Original Article • Rev. bras. Epidemiol. 27 16 Dec 20242024 • https://doi.org/10.1590/1980-549720240064   copy

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

Leila del Castillo Saad Francisco Chiaravalloti-Neto About the authors

ABSTRACT

Objective:

to present a comprehensive analysis of YF occurrence of in the state of São Paulo since its reemergence, and the ongoing process of structuring the surveillance of epizootics in non-human primates in a one health approach.

Methods:

descriptive study of human cases and epizootics in non-human primates, structuring actions and the one health approach used in the state of São Paulo for yellow fever surveillance from 2000 to 2023.

Results:

from 2000 to 2023, 679 human cases and 857 epizootics in NHPs confirmed for yellow fever were recorded. There was an intensification of epizootic surveillance actions in non-human primates from 2017, when the virus circulated in areas without vaccine recommendations in the state.

Conclusion:

Five outbreaks were registered during the evaluated period, and the surveillance of epizootics in non-human primates played a fundamental role in implementing disease prevention and control measures in areas without vaccination recommendation, guiding vaccination actions, and serving as an example of how a one health approach can be adopted within epidemiological surveillance, making it more resilient to emerging threats.

Keywords:
Yellow fever; Primates; Epidemiologic surveillance; One health

INTRODUCTION

More than two decades have passed since yellow fever (YF) was once again detected in the state of São Paulo (SP)11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... . This vector-borne, vaccine-preventable viral disease has a significant impact wherever it emerges22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,33 Silva NIO, Sacchetto L, Rezende IM, Trindade GS, LaBeaud AD, Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J 2020; 17(1): 9. https://doi.org/10.1186/s12985-019-1277-7
https://doi.org/10.1186/s12985-019-1277-... . In Brazil, two patterns of occurrence are recognized: sylvatic yellow fever (SYF) and urban yellow fever (UYF)11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600...

2 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... -33 Silva NIO, Sacchetto L, Rezende IM, Trindade GS, LaBeaud AD, Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J 2020; 17(1): 9. https://doi.org/10.1186/s12985-019-1277-7
https://doi.org/10.1186/s12985-019-1277-... . Numerous reports emphasize the critical importance of YF in the context of surveillance and control, given its high lethality in severe cases and its considerable potential for dissemination11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600...

2 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539...

3 Silva NIO, Sacchetto L, Rezende IM, Trindade GS, LaBeaud AD, Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J 2020; 17(1): 9. https://doi.org/10.1186/s12985-019-1277-7
https://doi.org/10.1186/s12985-019-1277-... -44 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento de Articulação Estratégica de Vigilância em Saúde e Ambiente. Guia de vigilância em saúde [Internet]. Brasília: Ministério da Saúde; 2023 [cited on Jan 20, 2024]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/svsa/vigilancia/guia-de-vigilancia-em-saude-volume-2-6a-edicao/view
https://www.gov.br/saude/pt-br/centrais-... . Although the urban cycle has not been observed in Brazil since 1942, the reurbanization of YF remains a major concern, as its urban vector, Aedes aegypti, is widespread in nearly all densely populated urban areas of the country55 Cunha MS, Tubaki RM, Menezes RMT, Pereira M, Caleiro GS, Coelho E, et al. Possible non-sylvatic transmission of yellow fever between non-human primates in São Paulo city, Brazil, 2017–2018. Sci Rep 2020; 10(1): 15751. https://doi.org/10.1038/s41598-020-72794-x
https://doi.org/10.1038/s41598-020-72794...

6 Gebreyes WA, Dupouy-Camet J, Newport MJ, Oliveira CJ, Schlesinger LS, Saif YM, et al. The global one health paradigm: challenges and opportunities for tackling infectious diseases at the human, animal, and environment interface in low-resource settings. PLoS Negl Trop Dis 2014; 8(11): e3257. https://doi.org/10.1371/journal.pntd.0003257
https://doi.org/10.1371/journal.pntd.000... -77 Kelly TR, Karesh WB, Johnson CK, Gilardi KVK, Anthony SJ, Goldstein T, et al. One health proof of concept: bringing a transdisciplinary approach to surveillance for zoonotic viruses at the human-wild animal interface. Prev Vet Med 2017; 137(Pt B): 112-8. https://doi.org/10.1016/j.prevetmed.2016.11.023
https://doi.org/10.1016/j.prevetmed.2016... .

YF is classified as a reemerging zoonosis. Of the pathogens identified as emerging or reemerging, 75% are of zoonotic origin66 Gebreyes WA, Dupouy-Camet J, Newport MJ, Oliveira CJ, Schlesinger LS, Saif YM, et al. The global one health paradigm: challenges and opportunities for tackling infectious diseases at the human, animal, and environment interface in low-resource settings. PLoS Negl Trop Dis 2014; 8(11): e3257. https://doi.org/10.1371/journal.pntd.0003257
https://doi.org/10.1371/journal.pntd.000... ,77 Kelly TR, Karesh WB, Johnson CK, Gilardi KVK, Anthony SJ, Goldstein T, et al. One health proof of concept: bringing a transdisciplinary approach to surveillance for zoonotic viruses at the human-wild animal interface. Prev Vet Med 2017; 137(Pt B): 112-8. https://doi.org/10.1016/j.prevetmed.2016.11.023
https://doi.org/10.1016/j.prevetmed.2016... . The health of humans, animals, and the environment are interconnected and inseparable, a concept that forms the basis of the One Health approach. This paradigm, which has gained prominence in recent years, plays a crucial role in discussions on expanded health across various contexts in which it is observed66 Gebreyes WA, Dupouy-Camet J, Newport MJ, Oliveira CJ, Schlesinger LS, Saif YM, et al. The global one health paradigm: challenges and opportunities for tackling infectious diseases at the human, animal, and environment interface in low-resource settings. PLoS Negl Trop Dis 2014; 8(11): e3257. https://doi.org/10.1371/journal.pntd.0003257
https://doi.org/10.1371/journal.pntd.000... ,77 Kelly TR, Karesh WB, Johnson CK, Gilardi KVK, Anthony SJ, Goldstein T, et al. One health proof of concept: bringing a transdisciplinary approach to surveillance for zoonotic viruses at the human-wild animal interface. Prev Vet Med 2017; 137(Pt B): 112-8. https://doi.org/10.1016/j.prevetmed.2016.11.023
https://doi.org/10.1016/j.prevetmed.2016... .

