The spectrum of neuropathological changes associated with congenital Zika virus infection

Acta Neuropathologica

Volumn 133, Issue 6, 2017, Pages 983-999

  Chimelli, Leila ^a   Melo, Adriana S O ^b,c   Avvad Portari, Elyzabeth ^d   Wiley, Clayton A ^e   Camacho, Aline H S ^a   Lopes, Vania S ^f   Machado, Heloisa N ^d   Andrade, Cecilia V ^d   Dock, Dione C A ^d   Moreira, Maria Elisabeth ^d   Tovar Moll, Fernanda ^g   Oliveira Szejnfeld, Patricia S ^h   Carvalho, Angela C G ^f   Ugarte, Odile N ^f   Batista, Alba G M ^c   Amorim, Melania M R ^b   Melo, Fabiana O ^b   Ferreira, Thales A ^b   Marinho, Jacqueline R L ^c   Azevedo, Girlene S ^b   Leal, Jeime I B F ^c   da Costa, Rodrigo F Madeiro ^g   Rehen, Stevens ^g   Arruda, Monica B ^a   Brindeiro, Rodrigo M ^a   Delvechio, Rodrigo ^a   Aguiar, Renato S ^a   Tanuri, Amilcar ^a   more..

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b Instituto de Pesquisa Professor Joaquim Amorim Neto   (Brazil)

^c Health Secretary Campina Grande   (Brazil)

^d INSTITUTO OSWALDO CRUZ   (Brazil)

^e PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

^f HOSPITAL UNIVERSITÁRIO ANTÔNIO PEDRO   (Brazil)

^g D OR INSTITUTE FOR RESEARCH AND EDUCATION IDOR   (Brazil)

^h Foundation Institute for Education and Research in Diagnostic Imaging (FIDI)   (Brazil)

Author keywords

Calcification; Congenital ZIKV infection; In situ hybridization; Microcephaly; Neuropathology; Zika virus

Indexed keywords

ADULT; AMNION FLUID; ARTHROGRYPOSIS; ARTICLE; AUTOPSY; BRAIN CORTEX; BRAZIL; CALCIFICATION; CONGENITAL INFECTION; ELECTRON MICROSCOPY; FEMALE; HEART INFARCTION; HEMISPHERE; HUMAN; HUMAN TISSUE; HYPOPLASIA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUNG HYPOPLASIA; MATERNAL HYPERTENSION; MICROPHTHALMIA; MULTIDETECTOR COMPUTED TOMOGRAPHY; NEUROIMAGING; NEUROPATHOLOGY; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PLACENTA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STILLBIRTH; TRANSMISSION ELECTRON MICROSCOPY; VIRUS HEPATITIS; ZIKA FEVER; ADOLESCENT; BRAIN; COMPLICATION; DIAGNOSTIC IMAGING; EYE; HYPOPHYSIS; MALE; MICROCEPHALY; PATHOLOGY; PREGNANCY; PREGNANCY COMPLICATION; SKELETAL MUSCLE; SPINAL CORD; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN; EYE; FEMALE; HUMANS; INFANT, NEWBORN; MALE; MICROCEPHALY; MUSCLE, SKELETAL; PITUITARY GLAND; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; SPINAL CORD; YOUNG ADULT; ZIKA VIRUS INFECTION;

EID: 85015944370     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-017-1699-5     Document Type: Article

References (49)

