Differential Yellow Fever Susceptibility in New World Nonhuman Primates, Comparison with Humans, and Implications for Surveillance

Overview

Journal Emerg Infect Dis

Specialty Infectious Diseases

Date 2020 Dec 22

PMID 33350931

Citations 21

Authors

Natalia C C de Azevedo Fernandes

Juliana M Guerra

Josue Diaz-Delgado

Mariana S Cunha

Leila delC Saad

Silvia D Iglezias

Rodrigo A Ressio

Cinthya Dos Santos Cirqueira

Cristina T Kanamura

Isis P Jesus

Adriana Y Maeda

Fernanda G S Vasami

Julia de Carvalho

Leonardo J T de Araujo

Renato Pereira de Souza

Juliana S Nogueira

Roberta M F Spinola

Jose L Catao-Dias

Affiliations

Soon will be listed here.

Abstract

A major outbreak of yellow fever (YF) occurred in Brazil during 2016-2018. Epizootics in New World nonhuman primates are sentinel events for YF virus circulation. However, genus-specific susceptibilities and suitability for YF surveillance remain poorly understood. We obtained and compared epidemiologic, histopathologic, immunohistochemical, and molecular results from 93 human and 1,752 primate cases submitted during the recent YF outbreak in Brazil (2017), with the support of the Brazilian National YF Surveillance Program. We detected heterogeneous YF-associated profiles among the various genera of primates we analyzed. Alouatta primates were the most reliable sentinel; Sapajus and Callicebus primates had higher viral loads but lower proportional mortality rates. Callithrix primates were the least sensitive, showing lower viral loads, lower proportional mortality rates, and no demonstrable YF virus antigen or extensive lesions in liver, despite detectable viral RNA. These differences in susceptibility, viral load, and mortality rates should be considered in strategic surveillance of epizootics and control measures for YF.

Citing Articles

Natural exposure to Chikungunya virus in golden-headed lion tamarin (Leontopithecus chrysomelas, Kuhl, 1820) from non-protected areas in southern Bahia, Brazil: Implications and significance.

Bernal-Valle S, Monteiro de Mello Mares-Guia M, Abreu F, Campos F, Oliveira C, Veloso Ramos A PLoS Negl Trop Dis. 2025; 19(1):e0012695.

PMID: 39854566 PMC: 11761120. DOI: 10.1371/journal.pntd.0012695.

Reemergence of yellow fever in the state of São Paulo: the structuring role of surveillance of epizootics in non-human primates in a one health approach.

Saad L, Chiaravalloti-Neto F Rev Bras Epidemiol. 2024; 27:e240064.

PMID: 39699461 PMC: 11654290. DOI: 10.1590/1980-549720240064.

Detection of neutralizing antibodies against arboviruses from liver homogenates.

Costa T, Arruda M, Garcia-Oliveira G, de Sousa Reis E, Guimaraes A, Moreira G PLoS Negl Trop Dis. 2024; 18(12):e0012740.

PMID: 39671423 PMC: 11676865. DOI: 10.1371/journal.pntd.0012740.

Coinfection with Canine Distemper Virus and Yellow Fever Virus in a Neotropical Primate in Brazil.

Monteiro de Mello Mares-Guia M, Furtado M, Chalhoub F, Portugal M, de Oliveira Coelho J, de Filippis A Viruses. 2024; 16(11).

PMID: 39599785 PMC: 11598961. DOI: 10.3390/v16111670.

Ecological Requirements for Abundance and Dispersion of Brazilian Yellow Fever Vectors in Tropical Areas.

Prado A, Prist P, Mucci L, de Freitas P Int J Environ Res Public Health. 2024; 21(5).

PMID: 38791823 PMC: 11120827. DOI: 10.3390/ijerph21050609.

References

KLION F, Schaffner F . The ultrastructure of acidophilic "Councilman-like" bodies in the liver. Am J Pathol. 1966; 48(5):755-67. PMC: 1907261. View

de Rezende I, Sacchetto L, de Mello E, Augusto Alves P, de Melo Iani F, Adelino T . Persistence of Yellow fever virus outside the Amazon Basin, causing epidemics in Southeast Brazil, from 2016 to 2018. PLoS Negl Trop Dis. 2018; 12(6):e0006538. PMC: 6002110. DOI: 10.1371/journal.pntd.0006538. View

Mulchandani R, Massebo F, Bocho F, Jeffries C, Walker T, Messenger L . A community-level investigation following a yellow fever virus outbreak in South Omo Zone, South-West Ethiopia. PeerJ. 2019; 7:e6466. PMC: 6387579. DOI: 10.7717/peerj.6466. View

Vieira W, Gayotto L, DE LIMA C, De Brito T . Histopathology of the human liver in yellow fever with special emphasis on the diagnostic role of the Councilman body. Histopathology. 1983; 7(2):195-208. DOI: 10.1111/j.1365-2559.1983.tb02235.x. View