After nearly 50 years of epidemiological silence, the state of São Paulo began detecting the reemergence of wild circulation of the yellow fever virus within its borders in 200011 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... . In 2003, the state's Epidemiological Surveillance Center (Centro de Vigilância Epidemiológica – CVE), in collaboration with the Ministry of Health (MoH) and municipalities, initiated a surveillance program for epizootics in non-human primates (NHPs). This effort aimed at early detection of viral circulation within its enzootic cycle, utilizing a One Health approach to facilitate prevention and control measures for YF. Since then, numerous training sessions, meetings, and qualifications have been conducted to enhance and improve epidemiological data on the presence or absence of the virus through NHP surveillance11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... .

YF continued to exhibit non-endemic behavior, making it challenging to predict its circulation patterns. Consequently, the state was divided into areas with vaccine recommendation (AWVR), which indicated evidence of viral circulation in vectors, NHPs, or humans, and areas without vaccine recommendation (AW/oVR). This classification remained in place until 2019, when the entire state was designated as AWVR22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,88 Moreno ES, Rocco IM, Bergo ES, Brasil RA, Siciliano MM, Suzuki A, et al. Reemergence of yellow fever: detection of transmission in the State of São Paulo, Brazil, 2008. Rev Soc Bras Med Trop 2011; 44(3): 290-6. https://doi.org/10.1590/S0037-86822011005000041
https://doi.org/10.1590/S0037-8682201100... ,99 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
https://bvsms.saude.gov.br/bvs/publicaco... .

Since 201622 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,77 Kelly TR, Karesh WB, Johnson CK, Gilardi KVK, Anthony SJ, Goldstein T, et al. One health proof of concept: bringing a transdisciplinary approach to surveillance for zoonotic viruses at the human-wild animal interface. Prev Vet Med 2017; 137(Pt B): 112-8. https://doi.org/10.1016/j.prevetmed.2016.11.023
https://doi.org/10.1016/j.prevetmed.2016... ,88 Moreno ES, Rocco IM, Bergo ES, Brasil RA, Siciliano MM, Suzuki A, et al. Reemergence of yellow fever: detection of transmission in the State of São Paulo, Brazil, 2008. Rev Soc Bras Med Trop 2011; 44(3): 290-6. https://doi.org/10.1590/S0037-86822011005000041
https://doi.org/10.1590/S0037-8682201100... , the state has experienced the highest level of viral circulation in its territory since the major UYF epidemics of the 19th century99 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
https://bvsms.saude.gov.br/bvs/publicaco... . In 2017, when YF reached populated regions previously classified as AW/oVR, epizootic surveillance in NHPs was essential not only for confirming the enzootic circulation of the virus but also for coordinating, designing, and planning vaccination efforts99 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
https://bvsms.saude.gov.br/bvs/publicaco... ,1010 Cunha MS, Costa AC, Fernandes NCCA, Guerra JM, Santos FCP, Nogueira JS, et al. Epizootics due to yellow fever virus in São Paulo state, Brazil: viral dissemination to new areas (2016–2017). Sci Rep 2019; 9(1): 5474. https://doi.org/10.1038/s41598-019-41950-3
https://doi.org/10.1038/s41598-019-41950... .

During the largest outbreak of viral circulation in the state of São Paulo in recent history, the yellow fever virus spread rapidly to areas where vaccination was not previously recommended. This situation necessitated the immunization of a large segment of the population within a short timeframe. Consequently, the state revised its existing approach, which was based on the Ministry of Health's strategy of vaccinating in affected areas and surrounding regions. The new methodology focused on vaccination through ecological corridors of viral dispersion, utilizing data generated from epizootic surveillance in NHPs22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,44 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento de Articulação Estratégica de Vigilância em Saúde e Ambiente. Guia de vigilância em saúde [Internet]. Brasília: Ministério da Saúde; 2023 [cited on Jan 20, 2024]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/svsa/vigilancia/guia-de-vigilancia-em-saude-volume-2-6a-edicao/view
https://www.gov.br/saude/pt-br/centrais-... ,99 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
https://bvsms.saude.gov.br/bvs/publicaco... .

This study aimed to describe, according to time, place, person, and NHP, the occurrence of YF in the state of SP since its reemergence, which began in 2000, as well as the ongoing process of structuring surveillance in NHPs. It will also identify and discuss the implications of these developments in the context of actions recommended for the prevention and control of the disease, and how the One Health approach has been essential in this context and should be expanded in the epidemiological methods applied to epidemiological surveillance.

METHODS

This descriptive study utilizes secondary data from the Notifiable Diseases Information System (Sistema de Informação de Agravos de Notificação – SINAN), specifically from the modules on YF and epizootics in NHPs. The data includes information on epidemiological investigations and technical reports developed by state and municipal surveillance technicians regarding autochthonous human cases and confirmed epizootics in NHPs from 2000 to 2023. This information is available through the Division of Vector-Borne Diseases and Zoonoses (DVZOO) of the São Paulo State Health Secretariat (SES) and spans two decades.

YF surveillance is conducted through notifications of suspected occurrences in both human cases and epizootics in NHPs; the definitions of suspected and confirmed cases are outlined in Chart 1.

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Chart 1
Definitions applied by epidemiological surveillance for yellow fever. Brazil, 2023.

The study site was the state of SP, which comprises 645 municipalities covering an area of 248,221.996 km² and an estimated population of 44,420,459 inhabitants, according to 2022 data from the Brazilian Institute of Geography and Statistics (Instituto Brasileiro de Geografia e Estatística – IBGE). Of the 645 municipalities, 509 have populations of fewer than 50,000 inhabitants. Despite their large number, these municipalities account for only 16% of the state's total population. Data from the 2022 census indicated that 1,676,948 people live in rural areas, highlighting the significant urbanization of São Paulo1111 Brasil. Instituto Brasileiro de Geografia e Estatística. Atlas do Censo Demográfico 2010 [Internet]. 2010 [cited on Nov 08, 2023]. Available at: https://censo2010.ibge.gov.br/apps/atlas/
https://censo2010.ibge.gov.br/apps/atlas... .

