Anti-chikungunya virus seroprevalence in Indigenous groups in the São Francisco Valley, Brazil

Jandir Mendonça Nicacio; Ricardo Khouri; Antônio Marconi Leandro da Silva; Manoel Barral-Netto; João Augusto Costa Lima; Ana Marice Teixeira Ladeia; Rodrigo Feliciano do Carmo; Anderson da Costa Armstrong

doi:10.1371/journal.pntd.0009468

. 2021 Jun 28;15(6):e0009468. doi: 10.1371/journal.pntd.0009468

Anti-chikungunya virus seroprevalence in Indigenous groups in the São Francisco Valley, Brazil

Jandir Mendonça Nicacio ^1,^2,^¤a,^*, Ricardo Khouri ^3,^4,^5,^¤b, Antônio Marconi Leandro da Silva ^1,^¤a, Manoel Barral-Netto ^3,^4,^6,^¤b, João Augusto Costa Lima ⁷, Ana Marice Teixeira Ladeia ⁸, Rodrigo Feliciano do Carmo ^2,⁹, Anderson da Costa Armstrong ^1,^2,^¤a,^*

Editor: Brett M Forshey¹⁰

¹Federal University of Vale do São Francisco School of Medicine-UNIVASF; Petrolina, Pernambuco, Brazil

²Postgraduate Program in Health and Biological Sciences, Federal University of Vale do São Francisco- UNIVASF, Petrolina, Pernambuco, Brazil

³Oswaldo Cruz Foundation/Fiocruz, Institute Gonçalo Moniz, Salvador, Brazil

⁴Federal University of Bahia School of Medicine–UFBA; Salvador, Bahia, Brazil

⁵Rega Institute for Medical Research, KU Leuven, Leuven, Belgium

⁶Instituto Nacional de Ciência e Tecnologia de Investigação em Imunologia, São Paulo, Brazil

⁷Cardiology from Johns Hopkins University, Baltimore, Maryland, United States of America

⁸Postgraduate Course in Medicine and Human Health, Bahiana School of Medicine and Public Health, Salvador, Brazil

⁹College of Pharmaceutical Sciences, Federal University of Vale do São Francisco- UNIVASF, Petrolina, Pernambuco, Brazil

¹⁰DoD - AFHSB, UNITED STATES

The authors have declared that no competing interests exist.

^¤a

Current address: Department of Medicine, Federal University of Vale do São Francisco- UNIVASF, Petrolina, Pernambuco, Brazil

^¤b

Current address: Oswaldo Cruz Foundation/Fiocruz, Institute Gonçalo Moniz, Salvador, Brazil

^✉

* E-mail: jandir.nicacio@univasf.edu.br (JMN); anderson.armstrong@univasf.edu.br (ACA)

Roles

Jandir Mendonça Nicacio: Conceptualization, Investigation, Methodology, Writing – original draft, Writing – review & editing

Ricardo Khouri: Data curation, Investigation, Methodology, Supervision, Writing – review & editing

Antônio Marconi Leandro da Silva: Conceptualization, Data curation, Investigation, Writing – review & editing

Manoel Barral-Netto: Data curation, Investigation, Methodology, Supervision, Writing – review & editing

João Augusto Costa Lima: Conceptualization, Investigation, Writing – review & editing

Ana Marice Teixeira Ladeia: Conceptualization, Investigation, Writing – original draft

Rodrigo Feliciano do Carmo: Data curation, Formal analysis, Investigation, Methodology, Supervision, Writing – original draft, Writing – review & editing

Anderson da Costa Armstrong: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Brett M Forshey: Editor

PMCID: PMC8238182 PMID: 34181663

Abstract

Background

Chikungunya fever (CHIKF) is a serious public health problem with a high rate of infection and chronic disabling manifestations that has affected more than 2 million people worldwide since 2005. In spite of this, epidemiological data on vulnerable groups such as Indigenous people are scarce, making it difficult to implement public policies in order to prevent this disease and assist these populations.

Objective

To describe the serological and epidemiological profile of chikungunya virus (CHIKV) in two Indigenous populations in Northeast Brazil, as well as in an urbanized control community, and to explore associations between CHIKV and anthropometric variables in these populations.

