genes
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G C A T
Article
Complex Modes of Inheritance in Hereditary Red Blood Cell
Disorders: A Case Series Study of 155 Patients
Immacolata Andolfo
1,2
, Stefania Martone
1,2
, Barbara Eleni Rosato
1,2
, Roberta Marra
1,2
, Antonella Gambale
2,3
,
Gian Luca Forni
4
, Valeria Pinto
4
, Magnus Göransson
5
, Vasiliki Papadopoulou
6
, Mathilde Gavillet
6
,
Mohsen Elalfy
7
, Antonella Panarelli
2
, Giovanna Tomaiuolo
2,8
, Achille Iolascon
1,2,
* and Roberta Russo
1
Citation: Andolfo, I.; Martone, S.;
Rosato, B.E.; Marra, R.; Gambale, A.;
Forni, G.L.; Pinto, V.; Göransson, M.;
Papadopoulou, V.; Gavillet, M.; et al.
Complex Modes of Inheritance in
Hereditary Red Blood Cell Disorders:
A Case Series Study of 155 Patients.
Genes 2021, 12, 958. https://doi.org/
10.3390/genes12070958
Academic Editor: Julia Horsfield
Received: 27 May 2021
Accepted: 19 June 2021
Published: 23 June 2021
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1
Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi di Napoli Federico II,
80131 Napoli, Italy; andolfo@ceinge.unina.it (I.A.); stefaniamartone85@libero.it (S.M.);
rosato.barbara@gmail.com (B.E.R.); robertamarra.r@gmail.com (R.M.); roberta.russo@unina.it (R.R.)
2
CEINGE Biotecnologie Avanzate, 80145 Naples, Italy; antonellagambale@gmail.com (A.G.);
panarelli@ceinge.unina.it (A.P.); g.tomaiuolo@unina.it (G.T.)
3
Department of Laboratory Medicine (DAIMedLab), UOC Medical Genetics, ‘Federico II’ University Hospital,
80131 Naples, Italy
4
Centro della Microcitemia e delle Anemie Congenite, Ospedale Galliera, 16128 Genoa, Italy;
gianluca.forni@galliera.it (G.L.F.); valeria.pinto@galliera.it (V.P.)
5
Department of Paediatrics, The Queen Silvia Children’s Hospital, Sahlgrenska University Hospital,
41345 Gothenburg, Sweden; magnus.l.goransson@vgregion.se
6
Service and Central Laboratory of Haematology, Department of Oncology and Department of Laboratory
Medicine and Pathology, Lausanne University Hospital (CHUV), 1011 Lausanne, Switzerland;
vasiliki.papadopoulou@chuv.ch (V.P.); mathilde.gavillet@chuv.ch (M.G.)
7
Thalassemia Centre, Faculty of Medicine, Ain Shams University, Cairo 11566, Egypt; elalfym@hotmail.com
8
Department of Chemical Engineering, Materials and Industrial Production, ‘Federico II’ University of Naples,
80125 Naples, Italy
* Correspondence: achille.iolascon@unina.it
Abstract: Hereditary erythrocytes disorders include a large group of conditions with heteroge-
neous molecular bases and phenotypes. We analyzed here a case series of 155 consecutive patients
with clinical suspicion of hereditary erythrocyte defects referred to the Medical Genetics Unit from
2018 to 2020. All of the cases followed a diagnostic workflow based on a targeted next-generation
sequencing panel of 86 genes causative of hereditary red blood cell defects. We obtained an overall
diagnostic yield of 84% of the tested patients. Monogenic inheritance was seen for 69% (107/155),
and multi-locus inheritance for 15% (23/155). PIEZO1 and SPTA1 were the most mutated loci.
Accordingly, 16/23 patients with multi-locus inheritance showed dual molecular diagnosis of dehy-
drated hereditary stomatocytosis/xerocytosis and hereditary spherocytosis. These dual inheritance
cases were fully characterized and were clinically indistinguishable from patients with hereditary
spherocytosis. Additionally, their ektacytometry curves highlighted alterations of dual inheritance
patients compared to both dehydrated hereditary stomatocytosis and hereditary spherocytosis. Our
findings expand the genotypic spectrum of red blood cell disorders and indicate that multi-locus
inheritance should be considered for analysis and counseling of these patients. Of note, the genetic
testing was crucial for diagnosis of patients with a complex mode of inheritance.
Keywords: red blood cell defects; targeted next-generation sequencing; multi-locus inheritance;
PIEZO1; SPTA1
1. Introduction
Hereditary anemias are a heterogeneous group of conditions that are characterized
by complex genotype–phenotype correlations. Based on clinical manifestations and mor-
phological red blood cell (RBC) alterations, hereditary anemias can be broadly classified
into four different subtypes: (i) disorders of hemoglobin synthesis, such as thalassemia
Genes 2021, 12, 958. https://doi.org/10.3390/genes12070958 https://www.mdpi.com/journal/genes