All autochthonous human cases and confirmed epizootics in NHPs reported to the state of SP YF surveillance system from January 2000 to December 2023 were included in the study. The following variables were analyzed for human cases: date of symptom onset (month and year), gender, median age, lethality, and the municipality of the probable site of infection. For epizootics in NHPs, the variables analyzed were: date of occurrence, gender of the NHPs, and municipality of occurrence.

For over 20 years, the CVE DVZOO has coordinated efforts to implement and improve this component of disease surveillance in the state, including training, qualifications, and technical meetings with municipalities. Epidemiological data from disease surveillance were used to identify municipalities with viral circulation and to describe human cases and epizootics in NHPs. Additionally, technical documents available at the CVE DVZOO were utilized to present the continuous process of structuring surveillance in NHPs.

RESULTS

A total of 679 autochthonous human cases and 857 confirmed epizootics in NHPs for yellow fever have been recorded by the SES since the reemergence of the YF virus in 2000. During this period, five outbreaks were reported: in 2000, 2008, 2009, from 2016 to 2020, and in 2022 and 2023. The overall lethality rate was 35.7%, with a median age of 43.5 years. Men were predominantly affected, accounting for 73.7% of the cases (Table 1). The areas where viral circulation was detected expanded progressively over the more than 20-year period, increasing from two municipalities in 2000 to 140 in 2023, representing a 22% increase relative to the total number of municipalities in São Paulo.

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Table 1
Characteristics of confirmed cases of yellow fever in humans (n=679) and non-human primates (n=857). São Paulo, 2000–2023.

Surveillance of epizootics in NHPs that tested positive for YF has confirmed 857 events since 2003. Of these, 677 (79%) identified the genus of the affected primate, with a predominance of Alouatta sp (565, 83.4%) (Table 1). Initial confirmations of NHP deaths due to YF occurred in 2008 and 2009 in the regions of São José do Rio Preto and Botucatu, respectively, with subsequent occurrences in 2016, following the detection of a human case (fatality) also in the São José do Rio Preto region (Table 1 and Figures 1 and 2).

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Figure 1
A) Municipalities with confirmed human cases of yellow fever in the state of São Paulo, from 2000 to 2023; B) Municipalities with confirmed epizootics in non-human primates for yellow fever in the state of São Paulo, from 2008 to 2023.
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Figure 2
A) Heat map of confirmed human cases of yellow fever in the state of São Paulo, from 2000 to 2023; B) Heat map of confirmed epizootics in non-human primates for yellow fever in the state of São Paulo, from 2008 to 2023.

The successive transmissions of yellow fever from 2016 to 2019 accounted for approximately 94.8% of confirmed human cases. During this period, there was a marked increase in the surveillance of epizootics in NHPs, with 851 confirmed epizootic events between 2016 and 2020. This represents 99.3% of the total cases in the historical series analyzed (Table 1 and Figures 1 and 3).

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Figure 3
Historical series of confirmed human cases, lethality, and epizootics in non-human primates for yellow fever in the state of São Paulo, from 2000 to 2023.

The peak of yellow fever transmission occurred at the turn of 2017 to 2018, with over 350 confirmed events. The detection of epizootics in NHPs intensified in September 2017, reaching 127 recorded events by December. Human cases peaked in January and February 2018, with over 300 confirmed cases, with the municipality of Mairiporã identified as the likely site of infection for 181 of these cases (Figures 1, 2, and 3).

The virus continued its spread toward the southern region of the state, reaching the Ribeira Valley by the end of 2018, with the identification of 67 human cases and a few confirmed epizootic events in NHPs, with the lowest lethality rate of the entire transmission period (19.4%) at the beginning of 2019 (Figures 1, 2 and 3).

Since 2017, following the detection of human and NHP cases in 2016, a technical group was formed comprising professionals from SES, the Secretariat of the Environment (Secretaria de Meio Ambiente – SMA), now the Secretariat of Infrastructure and Environment (Secretaria de Infraestrutura e Meio Ambiente – SIMA), and the Department of Wildlife (Departamento de Fauna – DeFau), which coordinates ex situ and in situ Wildlife Management Centers. Additionally, the São Paulo Pro-Primate Commission, also linked to SMA, the Military Environmental Police, and the Technical Commission for Veterinary Public Health, composed of members from the Regional Council of Veterinary Medicine of São Paulo, participated in this group. In collaboration, these institutions developed several alerts, training sessions, and guidelines aimed at expanding the network of veterinarians, biologists, and zootechnicians, among other professionals. Their efforts focused on addressing events involving the death and/or illness of primates in SP, thereby improving the quality of information generated from NHP surveillance.

After the virus spread to the southern part of the state, two epizootic events in NHPs were detected in 2020, in the municipalities of Barueri and São José do Rio Preto. The most recent yellow fever circulation events during the period analyzed occurred in 2023, with confirmed epizootics in NHPs and human cases in the São João da Boa Vista region (Table 1 and Figures 1 and 3).

DISCUSSION

The data presented here must be analyzed from a different perspective, considering advances in scientific knowledge and the surveillance tools available during each transmission period. In 2000, molecular biology diagnostic tools were not as widely used, applied, or sensitive as they are today, which limited the methods for confirming and investigating suspected cases at that time11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... ,88 Moreno ES, Rocco IM, Bergo ES, Brasil RA, Siciliano MM, Suzuki A, et al. Reemergence of yellow fever: detection of transmission in the State of São Paulo, Brazil, 2008. Rev Soc Bras Med Trop 2011; 44(3): 290-6. https://doi.org/10.1590/S0037-86822011005000041
https://doi.org/10.1590/S0037-8682201100... . Additionally, epizootic surveillance in NHPs was not yet a standard practice in disease surveillance and was only implemented in 2003. It was not until detections outside the vaccination recommendation areas in 2017 that this method was recognized as a robust tool for detecting viral circulation11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... ,22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,1212 Possas C, Lourenço-de-Oliveira R, Tauil PL, Pinheiro FP, Pissinatti A, Cunha RV, et al. Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz 2018; 113(10): e180278. https://doi.org/10.1590/0074-02760180278
https://doi.org/10.1590/0074-02760180278...