Methodology/Principal findings

This is a cross-sectional ancillary study of the Project of Atherosclerosis among Indigenous Populations (PAI) that included people 30 to 70 years old, recruited from two Indigenous tribes (the less urbanized Fulni-ô and the more urbanized Truká people) and an urbanized non-Indigenous control group from the same area. Subjects underwent clinical evaluation and were tested for anti-CHIKV IgG by enzyme-linked immunosorbent assay. Serological profile was described according to ethnicity, sex, and age. The study population included 433 individuals distributed as follows: 109 (25·2%) Truká, 272 (62·8%) Fulni-ô, and 52 (12%) from the non-Indigenous urbanized control group. Overall prevalence of CHIKV IgG in the study sample was 49.9% (216; 95% CI: 45·1–54·7). When the sample was stratified, positive CHIKV IgG was distributed as follows: no individuals in the Truká group, 78·3% (213/272; 95% CI: 72·9–83·1) in the Fulni-ô group, and 5.8% (3/52; 95% CI: 1.21–16) in the control group.

Conclusions/Significance

Positive tests for CHIKV showed a very high prevalence in a traditional Indigenous population, in contrast to the absence of anti-CHIKV serology in the Truká people, who are more urbanized with respect to physical landscape, socio-cultural, and historical aspects, as well as a low prevalence in the non-Indigenous control group, although all groups are located in the same area.

Author summary

Chikungunya fever is a serious public health problem, with a high rate of infection and disease. Chikungunya virus (CHIKV) is a cosmopolitan virus, which has inflicted severe damage in 50 countries in the Americas and is responsible for chronic disabling manifestations. In spite of this, epidemiological data on vulnerable groups such as Indigenous people are scarce. We report on a cross-sectional study describing the seroprevalence of CHIKV in Indigenous groups in the São Francisco Valley, Brazil, in association with anthropometric data. The study population included 433 individuals distributed in the following ethnic groups: 109 (25.2%) Truká, 272 (62·8%) Fulni-ô, and 52 (12%) from the non-Indigenous urbanized control group When the sample was stratified, positive CHIKV IgG was distributed as follows: no individuals in the Truká group, 213/272 (78.3%; 95% CI: 72·9–83·1) individuals in the Fulni-ô group, and 3/52 (5.8%; 95% CI: 1·21–16) individuals in the control group. This study shows, for the first time, that CHIKV circulated in an Indigenous population (Fulni-ô) in the São Francisco Valley, in 2016 and 2017. The finding strikingly differs from the absence of anti-CHIKV serology found in the Truká people and from the low prevalence in the urban region of Juazeiro, Bahia.

Introduction

The last decades have been marked by arbovirosis outbreaks with impact on public health. Among these, chikungunya fever (CHIKF) stands out, in the early 2000s with rapid spread, reaching global proportions [1]. Despite this, little is known about the behavior of this arbovirosis in restricted access groups, considering the ethnic characteristics of each population.

CHIKF, which is caused by the chikungunya virus (CHIKV), was silent for three decades until major outbreaks affected people in Kenya and India in 2004 and 2005, respectively [2,3]. In 2013, the disease reached the Americas, and it affected approximately 50 countries by the end of 2014, with almost 23,000 confirmed autochthonous cases [4,5]. In 2014, the disease officially arrived in Brazil, and the first autochthonous cases were registered, almost simultaneously in the semi-arid region of the Brazilian Northeast (the poorest region in the country) and in the Amazon Forest Region [6]. Within about two years, nearly one million cases of CHIKF had been registered in the Americas, Aedes aegypti being the main vector [7,8]. However, the impact of CHIKV on Brazilian Indigenous populations is still unknown.

In Brazil, there are officially 760,350 Indigenous people, composing 416 ethnic groups and 6,238 villages, who receive health care assistance from 1,199 Indigenous Primary Health Units [9]. Indigenous groups are distributed throughout the vast territory of Brazil, living in various stages of urbanization. The Northeast Region of Brazil, where European colonization began, is home to Indigenous peoples with diverse ethnicities and traditions [10]. However, very few studies have evaluated the impact of new epidemics on Indigenous communities [11].

To date, in Brazil, the largest records of probable case reports of CHIKF were published in the years 2016 and 2017, with 277,882 and 185,605 cases, respectively, and more than 151,000 confirmed cases during these years. The states in the Northeast Region had the highest incidence rates in 2016 and 2017 (420·3 cases/100,000 inhabitants and 249·5 cases/100,000 inhabitants, respectively) [12]. In 2018, the Northeast Region showed a significant drop in notifications, becoming fourth out of five regions in terms of incidence (19·5 cases/100,000 inhabitants) [13]. In 2020, up to epidemiological week (EW) 46, the Northeast registered an incidence of 37·5 cases/100,000 inhabitants, showing an increase in cases compared to the previous year [14].

Currently, the Northeast state of Pernambuco, which registered new CHIKV case rates of 531·4 cases/100,000 inhabitants in 2016, has an incidence of 34 cases/100,000 inhabitants by EW 38 of 2020 [12,14]. These notifications, however, did not take the country’s vulnerable Indigenous populations into consideration.

