh T, et al. Inherited thrombocytopenia associated with mutation of UDP-galactose-4-epimerase (GALE). Hum Mol Genet. 2019;28(1):133–42.PubMedCrossRef

85.

Motta I, Consonni D, Stroppiano M, Benedetto C, Cassinerio E, Tappino B, et al. Predicting the probability of Gaucher disease in subjects with splenomegaly and thrombocytopenia. Sci Rep. 2021;11(1):2594.PubMedPubMedCentralCrossRef

86.

Bermejo N, Prieto J, Arcos M. Sea-blue histiocytosis in bone marrow of a patient with chronic thrombocytopenia. Acta Haematol. 2014;20(133):277–8.

87.

Wortmann SB, Van Hove JLK, Derks TGJ, Chevalier N, Knight V, Koller A, et al. Treating neutropenia and neutrophil dysfunction in glycogen storage disease type Ib with an SGLT2 inhibitor. Blood. 2020;136(9):1033–43.PubMedPubMedCentralCrossRef

88.

Pang J, Bao Y, Mitchell-Silbaugh K, Veevers J, Fang X. Barth syndrome cardiomyopathy: an update. Genes. 2022;13(4):656.PubMedPubMedCentralCrossRef

89.

Taylor C, Rao ES, Pierre G, Chronopoulou E, Hornby B, Heyman A, et al. Clinical presentation and natural history of Barth syndrome: an overview. J Inherit Metab Dis. 2022;45(1):7–16. https://doi.org/10.1002/jimd.12422.CrossRefPubMed

90.

Gnanaraj J, Parnes A, Francis CW, Go RS, Takemoto CM, Hashmi SK. Approach to pancytopenia: diagnostic algorithm for clinical hematologists. Blood Rev. 2018;32(5):361–7.PubMedCrossRef

91.

MacFarland S, Hartung H. Pancytopenia in a patient with methylmalonic acidemia. Blood. 2015;125(11):1840.PubMedCrossRef

92.

Dimitrov B, Molema F, Williams M, Schmiesing J, Mühlhausen C, Baumgartner MR, et al. Organic acidurias: major gaps, new challenges, and a yet unfulfilled promise. J Inherit Metab Dis. 2021;44(1):9–21. https://doi.org/10.1002/jimd.12254.CrossRefPubMed

93.

Mauhin W, Habarou F, Gobin S, Servais A, Brassier A, Grisel C, et al. Update on lysinuric protein intolerance, a multi-faceted disease retrospective cohort analysis from birth to adulthood. Orphanet J Rare Dis. 2017;12(1):1–12. https://doi.org/10.1186/s13023-016-0550-8.CrossRef

94.

Lysinuric protein intolerance presenting as pancytopenia and splenomegaly mimicking acute leukaemia: a case report - PMC. Available from: https://www-ncbi-nlm-nih-gov.proxy.scd.univ-tours.fr/pmc/articles/PMC10391768/.

95.

Weinreb NJ, Rosenbloom BE. Splenomegaly, hypersplenism, and hereditary disorders with splenomegaly. Open J Genet. 2013;3(1):24–43.CrossRef

96.

Lv Y, Lau WY, Li Y, Deng J, Han X, Gong X, et al. Hypersplenism: History and current status. Exp Ther Med. 2016;12(4):2377–82.PubMedPubMedCentralCrossRef

97.

Invernizzi R. Images from the Haematologica Atlas of Hematologic Cytology: Gaucher disease. Haematologica. 2022;107(11):2527.PubMedPubMedCentralCrossRef

98.

Green R, Dwyre DM. Evaluation of macrocytic anemias. Semin Hematol. 2015;52(4):279–86.PubMedCrossRef

Title: Blood cytopenias as manifestations of inherited metabolic diseases: a narrative review
Authors: Yannick Moutapam-Ngamby—Adriaansen
François Maillot
François Labarthe
Bertrand Lioger
Publication date: 01-12-2024
Publisher: BioMed Central
Keywords: Sideroblastic Anemia
Anemia
Microcytic Anemia
Neutropenia
Hemolytic Anemia
Published in: Orphanet Journal of Rare Diseases / Issue 1/2024
Electronic ISSN: 1750-1172
DOI: https://doi.org/10.1186/s13023-024-03074-4

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Blood cytopenias as manifestations of inherited metabolic diseases: a narrative review

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