Circulating endothelial progenitor cells during pregnancy in multiple sclerosis.
Circulating endothelial progenitor cells
Cord blood
EPC
Multiple sclerosis
Pregnancy
Journal
Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
11
04
2020
accepted:
01
08
2020
pubmed:
18
8
2020
medline:
11
5
2021
entrez:
18
8
2020
Statut:
ppublish
Résumé
Endothelial progenitor cells (EPCs) have been shown to increase during physiological pregnancy and are believed to play a fundamental role in the process of placentation. Reduced levels of EPCs during pregnancy have been associated with preeclampsia and miscarriage. Women with multiple sclerosis (MS) are not at increased risk of preeclampsia nor of general adverse obstetric outcome, in contrast with some other autoimmune diseases. The aim of this study was to evaluate circulating EPCs levels in pregnant patients with MS. CD34+ and CD133+ were longitudinally detected by flow cytometry in the maternal plasma of 29 healthy controls and 9 MS patients and in the cord blood of their newborns. EPCs were affected by pregnancy with the same trend in both groups (CD34+ p = 0.0342; CD133+ p = 0.0347). EPCs during pregnancy were increased in MS (mean ± SD: CD34+ cells 0.038 ± 0.010; CD133+ 0.024 ± 0.009) with respect to healthy controls (mean ± SD: CD34+ cells 0.022 ± 0.006; CD133+ 0.016 ± 0.004), CD34+ p = 0.0004; CD133+ p = 0.0109. EPCs levels of the cord blood of MS patients' newborns mild correlated with maternal EPC levels at delivery (CD34+: spearman's Rho 0.658, p = 0.054; CD133+: spearman's Rho 0.758, p = 0.018). This work identified increased circulating EPC levels during pregnancy, following the same trend both in MS patients and healthy controls. Despite the similar trend, the levels of circulating EPCs were significantly higher in MS patients with respect to the control population. A correlation was also found in MS patients between cord blood EPCs and circulating EPCs at delivery.
Sections du résumé
BACKGROUND
BACKGROUND
Endothelial progenitor cells (EPCs) have been shown to increase during physiological pregnancy and are believed to play a fundamental role in the process of placentation. Reduced levels of EPCs during pregnancy have been associated with preeclampsia and miscarriage. Women with multiple sclerosis (MS) are not at increased risk of preeclampsia nor of general adverse obstetric outcome, in contrast with some other autoimmune diseases.
OBJECTIVE
OBJECTIVE
The aim of this study was to evaluate circulating EPCs levels in pregnant patients with MS.
METHODS
METHODS
CD34+ and CD133+ were longitudinally detected by flow cytometry in the maternal plasma of 29 healthy controls and 9 MS patients and in the cord blood of their newborns.
RESULTS
RESULTS
EPCs were affected by pregnancy with the same trend in both groups (CD34+ p = 0.0342; CD133+ p = 0.0347). EPCs during pregnancy were increased in MS (mean ± SD: CD34+ cells 0.038 ± 0.010; CD133+ 0.024 ± 0.009) with respect to healthy controls (mean ± SD: CD34+ cells 0.022 ± 0.006; CD133+ 0.016 ± 0.004), CD34+ p = 0.0004; CD133+ p = 0.0109. EPCs levels of the cord blood of MS patients' newborns mild correlated with maternal EPC levels at delivery (CD34+: spearman's Rho 0.658, p = 0.054; CD133+: spearman's Rho 0.758, p = 0.018).
CONCLUSIONS
CONCLUSIONS
This work identified increased circulating EPC levels during pregnancy, following the same trend both in MS patients and healthy controls. Despite the similar trend, the levels of circulating EPCs were significantly higher in MS patients with respect to the control population. A correlation was also found in MS patients between cord blood EPCs and circulating EPCs at delivery.