Seroprevalence studies on arbovirosis in Indigenous groups in the Americas are rare. In 2004, one study identified the seroprevalence of dengue IgG in the Yukpa and Barí Indigenous tribes in Venezuela [15]. Later, in 2015, a seroprevalence study of CHIKV, hantavirus, and rickettsia was conducted in the Tuchín Indigenous community in Northern Colombia, finding no cases of CHIKV in the study population [16].

This study describes the serological and epidemiological profile of CHIKV in two Indigenous populations in the Northeast Region of Brazil, at different stages of urbanization, in addition to an urbanized control community in the same region. Our hypothesis was that the groups with lower degrees of urbanization, socio-cultural confinement behavior, and conditions strongly related to worse sanitation and health education would have the highest prevalence of CHIKV. Furthermore, this study explores the associations between the serological profile of CHIKV and anthropometric variables usually related to worse outcomes in arbovirosis outbreaks [17].

Methods

Ethics statement

The research was approved by the National Research Ethics Council (CONEP number 1.488.268), the National Indigenous Foundation (Fundação Nacional do Índio [FUNAI]; process number 08620.028965/2015-66), and the Indigenous leaders of the participating groups. All participants provided written informed consent before taking part in the study [18,19].

Study design and sample selection

This is a descriptive, cross-sectional, seroprevalence study, with stratified sample according to the degree of urbanization, carried out in specific populations of the São Francisco Valley in Northeast Brazil, composed of Indigenous groups from two tribes (Fulni-ô and Truká) and a non-Indigenous urbanized control group (from Juazeiro city, state of Bahia). The current analysis was carried out as an ancillary study of the Project of Atherosclerosis among Indigenous Populations (PAI) study.

The PAI study protocol has been previously described in detail [18]. In summary, PAI was initiated in 2016 as an observational study, whose primary aim was to access cardiovascular health in two Indigenous groups with different degrees of urbanization and a totally urbanized control group. The PAI study included individuals of both sexes, 30 to 70 years old, without known cardiovascular disease or renal failure requiring hemodialysis, who provided authorization to conduct the study and signed the informed consent term [10,18]. The initial phase of the PAI study was completed in 2017, after including a total of 1061 participants: 321 from Fulni-ô tribe, 351 from Truká tribe, and 389 from the city of Juazeiro.

Indigenous groups

The following three groups were included: one Indigenous tribe characterized by low level of urbanization (Fulni-ô, located on the banks of the Ipanema River in the São Francisco Basin); one tribe already affected by the urbanization process (Truká, whose territory is crossed by the northern axis of the São Francisco River Transposition Project); and a control group located in a city with a totally urbanized area and a low profile of migration in the municipality of Juazeiro, Bahia, which is also on the banks of the São Francisco River [18].

The Fulni-ô Indigenous tribe is located in the municipalities of Águas Belas and Itaíba, in the agreste region of the state of Pernambuco, and it comprises an area of 12,000 m² with 4,689 people, showing signs of less urbanization [18]. Once a year, the Fulni-ô people are required to be confined in isolation from non-Indigenous people for three months in a separate area adjacent to the tribe for the ritual known as Ouricuri. The Fulni-ô is the only Indigenous group in Northeast Brazil to maintain their original language for daily use [9,18].

The Truká group, on the other hand, comprises people located in the semi-arid region of the same state, in the middle of the São Francisco River; the population comprises 2,981 people, in an area of 6,000 m², in the municipality of Cabrobó, on the island known as Ilha de Assunção or Ilha Grande, which is part of the archipelago of Asunción, showing anthropological signs of greater urbanization [9,18]. They are known as a rural community. The geographical locations of the Truká, Fulni-ô, and control group are shown in Fig 1.

Fig 1 — Map base layers were obtained from <http://www.naturalearthdata.com/about/terms-of-use/> covered by a Creative Commons Attribution 4.0 International (CC BY) License (https://creativecommons.org/licenses/by/4.0/legalcode). Map base layers were modified in QGIS software version 2.18.

The definition of urbanization in this study refers not only to population density, soil permeability to rainfall, scarcity of vegetation, and the characteristics of buildings, as defined by the Brazilian Institute of Geography and Statistics, but also to the historical and cultural aspects of the Indigenous groups [20]. In this context, the Fulni-ô group has no paved roads, and their houses are more isolated. Furthermore, they practice an annual three-month period of isolation from non-Indigenous peoples, in a ritual known as Ouricuri, and they preserve their original language, Yathê, in schools, along with Portuguese [18,19]. From this point of view, the Fulni-ô group was considered to be less urbanized. In contrast with the Fulni-ô, the Truká group presents intermediate characteristics of urbanization, with lifestyle changes and major infrastructural landscape transformation [18,19].

