I have a B.S. in Biology, M.Sc. in Immunology and Infectious diseases, Ph.D. in Microbiology, and a broad background in virology/microbiology and molecular biology applied to viral infectious diseases. I have a vast knowledge of classical virology, molecular biology, phylogenetic analysis, serological, and molecular diagnosis. I am working on recent YF outbreaks, focusing on viral dynamics, ecology, diagnosis, and the investigation of virological, immunological, and clinical aspects during the course of infection. We have supported the hospital and Secretary of Health of Minas Gerais with some laboratory testing applied to diagnosis of YF, viral genotyping related to YF patients suspected to have adverse events following vaccination, and other analysis. We also have been working on dynamics of the outbreak, on the virological, epidemiological, and immunological aspects during the course of yellow fever. During the COVID-19 pandemic, we also supported the Brazilian Ministry of Health with the SARS-CoV-2 diagnosis in human samples and also in the investigation of the SARS-CoV-2 RNA in surfaces of density public areas of Belo Horizonte. Since Nov/2018 I had been an editor in the journal Docência do Ensino Superior (RDES / GIZ / UFMG) and in Jan/2020 I became Editor-in-Chief.
Honors & Awards
Highlighted poster, 7th Pan-American Dengue Research Network Meeting (2020)
Oral presentation, IV FAMERP-UTMB: Emerging infections in the Americas (2019)
Travel Grant: 16th International Course on Dengue, Zika, and other Emergent Arboviruses., Institute of Tropical Medicine Pedro Kourí. La Havana, Cuba. Scholarship: OPAS (2019)
Travel grant for oral abstract presentation, 6th Pan-American Dengue Research Network Meeting (2018)
Travel Grant for arboviruses course participation, São Paulo School of Advanced Science (2017)
Travel grant: Molecular Epidemiology in Infectious Diseases of Global Significance, ICOPHAI and Centre for Genetic Engineering and Biotechnology (ICGEB) (2013)
Boards, Advisory Committees, Professional Organizations
Editor-in-Chief, Revista Docência do Ensino Superior (UFMG - Brazil) https://periodicos.ufmg.br/index.php/rdes (2020 - Present)
Member, American Society of Tropical Medicine and Hygiene (2020 - Present)
Member, Brazilian Society of Virology (2012 - Present)
Jason Andrews, Postdoctoral Faculty Sponsor
Late-Relapsing Hepatitis after Yellow Fever
2020; 12 (2)
One patient presented hyporexia, asthenia, adynamia, and jaundice two months after acute yellow fever (YF) onset; plus laboratory tests indicating hepatic cytolysis and a rebound of alanine and aspartate transaminases, and total and direct bilirubin levels. Laboratory tests discarded autoimmune hepatitis, inflammatory or metabolic liver disease, and new infections caused by hepatotropic agents. Anti-YFV IgM, IgG and neutralizing antibodies were detected in different times, but no viremia. A liver biopsy was collected three months after YF onset and tested positive for YFV antigens and wild-type YFV-RNA (364 RNA-copies/gram/liver). Transaminases and bilirubin levels remained elevated for five months, and the arresting of symptoms persisted for six months after the acute YF onset. Several serum chemokines, cytokines, and growth factors were measured. A similar immune response profile was observed in the earlier phases of the disease, followed by more pronounced changes in the later stages, when transaminases levels returned to normal. The results indicated viral persistence in the liver and continual liver cell damage three months after YF onset and reinforced the need for extended follow-ups of YF patients. Further studies to investigate the role of possible viral persistence and the immune response causing relapsing hepatitis following YF are also necessary.
View details for DOI 10.3390/v12020222
View details for Web of Science ID 000521256600063
View details for PubMedID 32079143
View details for PubMedCentralID PMC7077229
Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease.
2020; 17 (1): 9
Yellow fever (YF) is an acute viral disease, affecting humans and non-human primates (NHP), caused by the yellow fever virus (YFV). Despite the existence of a safe vaccine, YF continues to cause morbidity and mortality in thousands of people in Africa and South America. Since 2016, massive YF outbreaks have taken place in Brazil, reaching YF-free zones, causing thousands of deaths of humans and NHP. Here we reviewed the main epidemiological aspects, new clinical findings in humans, and issues regarding YFV infection in vectors and NHP in Brazil. The 2016-2019 YF epidemics have been considered the most significant outbreaks of the last 70 years in the country, and the number of human cases was 2.8 times higher than total cases in the previous 36 years. A new YFV lineage was associated with the recent outbreaks, with persistent circulation in Southeast Brazil until 2019. Due to the high number of infected patients, it was possible to evaluate severity and death predictors and new clinical features of YF. Haemagogus janthinomys and Haemagogus leucocelaenus were considered the primary vectors during the outbreaks, and no human case suggested the occurrence of the urban transmission cycle. YFV was detected in a variety of NHP specimens presenting viscerotropic disease, similar to that described experimentally. Further studies regarding NHP sensitivity to YFV, YF pathogenesis, and the duration of the immune response in NHP could contribute to YF surveillance, control, and future strategies for NHP conservation.
