Telomeres and oocyte maturation rate are not reduced by COVID-19 except in severe cases

in Reproduction
Authors:
L Chico-Sordo IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain

Search for other papers by L Chico-Sordo in
Current site
Google Scholar
PubMed
Close
,
A M Polonio IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain

Search for other papers by A M Polonio in
Current site
Google Scholar
PubMed
Close
,
I Córdova-Oriz IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain

Search for other papers by I Córdova-Oriz in
Current site
Google Scholar
PubMed
Close
,
M Medrano IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain

Search for other papers by M Medrano in
Current site
Google Scholar
PubMed
Close
,
S Herraiz IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain

Search for other papers by S Herraiz in
Current site
Google Scholar
PubMed
Close
,
F Bronet IVIRMA Madrid, Madrid, Spain

Search for other papers by F Bronet in
Current site
Google Scholar
PubMed
Close
,
J A García-Velasco IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain
IVIRMA Madrid, Madrid, Spain
Rey Juan Carlos University, Edificio Departamental II, Alcorcón, Madrid, Spain

Search for other papers by J A García-Velasco in
Current site
Google Scholar
PubMed
Close
, and
E Varela IVI Foundation, The Health Research Institute La Fe (IIS La Fe) – Edificio Biopolo, Valencia, Spain
Rey Juan Carlos University, Edificio Departamental II, Alcorcón, Madrid, Spain

Search for other papers by E Varela in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-5361-3877

Correspondence should be addressed to E Varela; Email: Mariaelisa.Varela@ivirma.com
Restricted access
Rent on DeepDyve

Sign up for journal news

In brief

COVID-19 does not affect the telomeres or fertility outcomes in mild cases. However, in women with severe symptoms, telomeres of granulosa cells are shorter, and the oocyte maturation rate is decreased.

Abstract

The coronavirus SARS-CoV-2 causes COVID-19 disease and affects primarily the lungs and also other organs, causing accelerated cell aging. One of the main pathways involved in aging is telomere attrition, which ultimately leads to defective tissue regeneration and organ dysfunction. Indeed, short telomeres in aged people aggravate the COVID-19 symptoms, and COVID-19 survivors showed shorter telomeres in blood cells. The SARS-CoV-2 has been detected in testis, but the ovaries, which express the viral entry factors, have not been fully explored. Our objective was to analyze telomeres and reproductive outcomes in women who had COVID-19 and controls. In this prospective cohort study, granulosa cells (GCs) and blood were collected from 65 women. Telomere length (TL) was measured by high-throughput in situ hybridization. Mean TL of GCs and peripheral blood mononuclear cells (PBMCs) was alike in control and mild cases. However, mean TL of GCs was lower in severe cases compared to controls (P = 0.017). Control and COVID groups had similar ovarian reserve and number of total oocytes after puncture. However, the oocyte maturation rate was lower in severe cases (P =  0.018). Interestingly, a positive correlation between the oocyte maturation rate and TL of GCs was found in the control group (P = 0.024). Our findings point to a potential impact of the coronavirus infection on telomeres and reproductive outcomes in severe cases. This might be considered upon possible new SARS-CoV threats, to favor treatments that enhance oocyte maturation in women severely affected by coronavirus undergoing ART.

 

  • Collapse
  • Expand
  • Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, Vanstapel A, Werlein C, Stark H & Tzankov A et al.2020 Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. New England Journal of Medicine 383 120128. (https://doi.org/10.1056/NEJMoa2015432)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, Futcher AB, Greider CW & Harley CB 1992 Telomere length predicts replicative capacity of human fibroblasts. PNAS 89 1011410118. (https://doi.org/10.1073/pnas.89.21.10114)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Benetos A, Lai TP, Toupance S, Labat C, Verhulst S, Gautier S, Ungeheuer MN, Perret-Guillaume C, Levy D & Susser E et al.2021 The nexus between telomere length and lymphocyte count in seniors hospitalized with COVID-19. Journals of Gerontology: Series A, Biological Sciences and Medical Sciences 76 e97e101. (https://doi.org/10.1093/gerona/glab026)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bentov Y, Beharier O, Moav-Zafrir A, Kabessa M, Godin M, Greenfield CS, Ketzinel-Gilad M, Ash Broder E, Holzer HEG & Wolf D et al.2021 Ovarian follicular function is not altered by SARS-CoV-2 infection or BNT162b2 mRNA COVID-19 vaccination. Human Reproduction 36 25062513. (https://doi.org/10.1093/humrep/deab182)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Blackburn EH 1991 Structure and function of telomeres. Nature 350 569573. (https://doi.org/10.1038/350569a0)

