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Transmission, seroprevalence, and maternal-fetal impact of lymphocytic choriomeningitis virus

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Abstract

Congenital infections can have devastating short- and long-term impacts on the developing fetus. Lymphocytic choriomeningitis virus (LCMV) is a zoonotic pathogen of concern that causes a severe congenital syndrome but is under-recognized and under-studied. Herein we review data on the natural animal reservoirs of LCMV, modes of transmission to humans, seroprevalence of LCMV worldwide in both pregnant and non-pregnant individuals, mechanisms of viral dissemination to placenta and fetus, and impact of climate change on viral transmission. We highlight opportunities to enhance awareness of congenital LCMV and provide recommendations for prevention and monitoring among at-risk pregnant people.

Impact

  • Key message of the article: LCMV is a zoonotic virus that poses a major threat to maternal-fetal health.

  • Adds to the existing literature: We comprehensively address transmission of LCMV from the natural reservoir to the pregnant individual, placenta, and fetus.

  • Impact: Available data call for enhanced patient and provider awareness about congenital LCMV during pregnancy, as well as a need for efforts to better define the seroprevalence and impact of congenital LCMV worldwide.

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References

  1. Pereira, L. Congenital viral infection: Traversing the uterine-placental interface. Annu. Rev. Virol. 5, 273–299 (2018).

    Article  CAS  PubMed  Google Scholar 

  2. Nahmias, A. J., Walls, K. W., Stewart, J. A., Herrmann, K. L. & Flynt, W. J. The ToRCH complex-perinatal infections associated with toxoplasma and rubella, cytomegol- and herpes simplex viruses. Pediatr. Res. 5, 405–406 (1971).

    Article  Google Scholar 

  3. Money, D. et al. Guidelines for the management of herpes simplex virus in pregnancy. J. Obstet. Gynaecol. Can. 30, 514–519 (2008).

    Article  PubMed  Google Scholar 

  4. Panchaud, A., Stojanov, M., Ammerdorffer, A., Vouga, M. & Baud, D. Emerging role of Zika virus in adverse fetal and neonatal outcomes. Clin. Microbiol Rev. 29, 659–694 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Peyron, F. et al. Maternal and congenital toxoplasmosis: Diagnosis and treatment recommendations of a french multidisciplinary working group. Pathogens 8, 24 (2019).

    Article  MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wang, Z., Tao, X., Liu, S., Zhao, Y. & Yang, X. An update review on listeria infection in pregnancy. Infect. Drug Resist. 14, 1967–1978 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Armstrong, C. & Lillie, R. D. Experimental lymphocytic choriomeningitis of monkeys and mice produced by a virus encountered in studies of the 1933 St. Louis encephalitis epidemic. Public Health Rep. (1896–1970) 49, 1019–1027 (1934).

    Article  Google Scholar 

  8. Traub, E. A filterable virus recovered from white mice. Science 81, 298–299 (1935).

    Article  CAS  PubMed  ADS  Google Scholar 

  9. Meyer, H. M., Johnson, R. T., Crawford, I. P., Dascomb, H. E. & Rogers, N. G. Central nervous system syndromes of “viral” etiology A study of 713 cases. Am. J. Med. 29, 334–347 (1960).

    Article  PubMed  Google Scholar 

  10. Gregg, M. B. Recent outbreaks of lymphocytic choriomeningitis in the United States of America. Bull. World Heal. Organ. 52, 549–553 (1975).

    CAS  Google Scholar 

  11. Ackermann, R. et al. Syrische goldhamster als uberträger von lymphozytärer choriomeningitis. Dtsch. Medizinische Wochenschr. 97, 1725–1731 (1972).

    Article  CAS  Google Scholar 

  12. Vilibic-Cavlek, T. et al. Lymphocytic choriomeningitis—emerging trends of a neglected virus: A narrative review. Trop. Med. Infect. Dis. 6, 88 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bonthius, D. J. et al. Congenital lymphocytic choriomeningitis virus infection: spectrum of disease. Ann. Neurol. 62, 347–355 (2007).

    Article  PubMed  Google Scholar 

  14. Bonthius, D. J. Lymphocytic choriomeningitis virus: A prenatal and postnatal threat. Adv. Pediatr. 56, 75–86 (2009).

    Article  PubMed  Google Scholar 

  15. Bonthius, D. J. Lymphocytic choriomeningitis virus: An under-recognized cause of neurologic disease in the fetus, child, and adult. Semin Pediatr. Neurol. 19, 89–95 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bishop, D. H. L. & Auperin, D. D. Arenavirus gene structure and organization. in Arenaviruses vol. 133 5–17 (Springer, 1987).