View details for DOI 10.1186/s12985-019-1277-7
View details for PubMedID 31973727
Genomic and epidemiological monitoring of yellow fever virus transmission potential
2018; 361 (6405): 894-+
The yellow fever virus (YFV) epidemic in Brazil is the largest in decades. The recent discovery of YFV in Brazilian Aedes species mosquitos highlights a need to monitor the risk of reestablishment of urban YFV transmission in the Americas. We use a suite of epidemiological, spatial, and genomic approaches to characterize YFV transmission. We show that the age and sex distribution of human cases is characteristic of sylvatic transmission. Analysis of YFV cases combined with genomes generated locally reveals an early phase of sylvatic YFV transmission and spatial expansion toward previously YFV-free areas, followed by a rise in viral spillover to humans in late 2016. Our results establish a framework for monitoring YFV transmission in real time that will contribute to a global strategy to eliminate future YFV epidemics.
View details for DOI 10.1126/science.aat7115
View details for Web of Science ID 000443547000033
View details for PubMedID 30139911
View details for PubMedCentralID PMC6874500
Persistence of Yellow fever virus outside the Amazon Basin, causing epidemics in Southeast Brazil, from 2016 to 2018
PLOS NEGLECTED TROPICAL DISEASES
2018; 12 (6): e0006538
Yellow fever (YF) is endemic in the Brazilian Amazon Basin, and sporadic outbreaks take place outside the endemic area in Brazil. Since 2016, YF epidemics have been occurring in Southeast Brazil, with more than 1,900 human cases and more than 1,600 epizooties of non-human primates (NHPs) reported until April 2018. Previous studies have demonstrated that Yellow fever virus (YFV) causing outbreaks in 2017 formed a monophyletic group.Aiming to decipher the origin of the YFV responsible for the recent epidemics, we obtained nucleotide sequences of YFV detected in humans (n = 6) and NHPs (n = 10) from Minas Gerais state during 2017-2018. Next, we performed evolutionary analyses and discussed the results in the light of epidemiological records (official numbers of YFV cases at each Brazilian Federative unit, reported by the Brazilian Ministry of Health). Nucleotide sequences of YFV from Southeast Brazil from 2016 to 2018 were highly conserved and formed a monophyletic lineage (BR-YFV_2016/18) within the genotype South America I. Different clusters were observed within lineage BR-YFV_2016/18, one containing the majority of isolates (from humans and NHPs), indicating the sylvatic transmission of YFV. We also detected a cluster characterized by two synapomorphies (amino acid substitutions) that contained YFV only associated with NHP what should be further investigated. The topology of lineage BR-YFV_2016/18 was congruent with epidemiological and temporal patterns of the ongoing epidemic. YFV isolates detected in 2016, in São Paulo state were located in the most basal position of the lineage, followed by the isolates from Minas Gerais and Espírito Santo obtained in 2017 and 2018. The most recent common ancestor of the lineage BR-YFV_2016/18 dated to 2015 (95% credible intervals = 2014-2016), in a period that was coincident with the reemergence of YFV in the Midwest region of Brazil.The results demonstrated a single introduction of YFV in the Southeast region and the silent viral circulation before the onset of the outbreaks in 2016. Evolutionary analyses combined with epidemiological records supported the idea that BR-YFV_2016/18 was probably introduced from the Midwest into the Southeast region, possibly in São Paulo state. The persistence of YFV in the Southeast region, causing epidemics from 2016 to 2018, suggests that this region presents suitable ecological and climatic conditions for YFV maintenance during the epidemic and interepidemic seasons. This fact poses risks for the establishing of YF enzootic cycles and epidemics, outside the Amazon Basin in Brazil. YF surveillance and studies of viral dynamics deserve particular attention, especially in Midwest, Southeast and neighbor regions which are the main areas historically associated with YF outbreaks outside the Amazon Basin. YFV persistence in Southeast Brazil should be carefully considered in the context of public health, especially for public health decision-makers and researchers.