Both groups are assisted by a family group of health professionals, comprising a physician, a nurse, and a group of assistants and local community workers.

Anthropometric data collection

Weight, age, height, and body mass index (BMI) were collected from August 2016 (EW 34) to June 2017 (EW 22), in two collection periods. During EW 34/2016, anthropometric data and biological samples were collected only in the Fulni-ô group. In EW 22/2017, a second moment of anthropometric data and biological sample collection was performed, not only in the Fulni-ô group, but also in the Truká tribe and in the control group. Data collection followed the criteria of the PAI Study [19]. For analysis, age was stratified as 30 to 40 years, 41 to 50 years, 51 to 60 years, and 61 to 70 years.

Obesity has been described as a major risk factor for severe clinical presentations of arbovirosis [17]. Therefore, we included obesity data in our analysis, as measured by BMI, according to the World Health Organization recommendations. In relation to BMI (kg/m²), individuals were classified in a simplified manner as underweight (< 18·5), normal (≥ 18·5 and < 25), overweight (≥ 25 and < 30), and obese (≥ 30), in accordance with the World Health Organization [21].

Collection of biological material

Peripheral blood collections were also performed between EW 34/2016 and EW 22/2017 with right or left antecubital fossa venipuncture. After appropriate antisepsis, 5 to 10 ml of venous blood were removed and transported in refrigerated boxes at 2 to 8°C. Afterwards, serum was centrifuged in 1.5 ml Eppendorf tubes and conserved at −20 to −70°C. These samples were stored at the Instituto Gonçalo Moniz, FIOCRUZ Bahia and the Laboratory of Clinical Analysis, LPC, Salvador, Bahia.

Serological tests

Serological tests for anti-chikungunya virus IgG by enzyme-linked immunosorbent assay (ELISA) from Euromimmun (Code: EI 293a-9601G) were performed following manufacturer instructions. Values with relative index ≥ 1·1 were considered positive; values ≥ 0·8 and < 1·1 were considered borderline, and values < 0·8 were considered negative. Serological tests were performed on 451 participants of the PAI study who agreed to be included and who had viable serum samples at the time the test became available for the study, during 2019. Only 3 borderline samples from the Fulni-ô group were discarded. A total of 15 lipemic, icteric, hemolyzed, or failed samples were discarded from the 3 groups. No other serological tests were performed for other arboviruses in this study.

Although cross-reaction is a challenge in seroprevalence studies for arbovirus, it is particularly problematic in arboviruses of the same family, such as dengue fever, yellow fever, and, more recently, Zika fever [22]. Regarding CHIKV, commercial ELISA diagnostic tests were evaluated, and they showed specificity and sensitivity of 95% and 88%, respectively, for IgG, with 18% false positive for IgM ELISA [23]. In addition, the EuroImmun anti-CHIKV ELISA IgG assay (EUROIMMUN AG, Lüebeck, Germany) showed 95·4% sensitivity and 100% specificity in validation studies on another specific population, in previous studies [24].

Statistical analysis

Sample size calculation for the PAI study was previously described [18,19], computing a total of 957 participants (319 from each of the three groups). For this ancillary study, the calculated sample size was a total of 364 participants, considering a population of 7580 Indigenous people, 95% confidence interval (CI), 5% precision, and an estimated prevalence of CHIKV of 46%, based on a previous prevalence study for a municipality in the state of Bahia in December 2015 [25,26], using an online tool <http://sampsize.sourceforge.net/iface/>. Our hypothesis was that the groups with lower degrees of urbanization, socio-cultural confinement behavior and conditions strongly related to worse sanitation and health education would have the highest prevalence of CHIKV.

The choice of a municipality in Bahia (also located in the Northeast Region) as a reference for the prevalence estimated in the sample calculation was due to the absence of seroprevalence data in the regions close to the tribes. Furthermore, this municipality has climatic and demographic similarities with the cities where the Truká and Fulni-ô groups are located [27].

Data were entered into the SPSS computer program (SPSS Inc., Chicago, IL, USA, Release 16·0·2, 2008) twice, with automatic consistency and amplitude checking. Categorical variables were presented as absolute and relative frequencies, and continuous variables were presented as median (first–third quartiles) after verification of data normality by the Kolmogorov-Smirnov test. The frequency of infection by CHIKV was described in terms of percentage and respective 95% CI. In univariate analysis, positive and negative individuals were compared by Mann-Whitney U test and Pearson’s chi-square (χ²) for continuous and categorical variables, respectively. The prevalence ratio was programmed to be calculated, using a multivariable model, only for those variables that showed a p value < 0·2 in the univariate analysis.