13 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076...

14 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100...

15 Fernandes NCCA, Guerra JM, Díaz-Delgado J, Cunha MS, Saad LDS, Iglezias SD, et al. 2021. Differential yellow fever susceptibility in new world non human primates, comparison with humans, and implications for surveillance. Emerg Infect Dis 2021; 27(1): 47-56. https://doi.org/10.3201/eid2701.191220
https://doi.org/10.3201/eid2701.191220... -1616 Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
https://doi.org/10.1111/1365-2664.14031... .

Significant effort and coordination were undertaken by state surveillance to assist municipalities in the timely collection and reporting of events. This discussion occurred within the framework of the Brazilian Unified Health System (Sistema Único de Saúde – SUS), specifically in the meetings of regional bipartite inter-management councils. During these meetings, municipalities deliberated on mutual aid actions to support the collection of samples from NHPs.

Over more than two decades of analysis in this study, YF has demonstrated unpredictable behavior in its spatial reemergence11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... ,1212 Possas C, Lourenço-de-Oliveira R, Tauil PL, Pinheiro FP, Pissinatti A, Cunha RV, et al. Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz 2018; 113(10): e180278. https://doi.org/10.1590/0074-02760180278
https://doi.org/10.1590/0074-02760180278...

13 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076...

14 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... -1515 Fernandes NCCA, Guerra JM, Díaz-Delgado J, Cunha MS, Saad LDS, Iglezias SD, et al. 2021. Differential yellow fever susceptibility in new world non human primates, comparison with humans, and implications for surveillance. Emerg Infect Dis 2021; 27(1): 47-56. https://doi.org/10.3201/eid2701.191220
https://doi.org/10.3201/eid2701.191220... ,1717 Abreu FVS, Ribeiro IP, Ferreira-de-Brito A, Santos AAC, Miranda RM, Bonelly IS, et. al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018. Emerg Microbes Infect 2019; 8(1): 218-31. https://doi.org/10.1080/22221751.2019.1568180
https://doi.org/10.1080/22221751.2019.15... , influenced by the context and routes of national dispersion that the virus has followed33 Silva NIO, Sacchetto L, Rezende IM, Trindade GS, LaBeaud AD, Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J 2020; 17(1): 9. https://doi.org/10.1186/s12985-019-1277-7
https://doi.org/10.1186/s12985-019-1277-... ,1313 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... . Since 2017, a discernible trend of dispersion has been observed, particularly as the virus reached the Atlantic Forest and Serra do Mar regions in SP22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,1313 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... ,1414 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... .

The endemicity suggested during the intense transmission of YF in the state since 2016 does not appear to have materialized. The unpredictability of its occurrence, influenced by numerous known and unknown factors favoring transmission, indicates a contrary scenario1818 Kuno G. Mechanisms of yellow fever transmission: gleaning the overlooked records of importance and identifying problems, puzzles, serious issues, surprises and research questions. Viruses 2024; 16(1): 84. https://doi.org/10.3390/v16010084
https://doi.org/10.3390/v16010084... . There remain significant gaps in understanding the transmission mechanisms, processes leading to outbreaks, and the dispersion and persistence of the virus in nature1818 Kuno G. Mechanisms of yellow fever transmission: gleaning the overlooked records of importance and identifying problems, puzzles, serious issues, surprises and research questions. Viruses 2024; 16(1): 84. https://doi.org/10.3390/v16010084
https://doi.org/10.3390/v16010084... ,1919 Garcia-Oliveira GF, Guimarães ACDS, Moreira GD, Costa TA, Arruda MS, Mello EM, et. al. YELLOW ALERT: persistent yellow fever virus circulation among non-human primates in urban areas of Minas Gerais State, Brazil (2021-2023). Viruses 2023; 16(1): 31. https://doi.org/10.3390/v16010031
https://doi.org/10.3390/v16010031... .

Given the unpredictability of identifying locations where YF reemerges1313 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... ,1414 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... ,1616 Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
https://doi.org/10.1111/1365-2664.14031... ,1818 Kuno G. Mechanisms of yellow fever transmission: gleaning the overlooked records of importance and identifying problems, puzzles, serious issues, surprises and research questions. Viruses 2024; 16(1): 84. https://doi.org/10.3390/v16010084
https://doi.org/10.3390/v16010084... ,1919 Garcia-Oliveira GF, Guimarães ACDS, Moreira GD, Costa TA, Arruda MS, Mello EM, et. al. YELLOW ALERT: persistent yellow fever virus circulation among non-human primates in urban areas of Minas Gerais State, Brazil (2021-2023). Viruses 2023; 16(1): 31. https://doi.org/10.3390/v16010031
https://doi.org/10.3390/v16010031... and its significant epidemiological importance, disease surveillance must be conducted sensitively, particularly through epizootic surveillance in NHPs1010 Cunha MS, Costa AC, Fernandes NCCA, Guerra JM, Santos FCP, Nogueira JS, et al. Epizootics due to yellow fever virus in São Paulo state, Brazil: viral dissemination to new areas (2016–2017). Sci Rep 2019; 9(1): 5474. https://doi.org/10.1038/s41598-019-41950-3
https://doi.org/10.1038/s41598-019-41950... ,1414 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... ,1616 Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
https://doi.org/10.1111/1365-2664.14031... . Strategies have been implemented to enhance engagement and sensitivity in NHP surveillance, involving collaboration among various state agencies within and outside the health sector. This has led to the establishment of an expanded NHP surveillance network, which includes key contributions from SIMA, the Environmental Military Police, universities, professional councils, independent veterinarians, and non-governmental organizations, among others.