  17. Buchmeier, M. J. & Zajac, A. J. Lymphocytic choriomeningitis virus. In Persistent Viral Infections. (eds Ahmed, R. & Chen, I.) pp. 575–605 (Wiley, New York, 1999).

  18. Meyer, B. J., Torre, J. C. D. L. & Southern, P. J. Arenaviruses: genomic RNAs, transcription, and replication. Arenaviruses I, Epidemiol., Mol. Cell Biol. Arenaviruses 262, 139–157 (2002).

    Article  CAS  Google Scholar 

  19. Rollin, P. E., Nichol, S. T., Zaki, S. & Ksiazek, T. G. Arenaviruses and Filoviruses. in Manual of Clinical Microbiology (eds. Jorgensen, J. H. et al.) 1669–1686 https://doi.org/10.1128/9781555817381.ch97 (ASM Press, 2015).

  20. Childs, J. E., Klein, S. L. & Glass, G. E. A case study of two rodent-borne viruses: Not always the same old suspects. Front. Ecol. Evolut. 7, (2019).

  21. Zhang, L. et al. Isolation and genomic characterization of lymphocytic choriomeningitis virus in ticks from northeastern China. Transbound. Emerg. Dis. 65, 1733–1739 (2018).

    Article  CAS  PubMed  Google Scholar 

  22. Danes, L., Benda, R. & Fuchs, M. Experimental inhalation with the lymphocytic choriomeningitis virus (WE strain) of the monkeys of the Macacus cynomolgus and Macacus rhesus species. Bratisl. Lék. List. 2, 71–79 (1963).

    CAS  Google Scholar 

  23. Mims, C. A. Effect on the fetus of maternal infection with lymphocytic choriomeningitis (LCM) virus. J. Infect. Dis. 120, 582–597 (1969).

    Article  CAS  PubMed  Google Scholar 

  24. Jamieson, D. J., Kourtis, A. P., Bell, M. & Rasmussen, S. A. Lymphocytic choriomeningitis virus: An emerging obstetric pathogen? Am. J. Obstet. Gynecol. 194, 1532–1536 (2006).

    Article  PubMed  Google Scholar 

  25. Ferenc, T., Vujica, M., Mrzljak, A. & Vilibic-Cavlek, T. Lymphocytic choriomeningitis virus: An under-recognized congenital teratogen. World J. Clin. Cases 10, 8922–8931 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Rajini, B., Zeng, J., Suvas, P. K., Dech, H. M. & Onami, T. M. both systemic and mucosal LCMV immunization generate robust viral-specific IgG in mucosal secretions, but elicit poor LCMV-specific IgA. Viral Immunol. 23, 377–384 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yin, C. et al. Dissemination of lymphocytic choriomeningitis virus from the gastric mucosa requires G protein-coupled signaling. J. Virol. 72, 8613–8619 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Childs, J. E., Glass, G. E., Korch, G. W., Ksiazek, T. G. & Leduc, J. W. Lymphocytic choriomeningitis virus infection and house mouse (mus musculus) distribution in urban baltimore. Am. J. Trop. Med. Hyg. 47, 27–34 (1992).

    Article  CAS  PubMed  Google Scholar 

  29. Riera, L. et al. Serological study of the lymphochoriomeningitis virus (LCMV) in an inner city of Argentina. J. Méd. Virol. 76, 285–289 (2005).

    Article  PubMed  Google Scholar 

  30. Ushijima, Y. et al. Identification of potential novel hosts and the risk of infection with lymphocytic choriomeningitis virus in humans in Gabon, Central Africa. Int. J. Infect. Dis. 105, 452–459 (2021).

    Article  CAS  PubMed  Google Scholar 

  31. Knust, B. et al. Lymphocytic choriomeningitis virus in employees and mice at multipremises feeder-rodent operation, United States, 2012. Emerg. Infect. Dis. 20, 240–247 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sarli, J., Lutermann, H., Alagaili, A. N., Mohammed, O. B. & Bennett, N. C. Seasonal reproduction in the Arabian spiny mouse, Acomys dimidiatus (Rodentia: Muridae) from Saudi Arabia: The role of rainfall and temperature. J. Arid Environ. 124, 352–359 (2016).

    Article  ADS  Google Scholar 

  33. Dantas, M. R. T., Souza-Junior, J. B. F., Castelo, T. S., Lago, A. E. A. & Silva, A. R. Understanding how environmental factors influence reproductive aspects of wild myomorphic and hystricomorphic rodents. Anim. Reprod. 18, e20200213 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sipari, S. et al. Climate change accelerates winter transmission of a zoonotic pathogen. Ambio 51, 508–517 (2022).