  • Butts S, Riethman H, Ratcliffe S, Shaunik A, Coutifaris C & Barnhart K 2009 Correlation of telomere length and telomerase activity with occult ovarian insufficiency. Journal of Clinical Endocrinology and Metabolism 94 48354843. (https://doi.org/10.1210/jc.2008-2269)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Canela A, Vera E, Klatt P & Blasco MA 2007 High-throughput telomere length quantification by FISH and its application to human population studies. PNAS 104 53005305. (https://doi.org/10.1073/pnas.0609367104)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chang EM, Song HS, Lee DR, Lee WS & Yoon TK 2014 In vitro maturation of human oocytes: its role in infertility treatment and new possibilities. Clinical and Experimental Reproductive Medicine 41 4146. (https://doi.org/10.5653/cerm.2014.41.2.41)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chico-Sordo L, Córdova-Oriz I, Polonio AM, S-Mellado LS, Medrano M, García-Velasco JA & Varela E 2021 Reproductive aging and telomeres: are women and men equally affected? Mechanisms of Ageing and Development 198 111541. (https://doi.org/10.1016/j.mad.2021.111541)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Crinion RA & Hofstad MS 1972 Pathogenicity of four serotypes of avian infectious bronchitis virus for the oviduct of young chickens of various ages. Avian Diseases 16 351363. (https://doi.org/10.2307/1588800)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • de Lange T 2005 Shelterin: the protein complex that shapes and safeguards human telomeres. Genes and Development 19 21002110. (https://doi.org/10.1101/gad.1346005)

  • Donate LE & Blasco MA 2011 Telomeres in cancer and ageing. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences 366 7684. (https://doi.org/10.1098/rstb.2010.0291)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dos Santos GA, Pimenta R, Viana NI, Guimaraes VR, Romao P, Candido P, De Camargo JA, Hatanaka DM, Queiroz PG & Teruya A et al.2021 Shorter leukocyte telomere length is associated with severity of COVID-19 infection. Biochemistry and Biophysics Reports 27 101056. (https://doi.org/10.1016/j.bbrep.2021.101056)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Erdel F, Kratz K, Willcox S, Griffith JD, Greene EC & De Lange T 2017 Telomere recognition and assembly mechanism of mammalian shelterin. Cell Reports 18 4153. (https://doi.org/10.1016/j.celrep.2016.12.005)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fabris AM, Cruz M, Legidos V, Iglesias C, Munoz M & Garcia-Velasco JA 2017 Dual triggering with gonadotropin-releasing hormone agonist and standard dose human chorionic gonadotropin in patients with a high immature oocyte rate. Reproductive Sciences 24 12211225. (https://doi.org/10.1177/1933719116682873)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Flores I, Canela A, Vera E, Tejera A, Cotsarelis G & Blasco MA 2008 The longest telomeres: a general signature of adult stem cell compartments. Genes and Development 22 654667. (https://doi.org/10.1101/gad.451008)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Franasiak JM, Forman EJ, Hong KH, Werner MD, Upham KM, Treff NR & Scott Jr RT 2014 The nature of aneuploidy with increasing age of the female partner: a review of 15,169 consecutive trophectoderm biopsies evaluated with comprehensive chromosomal screening. Fertility and Sterility 101 656.e1–663.e1. (https://doi.org/10.1016/j.fertnstert.2013.11.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Griffin D, Feinn R, Engmann L, Nulsen J, Budinetz T & Benadiva C 2014 Dual trigger with gonadotropin-releasing hormone agonist and standard dose human chorionic gonadotropin to improve oocyte maturity rates. Fertility and Sterility 102 405409. (https://doi.org/10.1016/j.fertnstert.2014.04.028)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hemann MT, Strong MA, Hao LY & Greider CW 2001 The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107 6777. (https://doi.org/10.1016/s0092-8674(0100504-9)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hodgens A & Gupta V 2022 Severe Acute Respiratory Syndrome. Treasure Island (FL): StatPearls. (https://doi.org/10.1038/nm1143)

