Arboviruses and pregnancy: are the threats visible or hidden?

Najeh Hcini1,2, Véronique Lambert1, Olivier Picone3, Jean-Francois Carod4, Gabriel Carles1, Léo Pomar5, Loïc Epelboin6, Mathieu Nacher7
1Department of Obstetrics and Gynecology, West French Guiana Hospital Center, Saint-Laurent-du-Maroni, French Guiana
2CIC Inserm 1424 and DFR Santé Université Guyane, Cayenne, French Guiana, France
3Department of Obstetrics and Gynecology, Hôpital Louis Mourier, Hôpitaux Universitaires Paris Nord Val de Seine, Assistance Publique : Hôpitaux de Paris, Université Paris Diderot, Colombes, France
4Department of Biology, West French Guiana Hospital Center, Saint-Laurent-du-Maroni, French Guiana
5Materno-Fetal and Obstetrics Research Unit, Department Woman-Mother-Child, Lausanne University Hospital, Lausanne, Switzerland
6Department of Infectious and Tropical Diseases, Cayenne General Hospital, Cayenne, French Guiana, France
7Centre d’Investigation Clinique Antilles Guyane, Inserm CIC1424, Centre Hospitalier de Cayenne, Cayenne, French Guiana

Tóm tắt

Mosquito-borne arboviral diseases are a global concern and can have severe consequences on maternal, neonatal, and child health. Their impact on pregnancy tends to be neglected in developing countries. Despite hundreds of millions of infections, 90% pregnancies being exposed, scientific data on pregnant women is poor and sometimes non-existent. Recently and since the 2016 Zika virus outbreak, there has been a newfound interest in these diseases. Through various neuropathogenic, visceral, placental, and teratogenic mechanisms, these arbovirus infections can lead to fetal losses, obstetrical complications, and a wide range of congenital abnormalities, resulting in long-term neurological and sensory impairments. Climate change, growing urbanization, worldwide interconnectivity, and ease of mobility allow arboviruses to spread to other territories and impact populations that had never been in contact with these emerging agents before. Pregnant travelers are also at risk of infection with potential subsequent complications. Beyond that, these pathologies show the inequalities of access to care on a global scale in a context of demographic growth and increasing urbanization. It is essential to promote research, diagnostic tools, treatments, and vaccine development to address this emerging threat. Background The vulnerability of pregnant women and fetuses to emergent and re-emergent pathogens has been notably illustrated by the outbreaks of Zika virus. Our comprehension of the complete scope and consequences of these infections during pregnancy remains limited, particularly among those involved in perinatal healthcare, such as obstetricians and midwives. This review aims to provide the latest information and recommendations regarding the various risks, management, and prevention for pregnant women exposed to arboviral infections.

Tài liệu tham khảo

Young PR. Arboviruses: A Family on the Move. In: Hilgenfeld R, Vasudevan SG, editors. Dengue and Zika: Control and Antiviral Treatment Strategies [Internet]. Singapore: Springer Singapore; 2018 [cited 2022 Mar 2]. p. 1–10. (Advances in Experimental Medicine and Biology; vol. 1062). Available from: http://link.springer.com/10.1007/978-981-10-8727-1_1 Pomar L, Malinger G, Benoist G, Carles G, Ville Y, Rousset D, et al. Association between Zika virus and fetopathy: a prospective cohort study in French Guiana. Ultrasound Obstet Gynecol. 