    Article  PubMed  ADS  Google Scholar 

  35. Evander, M. & Ahlm, C. Milder winters in northern Scandinavia may contribute to larger outbreaks of haemorrhagic fever virus. Glob. Heal. Action 2, 2020 (2009).

    Article  Google Scholar 

  36. Tian, H. et al. Interannual cycles of Hantaan virus outbreaks at the human–animal interface in Central China are controlled by temperature and rainfall. Proc. Natl Acad. Sci. 114, 8041–8046 (2017).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  37. Kallio, E. R. et al. Cyclic hantavirus epidemics in humans — Predicted by rodent host dynamics. Epidemics 1, 101–107 (2009).

    Article  PubMed  Google Scholar 

  38. Brown, L. M. & Laco, J. Rodent control and public health: A description of local rodent control programs. J. Environ. Heal. 78, 28–29 (2015).

    Google Scholar 

  39. Vilibic-Cavlek, T. et al. Prevalence and risk factors for lymphocytic choriomeningitis virus infection in continental croatian regions. Trop. Med. Infect. Dis. 6, 67 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Childs, J. E. et al. Human-rodent contact and infection with lymphocytic choriomeningitis and seoul viruses in an inner-city population. Am. J. Tropical Med. Hyg. 44, 117–121 (1991).

    Article  CAS  Google Scholar 

  41. Stephensen, C. B. et al. Prevalence of serum antibodies against lymphocytic choriomeningitis virus in selected populations from two U.S. cities. J. Méd. Virol. 38, 27–31 (1992).

    Article  CAS  PubMed  Google Scholar 

  42. Knust, B. et al. Exposure to lymphocytic choriomeningitis virus, New York, USA. Emerg. Infect. Dis. 17, 1324–1325 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  43. DeLamballerie, X., Fulhorst, C. F. & Charrel, R. N. Prevalence of antibodies to lymphocytic choriomeningitis virus in blood donors in southeastern France. Transfusion 47, 172–173 (2007).

    Article  Google Scholar 

  44. Marrie, T. J. & Saron, M. F. Seroprevalence of lymphocytic choriomeningitis virus in Nova Scotia. Am. J. Trop. Med. Hyg. 58, 47–49 (1998).

    Article  CAS  PubMed  Google Scholar 

  45. Lledó, L., Gegúndez, M. I., Saz, J. V., Bahamontes, N. & Beltrán, M. Lymphocytic choriomeningitis virus infection in a province of Spain: Analysis of sera from the general population and wild rodents. J. Méd. Virol. 70, 273–275 (2003).

    Article  PubMed  Google Scholar 

  46. Alburkat, H. et al. Lymphocytic Choriomeningitis Virus Infections and Seroprevalence, Southern Iraq. Emerg. Infect. Dis. 26, 3002–3006 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Fevola, C. et al. Seroprevalence of lymphocytic choriomeningitis virus and Ljungan virus in Finnish patients with suspected neurological infections. J. Méd. Virol. 90, 429–435 (2018).

    Article  CAS  PubMed  Google Scholar 

  48. Juncker-Voss, M. et al. [Screening for antibodies against zoonotic agents among employees of the Zoological Garden of Vienna, Schönbrunn, Austria]. Berl. und Munch. tierarztliche Wochenschr. 117, 404–409 (2004).

    Google Scholar 

  49. Kallio-kokko, H. et al. Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy. Epidemiol. Amp Infect. 134, 830–836 (2005).

    Article  Google Scholar 

  50. Cuong, N. V. et al. Rodents and risk in the mekong delta of Vietnam: seroprevalence of selected zoonotic viruses in rodents and humans. Vector-Borne Zoonotic Dis. 15, 65–72 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Dobec, M., Dzelalija, B., Punda‐Polic, V. & Zoric, I. High prevalence of antibodies to lymphocytic choriomeningitis virus in a murine typhus endemic region in Croatia. J. Méd. Virol. 78, 1643–1647 (2006).

    Article  CAS  PubMed  Google Scholar 

  52. Lehmann‐Grube, F., Kallay, M., Ibscher, B. & Schwartz, R. Serologic diagnosis of human infections with lymphocytic choriomeningitis virus: Comparative evaluation of seven methods. J. Méd. Virol. 4, 125–136 (1979).