Results

A total of 433 individuals with full available serological and clinical data were included; the majority were young women. Of the total, 124 (36·7%) individuals were considered obese, and 131 (38·8%) were considered overweight (Table 1).

Table 1. Description of characteristics of the total sample studied (n = 433).

Variables	N	%
*Sex*
Male	159	36·7
Female	274	63·2
*Group*
Control	52	12·0
Fulni-ô	272	62·8
Truká	109	25·2
Age group
30–40 years old	147	33·9
41–50 years old	118	27·3
51–60 years old	115	26·6
61–70 years old	53	12·2
Nutritional status^*
Underweight	1	0·3
Normal	82	24·1
Overweight	131	38·8
Obese	124	36·7
Variables	Median (1Q – 3Q)	Mean ± SD
Age, years	46·0 (38·0–55·0)	46·8 ± 10·7
Weight, kg	72·6 (63·1–83·3)	74·7 ± 16·5
Height, cm	160·0 (155·0–166·0)	160·4 ± 8·1
Body mass index, kg/m²	28·1 (25·0–31·6)	29·0 ± 5·9

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SD- standard deviation; 1Q- first quartile; 3Q- third quartile.

*95 individuals missing weight and/or height data.

The prevalence of anti-CHIKV IgG was 49·9% (216/433; 95% CI: 45·1–54·7). When evaluated separately by group, 3 (5·8%; 95% CI: 1·21–16), 213 (78·3%; 95% CI: 72·9–83·1), and 0 (zero) positive individuals were observed in the control, Fulni-ô, and Truká groups, respectively. When we evaluated the Fulni-ô individuals by collection period (EW 34/2016 and EW 22/2017), we observed that the percentage of individuals who were positive for anti-CHIKV IgG was maintained (79·6% and 78·1%, respectively).

Considering all participants, no significant associations were observed in CHIKV IgG seropositivity (n = 216; 49·9%) according to sex (male: 45·9%; female: 52·2%; p = 0·208) or age group (30 to 40 years: 52·3%; 41 to 50 years: 46·6%; 51 to 60 years: 48·7%; 61 to 70 years: 52·8%; p = 0·618). On the other hand, in relation to groups separated by degrees of urbanization, the Fulni-ô tribe showed a higher proportion of anti-CHIKV IgG in comparison to the Truká tribe and the control group, and this was not associated with sex, age group, or BMI categories (Table 2).

Table 2. Prevalence of CHIKV IgG antibodies in population groups (control, Fulni-ô, and Truká) and association with age, sex, and anthropometric data.

Variables	CHIKV IgG
	Control (n = 52)	Fulni-ô (n = 272)	P
	% (positive/total)	% (positive/total)
Group prevalence	5·8 (3/52)	78·3 (213/272)	<0·001
Sex
Male	0·0 (0/26)	75·2 (73/97)	0·213
Female	11·5 (3/26)	80 (140/175)	0·213
Age Group
30–40 years	5·9 (1/17)	78·4 (76/97)	0·650
41–50 years	6·7 (1/15)	81·8 (54/66)
51–60 years	0·0 (0/11)	75·7 (56/74)
61–70 years	11·1 (1/9)	77·1 (27/35)
BMI Group^*
Underweight	0·0 (0/0)	100 (1/1)	0·372
Normal	0·0 (0/12)	66·7 (32/48)
Overweight	6·3 (1/16)	45·8 (64/77)
Obese	9·1 (2/22)	80·0 (44/55)

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BMI- Body mass index

*72 CHIKV IgG+ individuals with missing weight and/or height, all from the Fulni-ô group. Pearson’s chi-square (χ2) was used to calculate p.

Considering participants anti-CHIKV IgG seropositives, there were no significant differences in median age between Fulni-ô people and urbanized controls (47·0; IQR: 37·0–54·0 years vs. 49·0; IQR: 41·0–59·0 years, respectively; p = 0·528), or regarding median values of BMI (28·1; IQR: 25·2–30·7 kg/m² vs. 30·1; IQR: 29·8–32·5 kg/m², respectively; p = 0·354). Also, there was no significant difference in median age or median values of BMI when assessing anti-CHIKV IgG seropositive and negative participants in these groups (S1 Table).

Discussion

Our study shows a high seroprevalence of CHIKV in one traditional Indigenous ethnicity, out of three study groups with different stages of urbanization and diverse environmental conditions. Our results suggest that the most traditional, less urbanized Indigenous community was the one most exposed to CHIKV, as demonstrated by the highest serological rate of infection.