2017;49(6):729–36. Pomar L, Vouga M, Lambert V, Pomar C, Hcini N, Jolivet A, et al. Maternal-fetal transmission and adverse perinatal outcomes in pregnant women infected with Zika virus: prospective cohort study in French Guiana. BMJ. 2018;31(363):k4431. Hcini N, Kugbe Y, Rafalimanana ZHL, Lambert V, Mathieu M, Carles G, et al. Association between confirmed congenital Zika infection at birth and outcomes up to 3 years of life. Nat Commun. 2021;(1):3270–12. Balakrishnan VS. WHO launches global initiative for arboviral diseases. The Lancet Microbe. 2022;3(6):e407. Lambert V, Enfissi A, Lefebvre M, Pomar L, Kedous S, Guimiot F, et al. Tonate virus and fetal abnormalities, French Guiana, 2019. Emerg Infect Dis. 2022;28(2):445–8. Musso D, Ko AI, Baud D. Zika virus infection - after the pandemic. N Engl J Med. 2019;381(15):1444–57. Torres JR, Falleiros-Arlant LH, Dueñas L, Pleitez-Navarrete J, Salgado DM, Castillo JBD. Congenital and perinatal complications of chikungunya fever: a Latin American experience. Int J Infect Dis. 2016;51:85–8. Douine M, Mosnier E, Le Hingrat Q, Charpentier C, Corlin F, Hureau L, et al. Illegal gold miners in French Guiana: a neglected population with poor health. BMC Public Health. 2017;18(1):23. Brady OJ, Gething PW, Bhatt S, Messina JP, Brownstein JS, Hoen AG, et al. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS Negl Trop Dis. 2012;6(8):e1760. Achee NL, Grieco JP, Vatandoost H, Seixas G, Pinto J, Ching-Ng L, et al. Alternative strategies for mosquito-borne arbovirus control. PLoS Negl Trop Dis. 2019;13(1):e0006822. De Filette M, Ulbert S, Diamond MS, Sanders NN. Recent progress in West Nile virus diagnosis and vaccination. Vet Res. 2012;43(1):16. Weaver SC, Salas R, Rico-Hesse R, Ludwig GV, Oberste MS, Boshell J, et al. Re-emergence of epidemic Venezuelan equine encephalomyelitis in South America. Lancet. 1996;348(9025):436–40. Sissoko D, Malvy D, Giry C, Delmas G, Paquet C, Gabrie P, et al. Outbreak of chikungunya fever in Mayotte, Comoros archipelago, 2005-2006. Trans R Soc Trop Med Hyg. 2008;102(8):780–6. Argolo AFLT, Féres VCR, Silveira LA, Oliveira ACM, Pereira LA, Júnior JBS, et al. Prevalence and incidence of dengue virus and antibody placental transfer during late pregnancy in Central Brazil. BMC Infect Dis. 2013;31(13):254. Carrillo-Hernández MY, Ruiz-Saenz J, Villamizar LJ, Gómez-Rangel SY, Martínez-Gutierrez M. Co-circulation and simultaneous co-infection of dengue, chikungunya, and zika viruses in patients with febrile syndrome at the Colombian-Venezuelan border. BMC Infect Dis. 2018;18(1):61. Khandia R, Munjal A, Dhama K, Karthik K, Tiwari R, Malik YS, et al. Modulation of dengue/Zika virus pathogenicity by antibody-dependent enhancement and strategies to protect against enhancement in Zika virus infection. Front Immunol. 2018;9:597. Zohrabian A, Meltzer MI, Ratard R, Billah K, Molinari NA, Roy K, et al. West Nile virus economic impact, Louisiana, 2002. Emerg Infect Dis. 2004;10:1736–44. Xiao Y, Beier JC, Cantrell RS, Cosner C, DeAngelis DL, Ruan S. Modelling the effects of seasonality and socioeconomic impact on the transmission of rift valley fever virus. PLoS Negl. Trop Dis. 2015;9(1):e3388. Burt FJ, Chen W, Miner JJ, Lenschow DJ, Merits A, Schnettler E, et al. Chikungunya virus: an update on the biology and pathogenesis of this emerging pathogen. Lancet Infect Dis. 2017;17(4):e107–17. Gossner CM, Ducheyne E, Schaffner F. Increased risk for autochthonous vector-borne infections transmitted by Aedes albopictus in continental Europe. Euro Surveill. 2018;23(24):1800268. Tomasello D, Schlagenhauf P. Chikungunya and dengue autochthonous cases in Europe, 2007-2012. Travel Med Infect Dis. 2013;11(5):274–84. Guzmán-Terán C, Calderón-Rangel A, Rodriguez-Morales A, Mattar S. Venezuelan equine encephalitis virus: the problem is not over for tropical America. Ann Clin Microbiol Antimicrob [Internet]. 