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CC BY 4.0 · Rev Bras Ginecol Obstet 2020; 42(09): 577-585
DOI: 10.1055/s-0040-1712126
Review Article

Characterization of Placental Infection by Zika Virus in Humans: A Review of the Literature

Caracterização da infecção placentária pelo vírus zika em humanos: Uma revisão da literatura
Emanuella Meneses Venceslau 
1   Departament of Gynecology and Obstetrics, Universidade Estadual de Campinas, Campinas, SP, Brazil
,
José Paulo Guida 
1   Departament of Gynecology and Obstetrics, Universidade Estadual de Campinas, Campinas, SP, Brazil
,
Eliana Amaral 
1   Departament of Gynecology and Obstetrics, Universidade Estadual de Campinas, Campinas, SP, Brazil
,
José Luis Proença Modena 
2   Departament of Genetics, Evolution and Bioagents, Universidade Estadual de Campinas, Campinas, SP, Brazil
,
Maria Laura Costa 
1   Departament of Gynecology and Obstetrics, Universidade Estadual de Campinas, Campinas, SP, Brazil
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Abstract

Objective The aim of the current review is to present a systematic evaluation of reported human placental findings in cases of zika virus (ZIKV) infection.

Data sources We reviewed the EMBASE, PUBMED, and SCIELO databases until June 2019, without language restrictions.

Selection of studies The search terms placenta AND zika virus were used. The inclusion criteria of the studies were studies that reported placental findings in humans. Experimental studies, reviews, notes or editorials were excluded. A total of 436 studies were retrieved; after duplicate exclusion, 243 articles had their titles screened, and 128 had their abstract read; of those, 32 were included in the final analysis (18 case reports, 10 case series, and 4 cohorts)

Data collection We collected data concerning the author, year of publication, study design, number of participants, number of placental samples, onset of symptoms, perinatal outcomes, and main findings on histological analysis.

Data synthesis The placental pathologic findings were described as mild and nonspecific, similar to those of other placental infections, including chronic placentitis, chronic villitis, increased Hofbauer cells, irregular fibrin deposits, increased mononuclear cells in the villus stroma, villous immaturity, edema, hypervascularization, stromal fibrosis, calcification, and focal necrosis of syncytiotrophoblasts.

Conclusion Zika infection presents unspecific placental findings, similar to other infections in the toxoplasmosis, other agents, rubella, cytomegalovirus, and herpes (TORCH)group. Characterizing and standardizing placental findings after zika virus infection is key to understanding the mechanisms of congenital diseases.

Resumo

Objetivo O objetivo desta revisão é apresentar uma avaliação sistemática dos achados relacionados à infecção por zika vírus (ZIKV) na placenta humana.

Fontes de dados As bases de dados EMBASE, PUBMED, e SCIELO foram pesquisadas, até junho de 2019, sem qualquer restrição de língua.

Seleção dos estudos Os termos placenta E zika virus foram utilizados na busca. Foram incluídos estudos que reportassem achados placentários de infecção em seres humanos, enquanto estudos experimentais, revisões, notas e editoriais foram excluídos. Um total de 436 estudos foram identificados, e 243 tiveram seus títulos lidos após a exclusão de duplicatas. Cento e vinte e oito artigos tiveram seus resumos avaliados, dos quais 32 foram incluídos na análise final (18 relatos de caso, 10 séries de casos, e 4 estudos de coorte).

Dados obtidos Foram pesquisados dados relativos ao autor, ano da publicação, desenho do estudo, número de participantes, número de amostras de placenta, início dos sintomas, desfechos perinatais, e principais achados histológicos.

Síntese dos dados Os principais achados placentários descritos foram leves e inespecíficos, similares a outras infecções placentárias, incluindo infecção placentária crônica, vilosite crônica, aumento das células de Hofbauer, depósitos irregulares de fibrina, aumento das células mononucleares no estroma viloso, imaturidade vilosa, edema, hipervascularização, fibrose estromal, calcificação, e necrose focal dos sincicitrofoblastos.