1. Alpert SG, Fergerson J, Noël LP (2003) Intrauterine West Nile virus: ocular and systemic findings. Am J Ophthalmol 136:733–735. doi:10.1016/S0002-9394(03)00452-5
2. Araujo AQ, Silva MT, Araujo AP (2016) Zika virus-associated neurological disorders: a review. Brain 139:2122–2130. doi:10.1093/brain/aww158
3. Basurko C, Carles G, Youssef M, Guindi WEL (2009) Maternal and fetal consequences of dengue fever during pregnancy. Eur J Obstet Gynecol Reprod Biol 147:29–32. doi:10.1016/j.ejogrb.2009.06.028
4. Besnard M, Eyrolle-Guignot D, Guillemette-Artur P, Lastère S, Bost-Bezeaud F, Marcelis L et al (2016) Congenital cerebral malformations and dysfunction in fetuses and newborns following the 2013–2014 Zika virus epidemic in French Polynesia. Euro Surveill. doi:10.2807/1560-7917.ES.2016.21.13.30181
5. Brasil P, Pereira JP Jr, Raja Gabaglia C, Damasceno L, Wakimoto M, Ribeiro Nogueira RM et al (2016) Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med 375:2321–2334. doi:10.1056/NEJMoa1602412
6. Brien JD, Uhrlaub JL, Hirsch A, Wiley CA, Nikolich-Zugich J (2009) Key role of T cell defects in age-related vulnerability to West Nile virus. J Exp Med 206:2735–2745. doi:10.1084/jem.20090222
7. Campos GS, Bandeira AC, Sardi SI (2015) Zika virus outbreak, Bahia, Brazil. Emerg Infect Dis 21:1885–1886. doi:10.3201/eid2110.150847
8. Carteaux G, Maquart M, Bedet A, Contou D, Brugieres P, Fourati S et al (2016) Zika virus associated with meningoencephalitis. N Engl J Med 374:1595–1596. doi:10.1056/NEJMc1602964
9. Cugola FR, Fernandes IR, Russo FB, Freitas BC, Dias JLM, Guimarães KP et al (2016) The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534:267–271. doi:10.1038/nature18296
10. Dasti JI (2016) Zika virus infections: an overview of current scenario. Asian Pac J Trop Med 9:621–625. doi:10.1016/j.apjtm.2016.05.010
11. de Fatima Vasco Aragao M, van der Linden V, Brainer-Lima AM, Coeli RR, Rocha MA, Sobral da Silva P et al (2016) Clinical features and neuroimaging (CT and MRI) findings in presumed Zika virus related congenital infection and microcephaly: retrospective case series study. BMJ 353:i1901. doi:10.1136/bmj.i1901
12. de Noronha L, Zanluca C, Azevedo MLV, Luz KG, dos Santos CND (2016) Zika virus damages the human placental barrier and presents marked fetal neurotropism. Mem Inst Oswaldo Cruz 111:287–293. doi:10.1590/0074-02760160085
13. Dick GWA (1952) Zika virus (I). Isolations and serological specificity. Trans R Soc Trop Med Hyg 46:509–520. doi:10.1016/0035-9203(52)90042-4
14. Driggers RW, Ho C-Y, Korhonen EM, Kuivanen S, Jääskeläinen AJ, Smura T et al (2016) Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N Engl J Med 374:2142–2151. doi:10.1056/NEJMoa1601824
15. Duffy MR, Chen T-H, Hancock WT, Powers AM, Kool JL, Lanciotti RS et al (2009) Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 360:2536–2543. doi:10.1056/NEJMoa0805715
16. Ellison D, Love S, Chimelli LMC, Harding B, Lowe JS, Vinters HV et al (2012) Neuropathology: a reference text of CNS pathology. Elsevier, Amsterdam
17. Garcez PP, Loiola EC, Madeiro da Costa R, Higa LM, Trindade P, Delvecchio R et al (2016) Zika virus impairs growth in human neurospheres and brain organoids. Science 352:816–818. doi:10.1126/science.aaf6116
