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

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Differential Yellow Fever Susceptibility in New World Nonhuman Primates, Comparison with Humans, and Implications for Surveillance Natália C.C Differential Yellow Fever Susceptibility in New World Nonhuman Primates, Comparison with Humans, and Implications for Surveillance Natália C.C. de Azevedo Fernandes, Juliana M. Guerra, Josué Díaz-Delgado, Mariana S. Cunha, Leila del C. Saad, Silvia D. Iglezias, Rodrigo A. Ressio, Cinthya dos Santos Cirqueira, Cristina T. Kanamura, Isis P. Jesus, Adriana Y. Maeda, Fernanda G.S. Vasami, Júlia de Carvalho, Leonardo J.T. de Araújo, Renato Pereira de Souza, Juliana S. Nogueira, Roberta M.F. Spinola, José L. Catão-Dias ellow fever (YF) is a zoonosis caused by YF vi- A major outbreak of yellow fever (YF) occurred in Brazil rus (YFV; family Flaviviridae, genus Flavivirus) during 2016–2018. Epizootics in New World nonhuman Y primates are sentinel events for YF virus circulation. that has 2 established cycles in South America: urban However, genus-specific susceptibilities and suitability and sylvatic. The sylvatic cycle is maintained by for- for YF surveillance remain poorly understood. We ob- est canopy mosquitoes (Sabethes spp. and Haemagogus tained and compared epidemiologic, histopathologic, spp.) and New World primates (NWPs); humans immunohistochemical, and molecular results from 93 are accidental hosts (1,2). During 2016–2018, YF re- human and 1,752 primate cases submitted during the emerged in Brazil, posing new threats with major recent YF outbreak in Brazil (2017), with the support of epidemic waves in areas with low viral circulation, the Brazilian National YF Surveillance Program. We de- although without evidence of the urban cycle (3). The tected heterogeneous YF-associated profiles among the national surveillance program in Brazil for YF primar- various genera of primates we analyzed. Alouatta pri- ily relies on YF investigation in deceased free-ranging mates were the most reliable sentinel; Sapajus and Cal- NWPs (4). Surveillance of epizootics in NWPs plays licebus primates had higher viral loads but lower propor- tional mortality rates. Callithrix primates were the least a pivotal role for deployment of prevention actions, sensitive, showing lower viral loads, lower proportional emphasizing immediate vaccination of susceptible mortality rates, and no demonstrable YF virus antigen or human populations (5). extensive lesions in liver, despite detectable viral RNA. Brazil has broad and heterogeneous NWP (sub- These differences in susceptibility, viral load, and mortal- order Platyrrhini) diversity: 5 families, 21 genera, ity rates should be considered in strategic surveillance of and 176 species (6). Nevertheless, knowledge of epizootics and control measures for YF. YF in NWP species is limited; most efforts have fo- cused on serologic testing of the species Leontopithe- Author affilations: Instituto Adolfo Lutz, São Paulo, Brazil cus chrysomelas (7), Alouatta spp. (8,9), Cebus spp.(10), (N.C.C. de Azevedo Fernandes, J.M. Guerra, J. Díaz-Delgado, and Saguinus spp. and Saimiri spp. (10). Only howler M.S. Cunha, S.D. Iglezias, R.A. Ressio, C. dos Santos Cirqueira, monkeys (Alouatta sp.) have well-documented liver C.T. Kanamura, I.P. Jesus, A.Y. Maeda, F.G.S. Vasami, involvement in consequence of natural YF infection J. de Carvalho, L.T. de Araújo, R. Pereira de Souza, (11) and are considered reliable sentinels of YFV cir- J.S. Nogueira); Universidade de São Paulo, São Paulo culation, because they show higher susceptibility to (N.C.C. de Azevedo Fernandes, J.M. Guerra, J. Díaz-Delgado, YF than humans and develop a fatal hepatic failure J.L. Catão-Dias); Texas A&M Veterinary Medical Diagnostic with massive cellular death (1,4,12). Howler monkeys Laboratory, College Station, Texas, USA (J. Díaz-Delgado); Centro and laboratory NWP models usually have hepatic de Vigilância Epidemiológica Prof. Alexandre Vranjac, São Paulo changes similar to those found in humans (3,11): mas- (L.D.C. Saad, R.M.F. Spinola) sive necrosis/apoptosis associated with Councilman– DOI: https://doi.org/10.3201/eid2701.191220 Rocha Lima bodies, steatosis, and mild inflammatory Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 1, January 2021 47 RESEARCH infiltrates (13,14), although diverging pathologic fea- liver samples were included. Adverse vaccine effects tures might also be seen (3). Further knowledge of and transplant cases were excluded. All procedures YF pathogenic aspects is needed to guarantee that were approved by the Animal Use and Research Ethi- samples from various species of NWPs would be ad- cal Committees of the Adolfo Lutz Institute (CEUA- equately used for YF surveillance purposes to ensure IAL no. 11/2016 and CEP-IAL no. 3.121.328–caaee appropriate diagnoses and subsequent public health 96138818.0.0000.0059) and the Instituto Chico Mendes responses. In addition, this knowledge will clarify the de Conservação da Biodiversidade protocol 50551–3. effect of YF in the wide range of NWPs in Brazil. During the last YF outbreak in Brazil (2016–2018), Spatial Analysis we observed differences among genera