Identifiants
pubmed: 32804349
doi: 10.1007/s10072-020-04648-3
pii: 10.1007/s10072-020-04648-3
pmc: PMC7956006
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1443-1451Subventions
Organisme : Ministero della Salute
ID : Current Research Project N. 10 901-rcr2017i-23 years 2017-2020
Références
Mallucci G, Peruzzotti-Jametti L, Bernstock JD, Pluchino S (2015) The role of immune cells, glia and neurons in white and gray matter pathology in multiple sclerosis. Prog Neurobiol 127–128:1–22
doi: 10.1016/j.pneurobio.2015.02.003
Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O (2018) Multiple sclerosis. Lancet 391:1622–1636
doi: 10.1016/S0140-6736(18)30481-1
Van Der Kop ML, Pearce MS, Dahlgren L et al (2011) Neonatal and delivery outcomes in women with multiple sclerosis. Ann Neurol 70:41–50. https://doi.org/10.1002/ana.22483
doi: 10.1002/ana.22483
pubmed: 21710652
pmcid: 3625744
Voskuhl R, Momtazee C (2017) Pregnancy: effect on multiple sclerosis, treatment considerations, and breastfeeding. Neurotherapeutics 14:974–984
doi: 10.1007/s13311-017-0562-7
Nguyen A-L, Eastaugh A, van der Walt A, Jokubaitis VG (2019) Pregnancy and multiple sclerosis: clinical effects across the lifespan. Autoimmun Rev 18:102360. https://doi.org/10.1016/j.autrev.2019.102360
doi: 10.1016/j.autrev.2019.102360
pubmed: 31401345
MacDonald SC, McElrath TF, Hernández-Díaz S (2019) Pregnancy outcomes in women with multiple sclerosis. Am J Epidemiol 188:57–66. https://doi.org/10.1093/aje/kwy197
doi: 10.1093/aje/kwy197
pubmed: 30165561
Houtchens MK, Edwards NC, Schneider G, Stern K, Phillips AL (2018) Pregnancy rates and outcomes in women with and without MS in the United States. Neurology 91:e1559–e1569. https://doi.org/10.1212/WNL.0000000000006384
doi: 10.1212/WNL.0000000000006384
pubmed: 30266889
pmcid: 6205683
Asahara T, Murohara T, Sullivan A et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(80):964–967. https://doi.org/10.1126/science.275.5302.964
doi: 10.1126/science.275.5302.964
pubmed: 9020076
Bianconi V, Sahebkar A, Kovanen P, Bagaglia F, Ricciuti B, Calabrò P, Patti G, Pirro M (2018) Endothelial and cardiac progenitor cells for cardiovascular repair: a controversial paradigm in cell therapy. Pharmacol Ther 181:156–168. https://doi.org/10.1016/j.pharmthera.2017.08.004
doi: 10.1016/j.pharmthera.2017.08.004
pubmed: 28827151
Luppi P, Powers RW, Verma V, Edmunds L, Plymire D, Hubel CA (2010) Maternal circulating CD34+VEGFR-2+ and CD133+VEGFR-2+ progenitor cells increase during normal pregnancy but are reduced in women with preeclampsia. Reprod Sci 17:643–652. https://doi.org/10.1177/1933719110366164
doi: 10.1177/1933719110366164
pubmed: 20360595
pmcid: 2893245
Flo K, Blix ES, Husebekk A, Thommessen A, Uhre AT, Wilsgaard T, Vårtun Å, Acharya G (2016) A longitudinal study of maternal endothelial function, inflammatory response and uterine artery blood flow during the second half of pregnancy. Acta Obstet Gynecol Scand 95:225–232. https://doi.org/10.1111/aogs.12802
doi: 10.1111/aogs.12802
pubmed: 26462064
Sugawara J, Mitsui-Saito M, Hoshiai T, Hayashi C, Kimura Y, Okamura K (2005) Circulating endothelial progenitor cells during human pregnancy. J Clin Endocrinol Metab 90:1845–1848. https://doi.org/10.1210/jc.2004-0541