In the historical series analyzed, 79% (n=677) of the epizootics in NHPs confirmed for yellow fever had gender identification, with monkeys of the species Alouatta spp and Callithrix spp being the most frequently infected. Few occurrences were recorded in species of the genera Cebus spp and Callicebus spp. These results align with previous findings, confirming that Alouatta spp and Callithrix spp are more frequently affected by the disease and are more commonly recorded than other species present in the state of SP88 Moreno ES, Rocco IM, Bergo ES, Brasil RA, Siciliano MM, Suzuki A, et al. Reemergence of yellow fever: detection of transmission in the State of São Paulo, Brazil, 2008. Rev Soc Bras Med Trop 2011; 44(3): 290-6. https://doi.org/10.1590/S0037-86822011005000041
https://doi.org/10.1590/S0037-8682201100... ,1313 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... ,1515 Fernandes NCCA, Guerra JM, Díaz-Delgado J, Cunha MS, Saad LDS, Iglezias SD, et al. 2021. Differential yellow fever susceptibility in new world non human primates, comparison with humans, and implications for surveillance. Emerg Infect Dis 2021; 27(1): 47-56. https://doi.org/10.3201/eid2701.191220
https://doi.org/10.3201/eid2701.191220... ,1919 Garcia-Oliveira GF, Guimarães ACDS, Moreira GD, Costa TA, Arruda MS, Mello EM, et. al. YELLOW ALERT: persistent yellow fever virus circulation among non-human primates in urban areas of Minas Gerais State, Brazil (2021-2023). Viruses 2023; 16(1): 31. https://doi.org/10.3390/v16010031
https://doi.org/10.3390/v16010031... .

Other states affected by yellow fever have struggled to produce qualified information regarding the occurrence of the disease in NHPs. Similar studies indicated that only 10% of confirmed epizootics were identified by gender1212 Possas C, Lourenço-de-Oliveira R, Tauil PL, Pinheiro FP, Pissinatti A, Cunha RV, et al. Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz 2018; 113(10): e180278. https://doi.org/10.1590/0074-02760180278
https://doi.org/10.1590/0074-02760180278...

13 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... -1414 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... . During the outbreak from 2016 to 2018, Minas Gerais confirmed 1,006 human cases and 448 epizootics in NHPs1313 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... . The occurrence of more human cases following the detection of circulation in NHPs underscores the essential role of NHP surveillance in monitoring yellow fever by detecting viral circulation while it remains in its enzootic cycle33 Silva NIO, Sacchetto L, Rezende IM, Trindade GS, LaBeaud AD, Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J 2020; 17(1): 9. https://doi.org/10.1186/s12985-019-1277-7
https://doi.org/10.1186/s12985-019-1277-... ,44 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento de Articulação Estratégica de Vigilância em Saúde e Ambiente. Guia de vigilância em saúde [Internet]. Brasília: Ministério da Saúde; 2023 [cited on Jan 20, 2024]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/svsa/vigilancia/guia-de-vigilancia-em-saude-volume-2-6a-edicao/view
https://www.gov.br/saude/pt-br/centrais-... ,1212 Possas C, Lourenço-de-Oliveira R, Tauil PL, Pinheiro FP, Pissinatti A, Cunha RV, et al. Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz 2018; 113(10): e180278. https://doi.org/10.1590/0074-02760180278
https://doi.org/10.1590/0074-02760180278... . Therefore, the strategy adopted by the state of SP was successful, facilitating the vaccination of susceptible populations and recording a lower lethality rate than that reported by the Ministry of Health22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,44 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento de Articulação Estratégica de Vigilância em Saúde e Ambiente. Guia de vigilância em saúde [Internet]. Brasília: Ministério da Saúde; 2023 [cited on Jan 20, 2024]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/svsa/vigilancia/guia-de-vigilancia-em-saude-volume-2-6a-edicao/view
https://www.gov.br/saude/pt-br/centrais-... ,99 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
https://bvsms.saude.gov.br/bvs/publicaco... .

The collaborative, intersectoral, multidisciplinary, networked action, with a broader perspective within the One Health framework, facilitated better data qualification by providing georeferenced information from epizootic surveillance in NHPs. This data was instrumental in developing a new vaccination strategy based on the methodology of ecological corridors of viral dispersion, particularly in a context of national shortages of immunobiologicals due to YF circulation in several Brazilian states22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,99 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
https://bvsms.saude.gov.br/bvs/publicaco... ,1414 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... ,1616 Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
https://doi.org/10.1111/1365-2664.14031... . Such information led to significant scientific contributions, enhancing not only YF surveillance in NHPs but also the conservation of these animals1515 Fernandes NCCA, Guerra JM, Díaz-Delgado J, Cunha MS, Saad LDS, Iglezias SD, et al. 2021. Differential yellow fever susceptibility in new world non human primates, comparison with humans, and implications for surveillance. Emerg Infect Dis 2021; 27(1): 47-56. https://doi.org/10.3201/eid2701.191220
https://doi.org/10.3201/eid2701.191220... ,1616 Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
https://doi.org/10.1111/1365-2664.14031... , thereby supporting a shift away from an anthropocentric paradigm of surveillance.

When comparing information from animal surveillance with that from investigations into human cases, where surveillance practices have often been limited to merely confirming/discarding cases, frequently without assessing the probable site of infection, it becomes evident that data from animal surveillance can provide a more comprehensive understanding of the phenomenon. This is particularly relevant given the occurrence of the disease in wild conditions over the more than 20 years of re-emergence11 Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
https://doi.org/10.5123/s1679-4974201600... ,22 Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
https://doi.org/10.1038/s41598-021-95539... ,1313 Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
https://doi.org/10.1590/0074-02760190076... ,1414 Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
https://doi.org/10.1371/journal.ppat.100... ,1616 Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
https://doi.org/10.1111/1365-2664.14031... ,1717 Abreu FVS, Ribeiro IP, Ferreira-de-Brito A, Santos AAC, Miranda RM, Bonelly IS, et. al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018. Emerg Microbes Infect 2019; 8(1): 218-31. https://doi.org/10.1080/22221751.2019.1568180
https://doi.org/10.1080/22221751.2019.15... .