View details for DOI 10.1371/journal.pntd.0006538
View details for Web of Science ID 000437442000027
View details for PubMedID 29864115
View details for PubMedCentralID PMC6002110
Yellow Fever Molecular Diagnosis Using Urine Specimens during Acute and Convalescent Phases of the Disease.
Journal of clinical microbiology
Prior studies have demonstrated prolonged presence of yellow fever virus (YFV) RNA in saliva and urine as an alternative to serum. To investigate the presence of YFV RNA in urine, we used RT-PCR for YFV screening in 60 urine samples collected from a large cohort of naturally infected yellow fever (YF) patients during acute and convalescent phases of YF infection from recent YF outbreaks in Brazil (2017 to 2018). Fifteen urine samples from acute phase infection (up to 15days post-symptom onset) and four urine samples from convalescent phase infection (up to 69days post-symptom onset), were YFV PCR-positive. We genotyped YFV detected in seven urine samples (five collected during the acute phase and two collected during the YF convalescent phase). Genotyping indicated the presence of YFV South American I genotype in these samples. To our knowledge, this is the first report of wild-type YFV RNA detection in the urine this far out from symptom onset (up to 69 DPS), including YFV RNA detection during the convalescent phase of YF infection. The detection of YFV RNA in urine is an indicative of YFV infection; however, the results of RT-PCR using urine as sample should be interpreted with care, since a negative result does not exclude the possibility of YFV infection. With a possible prolonged period of detection beyond the viremic phase, the use of urine samples coupled with serological tests, epidemiologic inquiry, and clinical assessment could provide a longer diagnostic window for laboratory YF diagnosis.
View details for DOI 10.1128/jcm.00254-22
View details for PubMedID 35916519
Urban risk factors for human Rift Valley fever virus exposure in Kenya.
PLOS global public health
2022; 2 (7): e0000505
The Rift Valley fever virus (RVFV) is a zoonotic arbovirus that can also transmit directly to humans from livestock. Previous studies have shown consumption of sick animal products are risk factors for RVFV infection, but it is difficult to disentangle those risk factors from other livestock rearing activities. Urban areas have an increased demand for animal source foods, different vector distributions, and various arboviruses are understood to establish localized urban transmission cycles. Thus far, RVFV is an unevaluated public health risk in urban areas within endemic regions. We tested participants in our ongoing urban cohort study on dengue (DENV) and chikungunya (CHIKV) virus for RVFV exposure and found 1.6% (57/3,560) of individuals in two urban areas of Kenya had anti-RVFV IgG antibodies. 88% (50/57) of RVFV exposed participants also had antibodies to DENV, CHIKV, or both. Although livestock ownership was very low in urban study sites, RVFV exposure was overall significantly associated with seeing goats around the homestead (OR = 2.34 (CI 95%: 1.18-4.69, p = 0.02) and in Kisumu, RVFV exposure was associated with consumption of raw milk (OR = 6.28 (CI 95%: 0.94-25.21, p = 0.02). In addition, lack of piped water and use of small jugs (15-20 liters) for water was associated with a higher risk of RVFV exposure (OR = 5.36 (CI 95%: 1.23-16.44, p = 0.01) and this may contribute to interepidemic vector-borne maintenance of RVFV. We also investigated perception towards human vaccination for RVFV and identified high acceptance (91% (97/105) at our study sites. This study provides baseline evidence to guide future studies investigating the urban potential of RVFV and highlights the unexplored role of animal products in continued spread of RVFV.