Conclusão Infecções por ZIKV têm achados placentários inespecíficos, similares aos de outras infecções do grupo toxoplasmose, rubéola, citomegalovírus e herpes (TORCH). Caracterizar e padronizar os achados placentários após infecção por ZIKV é fundamental para entender o mecanismo das infecções congênitas.

Keywords

Zika virus - ZIKV - placenta - Hofbauer cells - TORCH

Palavras-chave

Zika vírus - ZIKV - placenta - células de Hofbauer - TORCH

Contributions

Venceslau E. M. and Guida J. P. S. contributed by collecting data and writing the first draft; Amaral E. and Modena J. L. P. reviewed the first draft; and Costa M. L. had the original idea for the present study and coordinated it, supervised the data collection, and reviewed the first draft.




Publikationsverlauf

Eingereicht: 23. Januar 2020

Angenommen: 16. März 2020

Artikel online veröffentlicht:
19. Juni 2020

© 2020. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/).

Thieme Revinter Publicações Ltda
Rio de Janeiro, Brazil

 

  • References

  • 1 Baud D, Gubler DJ, Schaub B, Lanteri MC, Musso D. An update on Zika virus infection. Lancet 2017; 390 (10107): 2099-2109
    CrossrefPubMedSuche in Google Scholar
  • 2 Duffy MR, Chen TH, Hancock WT, Powers AM, Kool JL, Lanciotti RS. , et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 2009; 360 (24) 2536-2543
    CrossrefPubMedSuche in Google Scholar
  • 3 Song BH, Yun SI, Woolley M, Lee YM. Zika virus: History, epidemiology, transmission, and clinical presentation. J Neuroimmunol 2017; 308: 50-64
    CrossrefPubMedSuche in Google Scholar
  • 4 Proenca-Modena JL, Milanez GP, Costa ML, Judice CC, Maranhão Costa FT. Zika virus: lessons learned in Brazil. Microbes Infect 2018; 20 (11-12): 661-669
    CrossrefPubMedSuche in Google Scholar
  • 5 Melo ASO, Chimelli L, Tanuri A. Congenital Zika virus infection: beyond neonatal microcephaly-reply. JAMA Neurol 2017; 74 (05) 610-611
    CrossrefPubMedSuche in Google Scholar
  • 6 Coyne CB, Lazear HM. Zika virus - reigniting the TORCH. Nat Rev Microbiol 2016; 14 (11) 707-715
    CrossrefPubMedSuche in Google Scholar
  • 7 Burton GJ, Jauniaux E. The cytotrophoblastic shell and complications of pregnancy. Placenta 2017; 60: 134-139
    CrossrefPubMedSuche in Google Scholar
  • 8 Reyes L, Wolfe B, Golos T. Hofbauer cells: placental macrophages of fetal origin. Results Probl Cell Differ 2017; 62: 45-60
    CrossrefPubMedSuche in Google Scholar
  • 9 Rosenberg AZ, Yu W, Hill DA, Reyes CA, Schwartz DA. Placental pathology of Zika virus: viral infection of the placenta induces villous stromal macrophage (Hofbauer Cell) proliferation and hyperplasia. Arch Pathol Lab Med 2017; 141 (01) 43-48
    CrossrefPubMedSuche in Google Scholar
  • 10 Ritter JM, Martines RB, Zaki SR. Zika virus: pathology from the pandemic. Arch Pathol Lab Med 2017; 141 (01) 49-59
    CrossrefPubMedSuche in Google Scholar
  • 11 Martines RB, Bhatnagar J, Keating MK, Silva-Flannery L, Muehlenbachs A, Gary J. , et al. Notes from the field: evidence of zika virus infection in brain and placental tissues from two congenitally infected newborns and two fetal losses–Brazil, 2015. MMWR Morb Mortal Wkly Rep 2016; 65 (06) 159-160
    CrossrefPubMedSuche in Google Scholar