2020 May 19 [cited 2021 Apr 12];19. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7236962/ Counotte MJ, Kim CR, Wang J, Bernstein K, Deal CD, Broutet NJN, et al. Sexual transmission of Zika virus and other flaviviruses: a living systematic review. PLoS Med. 2018;15(7):e1002611. Blitvich BJ, Magalhaes T, Laredo-Tiscareño SV, Foy BD. Sexual transmission of arboviruses: a systematic review. Viruses. 2020;12(9):933. CDC. Centers for Disease Control and Prevention. 2021 [cited 2021 Jul 18]. Congenital Zika Syndrome & Other Birth Defects | CDC. Available from: https://www.cdc.gov/pregnancy/zika/testing-follow-up/zika-syndrome-birth-defects.html CDC [Internet]. 2014 [cited 2023 Mar 4]. Zika Virus. Available from: https://www.cdc.gov/zika/hc-providers/clinical-guidance/sexualtransmission.html Nicastri E, Castilletti C, Liuzzi G, Iannetta M, Capobianchi MR, Ippolito G. Persistent detection of Zika virus RNA in semen for six months after symptom onset in a traveller returning from Haiti to Italy, February 2016. Euro Surveill. 2016;21(32):30314. Cordeiro CN, Bano R, Washington Cross CI, Segars JH. Zika virus and assisted reproduction. Curr Opin Obstet Gynecol. 2017;29(3):175–9. Den Boon S, Marston BJ, Nyenswah TG, Jambai A, Barry M, Keita S, et al. Ebola virus infection associated with transmission from survivors. Emerg Infect Dis. 2019;25(2):240–6. Petersen LR, Busch MP. Transfusion-transmitted arboviruses. Vox Sang. 2010;98(4):495–503. Giménez-Richarte Á, Ortiz de Salazar MI, Giménez-Richarte MP, Collado M, Fernández PL, Clavijo C, et al. Transfusion-transmitted arboviruses: update and systematic review. PLoS Negl Trop Dis. 2022;16(10):e0010843. Blumberg EA, Fishman JA. Zika virus in transplantation: emerging infection and opportunities. Am J Transplant. 2017;17(3):599–600. Nogueira ML, Estofolete CF, Terzian ACB, do Vale EM, da Silva RC, Da Silva RF, et al. Zika virus infection and solid organ transplantation: a new challenge. Am J Transplant. 2017;17(3):791–5. Charatan F. Organ transplants and blood transfusions may transmit West Nile virus. BMJ. 2002;325(7364):566. Langgartner J, Audebert F, Schölmerich J, Glück T. Dengue virus infection transmitted by needle stick injury. J Inf Secur. 2002;44(4):269–70. Wagner D, de With K, Huzly D, Hufert F, Weidmann M, Breisinger S, et al. Nosocomial acquisition of dengue. Emerg Infect Dis. 2004;10:1872–3. Grischott F, Puhan M, Hatz C, Schlagenhauf P. Non-vector-borne transmission of Zika virus: a systematic review. Travel Med Infect Dis. 2016;14(4):313–30. Ades AE, Soriano-Arandes A, Alarcon A, Bonfante F, Thorne C, Peckham CS, et al. Vertical transmission of Zika virus and its outcomes: a Bayesian synthesis of prospective studies. Lancet Infect Dis. 2021;21(4):537–45. Basurko C, Everhard S, Matheus S, Restrepo M, Hildéral H, Lambert V, et al. A prospective matched study on symptomatic dengue in pregnancy. PloS One. 2018;13(10):e0202005. Basurko C, Hcini N, Demar M, Abboud P, Nacher M, Carles G, et al. Symptomatic chikungunya virus infection and pregnancy outcomes: a nested case-control study in French Guiana. Viruses. 2022 14(‘):2705. Ferreira FC, da Silva AS, Recht J, Guaraldo L, Moreira ME, de Siqueira AM, et al. Vertical transmission of chikungunya virus: a systematic review. PloS One. 2021;16(4):e0249166. Charlier C, Beaudoin MC, Couderc T, Lortholary O, Lecuit M. Arboviruses and pregnancy: maternal, fetal, and neonatal effects. Lancet Child Adolesc Health. 