View details for DOI 10.1371/journal.pgph.0000505
View details for PubMedID 36962424
View details for PubMedCentralID PMC10021321
Characterizing the Severity of SARS-CoV-2 Variants at a Single Pediatric Center
FRONTIERS IN MEDICINE
2022; 9: 896352
Since March 2020, SARS-CoV-2 has plagued the world with COVID-19 and individuals of all ages have experienced varying symptoms of disease. Older adults were experiencing more severe disease compared to children and were prioritized by vaccination efforts. While biologic therapies and vaccinations were implemented, there were changes in public health restrictions with subsequent surges resulting in more infected children. During these surges there was a rise of different SARS-CoV-2 variants with the dominant variant initially alpha (B.1.1.7 and other Pango lineages) and epsilon (B.1.427/B.1.429) in early 2021 and a dramatic shift to delta (B.1.617.2 and other Pango lineages) by mid-summer 2021. In this study we aimed to characterize the clinical severity and host factors associated with disease by SARS-CoV-2 variant and evaluate if there are differences in disease severity by circulating variant. We retrospectively included all individuals 0-25 years of age who presented to our center and had a positive SARS-CoV-2 RT-PCR, SARS-CoV-2 variant mutation testing, and documented clinical notes from 1 January 2021 through 31 December 2021. We identified 745 individuals who met inclusion criteria and found the delta variant was associated with severe/critical disease compared to the other variants studied. The results of the model showed that underlying respiratory disease and diabetes were risk factors for progression to severe disease. These insights are important when evaluating public health measures and treatment options for children as more variants arise.
View details for DOI 10.3389/fmed.2022.896352
View details for Web of Science ID 000807127000001
View details for PubMedID 35677819
View details for PubMedCentralID PMC9168367
URINE AS A POSSIBLE RESOURCE FOR YELLOW FEVER DIAGNOSIS
AMER SOC TROP MED & HYGIENE. 2021: 187
View details for Web of Science ID 000778105602276
RISK-STRATIFYING YELLOW FEVER PATIENTS AT THE TIME OF ADMISSION
AMER SOC TROP MED & HYGIENE. 2021: 436
View details for Web of Science ID 000778105603453
DESCRIBING PREDICTOR RISK FACTORS FOR LATE-RELAPSING HEPATITIS AFTER YELLOW FEVER
AMER SOC TROP MED & HYGIENE. 2021: 270-271
View details for Web of Science ID 000778105602535
Neighbor danger: Yellow fever virus epizootics in urban and urban-rural transition areas of Minas Gerais state, during 2017-2018 yellow fever outbreaks in Brazil.
PLoS neglected tropical diseases
2020; 14 (10): e0008658
From the end of 2016 until the beginning of 2019, Brazil faced a massive sylvatic yellow fever (YF) outbreak. The 2016-2019 YF epidemics affected densely populated areas, especially the Southeast region, causing thousands of deaths of humans and non-human primates (NHP).We conducted a molecular investigation of yellow fever virus (YFV) RNA in 781 NHP carcasses collected in the urban, urban-rural interface, and rural areas of Minas Gerais state, from January 2017 to December 2018. Samples were analyzed according to the period of sampling, NHP genera, sampling areas, and sampling areas/NHP genera to compare the proportions of YFV-positive carcasses and the estimated YFV genomic loads. YFV infection was confirmed in 38.1% of NHP carcasses (including specimens of the genera Alouatta, Callicebus, Callithrix, and Sapajus), from the urban, urban-rural interface, and rural areas. YFV RNA detection was positively associated with epidemic periods (especially from December to March) and the rural environment. Higher median viral genomic loads (one million times) were estimated in carcasses collected in rural areas compared to urban ones.The results showed the wide occurrence of YF in Minas Gerais in epidemic and non-epidemic periods. According to the sylvatic pattern of YF, a gradient of viral dissemination from rural towards urban areas was observed. A high YF positivity was observed for NHP carcasses collected in urban areas with a widespread occurrence in 67 municipalities of Minas Gerais, including large urban centers. Although there was no documented case of urban/Aedes YFV transmission to humans in Brazil during the 2016-2019 outbreaks, YFV-infected NHP in urban areas with high infestation by Aedes aegypti poses risks for YFV urban/Aedes transmission and urbanization.
View details for DOI 10.1371/journal.pntd.0008658
View details for PubMedID 33017419
Yellow Fever Virus Genotyping Tool and Investigation of Suspected Adverse Events Following Yellow Fever Vaccination
2019; 7 (4)
The yellow fever (YF) vaccine consists of an attenuated virus, and despite its relative safety, some adverse events following YF vaccination have been described. At the end of 2016, Brazil experienced the most massive sylvatic yellow fever outbreak over the last 70 years and an intense campaign of YF vaccination occurred in Minas Gerais state in Southeast Brazil from 2016 to 2018. The present study aimed to develop a genotyping tool and investigate 21 cases of suspected adverse events following YF vaccination. Initial in silico analyses were performed using partial NS5 nucleotide sequences to verify the discriminatory potential between wild-type and vaccine viruses. Samples from patients were screened for the presence of the YFV RNA, using 5'UTR as the target, and then used for amplification of partial NS5 gene amplification, sequencing, and phylogenetic analysis. Genotyping indicated that 17 suspected cases were infected by the wild-type yellow fever virus, but four cases remained inconclusive. The genotyping tool was efficient in distinguishing the vaccine from wild-type virus, and it has the potential to be used for the differentiation of all yellow fever virus genotypes.