  • 12 Martines RB, Bhatnagar J, de Oliveira Ramos AM, Davi HP, Iglezias SP, Kanamura CT. , et al. Pathology of congenital Zika syndrome in Brazil: a case series. Lancet 2016; 388 (10047): 898-904
    CrossrefPubMedSuche in Google Scholar
  • 13 Noronha Ld, Zanluca C, Azevedo ML, Luz KG, Santos CN. Zika virus damages the human placental barrier and presents marked fetal neurotropism. Mem Inst Oswaldo Cruz 2016; 111 (05) 287-293
    CrossrefPubMedSuche in Google Scholar
  • 14 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) 2142-2151
    CrossrefPubMedSuche in Google Scholar
  • 15 Melo ASO, Aguiar RS, Amorim MM, Arruda MB, Melo FO, Ribeiro ST. , et al. Congenital Zika virus infection: beyond neonatal microcephaly. JAMA Neurol 2016; 73 (12) 1407-1416
    CrossrefPubMedSuche in Google Scholar
  • 16 Mlakar J, Korva M, Tul N, Popović M, Poljšak-Prijatelj M, Mraz J. , et al. Zika virus associated with microcephaly. N Engl J Med 2016; 374 (10) 951-958
    CrossrefPubMedSuche in Google Scholar
  • 17 Sarno M, Sacramento GA, Khouri R, do Rosário MS, Costa F, Archanjo G. , et al. Zika virus infection and stillbirths: a case of hydrops fetalis, hydranencephaly and fetal demise. PLoS Negl Trop Dis 2016; 10 (02) e0004517
    CrossrefPubMedSuche in Google Scholar
  • 18 van der Eijk AA, van Genderen PJ, Verdijk RM, Reusken CB, Mögling R, van Kampen JJ. , et al. Miscarriage associated with Zika virus infection. N Engl J Med 2016; 375 (10) 1002-1004
    CrossrefPubMedSuche in Google Scholar
  • 19 Acosta-Reyes J, Navarro E, Herrera MJ, Goenaga E, Ospina ML, Parra E. , et al. Severe neurologic disorders in 2 fetuses with Zika virus infection, Colombia. Emerg Infect Dis 2017; 23 (06) 982-984
    CrossrefPubMedSuche in Google Scholar
  • 20 Bhatnagar J, Rabeneck DB, Martines RB, Reagan-Steiner S, Yokabed E, Estetter LBC. , et al. Zika virus RNA replication and persistence in brain and placental tissue. Emerg Infect Dis 2017; 23 (03) 405-414
    CrossrefPubMedSuche in Google Scholar
  • 21 Chen L, Hafeez F, Curry CL, Elgart G. Cutaneous eruption in a U.S. woman with locally acquired Zika virus infection. N Engl J Med 2017; 376 (04) 400-401
    CrossrefPubMedSuche in Google Scholar
  • 22 Mattar S, Ojeda C, Arboleda J, Arrieta G, Bosch I, Botia I. , et al. Case report: microcephaly associated with Zika virus infection, Colombia. BMC Infect Dis 2017; 17 (01) 423
    CrossrefPubMedSuche in Google Scholar
  • 23 Rabelo K, de Souza Campos Fernandes RC, de Souza LJ, Louvain de Souza T, Dos Santos FB, Guerra Nunes PC. , et al. Placental histopathology and clinical presentation of severe congenital Zika syndrome in a human immunodeficiency virus-exposed uninfected infant. Front Immunol 2017; 8: 1704
    CrossrefPubMedSuche in Google Scholar
  • 24 Reagan-Steiner S, Simeone R, Simon E, Bhatnagar J, Oduyebo T, Free R. et al; U.S. Zika Pregnancy Registry Collaboration; Zika Virus Response Epidemiology and Surveillance Task Force Pathology Team. Evaluation of placental and fetal tissue specimens for Zika virus infection - 50 states and district of Columbia, January-December, 2016. MMWR Morb Mortal Wkly Rep 2017; 66 (24) 636-643
    CrossrefPubMedSuche in Google Scholar