18. Garcez PP, Nascimento JM, Mota de Vasconcelos J, Madeiro da Costa R, Delvecchio R, Trindade P et al (2016) Zika virus disrupts molecular fingerprinting of human neurospheres. Sci Rep. 7:40780. doi:10.1038/srep40780
19. Hanners NW, Eitson JL, Usui N, Richardson RB, Wexler EM, Konopka G et al (2016) Western Zika virus in human fetal neural progenitors persists long term with partial cytopathic and limited immunogenic effects. Cell Rep 15:2315–2322. doi:10.1016/j.celrep.2016.05.075
20. Hazin AN, Poretti A, Di Cavalcanti Souza Cruz D, Tenorio M, van der Linden A, Pena LJ, Brito C et al (2016) Computed tomographic findings in microcephaly associated with Zika virus. N Engl J Med 374:2193–2195. doi:10.1056/NEJMc1603617
21. Ioos S, Mallet HP, Leparc Goffart I, Gauthier V, Cardoso T, Herida M (2014) Current Zika virus epidemiology and recent epidemics. Med Mal Infect 44:302–307. doi:10.1016/j.medmal.2014.04.008
22. Johansson MA, Mier-y-Teran-Romero L, Reefhuis J, Gilboa SM, Hills SL (2016) Zika and the risk of microcephaly. N Engl J Med 375:1–4. doi:10.1056/NEJMp1605367
23. Klase ZA, Khakhina S, Schneider ADB, Callahan MV, Glasspool-Malone J, Malone R (2016) Zika fetal neuropathogenesis: etiology of a viral syndrome. PLoS Negl Trop Dis 10:1–32. doi:10.1371/journal.pntd.0004877
24. Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ et al (2008) Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 14:1232–1239. doi:10.3201/eid1408.080287
25. Larroche J-C (1977) Developmental pathology of the neonate. Excerpta Medica, Amsterdam, pp 1–21
26. Likos A, Griffin I, Bingham AM, Stanek D, Fischer M, White S et al (2016) Local mosquito-borne transmission of Zika virus–Miami-Dade and Broward Counties, Florida, June–August 2016. MMWR Morb Mortal Wkly Rep 65:1032–1038. doi:10.15585/mmwr.mm6538e1
27. Love S, Wiley CA, Lucas S (2015) Viral infections. In: Love S, Perry A, Ironside J, Budka H (eds) Greenfield’s Neuropathology, 9th edn. CRC Press, London, pp 1087–1191
28. Malone RW, Homan J, Callahan MV, Glasspool-Malone J, Damodaran L et al (2016) Zika virus: medical countermeasure development challenges. PLoS Negl Trop Dis 10:e0004530. doi:10.1371/journal.pntd.0004530
29. Martines RB, Bhatnagar J, de Oliveira Ramos AM, Davi HPF, Iglezias SDA, Kanamura CT et al (2016) Pathology of congenital Zika syndrome in Brazil: a case series. Lancet 388:898–904. doi:10.1016/S0140-6736(16)30883-2
30. Mécharles S, Herrmann C, Poullain P, Tran T, Deschamps N, Mathon G et al (2016) Case report acute myelitis due to Zika virus infection. Lancet 8:6736. doi:10.1136/bcr-2012-007094.4
31. Melo AS, Aguiar RS, Amorim MMR, Arruda MB, de Melo FO, Ribeiro STC et al (2016) Congenital Zika virus infection: Beyond neonatal microcephaly. JAMA Neurol 73:1407–1416. doi:10.1001/jamaneurol.2016.3720
32. Mlakar J, Korva M, Tul N, Popović M, Poljšak-Prijatelj M, Mraz J et al (2016) Zika virus associated with microcephaly. N Engl J Med 374:951–958. doi:10.1056/NEJMoa1600651
33. Nowakowski TJ, Pollen AA, Di Lullo E, Sandoval-Espinosa C, Bershteyn M, Kriegstein AR (2016) Expression analysis highlights AXL as a candidate zika virus entry receptor in neural stem cells. Cell Stem Cell 18:591–596. doi:10.1016/j.stem.2016.03.012
34. Oliveira Melo AS, Malinger G, Ximenes R, Szejnfeld PO, Alves Sampaio S, Bispo De Filippis AM (2016) Zika virus intrauterine infection causes fetal brain abnormality and microcephaly: tip of the iceberg? Ultrasound Obstet Gynecol 47:6–7. doi:10.1002/uog.15831