  • Hoffmann M, Kleine-Weber H, Schroeder S, Kruger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH & Nitsche A et al.2020 SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 181 271.e8–280.e8. (https://doi.org/10.1016/j.cell.2020.02.052)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J & Gu X et al.2020 Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395 497506. (https://doi.org/10.1016/S0140-6736(2030183-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kashani KB 2020 Hypoxia in COVID-19: sign of severity or cause for poor outcomes. Mayo Clinic Proceedings 95 10941096. (https://doi.org/10.1016/j.mayocp.2020.04.021)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kohlrausch FB, Wang F, Chamani I & Keefe DL 2021 Telomere shortening and fusions: a link to aneuploidy in early human embryo development. Obstetrical and Gynecological Survey 76 429436. (https://doi.org/10.1097/OGX.0000000000000907)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kyle MH, Glassman ME, Khan A, Fernandez CR, Hanft E, Emeruwa UN, Scripps T, Walzer L, Liao GV & Saslaw M et al.2020 A review of newborn outcomes during the COVID-19 pandemic. Seminars in Perinatology 44 151286. (https://doi.org/10.1016/j.semperi.2020.151286)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lara-Molina EE, Franasiak JM, Marin D, Tao X, Diaz-Gimeno P, Florensa M, Martin M, Seli E & Pellicer A 2020 Cumulus cells have longer telomeres than leukocytes in reproductive-age women. Fertility and Sterility 113 217223. (https://doi.org/10.1016/j.fertnstert.2019.08.089)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liu W & Zhu GJ 2003 Expression of telomerase in human ovarian luteinized granulosa cells and its relationship to ovarian function. Zhonghua Fu Chan Ke Za Zhi 38 402404.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liu L, Bailey SM, Okuka M, Munoz P, Li C, Zhou L, Wu C, Czerwiec E, Sandler L & Seyfang A et al.2007 Telomere lengthening early in development. Nature Cell Biology 9 14361441. (https://doi.org/10.1038/ncb1664)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lopez-Otin C, Blasco MA, Partridge L, Serrano M & Kroemer G 2013 The hallmarks of aging. Cell 153 11941217. (https://doi.org/10.1016/j.cell.2013.05.039)

  • Luay A, Al-Kawaz U & Mohsin E 2022 O-253 impact of Covid-19 infection on male seminal and hormonal parameters. Human Reproduction 37 deac106 .035. (https://doi.org/10.1093/humrep/deac106.035)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ma X, Guan C, Chen R, Wang Y, Feng S, Wang R, Qu G, Zhao S, Wang F & Wang X et al.2021 Pathological and molecular examinations of postmortem testis biopsies reveal SARS-CoV-2 infection in the testis and spermatogenesis damage in COVID-19 patients. Cellular and Molecular Immunology 18 487489. (https://doi.org/10.1038/s41423-020-00604-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Martinez P & Blasco MA 2017 Telomere-driven diseases and telomere-targeting therapies. Journal of Cell Biology 216 875887. (https://doi.org/10.1083/jcb.201610111)