Variable results of anti-CHIKV seropositivity have been found in urbanized areas in Brazil. A study evaluated the prevalence in two cities in the state of Bahia, Feira de Santana and Riachão do Jacuípe, showing a total seropositivity of 51% in December 2015 [25], whereas, in Chapada, a district of Riachão do Jacuípe, a rate of 20% positivity was observed in April 2016, and 11.8% seropositivity was observed in a community of Salvador, Bahia between November 2016 and January 2017 [28,29]. An epidemiological study evaluating two nearby regions, with the same climatic conditions during the same EWs, found different prevalences of 57·1% and 45·7% [25]. This difference in seroprevalence in areas with similar climatic and geographical characteristics is possibly related to several factors, such as population density, sampling type, degree of vector mosquito infestation, sanitary structure of neighborhoods, and commercial activity in the city [10,11,25].

The present report draws attention to the fact that CHIKV seems to have had a particular impact on the Fulni-ô people, the least urbanized Indigenous group in the Northeast Region of Brazil, showing more than 70% seroprevalence, in contrast to the absence of anti-CHIKV IgG in the Truká tribe. This significant and unexpected result in the Fulni-ô tribe differs from most epidemiological studies in the Americas, where estimated and found prevalence has been less than 50% [28–30]. To date, few studies have recorded such high prevalences. Among those that have, we highlight 75% in Comoros Island in 2004, 63% in Kenya in 2005 [31,32], and 75·6% in Haiti, in children aged 2 to 14 years, in 2014 [33]. It is, however, important to mention that these studies were conducted in non-Indigenous communities, with different degrees of urbanization.

Interestingly, our findings suggest that the more traditional Indigenous tribes might have very particular epidemiological dynamics, regarding viral outbreaks. On the other hand, when assessing non-Indigenous areas around the Fulni-ô tribe (Águas Belas and Itaíba), official data indicate a low rate of notification of suspected cases based on clinical evaluation, considering the cumulative period of 2015 to 2020. Importantly, there are no official data on serological prevalence of CHIKV in this area. The municipality of Águas Belas has a population of 40,235 people, and it reported a total of 167 suspected cases in 2016, remaining below 12 cases/year in subsequent years (2017 to 2020). The municipality of Itaíba (total population of 26,256 people), which is adjacent to Águas Belas, reported 143 cases of CHIKV between the years 2015 and 2017. In 2016, of the 167 cases of suspected CHIKV notified in Águas Belas, 55% were confirmed by laboratory and/or clinical epidemiological criteria. Of the total of 11 cases notified in Itaíba for 2017, only 1 case was confirmed by serological testing. The raw data for the non-Indigenous municipalities were acquired from the official epidemiological vigilance and are available as Supplementary Material (S1 and S2 Appendices).

Regarding the degree of urbanization in isolated communities, our study also differs from previous assessment of seroprevalence of dengue in the Yukpa (most influenced by urbanization, concerning aspects of the physical landscape, house structure, sanitation conditions, as well as population traffic) and Barí Indigenous groups, in Sierra de Perija, Venezuela, which found higher prevalence in the most urbanized tribe, with greater transit of individuals with the virus within the community, precarious health structure, and higher infestation of Ae. Aegypti [15].

There are no official data for vector mosquito presence that are specific for the studied tribes. Nevertheless, since 2002, the Brazilian Ministry of Health has been conducting a survey in the nearby cities (Ae. aegypti Infestation Index Rapid Survey LIRAa). It consists of a method of monitoring the levels of infestation of Ae. aegypti larvae in homes, performed by periodical sampling technique, allowing an entomo-epidemiological survey of the region [34]. In 2017, Águas Belas showed an Ae. aegypti Infestation Index Rapid Survey of 2.0, which is considered alert, while, in the city of Cabrobó (adjacent to where the Truká tribe is located), the index was 0·2, which is considered low. In the same period, the city of Juazeiro (control group) showed an Index of 0·8 (considered low or satisfactory) [34]. The different levels of infestation of the vector mosquito might partially explain the higher prevalence of CHIKV in the Fulni-ô people, when compared to the Truká people.

Another important aspect for our finding of diverse CHIKV prevalence ratios may be the specifics of weather conditions in different regions. While the tribes are located along the São Francisco River Valley, in an area with tropical climate, the Fulni-ô group is located in the agreste region, where rainfall is slightly higher than in the Truká group area; this may favor greater vector mosquito infestation. [35]. However, this does not fully explain our results, given that other cities with similar weather conditions show variable notifications of suspected CHIKF cases in the same period [36].