doi: 10.1210/jc.2004-0541
pubmed: 15585564
Buemi M, Allegra A, D’Anna R et al (2007) Concentration of circulating endothelial progenitor cells (EPC) in normal pregnancy and in pregnant women with diabetes and hypertension. Am J Obstet Gynecol 196:68.e1–68.e6. https://doi.org/10.1016/j.ajog.2006.08.032
doi: 10.1016/j.ajog.2006.08.032
Kanki K, Ii M, Terai Y et al (2016) Bone marrow-derived endothelial progenitor cells reduce recurrent miscarriage in gestation. Cell Transplant 25:2187–2197. https://doi.org/10.3727/096368916X692753
doi: 10.3727/096368916X692753
pubmed: 27513361
Giordano D, Loddo S, Laganà AS, Coppolino G, Zoccali G, di Benedetto A, Santamaria A, Buemi M, D’Anna R (2018) Peripheral blood CD34+ cells as a novel and noninvasive early marker of first trimester miscarriage: results from a case-control analysis. J Matern Fetal Neonatal Med 31:258–260. https://doi.org/10.1080/14767058.2016.1277703
doi: 10.1080/14767058.2016.1277703
pubmed: 28110587
Grisar J, Aletaha D, Steiner CW, Kapral T, Steiner S, Seidinger D, Weigel G̈, Schwarzinger I, Wolozcszuk W, Steiner G̈, Smolen JS (2005) Depletion of endothelial progenitor cells in the peripheral blood of patients with rheumatoid arthritis. Circulation 111:204–211. https://doi.org/10.1161/01.CIR.0000151875.21836.AE
doi: 10.1161/01.CIR.0000151875.21836.AE
pubmed: 15642766
Adawi M, Pastukh N, Saaida G, Sirchan R, Watad A, Blum A (2018) Inhibition of endothelial progenitor cells may explain the high cardiovascular event rate in patients with rheumatoid arthritis. QJM 111:525–529. https://doi.org/10.1093/qjmed/hcy099
doi: 10.1093/qjmed/hcy099
pubmed: 29788448
Nevskaya T, Bykovskaia S, Lyssuk E et al Circulating endothelial progenitor cells in systemic sclerosis: relation to impaired angiogenesis and cardiovascular manifestations. Clin Exp Rheumatol 26(3):421–429
Patschan S, Tampe D, Müller C, Seitz C, Herink C, Müller GA, Zeisberg E, Zeisberg M, Henze E, Patschan D (2016) Early endothelial progenitor cells (eEPCs) in systemic sclerosis (SSc) - dynamics of cellular regeneration and mesenchymal transdifferentiation. BMC Musculoskelet Disord 17:339. https://doi.org/10.1186/s12891-016-1197-2
doi: 10.1186/s12891-016-1197-2
pubmed: 27519706
pmcid: 4983068
Benyamine A, Magalon J, Cointe S et al (2017) Increased serum levels of fractalkine and mobilisation of CD34+CD45- endothelial progenitor cells in systemic sclerosis. Arthritis Res Ther 19. https://doi.org/10.1186/s13075-017-1271-7
Haque S, Alexander MY, Bruce IN (2012) Endothelial progenitor cells: a new player in lupus? Arthritis Res Ther 14:203. https://doi.org/10.1186/ar3700
doi: 10.1186/ar3700
pubmed: 22356717
pmcid: 3392811
Nathan NO, Mørch LS, Wu CS, Olsen J, Hetland ML, Li J, Rom AL (2019) Rheumatoid arthritis and risk of spontaneous abortion: a Danish nationwide cohort study. Rheumatology (Oxford) 59:1984–1991. https://doi.org/10.1093/rheumatology/kez565
doi: 10.1093/rheumatology/kez565
Blagojevic J, AlOdhaibi KA, Aly AM et al (2019) Pregnancy in systemic sclerosis: results of a systematic review and Metaanalysis. J Rheumatol jrheum.181460. https://doi.org/10.3899/jrheum.181460
Moroni G, Ponticelli C (2016) Pregnancy in women with systemic lupus erythematosus (SLE). Eur J Intern Med 32:7–12