It is understandable that municipalities struggle to improve the quality of information, given the successive cuts and dismantling that SUS has faced over the years2020 Pitombeira DF, Oliveita LC. Pobreza e desigualdades sociais: tensões entre direitos, austeridade e suas implicações na atenção primária. Ciênc Saúde Coletiva 2020; 25(5): 1699-708. https://doi.org/10.1590/1413-81232020255.33972019
https://doi.org/10.1590/1413-81232020255... . Moreover, this reflects a fragile understanding of the role of epidemiological surveillance and the health-disease model that has been applied, executed, and discussed2020 Pitombeira DF, Oliveita LC. Pobreza e desigualdades sociais: tensões entre direitos, austeridade e suas implicações na atenção primária. Ciênc Saúde Coletiva 2020; 25(5): 1699-708. https://doi.org/10.1590/1413-81232020255.33972019
https://doi.org/10.1590/1413-81232020255... ,2121 Barata RB. Epidemiologia social. Rev Bras Epidemiol 2005; 8(1): 7-17. https://doi.org/10.1590/S1415-790X2005000100002
https://doi.org/10.1590/S1415-790X200500... . It is important to systematically improve the quality of information to comprehend phenomena and, thus, expand the discussion of anthropocentric epidemiological surveillance2121 Barata RB. Epidemiologia social. Rev Bras Epidemiol 2005; 8(1): 7-17. https://doi.org/10.1590/S1415-790X2005000100002
https://doi.org/10.1590/S1415-790X200500... ,2222 Felisberto E, Sousa AIA, Souza NC, Guerra S, Samico I, Dubeux LS, et al. Avaliação das ações de vigilância sanitária: construção participativa de mecanismos para o monitoramento do desempenho da gestão. Vigil Sanit Debate 2022; 10(1): 2-13. https://doi.org/10.22239/2317-269x.01903
https://doi.org/10.22239/2317-269x.01903... to a One Health approach2121 Barata RB. Epidemiologia social. Rev Bras Epidemiol 2005; 8(1): 7-17. https://doi.org/10.1590/S1415-790X2005000100002
https://doi.org/10.1590/S1415-790X200500...

22 Felisberto E, Sousa AIA, Souza NC, Guerra S, Samico I, Dubeux LS, et al. Avaliação das ações de vigilância sanitária: construção participativa de mecanismos para o monitoramento do desempenho da gestão. Vigil Sanit Debate 2022; 10(1): 2-13. https://doi.org/10.22239/2317-269x.01903
https://doi.org/10.22239/2317-269x.01903... -2323 Di Giulio GM, Waldman EA, Nunes J, Buss PM, Jaime PC, Campelo T, et al. Global health and planetary health: perspectives for a transition to a more sustainable world post COVID-19. Cien Saude Colet 2021; 26(10): 4373-82. https://doi.org/10.1590/1413-812320212610.14332021
https://doi.org/10.1590/1413-81232021261... .

Surveillance of epizootics in NHPs (and other animal diseases) is primarily conducted by veterinarians and biologists working within SUS. These professionals, who are already limited in municipal staffing, have become even scarcer following the federal funding cuts in 2019 that affected the operation of the Family Health Support Centers (Núcleos de Apoio à Saúde da Família – NASFs)1717 Abreu FVS, Ribeiro IP, Ferreira-de-Brito A, Santos AAC, Miranda RM, Bonelly IS, et. al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018. Emerg Microbes Infect 2019; 8(1): 218-31. https://doi.org/10.1080/22221751.2019.1568180
https://doi.org/10.1080/22221751.2019.15... ,2424 Giatti LL, Ribeiro RA, Nava AFD, Gutberlet J. Emerging complexities and rising omission: Contrasts among socio-ecological contexts of infectious diseases, research and policy in Brazil. Genet Mol Biol 2021; 44(1 Suppl1): e20200229. https://doi.org/10.1590/1678-4685-GMB-2020-0229
https://doi.org/10.1590/1678-4685-GMB-20... , which included provisions for veterinarians’ participation in primary care. These professionals understand the concept of One Health, as it is intrinsic to their activities. This understanding reflects a movement toward implementation, capillarization, and discussion in the daily routine of expanded actions, supported by the principles of comprehensiveness and multidisciplinarity within the health system2222 Felisberto E, Sousa AIA, Souza NC, Guerra S, Samico I, Dubeux LS, et al. Avaliação das ações de vigilância sanitária: construção participativa de mecanismos para o monitoramento do desempenho da gestão. Vigil Sanit Debate 2022; 10(1): 2-13. https://doi.org/10.22239/2317-269x.01903
https://doi.org/10.22239/2317-269x.01903...

23 Di Giulio GM, Waldman EA, Nunes J, Buss PM, Jaime PC, Campelo T, et al. Global health and planetary health: perspectives for a transition to a more sustainable world post COVID-19. Cien Saude Colet 2021; 26(10): 4373-82. https://doi.org/10.1590/1413-812320212610.14332021
https://doi.org/10.1590/1413-81232021261...

24 Giatti LL, Ribeiro RA, Nava AFD, Gutberlet J. Emerging complexities and rising omission: Contrasts among socio-ecological contexts of infectious diseases, research and policy in Brazil. Genet Mol Biol 2021; 44(1 Suppl1): e20200229. https://doi.org/10.1590/1678-4685-GMB-2020-0229
https://doi.org/10.1590/1678-4685-GMB-20...

25 Mattos MP, Gutierrez AC, Campos GWS. Construção do referencial histórico-normativo do Núcleo Ampliado de Saúde da Família. Ciênc Saúde Coletiva 2022; 27(09): 3503-16. https://doi.org/10.1590/1413-81232022279.01472022
https://doi.org/10.1590/1413-81232022279... -2626 Steele SG, Toribio JALML, Mor SM. Global health security must embrace a One Health approach: contributions and experiences of veterinarians during the COVID-19 response in Australia. One Health 2021; 13: 100314. https://doi.org/10.1016/j.onehlt.2021.100314
https://doi.org/10.1016/j.onehlt.2021.10... .