There has been much discussion about the role of poorly planned urbanization and disorderly growth in the health of the population, especially with regard to contagious or insect borne diseases [37]. The high prevalence of CHIKV in the Fulni-ô people may be favored by the degree of urbanization, with unpaved streets, houses that preserve original constructions, which are partly made of clay, and less sanitary structure [9,18]. The Fulni-ô people also struggle for access to adequate water supply, and they usually store still water, what might be related to mosquito proliferation. This association of CHIKV with the condition of socioeconomic vulnerability has already been identified in previous studies in the Americas, including in a non-Indigenous community in the Brazilian Northeast [28,38]. These factors, in conjunction with a lifestyle characterized by social coexistence, with strong cultural exchange between families and the preservation of confinement rituals (Ouricuri), have probably influenced the high rate of infectivity and transmissibility, since people live close together with multiple close social interactions, in the same environment of the mosquito vector, making the Fulni-ô Indigenous Reserve an environment conducive to maintaining humans in the viral cycle over the years [9,18].

This study has important limitations that must be considered. Serology was not conducted for other arboviruses that are prevalent in Brazil, and potential serological cross-reactions could not be addressed. The sample was not homogeneous with respect to the proportion of participants in each subgroup. There was a gap between the blood sample collection and the serum analysis. We assessed all blood samples that were properly stored in a sufficient amount for serological testing. The number of tested participants exceeded the sample size estimate, but a relevant number of participants from the main PAI study were not included in this ancillary analysis. Furthermore, there was a lack of clinical data to analyze the association of signs and symptoms with seroprevalence data; thus, we could not address the entire dimension of the clinical relevance related to the chikungunya disease burden in these Indigenous populations. It is, however, necessary to highlight that working with closed populations, who are distant from large urban centers and who have distinct social behaviors, makes it difficult to execute projects in this profile, in addition to the intrinsic logistical limitations to approach and data collection in more isolated populations of difficult access.

Chikungunya compromises quality of life, interfering with social and work relationships and often leading to psychiatric disorders [39,40]. This acutely debilitating febrile illness is a serious public health problem, with the risk of evolving into chronic forms. Indigenous people in the Americas have been through known recurrent infectious diseases outbreaks since colonial times, but little is known regarding the dynamics of the disease, as well as the long-term impact on these populations [41]. It is important to understand the epidemiological dynamics of chikungunya, as well as other new infectious diseases, in traditional vulnerable populations such as Indigenous people, in order to aid public health policies directed to the management of chronic forms of the disease and the control of future outbreaks.

In conclusion, our study shows a high serological prevalence for CHIKV in a traditional Indigenous population (Fulni-ô) in the São Francisco Valley between 2016 and 2017, regardless of age and sex. This finding differs from the low prevalence found in the more urbanized Truká people and in the non-Indigenous urban control group, although all communities are located in the same region. Understanding the dynamics of epidemics in various locations and their peculiarities in diverse population groups will allow for more appropriate planning of prevention and containment of future epidemics.

Supporting information

S1 Appendix. Notification of suspected cases of chikungunya fever in Águas Belas municipality, from 2016 to 2020.

(XLSX)

Click here for additional data file.^{(13.1KB, xlsx)}

S2 Appendix. Notification of suspected cases of chikungunya fever in Itaíba municipality, from 2015 to 2017.

(XLSX)

Click here for additional data file.^{(11.4KB, xlsx)}

S1 Table. Analysis of median values of age and BMI with anti-chikungunya virus seroprevalence.

(DOCX)

Click here for additional data file.^{(15.3KB, docx)}

Acknowledgments

We would like to thank the Executive Secretariat of Health Surveillance, particularly the members of the team of the Arboviruses Surveillance Management of the State of Pernambuco and V Regional Health Management for their collaborative efforts on the interpretation of the official data for non-Indigenous areas. We also thank Acácio Willian Faustino de Andrade for helping us to edit the figure referring to the location map of the Fulni-ô and Truká tribes.

Data Availability

All data, including identification of the indigenous people, cannot be shared publicly due to the information protection policy of the National Indian Foundation (FUNAI) and the Special Indigenous Health Secretariat (SESAI) of Brazil. Regarding the data availability statement, as per guidance, we are providing contact details of a third, non-author third party who can make the data available, whenever necessary, while maintaining the anonymity of the indigenous people: Carlos Dorneles Freire de Souza, MSc, PhD Institutional e-mail: carlos.freire@arapiraca.ufal.br Affiliation: Federal University of Alagoas School of Medicine - UFAL, Arapiraca, Alagoas, Brazil The data can be found on the Special Indigenous Health Secretariat - SESAI and National Indian Foundation (FUNAI), Brazil. Link: https://saudeindigena.saude.gov.br/ and https://www.gov.br/funai/pt-br Part of the information, however, is published in the Supporting Information (supplementary material).