    Article  PubMed  Google Scholar 

  53. Enninga, E. A. L. & Theiler, R. N. Lymphocytic choriomeningitis virus infection demonstrates higher replicative capacity and decreased antiviral response in the first-trimester placenta. J. Immunol. Res. 2019, 7375217 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Barton, L. L., Mets, M. B. & Beauchamp, C. L. Lymphocytic choriomeningitis virus: Emerging fetal teratogen. Am. J. Obstet. Gynecol. 187, 1715–1716 (2002).

    Article  PubMed  Google Scholar 

  55. Constantin, C. M. et al. Normal establishment of virus-specific memory CD8 T cell pool following primary infection during pregnancy. J. Immunol. 179, 4383–4389 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. León-Juárez, M. et al. Cellular and molecular mechanisms of viral infection in the human placenta. Pathog. Dis. 75, ftx093 (2017).

    Article  PubMed  Google Scholar 

  57. Beyer, W. R., Pöpplau, D., Garten, W., von Laer, D. & Lenz, O. Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J. Virol. 77, 2866–2872 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Spiropoulou, C. F., Kunz, S., Rollin, P. E., Campbell, K. P. & Oldstone, M. B. A. New World Arenavirus Clade C, but Not Clade A and B Viruses, Utilizes α-Dystroglycan as Its Major Receptor. J. Virol. 76, 5140–5146 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Cao, W. et al. Identification of α-dystroglycan as a receptor for lymphocytic choriomeningitis virus and lassa fever virus. Science 282, 2079–2081 (1998).

    Article  CAS  PubMed  ADS  Google Scholar 

  60. Borrow, P. & Oldstone, M. B. Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J. Virol. 66, 7270–7281 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Simone, C. D., Zandonatti, M. A. & Buchmeier, M. J. Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike. Virology 198, 455–465 (1994).

    Article  PubMed  Google Scholar 

  62. Eschli, B. et al. Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J. Virol. 80, 5897–5907 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Burns, J. W. & Buchmeier, M. J. Protein-protein interactions in lymphocytic choriomeningitis virus. Virology 183, 620–629 (1991).

    Article  CAS  PubMed  Google Scholar 

  64. Liu, J. et al. Genome-wide knockout screen identifies human sialomucin CD164 as an essential entry factor for lymphocytic choriomeningitis virus. mBio 13, e00205–e00222 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Negi, V. D., Khurana, S. & Bonney, E. A. Interleukin-10 delays viral clearance in the placenta and uterus of mice with acute lymphocytic choriomeningitis virus infection during pregnancy. Front. Virol. 2, (2022).

  66. Antoniou, A. N. & Powis, S. J. Pathogen evasion strategies for the major histocompatibility complex class I assembly pathway. Immunology 124, 1–12 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ackermann, R. et al. Fetal infection of the baboon(Papio cynocephalus) with lymphocytic choriomeningitis virus. Arch. Virol. 60, 311–323 (1979).

    Article  CAS  PubMed  Google Scholar 

  68. Takagi, T., Ohsawa, M., Morita, C., Sato, H. & Ohsawa, K. Genomic analysis and pathogenic characteristics of lymphocytic choriomeningitis virus strains isolated in Japan. Comp. Med. 62, 185–192 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Takagi, T. et al. Difference of two new LCMV strains in lethality and viral genome load in tissues. Exp. Anim. 66, 16–0097 (2017).

    Article  Google Scholar 

  70. Buchmeier, M. J., Welsh, R. M., Dutko, F. J. & Oldstone, M. B. A. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30, 275–331 (1980).

    Article  CAS  PubMed  Google Scholar 

  71. Amman, B. R. et al. Pet rodents and fatal lymphocytic choriomeningitis in transplant patients. Emerg. Infect. Dis. 13, 719–725 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Emonet, S., Retornaz, K., Gonzalez, J. P., de Lamballerie, X. & Charrel, R. N. Mouse-to-human transmission of variant lymphocytic choriomeningitis virus. Emerg. Infect. Dis. 13, 472–475 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Gustavo, P. et al. A new arenavirus in a cluster of fatal transplant-associated diseases. N. Engl. J. Med. 358, 991–998 (2008).

    Article  Google Scholar 

  74. Bonthius, D. J., Nichols, B., Harb, H., Mahoney, J. & Karacay, B. Lymphocytic choriomeningitis virus infection of the developing brain: critical role of host age. Ann. Neurol. 62, 356–374 (2007).

    Article  PubMed  Google Scholar 

  75. Baines, K. J. et al. Antiviral inflammation during early pregnancy reduces placental and fetal growth trajectories. J. Immunol. 204, 694–706 (2020).