The incorporation of a perspective centered on the social determination of diseases2020 Pitombeira DF, Oliveita LC. Pobreza e desigualdades sociais: tensões entre direitos, austeridade e suas implicações na atenção primária. Ciênc Saúde Coletiva 2020; 25(5): 1699-708. https://doi.org/10.1590/1413-81232020255.33972019
https://doi.org/10.1590/1413-81232020255... places us in a paradigm of reflection-action in health that extends beyond human health (alone). It is essential and urgent to engage in discussions that encompass mechanisms within surveillance, facilitating not only the systematic and qualified collection of data but also the creation of dialogic and reflective spaces on the subject.

Although the concept of One Health is not new and has been central to interdisciplinary and multisectoral discussions for years, there is currently a growing interest in applying this approach and translating it into action. This trend reinforces its general objectives and, in particular, emphasizes ecohealth (highlighting the ecocentric versus anthropocentric scope) and planetary health, explicitly recognizing the importance of environmental and ecosystem health.

The limitations identified in this study are inherent to research utilizing secondary databases, specifically those derived from passive notification processes. These limitations can result in inaccuracies in applying case definitions, as well as in the suspicion and confirmation of suspected cases. Additionally, they can affect the notification, epidemiological investigation, and registration of cases within the system.

This study highlights the potential for systematically incorporating the One Health approach into epidemiological surveillance methods, thereby advancing a paradigm that expands the scope of anthropocentric surveillance.

During the period analyzed in this research, five outbreaks of yellow fever were recorded in the state of São Paulo, resulting in the confirmation of 679 autochthonous human cases and 857 epizootics in NHPs. The most severe transmission occurred since 2016, when the virus reached areas and populations that had (previously) not been included in vaccine recommendations, necessitating the expansion of animal surveillance strategies to inform decision-making. This successful strategy, proposed by the Ministry of Health since 2003, underscores the effectiveness of the One Health approach in actions undertaken at all three levels of SUS management, enhancing the system's resilience and sensitivity to the emergence/reemergence of zoonotic diseases.

  • FUNDING:

    none.

  • APPROVAL BY THE RESEARCH ETHICS COMMITTEE:

    The study project was approved by the Research Ethics Committee of the School of Public Health at Universidade de São Paulo (CEP/FSP/USP), under Opinion No. 5.536.721.