2017;1(2):134–46. Touret Y, Randrianaivo H, Michault A, Schuffenecker I, Kauffmann E, Lenglet Y, et al. Early maternal-fetal transmission of the chikungunya virus. Presse Med. 2006;35(11 Pt 1):1656–8. Pomar L, Lambert V, Madec Y, Vouga M, Pomar C, Matheus S, et al. Placental infection by Zika virus in French Guiana. Ultrasound Obstet Gynecol. 2020;56(5):740–8. Robillard PY, Boumahni B, Gérardin P, Michault A, Fourmaintraux A, Schuffenecker I, et al. Vertical maternal fetal transmission of the chikungunya virus. Ten cases among 84 pregnant women. Presse Med. 2006;35(5 Pt 1):785–8. Basurko C, Matheus S, Hildéral H, Everhard S, Restrepo M, Cuadro-Alvarez E, et al. Estimating the risk of vertical transmission of dengue: a prospective study. Am J Trop Med Hyg. 2018 Jun;98(6):1826–32. S D, M H, A G, Pe C, A V. Mother-to-Child Transmission of Arboviruses during Breastfeeding: From Epidemiology to Cellular Mechanisms. Viruses [Internet]. 2021 Jul 7 [cited 2023 Mar 12];13(7). Available from: https://pubmed.ncbi.nlm.nih.gov/34372518/ Hubert M, Jeannin P, Burlaud-Gaillard J, Roingeard P, Gessain A, Ceccaldi PE, et al. Evidence that Zika virus is transmitted by breastfeeding to newborn A129 (Ifnar1 Knock-out) mice and is able to infect and Cross a tight monolayer of human intestinal epithelial cells. Front Microbiol. 2020;11:524678. Blohm GM, Lednicky JA, Márquez M, White SK, Loeb JC, Pacheco CA, et al. Evidence for mother-to-child transmission of Zika virus through breast Milk. Clin Infect Dis. 2018;66(7):1120–1. Hinckley AF, O’Leary DR, Hayes EB. Transmission of West Nile virus through human breast milk seems to be rare. Pediatrics. 2007;119(3):e666–71. Lawrence RM, Lawrence RA. Breast milk and infection. Clin Perinatol. 2004;31(3):501–28. Pierson TC, Diamond MS. The continued threat of emerging flaviviruses. Nat Microbiol. 2020;5(6):796–812. Stewart RD, Bryant SN, Sheffield JS. West nile virus infection in pregnancy. Case Rep Infect Dis. 2013;2013:351872. Domingues RB, Kuster GW, Onuki-Castro FL, Souza VA, Levi JE, Pannuti CS. Involvement of the central nervous system in patients with dengue virus infection. J Neurol Sci. 2008;267(1–2):36–40. Domingues RB, Kuster GW, Onuki de Castro FL, Souza VA, Levi JE, Pannuti CS. Headache features in patients with dengue virus infection. Cephalalgia. 2006;26(7):879–82. Flamand C, Fritzell C, Matheus S, Dueymes M, Carles G, Favre A, et al. The proportion of asymptomatic infections and spectrum of disease among pregnant women infected by Zika virus: systematic monitoring in French Guiana, 2016. Euro Surveill. 2017;22(44):17-00102. Foeller ME, Nosrat C, Krystosik A, Noel T, Gérardin P, Cudjoe N, et al. Chikungunya infection in pregnancy - reassuring maternal and perinatal outcomes: a retrospective observational study. BJOG. 2021;128(6):1077–86. Evangelista GD, Carvalho RH, Menezes GS, de Abreu YC, Sardi SI, Campos GS. Meningoencephalitis associated with Zika virus and chikungunya virus infection. Jpn J Infect Dis. 2021;74(6):584–6. Cao-Lormeau VM, Blake A, Mons S, Lastère S, Roche C, Vanhomwegen J, et al. Guillain-Barré syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet. 2016;387(10027):1531–9. Ravi V, Taly AB, Shankar SK, Shenoy PK, Desai A, Nagaraja D, et al. Association of Japanese encephalitis virus infection with Guillain-Barré syndrome in endemic areas of South India. Acta Neurol Scand. 