35. Ramos da Silva S, Gao SJ (2016) Zika virus: an update on epidemiology, pathology, molecular biology, and animal model. J Med Virol 88:1291–1296. doi:10.1002/jmv.24563
36. Sarno M, Sacramento GA, Khouri R, do Rosário MS, Costa F, Archanjo G et al (2016) Zika virus infection and stillbirths: a case of hydrops fetalis, hydranencephaly and fetal demise. PLoS Negl Trop Dis 10:e0004517. doi:10.1371/journal.pntd.0004517
37. Schuler-Faccini L, Ribeiro EM, Feitosa IML, Horovitz DDG, Cavalcanti DP, Pessoa A et al (2016) Possible association between zika virus infection and microcephaly—Brazil, 2015. MMWR Morb Mortal Wkly Rep 65:59–62. doi:10.15585/mmwr.mm6503e2
38. Schwartz DA (2016) Autopsy and postmortem studies are concordant: pathology of Zika virus infection is neurotropic in fetuses and infants with microcephaly following transplacental transmission. Arch Pathol Lab Med 141(1):68–72. doi:10.5858/arpa.2016-0343-OA
39. Slavov SN, Otaguiri KK, Kashima S, Covas DT (2016) Overview of Zika virus (ZIKV) infection in regards to the Brazilian epidemic. Brazilian J Med Biol Res 49:e5420. doi:10.1590/1414-431X20165420
40. Snijders RJ, Nicolaides KH (1994) Fetal biometry at 14–40 weeks’ gestation. Ultrasound Obstet Gynecol 4:34–48. doi:10.1177/875647939401000434
41. Soares de Oliveira-Szejnfeld P, Levine D, de O Melo AS, Amorim MMR, Batista AGM, Chimelli L et al (2016) Congenital brain abnormalities and zika virus: what the radiologist can expect to see prenatally and postnatally. Radiology 281:203–218. doi:10.1148/radiol.2016161584
42. Solomon IH, Milner DA, Folkerth RD (2016) Neuropathology of Zika virus infection. J Neuroinfect Dis 7(2):220
43. Souza BS, Sampaio GL, Pereira CS, Campos GS, Sardi SI, Freitas LAR et al (2016) Zika virus infection induces mitosis abnormalities and apoptotic cell death of human neural progenitor cells. Sci Rep 6:39775. doi:10.1038/srep39775
44. Štrafela P, Vizjak A, Mraz J, Mlakar J, Pižem J, Tul N et al (2016) Zika virus-associated micrencephaly: a thorough description of neuropathologic findings in the fetal central nervous system. Arch Pathol Lab Med 141:73–81. doi:10.5858/arpa.2016-0341-SA
45. Tadros MA, Lim R, Hughes DI, Brichta AM, Callister RJ (2015) Electrical maturation of spinal neurons in the human fetus: comparison of ventral and dorsal horn. J Neurophysiol 114:2661–2671. doi:10.1152/jn.00682.2015
46. Tang H, Hammack C, Ogden SC, Wen Z, Qian X, Li Y et al (2016) Zika virus infects human cortical neural progenitors and attenuates their growth brief report Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18:587–590. doi:10.1016/j.stem.2016.02.016
47. Teissier N, Fallet-Bianco C, Delezoide A-L, Laquerrière A, Marcorelles P, Khung-Savatovsky S et al (2014) Cytomegalo virus-induced brain malformations in fetuses. J Neuropathol Exp Neurol 73:143–158. doi:10.1097/NEN.0000000000000038
48. Wells MF, Salick MR, Wiskow O, Ho DJ, Worringer KA, Ihry RJ et al (2016) Genetic ablation of AXL does not protect human neural progenitor cells and cerebral organoids from Zika virus infection. Cell Stem Cell 19:703–708. doi:10.1016/j.stem.2016.11.011
49. Zanluca C, Melo VC, Mosimann AL, dos Santos GI, dos Santos CN, Luz K (2015) First report of autochthonous transmission of Zika virus in Brazil. Mem Inst Oswaldo Cruz 110:569–572. doi:10.1590/0074-02760150192