REFERENCES

  • 1
    Saad LDC, Barata RB. Surtos de febre amarela no estado de São Paulo, 2000-2010. Epidemiol Serv Saúde 2016; 25(3): 531-40. https://doi.org/10.5123/s1679-49742016000300009
    » https://doi.org/10.5123/s1679-49742016000300009
  • 2
    Lacerda AB, Saad LDC, Ikefuti PV, Pinter A, Chiavaralloti-Neto F. Diffusion of sylvatic yellow fever in the state of São Paulo, Brazil. Sci Rep 2021; 11(1): 16277 https://doi.org/10.1038/s41598-021-95539-w
    » https://doi.org/10.1038/s41598-021-95539-w
  • 3
    Silva NIO, Sacchetto L, Rezende IM, Trindade GS, LaBeaud AD, Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J 2020; 17(1): 9. https://doi.org/10.1186/s12985-019-1277-7
    » https://doi.org/10.1186/s12985-019-1277-7
  • 4
    Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento de Articulação Estratégica de Vigilância em Saúde e Ambiente. Guia de vigilância em saúde [Internet]. Brasília: Ministério da Saúde; 2023 [cited on Jan 20, 2024]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/svsa/vigilancia/guia-de-vigilancia-em-saude-volume-2-6a-edicao/view
    » https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/svsa/vigilancia/guia-de-vigilancia-em-saude-volume-2-6a-edicao/view
  • 5
    Cunha MS, Tubaki RM, Menezes RMT, Pereira M, Caleiro GS, Coelho E, et al. Possible non-sylvatic transmission of yellow fever between non-human primates in São Paulo city, Brazil, 2017–2018. Sci Rep 2020; 10(1): 15751. https://doi.org/10.1038/s41598-020-72794-x
    » https://doi.org/10.1038/s41598-020-72794-x
  • 6
    Gebreyes WA, Dupouy-Camet J, Newport MJ, Oliveira CJ, Schlesinger LS, Saif YM, et al. The global one health paradigm: challenges and opportunities for tackling infectious diseases at the human, animal, and environment interface in low-resource settings. PLoS Negl Trop Dis 2014; 8(11): e3257. https://doi.org/10.1371/journal.pntd.0003257
    » https://doi.org/10.1371/journal.pntd.0003257
  • 7
    Kelly TR, Karesh WB, Johnson CK, Gilardi KVK, Anthony SJ, Goldstein T, et al. One health proof of concept: bringing a transdisciplinary approach to surveillance for zoonotic viruses at the human-wild animal interface. Prev Vet Med 2017; 137(Pt B): 112-8. https://doi.org/10.1016/j.prevetmed.2016.11.023
    » https://doi.org/10.1016/j.prevetmed.2016.11.023
  • 8
    Moreno ES, Rocco IM, Bergo ES, Brasil RA, Siciliano MM, Suzuki A, et al. Reemergence of yellow fever: detection of transmission in the State of São Paulo, Brazil, 2008. Rev Soc Bras Med Trop 2011; 44(3): 290-6. https://doi.org/10.1590/S0037-86822011005000041
    » https://doi.org/10.1590/S0037-86822011005000041
  • 9
    Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Análise em Sáude e Vigilância de Doenças não Transmissíveis. Saúde Brasil 2019: uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização [Internet]. Brasília: Ministério da Saúde; 2019 [cited on Nov 22, 2023]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
    » https://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2019_analise_situacao.pdf
  • 10
    Cunha MS, Costa AC, Fernandes NCCA, Guerra JM, Santos FCP, Nogueira JS, et al. Epizootics due to yellow fever virus in São Paulo state, Brazil: viral dissemination to new areas (2016–2017). Sci Rep 2019; 9(1): 5474. https://doi.org/10.1038/s41598-019-41950-3
    » https://doi.org/10.1038/s41598-019-41950-3
  • 11
    Brasil. Instituto Brasileiro de Geografia e Estatística. Atlas do Censo Demográfico 2010 [Internet]. 2010 [cited on Nov 08, 2023]. Available at: https://censo2010.ibge.gov.br/apps/atlas/
    » https://censo2010.ibge.gov.br/apps/atlas/
  • 12
    Possas C, Lourenço-de-Oliveira R, Tauil PL, Pinheiro FP, Pissinatti A, Cunha RV, et al. Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz 2018; 113(10): e180278. https://doi.org/10.1590/0074-02760180278
    » https://doi.org/10.1590/0074-02760180278
  • 13
    Abreu FVS, Delatorre E, Santos AAC, Ferreira-de-Brito A, Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that Yellow Fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz 2019; 114: e190076. https://doi.org/10.1590/0074-02760190076
    » https://doi.org/10.1590/0074-02760190076
  • 14
    Hill SC, Souza R, Thézé J, Claro I, Aguiar RS, Abade L, et al. Genomic surveillance of yellow fever virus epizootic in São Paulo, Brazil, 2016 – 2018. PLoS Pathog 2020; 16(8): e1008699. https://doi.org/10.1371/journal.ppat.1008699
    » https://doi.org/10.1371/journal.ppat.1008699
  • 15
    Fernandes NCCA, Guerra JM, Díaz-Delgado J, Cunha MS, Saad LDS, Iglezias SD, et al. 2021. Differential yellow fever susceptibility in new world non human primates, comparison with humans, and implications for surveillance. Emerg Infect Dis 2021; 27(1): 47-56. https://doi.org/10.3201/eid2701.191220
    » https://doi.org/10.3201/eid2701.191220
  • 16
    Ribeiro Prist P, Reverberi Tambosi L, Filipe Mucci L, Pinter A, Pereira de Souza, R, Lara Muylaert R, et al. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 2021; 59(1): 4-17. https://doi.org/10.1111/1365-2664.14031
    » https://doi.org/10.1111/1365-2664.14031
  • 17
    Abreu FVS, Ribeiro IP, Ferreira-de-Brito A, Santos AAC, Miranda RM, Bonelly IS, et. al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018. Emerg Microbes Infect 2019; 8(1): 218-31. https://doi.org/10.1080/22221751.2019.1568180
    » https://doi.org/10.1080/22221751.2019.1568180
  • 18
    Kuno G. Mechanisms of yellow fever transmission: gleaning the overlooked records of importance and identifying problems, puzzles, serious issues, surprises and research questions. Viruses 2024; 16(1): 84. https://doi.org/10.3390/v16010084
    » https://doi.org/10.3390/v16010084
  • 19
    Garcia-Oliveira GF, Guimarães ACDS, Moreira GD, Costa TA, Arruda MS, Mello EM, et. al. YELLOW ALERT: persistent yellow fever virus circulation among non-human primates in urban areas of Minas Gerais State, Brazil (2021-2023). Viruses 2023; 16(1): 31. https://doi.org/10.3390/v16010031
    » https://doi.org/10.3390/v16010031
  • 20
    Pitombeira DF, Oliveita LC. Pobreza e desigualdades sociais: tensões entre direitos, austeridade e suas implicações na atenção primária. Ciênc Saúde Coletiva 2020; 25(5): 1699-708. https://doi.org/10.1590/1413-81232020255.33972019
    » https://doi.org/10.1590/1413-81232020255.33972019
  • 21
    Barata RB. Epidemiologia social. Rev Bras Epidemiol 2005; 8(1): 7-17. https://doi.org/10.1590/S1415-790X2005000100002
    » https://doi.org/10.1590/S1415-790X2005000100002
  • 22
    Felisberto E, Sousa AIA, Souza NC, Guerra S, Samico I, Dubeux LS, et al. Avaliação das ações de vigilância sanitária: construção participativa de mecanismos para o monitoramento do desempenho da gestão. Vigil Sanit Debate 2022; 10(1): 2-13. https://doi.org/10.22239/2317-269x.01903
    » https://doi.org/10.22239/2317-269x.01903
  • 23
    Di Giulio GM, Waldman EA, Nunes J, Buss PM, Jaime PC, Campelo T, et al. Global health and planetary health: perspectives for a transition to a more sustainable world post COVID-19. Cien Saude Colet 2021; 26(10): 4373-82. https://doi.org/10.1590/1413-812320212610.14332021
    » https://doi.org/10.1590/1413-812320212610.14332021
  • 24
    Giatti LL, Ribeiro RA, Nava AFD, Gutberlet J. Emerging complexities and rising omission: Contrasts among socio-ecological contexts of infectious diseases, research and policy in Brazil. Genet Mol Biol 2021; 44(1 Suppl1): e20200229. https://doi.org/10.1590/1678-4685-GMB-2020-0229
    » https://doi.org/10.1590/1678-4685-GMB-2020-0229
  • 25
    Mattos MP, Gutierrez AC, Campos GWS. Construção do referencial histórico-normativo do Núcleo Ampliado de Saúde da Família. Ciênc Saúde Coletiva 2022; 27(09): 3503-16. https://doi.org/10.1590/1413-81232022279.01472022
    » https://doi.org/10.1590/1413-81232022279.01472022
  • 26
    Steele SG, Toribio JALML, Mor SM. Global health security must embrace a One Health approach: contributions and experiences of veterinarians during the COVID-19 response in Australia. One Health 2021; 13: 100314. https://doi.org/10.1016/j.onehlt.2021.100314
    » https://doi.org/10.1016/j.onehlt.2021.100314

Publication Dates

  • Publication in this collection
    16 Dec 2024
  • Date of issue
    2024

History

  • Received
    30 Apr 2024
  • Reviewed
    01 Sept 2024
  • Accepted
    02 Sept 2024
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This is an open article distributed under the CC-BY 4.0 license, which allows copying and redistribution of the material in any format and for any purpose as long as the original authorship and publication credits are maintained.
Associação Brasileira de Pós -Graduação em Saúde Coletiva São Paulo - SP - Brazil
E-mail: revbrepi@usp.br
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