1994;90(1):67–72. Verma R, Junewar V, Praharaj HN. Unusual association of eclamptic encephalopathy and Japanese encephalitis. BMJ Case Rep. 2012;1(2012):bcr0220125840. Misra UK, Kalita J, Syam UK, Dhole TN. Neurological manifestations of dengue virus infection. J Neurol Sci. 2006;244(1–2):117–22. Chan DPL, Teoh SCB, Tan CSH, Nah GKM, Rajagopalan R, Prabhakaragupta MK, et al. Ophthalmic complications of dengue. Emerg Infect Dis. 2006;12(2):285–9. Casetta I, Ciorba A, Cesnik E, Trevisi P, Tugnoli V, Bovo R. West Nile virus neuroinvasive disease presenting with acute flaccid paralysis and bilateral sensorineural hearing loss. J Neurol. 2011;258(10):1880–1. Weatherhead JE, Miller VE, Garcia MN, Hasbun R, Salazar L, Dimachkie MM, et al. Long-term neurological outcomes in West Nile virus-infected patients: an observational study. Am J Trop Med Hyg. 2015;92(5):1006–12. Ribeiro BNF, Guimarães AC, Yazawa F, Takara TFM, de Carvalho GM, Zappelini CEM. Sensorineural hearing loss in hemorrhagic dengue? Int J Surg Case Rep. 2015;8C:38–41. Soni K, Bohra GK, Nair NP, Kaushal D, Patro SK, Goyal A. Sensorineural hearing loss in dengue: a pilot study. Iran J Otorhinolaryngol. 2021;33(116):157–61. Vinhaes ES, Santos LA, Dias L, Andrade NA, Bezerra VH, de Carvalho AT, et al. Transient hearing loss in adults associated With Zika virus infection. Clin Infect Dis. 2017;64(5):675–7. Abroug N, Khairallah M, Zina S, Ksiaa I, Amor HB, Attia S, et al. Ocular manifestations of emerging arthropod-borne infectious diseases. J Curr Ophthalmol. 2021;33(3):227–35. Borgherini G, Poubeau P, Jossaume A, Gouix A, Cotte L, Michault A, et al. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on Reunion island. Clin Infect Dis. 2008;47(4):469–75. Matusali G, Colavita F, Bordi L, Lalle E, Ippolito G, Capobianchi MR, et al. Tropism of the Chikungunya Virus. Viruses. 2019;11(2):175. Nicacio JM, Gomes OV, Carmo RF, Nunes SL, Rocha JR, Souza CD, et al. Heart disease and arboviruses: a systematic review and Meta-analysis. Viruses. 2022;14(9):1988. Brizzi K. Neurologic manifestation of chikungunya virus. Curr InfectDis Rep. 2017;19(2):6. van Enter BJD, Huibers MHW, van Rooij L, Steingrover R, van Hensbroek MB, Voigt RR, et al. Perinatal outcomes in vertically infected neonates during a chikungunya outbreak on the island of Curaçao. Am J Trop Med Hyg. 2018;99(6):1415–8. Diniz LMO, Romanelli RMC, de Carvalho AL, Teixeira DC, de Carvalho LFA, Ferreira Cury V, et al. Perinatal yellow fever: a case report. Pediatr Infect Dis J. 2019;38(3):300–1. Centers for Disease Control and Prevention (CDC). Intrauterine West Nile virus infection--New York, 2002. MMWR Morb Mortal Wkly Rep. 2002;51(50):1135–6. Bentlin MR, de Barros Almeida RAM, Coelho KIR, Ribeiro AF, Siciliano MM, Suzuki A, et al. Perinatal transmission of yellow fever, Brazil, 2009. Emerg Infect Dis. 2011;17(9):1779–80. Diouf K, Nour NM. Mosquito-borne diseases as a Global Health problem: implications for pregnancy and travel. Obstet Gynecol Surv. 2017;72(5):309–18. Pomar L, Lambert V, Matheus S, Pomar C, Hcini N, Carles G, et al. Prolonged maternal Zika viremia as a marker of adverse perinatal outcomes. Emerg Infect Dis. 2021;27(2):490–8. D MD, T O, Knd P, Jl W, Am B, Sa S, et al. Prolonged detection of Zika virus RNA in pregnant women. Obstetrics and gynecology [Internet] 2016 Oct [cited 2022 Jun 1];128(4). Available from: https://pubmed.ncbi.nlm.nih.gov/27479770/ Lozier MJ, Rosenberg ES, Doyle K, Adams L, Klein L, Muñoz-Jordan J, et al. Prolonged detection of Zika virus nucleic acid among symptomatic pregnant women: a cohort study. Clin Infect Dis. 2018;67(4):624–7. Driggers RW, Ho CY, Korhonen EM, Kuivanen S, Jääskeläinen AJ, Smura T, et al. Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N Engl J Med. 2016;374(22):2142–51. Gourinat AC, O’Connor O, Calvez E, Goarant C, Dupont-Rouzeyrol M. Detection of Zika virus in urine. Emerg Infect Dis. 2015;21(1):84–6. Magalhaes T, Braga C, Cordeiro MT, Oliveira ALS, Castanha PMS, Maciel APR, et al. Zika virus displacement by a chikungunya outbreak in Recife, Brazil. PLoS Negl Trop Dis. 2017;11:e0006055. Granger D, Hilgart H, Misner L, Christensen J, Bistodeau S, Palm J, et al. Serologic testing for Zika virus: comparison of three Zika virus IgM-screening enzyme-linked immunosorbent assays and initial laboratory experiences. J Clin Microbiol. 2017;55(7):2127–36. Mercado M, Ailes EC, Daza M, Tong VT, Osorio J, Valencia D, et al. Zika virus detection in amniotic fluid and Zika-associated birth defects. Am J Obstet Gynecol. 2020;222(6):610.e1–610.e13. Charrel RN, Leparc-Goffart I, Pas S, de Lamballerie X, Koopmans M, Reusken C. Background review for diagnostic test development for Zika virus infection. Bull World Health Organ. 2016;94(8):574–584D. Ahmad MU, Sharif KA, Qayyum H, Ehsanullah B, Balyasnikova S, Wale A, et al. Assessing the use of magnetic resonance imaging virtopsy as an alternative to autopsy: a systematic review and meta-analysis. Postgrad Med J. 2017;93(1105):671–8. Machado CR, Machado ES, Rohloff RD, Azevedo M, Campos DP, de Oliveira RB, et al. Is pregnancy associated with severe dengue? A review of data from the Rio de Janeiro surveillance information system. PLoS Negl Trop Dis. 2013;7(5):e2217. Adam I, Jumaa AM, Elbashir HM, Karsany MS. Maternal and perinatal outcomes of dengue in PortSudan, eastern Sudan. Virol J. 2010;13(7):153. Nwaiwu AU, Musekiwa A, Tamuzi JL, Sambala EZ, Nyasulu PS. The incidence and mortality of yellow fever in Africa: a systematic review and meta-analysis. BMC Infect Dis. 2021;21(1):1089. Rathore SS, Oberoi S, Hilliard J, Raja R, Ahmed NK, Vishwakarma Y, et al. Maternal and foetal-neonatal outcomes of dengue virus infection during pregnancy. Trop Med Int Health. 2022;27(7):619–29. Pshenichnaya NY, Leblebicioglu H, Bozkurt I, Sannikova IV, Abuova GN, Zhuravlev AS, et al. Crimean-Congo hemorrhagic fever in pregnancy: a systematic review and case series from Russia, Kazakhstan and Turkey. Int J Infect Dis. 2017;58:58–64. Düppers AL, Bohnhorst B, Bültmann E, Schulz T, Higgins-Wood L, von Kaisenberg CS. Severe fetal brain damage subsequent to acute maternal hypoxemic deterioration in COVID-19. Ultrasound Obstet Gynecol. 2021;58(3):490–1. Snyder RE, Cooksey GS, Kramer V, Jain S, Vugia DJ. West Nile virus-associated hospitalizations, California, 2004-2017. Clin Infect Dis. 2021;73(3):441–7. Mysorekar IU, Diamond MS. Modeling Zika virus infection in pregnancy. N Engl J Med. 2016;375(5):481–4. Martins-Filho PR, Tavares CS, Carvalho AC, Reis MC, Santos HP Jr, Santos VS. Association between arthrogryposis and mortality in infants With congenital Zika syndrome: a systematic review and Meta-analysis. Pediatr Neurol. 2020;110:20–4. Oymans J, Wichgers Schreur PJ, van Keulen L, Kant J, Kortekaas J. Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. PLoS Negl Trop Dis. 2020;14(1):e0007898. McMillen CM, Boyles DA, Kostadinov SG, Hoehl RM, Schwarz MM, Albe JR, et al. Congenital Rift Valley fever in Sprague Dawley rats is associated with diffuse infection and pathology of the placenta. PLoS Negl Trop Dis. 2022;16(10):e0010898. Rabelo K, de Souza LJ, Salomão NG, Machado LN, Pereira PG, Portari EA, et al. Zika induces human placental damage and inflammation. Front Immunol. 2020;11:2146. Odendaal L, Clift SJ, Fosgate GT, Davis AS. Ovine fetal and placental lesions and cellular tropism in natural Rift Valley fever virus infections. Vet Pathol. 