not only in Cases positive by IHC or qRT-PCR were tabulated YF prevalence but also in YF viral load, as reported and plotted. Plots were made by using a map of São (15). These differences might have implications for Paulo state and QGis software (https://qgis.org). NWP as amplifying hosts or as reservoirs in YF cycle. The term reservoir refers to an animal with persis- Histopathologic and Immunohistochemical Analyses tent infection, sometimes without clinical signs, and Protocols and procedures were conducted in the en- sufficient amount of pathogen to act as source of in- hanced laboratory Biosafety Level 2 facility of the Ad- fection. Amplifier, although used as a synonym, is a olfo Lutz Institute. All formalin-fixed, paraffin-embed- broad term referring to a host with high viral load ded liver tissue samples were processed and stained and source of infection (16). Thus, we hypothesized with hematoxylin and eosin for histopathologic exam- that there are different genus-specific susceptibilities ination. IHC was performed according to our labora- among NWPs that could affect YF surveillance/mon- tory protocols. Liver tissue sections were subjected to itoring. To reduce this knowledge gap, we character- antigen retrieval in a pressure cooker in citrate buffer ized and compared the histopathologic signature of for 3 min (120°C, pH 6.0) and then incubated over- YF-associated liver disease, viral antigen detection by night with polyclonal anti-YF (mouse hyperimmune immunohistochemical analysis (IHC), and molecular antiserum against wild strain; Núcleo de Doença de findings in samples from humans and NWPs infect- Transmissão Vetorial, Virology Center, Adolfo Lutz ed by YFV that were received during 2017 at Adolfo Institute) (3,12). Signal amplification was performed Lutz Institute (São Paulo, Brazil). by using the Horseradish Peroxidase–Conjugated Polymer Detection System (REVEAL Biotin-Free Methods Polyvalent; Spring Bioscience Corp., https://www. cmocro.com) and visualized by using diaminobenzi- Data and Sample Collection dine (D-5637; Sigma-Aldrich, https://www.sigma- We obtained formalin-fixed, paraffin-embedded and aldrich.com) and counterstaining with Harris hematox- fresh frozen (−70°C) liver samples from NWPs and ylin. In selected instances, amplification was performed humans from São Paulo state, Brazil, that were sub- by using AP conjugated polymer (MACH4 Universal mitted for YF diagnosis to the Adolfo Lutz Institute AP Polymer Kit; Biocare Medical, https://biocare.net) during 2017, according to the Brazilian National Sur- and visualized by using fast red chromogen (WARP veillance Program of YF by the Ministry of Health RED chromogen kit; Biocare Medical). Known NWPs of Brazil (4). The Adolfo Lutz Institute is an official and human positive and negative control tissues with laboratory for the diagnosis of YFV in humans and omitted first-layer antibody were included. primates. NWP samples came from standardized nec- NWP cases were classified according to the distri- ropsies performed by local surveillance agents. Epi- bution, extent, and nature of microscopic findings af- demiologic (carcass location and date) and biological ter staining with hematoxylin and eosin as described (genera, sex, age) data were obtained from notifica- (Appendix Table 1, https://wwwnc.cdc.gov/EID/ tion files (Sistema Nacional de Agravos de Notifica- article/27/1/19-1220-App1.pdf). For IHC, cases were ção) sent with the samples. Cases designated as Cebus classified as positive, negative, or inadequate on the spp. were reclassified as Sapajus spp., according to basis of YFV antigen detection and varying degrees Alfaro et al. (17). Only NWP cases with genera identi- of typical YF-associated lesions. Inadequate classifi- fied and formalin-fixed, paraffin-embedded liver tis- cation refers to highly autolyzed/decomposed cases sue were included in this study. For humans, samples with lack of immunolabeling. Human cases were from patients with suspected or confirmed YF who classified as full spectrum of YF-associated hepatic died were obtained; only cases with quantitative re- lesions or other histologic patterns. We provide a de- verse transcription PCR (qRT-PCR) results from fresh tailed description of other histologic patterns. 48 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 1, January 2021 Yellow Fever in New World Nonhuman Primates Molecular Analysis by Using qRT-PCR or sex (p = 0.72) difference between positive and neg- Total RNA was extracted from fresh frozen liver by ative groups was detected. using the QIAamp RNA Blood Mini Kit (QIAGEN, Microscopic evaluation of IHC-positive cases https://www.qiagen.com), according to the manu- identified 432 (92.3%) of 468 cases that had a full spec- facturer’s instructions. Amplification of YFV frag- trum of YF hepatic lesions (Figure 1). Three had other ments were performed by using a described protocol histologic patterns: 2 (0.4%) had apoptotic hepato- (18) that targets the highly conserved 5′ noncoding cytes, and 1 (0.2%) had mild degenerative and reac- region of the genome (112 bp) and is based on a Taq- tion findings. These 3 cases were Alouatta spp.
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