View details for DOI 10.3390/vaccines7040206
View details for Web of Science ID 000505709700001
View details for PubMedID 31817103
View details for PubMedCentralID PMC6963942
Circulation of Chikungunya virus East-Central-South Africa genotype during an outbreak in 2016-17 in Piaui State, Northeast Brazil
REVISTA DO INSTITUTO DE MEDICINA TROPICAL DE SAO PAULO
2019; 61: e57
Chikungunya virus (CHIKV) is an arbovirus that emerged in the Americas in 2013. Infection with CHIKV is symptomatic in most of the cases and patients can develop chronic arthralgia that lasts from months to years in over 40% of the cases. The East-Central-South Africa (ECSA) genotype was introduced in Brazil in 2014, in Bahia State. Here we report the circulation of the CHIKV ECSA genotype in Piaui State, Northeast Brazil, during the years 2016-2017. The phylogenetic analysis revealed a single introduction of this lineage probably in 2015 and its maintenance at least until 2017. This analysis has also demonstrated the proximity of this genotype with isolates from neighboring States, and its partial nucleotide sequence of the viral E1 gene revealed a synapomorphy synonyms. This finding highlights the spread of the ECSA genotype in Brazil and supports its circulation in the Brazilian Northeast.
View details for DOI 10.1590/S1678-9946201961057
View details for Web of Science ID 000489611000005
View details for PubMedID 31618377
View details for PubMedCentralID PMC6792355
Evidence of natural Zika virus infection in neotropical non-human primates in Brazil
2018; 8: 16034
In Africa, Old World Primates are involved in the maintenance of sylvatic circulation of ZIKV. However, in Brazil, the hosts for the sylvatic cycle remain unknown. We hypothesized that free-living NHPs might play a role in urban/periurban ZIKV dynamics, thus we undertook an NHP ZIKV investigation in two cities in Brazil. We identified ZIKV-positive NHPs and sequences obtained were phylogenetically related to the American lineage of ZIKV. Additionally, we inoculated four C. penicillata with ZIKV and our results demonstrated that marmosets had a sustained viremia. The natural and experimental infection of NHPs with ZIKV, support the hypothesis that NHPs may be a vertebrate host in the maintainance of ZIKV transmission/circulation in urban tropical settings. Further studies are needed to understand the role they may play in maintaining the urban cycle of the ZIKV and how they may be a conduit in establishing an enzootic transmission cycle in tropical Latin America.
View details for DOI 10.1038/s41598-018-34423-6
View details for Web of Science ID 000448727000004
View details for PubMedID 30375482
View details for PubMedCentralID PMC6207778
Molecular surveillance of dengue in Minas Gerais provides insights on dengue virus 1 and 4 circulation in Brazil
JOURNAL OF MEDICAL VIROLOGY
2017; 89 (6): 966–73
Dengue, caused by any of the four types of Dengue virus (DENV) is the most important arbovirus in the world. In this study we performed a molecular surveillance of dengue during the greatest dengue outbreak that took place in Divinópolis, Minas Gerais state, Southeast Brazil, in 2013. Samples from 100 patients with clinical symptoms of dengue were studied and 26 were positive. The capsid/premembrane (CprM) and envelope gene sequences of some samples were amplified and sequenced. Molecular analyses demonstrated that two DENV-1 lineages, belonging to genotype V were introduced and co-circulated in Divinópolis. When compared to each other, those lineages presented high genetic diversity and showed unique amino acids substitutions in the envelope protein, including in domains I, II, and III. DENV-4 strains from Divinópolis clustered within genotype IIb and the most recent common ancestor was probably introduced into the city three years before the 2013 epidemic. Here we demonstrated for the first time the circulation of DENV-4 and the co-circulation of two DENV-1 lineages in Midwest region of Minas Gerais, Brazil. Moreover our analysis indicated the introduction of five DENV-1 lineages, genotype V into Brazil, in different times. J. Med. Virol. 89:966-973, 2017. © 2016 Wiley Periodicals, Inc.
View details for DOI 10.1002/jmv.24729
View details for Web of Science ID 000398893900005
View details for PubMedID 27926790