    Article  CAS  PubMed  Google Scholar 

  76. Woods, L., Perez-Garcia, V. & Hemberger, M. Regulation of Placental Development and Its Impact on Fetal Growth—New Insights From Mouse Models. Front. Endocrinol. 9, (2018).

  77. Hemberger, M., Hanna, C. W. & Dean, W. Mechanisms of early placental development in mouse and humans. Nat. Rev. Genet. 21, 27–43 (2020).

    Article  CAS  PubMed  Google Scholar 

  78. Marsh, B. & Blelloch, R. Single nuclei RNA-seq of mouse placental labyrinth development. eLife 9, e60266 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Buchrieser, J. et al. IFITM proteins inhibit placental syncytiotrophoblast formation and promote fetal demise. Sci. (N. Y., N. Y.) 365, 176–180 (2019).

    Article  CAS  ADS  Google Scholar 

  80. Yu, W., Hu, X. & Cao, B. Viral infections during pregnancy: The big challenge threatening maternal and fetal health. Matern Fetal Med. 4, 72–86 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Jaremek, A., Jeyarajah, M. J., Bhattad, G. J. & Renaud, S. J. Omics approaches to study formation and function of human placental syncytiotrophoblast. Front. Cell Dev. Biol. 9, (2021).

  82. LaMarca, H. L., Nelson, A. B., Scandurro, A. B., Whitley, G. S. & Morris, C. A. Human cytomegalovirus-induced inhibition of cytotrophoblast invasion in a first trimester extravillous cytotrophoblast cell line. Placenta 27, 137–147 (2006).

    Article  CAS  PubMed  Google Scholar 

  83. Aldo, P. B., Mulla, M. J., Romero, R., Mor, G. & Abrahams, V. M. Viral ssRNA induces first trimester trophoblast apoptosis through an inflammatory mechanism. Am. J. Reprod. Immunol. 64, 27–37 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Campen, H. V. et al. Maternal influenza A virus infection restricts fetal and placental growth and adversely affects the fetal thymic transcriptome. Viruses 12, 1003 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Creisher, P. S. et al. Downregulation of transcriptional activity, increased inflammation, and damage in the placenta following in utero Zika Virus infection is associated with adverse pregnancy outcomes. Front. Virol. 2, (2022).

  86. Amirhessami-Aghili, N. et al. Human cytomegalovirus infection of human placental explants in culture: Histologic and immunohistochemical studies. Am. J. Obstet. Gynecol. 156, 1365–1374 (1987).

    Article  CAS  PubMed  Google Scholar 

  87. Pencole, L. et al. Congenital lymphocytic choriomeningitis virus: A review. Prenat. Diagn. 42, 1059–1069 (2022).

    Article  PubMed  Google Scholar 

  88. Meritet, J. F. et al. A case of congenital lymphocytic choriomeningitis virus (LCMV) infection revealed by hydrops fetalis. Prenat. Diagn. 29, 626–627 (2009).

    Article  CAS  PubMed  Google Scholar 

  89. Delaine, M. et al. Microcephaly caused by lymphocytic choriomeningitis virus. Emerg. Infect. Dis. 23, 1548–1550 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Tevaearai, F., Moser, L. & Pomar, L. Prenatal diagnosis of congenital lymphocytic choriomeningitis virus infection: A case report. Viruses 14, 2586 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Rawlinson, W. D. et al. Congenital cytomegalovirus infection in pregnancy and the neonate: Consensus recommendations for prevention, diagnosis, and therapy. Lancet Infect. Dis. 17, e177–e188 (2017).

    Article  PubMed  Google Scholar 

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Funding

This work was supported by NIH (NIAID) K08AI151265 and the Children’s Hospital of Philadelphia Research Institute (to S.M.G).

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  1. These authors contributed equally: Natalie R. Olivieri, Loui Othman.

Authors and Affiliations

  1. Division of Neonatology, Children’s Hospital of Philadelphia, Philadelphia, PA, USA

    Natalie R. Olivieri, Loui Othman, Dustin D. Flannery & Scott M. Gordon

  2. Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Dustin D. Flannery & Scott M. Gordon

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  1. Natalie R. Olivieri
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N.R.O., L.O., D.D.F., and S.M.G. conceptualized the article. N.R.O., L.O., and S.M.G. drafted the article. D.D.F. critically revised the article.

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Olivieri, N.R., Othman, L., Flannery, D.D. et al. Transmission, seroprevalence, and maternal-fetal impact of lymphocytic choriomeningitis virus. Pediatr Res 95, 456–463 (2024). https://doi.org/10.1038/s41390-023-02859-w

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