Quaresma J, Barros V, Pagliari C, Fernandes E, Guedes F, Takakura C . Revisiting the liver in human yellow fever: virus-induced apoptosis in hepatocytes associated with TGF-beta, TNF-alpha and NK cells activity. Virology. 2005; 345(1):22-30. DOI: 10.1016/j.virol.2005.09.058. View

Lynch Alfaro J, Silva Jr J, Rylands A . How different are robust and gracile capuchin monkeys? An argument for the use of sapajus and cebus. Am J Primatol. 2012; 74(4):273-86. DOI: 10.1002/ajp.22007. View

Faria N, Kraemer M, Hill S, Goes de Jesus J, Aguiar R, Iani F . Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science. 2018; 361(6405):894-899. PMC: 6874500. DOI: 10.1126/science.aat7115. View

de Azevedo Fernandes N, Cunha M, Guerra J, Ressio R, Dos Santos Cirqueira C, Iglezias S . Outbreak of Yellow Fever among Nonhuman Primates, Espirito Santo, Brazil, 2017. Emerg Infect Dis. 2017; 23(12):2038-2041. PMC: 5708241. DOI: 10.3201/eid2312.170685. View

Rifakis P, Benitez J, De-La-Paz-Pineda J, Rodriguez-Morales A . Epizootics of yellow fever in Venezuela (2004-2005): an emerging zoonotic disease. Ann N Y Acad Sci. 2006; 1081:57-60. DOI: 10.1196/annals.1373.005. View

10.

Davis N . THE SUSCEPTIBILITY OF MARMOSETS TO YELLOW FEVER VIRUS. J Exp Med. 2009; 52(3):405-16. PMC: 2131878. DOI: 10.1084/jem.52.3.405. View

11.

Catenacci L, Ferreira M, Martins L, De Vleeschouwer K, Cassano C, Oliveira L . Surveillance of Arboviruses in Primates and Sloths in the Atlantic Forest, Bahia, Brazil. Ecohealth. 2018; 15(4):777-791. DOI: 10.1007/s10393-018-1361-2. View

12.

Miagostovich M, Nogueira R, Cavalcanti S, Marzochi K, Schatzmayr H . Dengue epidemic in the state of Rio de Janeiro, Brazil: virological and epidemiological aspects. Rev Inst Med Trop Sao Paulo. 1993; 35(2):149-54. DOI: 10.1590/s0036-46651993000200006. View

13.

Sato M, Kojima M, Nagatsuma A, Nakamura Y, Saito N, Ochiai A . Optimal fixation for total preanalytic phase evaluation in pathology laboratories: a comprehensive study including immunohistochemistry, DNA, and mRNA assays. Pathol Int. 2014; 64(5):209-16. DOI: 10.1111/pin.12164. View

14.

Callender D . Management and control of yellow fever virus: Brazilian outbreak January-April, 2018. Glob Public Health. 2018; 14(3):445-455. DOI: 10.1080/17441692.2018.1512144. View

15.

Kuno G, Mackenzie J, Junglen S, Hubalek Z, Plyusnin A, Gubler D . Vertebrate Reservoirs of Arboviruses: Myth, Synonym of Amplifier, or Reality?. Viruses. 2017; 9(7). PMC: 5537677. DOI: 10.3390/v9070185. View

16.

Domingo C, Patel P, Yillah J, Weidmann M, Mendez J, Nakoune E . Advanced yellow fever virus genome detection in point-of-care facilities and reference laboratories. J Clin Microbiol. 2012; 50(12):4054-60. PMC: 3503008. DOI: 10.1128/JCM.01799-12. View

17.

Engelmann F, Josset L, Girke T, Park B, Barron A, Dewane J . Pathophysiologic and transcriptomic analyses of viscerotropic yellow fever in a rhesus macaque model. PLoS Negl Trop Dis. 2014; 8(11):e3295. PMC: 4238990. DOI: 10.1371/journal.pntd.0003295. View

18.

Hoyos M, Bloor P, Defler T, Vermeer J, Rohe F, Farias I . Phylogenetic relationships within the Callicebus cupreus species group (Pitheciidae: Primates): Biogeographic and taxonomic implications. Mol Phylogenet Evol. 2016; 102:208-19. DOI: 10.1016/j.ympev.2016.05.031. View

19.

Possas C, Lourenco-de-Oliveira R, Tauil P, De Paula Pinheiro F, Pissinatti A, da Cunha R . Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz. 2018; 113(10):e180278. PMC: 6135548. DOI: 10.1590/0074-02760180278. View

20.

Moreno E, Spinola R, Tengan C, Brasil R, Siciliano M, Coimbra T . Yellow fever epizootics in non-human primates, São Paulo state, Brazil, 2008-2009. Rev Inst Med Trop Sao Paulo. 2013; 55(1):45-50. DOI: 10.1590/s0036-46652013000100008. View