  • 25 Schaub B, Vouga M, Najioullah F, Gueneret M, Monthieux A, Harte C. , et al. Analysis of blood from Zika virus-infected fetuses: a prospective case series. Lancet Infect Dis 2017; 17 (05) 520-527
    CrossrefPubMedSuche in Google Scholar
  • 26 Schwartz DA. Viral infection, proliferation, and hyperplasia of Hofbauer cells and absence of inflammation characterize the placental pathology of fetuses with congenital Zika virus infection. Arch Gynecol Obstet 2017; 295 (06) 1361-1368
    CrossrefPubMedSuche in Google Scholar
  • 27 de Noronha L, Zanluca C, Burger M, Suzukawa AA, Azevedo M, Rebutini PZ. , et al. Zika virus infection at different pregnancy stages: anatomopathological findings, target cells and viral persistence in placental tissues. Front Microbiol 2018; 9: 2266
    CrossrefPubMedSuche in Google Scholar
  • 28 Esquivel M, Avaad-Portari E, Vasconcelos ZC, Moreira ME, Gaw SL. Vertical transmission and placental pathology of twin pregnancies from Zika virus infected mothers. Am J Obstet Gynecol 2018; 218 (1, Suppl) 520
    CrossrefPubMedSuche in Google Scholar
  • 29 Maykin M, Avaad-Portari E, Esquivel M, Pereira Jr. JP, Fisher SJ, Moreira ME. , et al. Placental histopathologic findings in Zika-infected pregnancies. Am J Obstet Gynecol 2018; 218 (1, Suppl) 520-521
    CrossrefPubMedSuche in Google Scholar
  • 30 Mletzko J, Schildgen O. Absence of Zika virus in abort and placental tissue in a German cohort. Rev Med Microbiol 2018; 29 (01) 17-19
    CrossrefPubMedSuche in Google Scholar
  • 31 Rabelo K, Souza LJ, Salomão NG, Oliveira ERA, Sentinelli LP, Lacerda MS. , et al. Placental inflammation and fetal injury in a rare Zika case associated with Guillain-Barré syndrome and abortion. Front Microbiol 2018; 9: 1018
    CrossrefPubMedSuche in Google Scholar
  • 32 Sassetti M, Zé-Zé L, Franco J, Cunha JD, Gomes A, Tomé A, Alves MJ. First case of confirmed congenital Zika syndrome in continental Africa. Trans R Soc Trop Med Hyg 2018; 112 (10) 458-462
    CrossrefPubMedSuche in Google Scholar
  • 33 Turley M, Valentine G, Seferovic M, Rac M, Eppes C, Major A. , et al. Importance of placental testing in congenital zika virus (zikv) infection and fetal malformation syndrome. Am J Obstet Gynecol 2018; 218 (1, Suppl) 54-55
    CrossrefPubMedSuche in Google Scholar
  • 34 Wongsurawat T, Jenjaroenpun P, Athipanyasilp N, Kaewnapan B, Leelahakorn N, Angkasekwinai N. , et al. Genome sequences of Zika virus strains recovered from amniotic fluid, placenta, and fetal brain of a microcephaly patient in Thailand, 2017. Microbiol Resour Announc 2018; 7 (11) e01020-e18
    CrossrefPubMedSuche in Google Scholar
  • 35 Felix A, Hallet E, Favre A, Kom-Tchameni R, Defo A, Fléchelles O. , et al. Cerebral injuries associated with Zika virus in utero exposure in children without birth defects in French Guiana: Case report. Medicine (Baltimore) 2017; 96 (51) e9178
    CrossrefPubMedSuche in Google Scholar
  • 36 Merriam AA, Nhan-Chang CL, Huerta-Bogdan BI, Wapner R, Gyamfi-Bannerman C. A single-center experience with a pregnant immigrant population and Zika virus serologic screening in New York City. Am J Perinatol 2019; ; [Epub ahead of print]
    Thieme ConnectPubMedSuche in Google Scholar