  • Martinez P, Thanasoula M, Munoz P, Liao C, Tejera A, Mcnees C, Flores JM, Fernandez-Capetillo O, Tarsounas M & Blasco MA 2009 Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes and Development 23 20602075. (https://doi.org/10.1101/gad.543509)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mongelli A, Barbi V, Gottardi Zamperla M, Atlante S, Forleo L, Nesta M, Massetti M, Pontecorvi A, Nanni S & Farsetti A et al.2021 Evidence for biological age acceleration and telomere shortening in COVID-19 survivors. International Journal of Molecular Sciences 22 6151. (https://doi.org/10.3390/ijms22116151)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Munoz-Lorente MA, Cano-Martin AC & Blasco MA 2019 Mice with hyper-long telomeres show less metabolic aging and longer lifespans. Nature Communications 10 4723. (https://doi.org/10.1038/s41467-019-12664-x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Olovnikov AM 1973 A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. Journal of Theoretical Biology 41 181190. (https://doi.org/10.1016/0022-5193(7390198-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Olsen KW, Castillo-Fernandez J, Zedeler A, Freiesleben NC, Bungum M, Chan AC, Cardona A, Perry JRB, Skouby SO & Borup R et al.2020 A distinctive epigenetic ageing profile in human granulosa cells. Human Reproduction 35 13321345. (https://doi.org/10.1093/humrep/deaa071)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ovali F 2020 SARS-CoV-2 infection and the newborn. Frontiers in Pediatrics 8 294. (https://doi.org/10.3389/fped.2020.00294)

  • Phan LT, Nguyen TV, Luong QC, Nguyen TV, Nguyen HT, Le HQ, Nguyen TT, Cao TM & Pham QD 2020 Importation and human-to-human transmission of a novel coronavirus in Vietnam. New England Journal of Medicine 382 872874. (https://doi.org/10.1056/NEJMc2001272)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Polonio AM, Chico-Sordo L, Cordova-Oriz I, Medrano M, Garcia-Velasco JA & Varela E 2020 Impact of ovarian aging in reproduction: from telomeres and mice models to ovarian rejuvenation. Yale Journal of Biology and Medicine 93 561569.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Prescott JC & Blackburn EH 2000 Telomerase RNA template mutations reveal sequence-specific requirements for the activation and repression of telomerase action at telomeres. Molecular and Cellular Biology 20 29412948. (https://doi.org/10.1128/MCB.20.8.2941-2948.2000)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rothe C, Schunk M, Sothmann P, Bretzel G, Froeschl G, Wallrauch C, Zimmer T, Thiel V, Janke C & Guggemos W et al.2020 Transmission of 2019-nCoV infection from an asymptomatic contact in Germany. New England Journal of Medicine 382 970971. (https://doi.org/10.1056/NEJMc2001468)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Russo V, Berardinelli P, Martelli A, Di Giacinto O, Nardinocchi D, Fantasia D & Barboni B 2006 Expression of telomerase reverse transcriptase subunit (tert) and telomere sizing in pig ovarian follicles. Journal of Histochemistry and Cytochemistry 54 443455. (https://doi.org/10.1369/jhc.4A6603.2006)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sanchez-Vazquez R, Guio-Carrion A, Zapatero-Gaviria A, Martinez P & Blasco MA 2021 Shorter telomere lengths in patients with severe COVID-19 disease. Aging 13 115. (https://doi.org/10.18632/aging.202463)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Segars J, Katler Q, Mcqueen DB, Kotlyar A, Glenn T, Knight Z, Feinberg EC, Taylor HS, Toner JP & Kawwass JF et al.2020. Prior and novel coronaviruses, coronavirus disease 2019 (COVID-19), and human reproduction: what is known?. Fertility and Sterility 113 11401149. (https://doi.org/10.1016/j.fertnstert.2020.04.025)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sfeir A, Kosiyatrakul ST, Hockemeyer D, Macrae SL, Karlseder J, Schildkraut CL & De Lange T 2009 Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138 90103. (https://doi.org/10.1016/j.cell.2009.06.021)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stanley KE, Thomas E, Leaver M & Wells D 2020 Coronavirus disease-19 and fertility: viral host entry protein expression in male and female reproductive tissues. Fertility and Sterility 114 3343. (https://doi.org/10.1016/j.fertnstert.2020.05.001)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stelzig KE, Canepa-Escaro F, Schiliro M, Berdnikovs S, Prakash YS & Chiarella SE 2020 Estrogen regulates the expression of SARS-CoV-2 receptor ACE2 in differentiated airway epithelial cells. American Journal of Physiology: Lung Cellular and Molecular Physiology 318 L1280L1281. (https://doi.org/10.1152/ajplung.00153.2020)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tumpel S & Rudolph KL 2012 The role of telomere shortening in somatic stem cells and tissue aging: lessons from telomerase model systems. Annals of the New York Academy of Sciences 1266 2839. (https://doi.org/10.1111/j.1749-6632.2012.06547.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Varela E & Blasco MA 2010 2009 Nobel prize in physiology or medicine: telomeres and telomerase. Oncogene 29 15611565. (https://doi.org/10.1038/onc.2010.15)