2020;57(6):791–806. Machain-Williams C, Raga E, Baak-Baak CM, Kiem S, Blitvich BJ, Ramos C. Maternal, fetal, and neonatal outcomes in pregnant dengue patients in Mexico. Biomed Res Int. 2018;2018:9643083. Brar R, Sikka P, Suri V, Singh MP, Suri V, Mohindra R, et al. Maternal and fetal outcomes of dengue fever in pregnancy: a large prospective and descriptive observational study. Arch Gynecol Obstet. 2021;304(1):91–100. Brasil P, Pereira JP, Moreira ME, Ribeiro Nogueira RM, Damasceno L, Wakimoto M, et al. Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med. 2016;375(24):2321–34. Basurko C, Carles G, Youssef M, Guindi WEL. Maternal and fetal consequences of dengue fever during pregnancy. Eur J Obstet Gynecol Reprod Biol. 2009;147(1):29–32. Paixão ES, Teixeira MG, Maria da Conceição NC, Rodrigues LC. Dengue during pregnancy and adverse fetal outcomes: a systematic review and meta-analysis. Lancet Infect Dis. 2016;16(7):857–65. Carles G, Peiffer H, Talarmin A. Effects of dengue fever during pregnancy in French Guiana. Clin Infect Dis. 1999;28(3):637–40. Linthicum KJ, Britch SC, Anyamba A. Rift Valley fever: an emerging mosquito-borne disease. Annu Rev Entomol. 2016;61:395–415. Baudin M, Jumaa AM, Jomma HJE, Karsany MS, Bucht G, Näslund J, et al. Association of rift valley fever virus infection with miscarriage in Sudanese women: a cross-sectional study. Lancet Glob Health. 2016;4(11):e864–71. Chaturvedi UC, Mathur A, Chandra A, Das SK, Tandon HO, Singh UK. Transplacental infection with Japanese encephalitis virus. J Infect Dis. 1980;141(6):712–5. Kumar S, Agrawal G, Wazir S, Kumar A, Dubey S, Balde M, et al. Experience of perinatal and neonatal chikungunya virus (CHIKV) infection in a tertiary care neonatal Centre during outbreak in North India in 2016: a case series. J Trop Pediatr. 2019;65(2):169–75. Besnard M, Lastere S, Teissier A, Cao-Lormeau V, Musso D. Evidence of perinatal transmission of Zika virus, French Polynesia, December 2013 and February 2014. Euro Surveill. 2014;19(13):20751. Arishi HM, Aqeel AY, Al Hazmi MM. Vertical transmission of fatal Rift Valley fever in a newborn. Ann Trop Paediatr. 2006;26(3):251–3. Adam I, Karsany MS. Case report: Rift Valley fever with vertical transmission in a pregnant Sudanese woman. J Med Virol. 2008;80(5):929. Nielsen-Saines K, Brasil P, Kerin T, Vasconcelos Z, Gabaglia CR, Damasceno L, et al. Delayed childhood neurodevelopment and neurosensory alterations in the second year of life in a prospective cohort of ZIKV-exposed children. Nat Med. 2019;25(8):1213–7. Khodr ZG, Hall C, Chang RN, Bukowinski AT, Gumbs GR, Conlin AMS. Japanese encephalitis vaccination in pregnancy among U.S. active duty military women. Vaccine. 2020;38(29):4529–35. Hall C, Khodr ZG, Chang RN, Bukowinski AT, Gumbs GR, Conlin AMS. Safety of yellow fever vaccination in pregnancy: findings from a cohort of active duty US military women. J Travel Med. 2020;27(6):taaa138. Wiwanitkit V. Aedes Mosquito Larva in the hospital: a note from Thailand. Infect Control Hosp Epidemiol. 2016;37(12):1519. Sylvestre E, Joachim C, Cécilia-Joseph E, Bouzillé G, Campillo-Gimenez B, Cuggia M, et al. Data-driven methods for dengue prediction and surveillance using real-world and big data: a systematic review. PLoS Negl Trop Dis. 2022;16(1):e0010056. Ruiz-Burga E, Bruijning-Verhagen P, Palmer P, Sandcroft A, Fernandes G, de Hoog M, et al. Detection of potential arbovirus infections and pregnancy complications in pregnant women in Jamaica using a smartphone app (ZIKApp): pilot evaluation study. JMIR Form Res. 2022;6(7):e34423.