  • 37 Rodó C, Suy A, Sulleiro E, Soriano-Arandes A, Maiz N, García-Ruiz A. , et al. Pregnancy outcomes after maternal Zika virus infection in a non-endemic region: prospective cohort study. Clin Microbiol Infect 2019; 25 (05) 633.e5-633.e9
    CrossrefPubMedSuche in Google Scholar
  • 38 Santos GR, Pinto CAL, Prudente RCS, Bevilacqua EMAF, Witkin SS, Passos SD. ; Zika Virus Cohort Study Group. Case report: histopathologic changes in placental tissue associated with vertical transmission of Zika virus. Int J Gynecol Pathol 2020; 39 (02) 157-162
    CrossrefPubMedSuche in Google Scholar
  • 39 Seferovic MD, Turley M, Valentine GC, Rac M, Castro ECC, Major AM. , et al. Clinical importance of placental testing among suspected cases of congenital Zika syndrome. Int J Mol Sci 2019; 20 (03) E712
    CrossrefPubMedSuche in Google Scholar
  • 40 Yarrington CD, Hamer DH, Kuohung W, Lee-Parritz A. Congenital Zika syndrome arising from sexual transmission of Zika virus, a case report. Fertil Res Pract 2019; 5: 1
    CrossrefPubMedSuche in Google Scholar
  • 41 Brasil P, Pereira Jr JP, Moreira ME, Nogueira RMR, Damasceno L, Wakimoto M. , et al. Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med 2016; 375 (24) 2321-2334
    CrossrefPubMedSuche in Google Scholar
  • 42 França GV, Schuler-Faccini L, Oliveira WK, Henriques CM, Carmo EH, Pedi VD. , et al. Congenital Zika virus syndrome in Brazil: a case series of the first 1501 livebirths with complete investigation. Lancet 2016; 388 (10047): 891-897
    CrossrefPubMedSuche in Google Scholar
  • 43 Mostoufi-zadeh M, Driscoll SG, Biano SA, Kundsin RB. Placental evidence of cytomegalovirus infection of the fetus and neonate. Arch Pathol Lab Med 1984; 108 (05) 403-406
    PubMedSuche in Google Scholar
  • 44 Gabrielli L, Bonasoni MP, Lazzarotto T, Lega S, Santini D, Foschini MP. , et al. Histological findings in foetuses congenitally infected by cytomegalovirus. J Clin Virol 2009; 46 (Suppl. 04) S16-S21
    CrossrefPubMedSuche in Google Scholar
  • 45 Pereira L. Congenital viral infection: traversing the uterine-placental interface. Annu Rev Virol 2018; 5 (01) 273-299
    CrossrefPubMedSuche in Google Scholar
  • 46 Adibi JJ, Marques Jr ETA, Cartus A, Beigi RH. Teratogenic effects of the Zika virus and the role of the placenta. Lancet 2016; 387 (10027): 1587-1590
    CrossrefPubMedSuche in Google Scholar
  • 47 Joerink M, Rindsjö E, van Riel B, Alm J, Papadogiannakis N. Placental macrophage (Hofbauer cell) polarization is independent of maternal allergen-sensitization and presence of chorioamnionitis. Placenta 2011; 32 (05) 380-385
    CrossrefPubMedSuche in Google Scholar
  • 48 Redline RW, Patterson P. Villitis of unknown etiology is associated with major infiltration of fetal tissue by maternal inflammatory cells. Am J Pathol 1993; 143 (02) 473-479
    PubMedSuche in Google Scholar
  • 49 Schwartz DA, Khan R, Stoll B. Characterization of the fetal inflammatory response to cytomegalovirus placentitis. An immunohistochemical study. Arch Pathol Lab Med 1992; 116 (01) 21-27
    PubMedSuche in Google Scholar
  • 50 Guttmacher Institute. Abortion in Latin America and the Caribbean. Fact sheet [Internet]. 2018 [cited 2019 Jan 12]. Available from: https://www.guttmacher.org/sites/default/files/factsheet/ib_aww-latin-america.pdf
    PubMedSuche in Google Scholar