doi: 10.1016/j.ejim.2016.04.005
Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, Correale J, Fazekas F, Filippi M, Freedman MS, Fujihara K, Galetta SL, Hartung HP, Kappos L, Lublin FD, Marrie RA, Miller AE, Miller DH, Montalban X, Mowry EM, Sorensen PS, Tintoré M, Traboulsee AL, Trojano M, Uitdehaag BMJ, Vukusic S, Waubant E, Weinshenker BG, Reingold SC, Cohen JA (2018) Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol 17:162–173
doi: 10.1016/S1474-4422(17)30470-2
Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 33:1444–1452. https://doi.org/10.1212/wnl.33.11.1444
doi: 10.1212/wnl.33.11.1444
pubmed: 6685237
Giovannoni G, Tomic D, Bright JR, Havrdová E (2017) “No evident disease activity”: the use of combined assessments in the management of patients with multiple sclerosis. Mult Scler 23:1179–1187
doi: 10.1177/1352458517703193
Bertino E, Di Nicola P, Varalda A, et al (2012) Neonatal growth charts. In: Journal of Maternal-Fetal and Neonatal Medicine. pp. 67–69
Davey DA, MacGillivray I (1988) The classification and definition of the hypertensive disorders of pregnancy. Am J Obstet Gynecol 158:892–898. https://doi.org/10.1016/0002-9378(88)90090-7
doi: 10.1016/0002-9378(88)90090-7
pubmed: 3364501
Cohain JS, Buxbaum RE, Mankuta D (2017) Spontaneous first trimester miscarriage rates per woman among parous women with 1 or more pregnancies of 24 weeks or more. BMC Pregnancy Childbirth 17:437. https://doi.org/10.1186/s12884-017-1620-1
doi: 10.1186/s12884-017-1620-1
pubmed: 29272996
pmcid: 5741961
De Carolis S, Moresi S, Rizzo F et al (2019) Autoimmunity in obstetrics and autoimmune diseases in pregnancy. Best Pract Res Clin Obstet Gynaecol 60:66–76
doi: 10.1016/j.bpobgyn.2019.03.003
Marder W, Littlejohn EA, Somers EC (2016) Pregnancy and autoimmune connective tissue diseases. Best Pract Res Clin Rheumatol 30:63–80
doi: 10.1016/j.berh.2016.05.002
Dobson R, Dassan P, Roberts M, Giovannoni G, Nelson-Piercy C, Brex PA (2019) UK consensus on pregnancy in multiple sclerosis: ‘Association of British Neurologists’ guidelines. Pract Neurol 19:106–114
doi: 10.1136/practneurol-2018-002060
Savvidou MD, Xiao Q, Kaihura C, Anderson JM, Nicolaides KH (2008) Maternal circulating endothelial progenitor cells in normal singleton and twin pregnancy. Am J Obstet Gynecol 198:414.e1–414.e5. https://doi.org/10.1016/j.ajog.2007.10.800
doi: 10.1016/j.ajog.2007.10.800
Frohman EM, Monaco MC, Remington G, Ryschkewitsch C, Jensen PN, Johnson K, Perkins M, Liebner J, Greenberg B, Monson N, Frohman TC, Douek D, Major EO (2014) JC virus in CD34+ and CD19+ cells in patients with multiple sclerosis treated with natalizumab. JAMA Neurol 71:596–602. https://doi.org/10.1001/jamaneurol.2014.63
doi: 10.1001/jamaneurol.2014.63
pubmed: 24664166
Mousavi SH, Abroun S, Zarrabi M, Ahmadipanah M (2017) The effect of maternal and infant factors on cord blood yield. Pediatr Blood Cancer 64(7). https://doi.org/10.1002/pbc.26381
Al-Sweedan SA, Musalam L, Obeidat B (2013) Factors predicting the hematopoietic stem cells content of the umbilical cord blood. Transfus Apher Sci 48:247–252. https://doi.org/10.1016/j.transci.2013.01.003
doi: 10.1016/j.transci.2013.01.003
pubmed: 23415410