  • Varela E, Schneider RP, Ortega S & Blasco MA 2011 Different telomere-length dynamics at the inner cell mass versus established embryonic stem (ES) cells. PNAS 108 1520715212. (https://doi.org/10.1073/pnas.1105414108)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Varela E, Munoz-Lorente MA, Tejera AM, Ortega S & Blasco MA 2016 Generation of mice with longer and better preserved telomeres in the absence of genetic manipulations. Nature Communications 7 11739. (https://doi.org/10.1038/ncomms11739)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vera E, Bernardes De Jesus B, Foronda M, Flores JM & Blasco MA 2012 The rate of increase of short telomeres predicts longevity in mammals. Cell Reports 2 732737. (https://doi.org/10.1016/j.celrep.2012.08.023)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang W, Chen H, Li R, Ouyang N, Chen J, Huang L, Mai M, Zhang N, Zhang Q & Yang D 2014 Telomerase activity is more significant for predicting the outcome of IVF treatment than telomere length in granulosa cells. Reproduction 147 649657. (https://doi.org/10.1530/REP-13-0223)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang M, Yang Q, Ren X, Hu J, Li Z, Long R, Xi Q, Zhu L & Jin L 2021a Investigating the impact of asymptomatic or mild SARS-CoV-2 infection on female fertility and in vitro fertilization outcomes: a retrospective cohort study. EClinicalMedicine 38 101013. (https://doi.org/10.1016/j.eclinm.2021.101013)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang Q, Codd V, Raisi-Estabragh Z, Musicha C, Bountziouka V, Kaptoge S, Allara E, Angelantonio ED, Butterworth AS & Wood AM et al.2021b Shorter leukocyte telomere length is associated with adverse COVID-19 outcomes: a cohort study in UK Biobank. EBiomedicine 70 103485. (https://doi.org/10.1016/j.ebiom.2021.103485)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wu C, Chen X, Cai Y, Xia J, Zhou X, Xu S, Huang H, Zhang L, Zhou X & Du C et al.2020 Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Internal Medicine 180 934943. (https://doi.org/10.1001/jamainternmed.2020.0994)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wu M, Ma L, Xue L, Zhu Q, Zhou S, Dai J, Yan W, Zhang J & Wang S 2021 Co-expression of the SARS-CoV-2 entry molecules ACE2 and TMPRSS2 in human ovaries: identification of cell types and trends with age. Genomics 113 34493460. (https://doi.org/10.1016/j.ygeno.2021.08.012)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xu X, Chen X, Zhang X, Liu Y, Wang Z, Wang P, Du Y, Qin Y & Chen ZJ 2017 Impaired telomere length and telomerase activity in peripheral blood leukocytes and granulosa cells in patients with biochemical primary ovarian insufficiency. Human Reproduction 32 201207. (https://doi.org/10.1093/humrep/dew283)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zaim S, Chong JH, Sankaranarayanan V & Harky A 2020 COVID-19 and multiorgan response. Current Problems in Cardiology 45 100618. (https://doi.org/10.1016/j.cpcardiol.2020.100618)

    • PubMed
    • Search Google Scholar
    • Export Citation