Funding Statement

Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq"- Ministry of Science, Technology, Innovations and Communications of Brazil (link: < https://www.gov.br/cnpq/pt-br>) provided logistical support and funding for the laboratory tests performed in the study. Funding was allocated to ACA. We acknowledge Fundação Maria Emilia for the grant regarding the publication fee and further research on this topic. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0009468.r001

Decision Letter 0

Brett M Forshey, Eugenia Corrales-Aguilar

14 Dec 2020

Dear Dr Nicacio,

Thank you very much for submitting your manuscript "Anti- chikungunya virus seroprevalence in indigenous groups in the São Francisco Valley, Brazil" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. In light of the reviews (below this email), we would like to invite the resubmission of a significantly-revised version that takes into account the reviewers' comments.

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Sincerely,

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Associate Editor

PLOS Neglected Tropical Diseases

Eugenia Corrales-Aguilar

Deputy Editor

PLOS Neglected Tropical Diseases

***********************

The reviewers provided a number of issues to address to improve the manuscript, including:

- The Methods section needs to be clarified in a number of places, as mentioned below. For example, there should be more description of the PAI study and the sampling methodology.

- The interpretation of the data needs to be better justified in some places, including the mention that this population is most endangered for new viral outbreaks. In addition, the data just seems surprising and the reasons for the outcome should be explored a bit more - the prevalence is extremely high in one relatively remote community, but zero or nearly zero in communities you'd expect to have higher exposure. Also, how many acute cases were reported from these regions? >78% attack rate is quite high - was there a recognized outbreak in recent years? Hard to imagine a 78% attack rate would've gone unnoticed, but there's no context provided here.

Other issues to address, in addition to the comments by the reviewers:

- The concept of a 'control' population is not clear in the manuscript. In what way would a more urbanized population be a control? Where these anticipated to be more highly positive? The hypothesis being tested that would make this population the control is not clear and should be explained.

- Line 10: Mentions a million cases in Kenya and India, but the references don't actually speak to those numbers. Were there really a million cases in Kenya?

- Line 23: "CHKF"

- Lines 49-51, Ethical issues: The PAI study was approved by the various stakeholders, but was this add-on CHIKV study specifically approved?

- Lines 58-63: A map might be helpful in explaining how these communities are situated relative to one another

- Methods: what was the timing of the sampling? Line 73 says there were two collection periods, but it wasn't clear which groups were sampled when.

- Lines 89-90: How many samples were discarded? How did that impact overall participant numbers?

- Lines 108-110: The wording in these sentences is odd. I don't usually see 'prevalence' represented first as a count number. I recommend referring to the proportion first, with the total number of positives in parentheses. E.g. "The prevalence of anti-CHIKV IgG in the study sample was 49.9% (216/433; 95% CI: 45.1 - 54.7)"

- Lines 115-116: The comment that anti-CHIKV antibodies were more common in females than males (66.2% vs 33.8%) is very confusing - this is largely just a function of the fact that more females participated in the study. Along these same lines, on Table 2, it would be easier to interpret if the data were presented as the percent antibody positive rather than the percent of each category. That is, the number in the bracket should be the percentage of each group/variable that are positive or negative for anti-CHIKV antibodies.

- Lines 128-130 and Table 3: I don't follow how the prevalence ratio calculation was approached. What was it adjusted for? How is Truka the reference category when the prevalence is zero? How should these numbers be interpreted?

- Lines 136-138: This statement is a repeat from earlier in the Results.

- Lines 167-175: This paragraph needs a great deal of additional clarification - the paragraph either needs to be rewritten or deleted entirely. How is "climate" involved here? What was the timing of the mosquito survey? What is a rainfall index and how does it relate to Aedes abundance? I would expect that all of these locations could harbor Aedes mosquitoes, so this paragraph should focus on explaining what mosquito surveys were done at all 3 locations and when, with what regularity, and how that might relate to understanding CHIKV transmission. Aedes populations can be quite dynamic, so a single survey might not really capture transmission potential.

- Lines 193-195: Mentions the long interval between sample collection and testing - please clarify. How long? In what way would this interfere with the results?

- Lines 193-200, Limitations: Recommend mentioning potential for serological cross-reaction.

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #1: In line 48 from the Methods section, the authors should provide more explication about the choice of the 30 to 70 years of age range for recruitment.

In line 48, the Authors should clearly state the approval number from Research Ethics Committee, regarding the work with Traditional Populations.

The authors used a commercial kit for detection of anti-chikungunya virus IgG by enzyme-linked immunosorbent assay. Since it is widely known the occurrence of cross-reactions in serological tests to detect arbovirus infections, the authors should provide more details whether other tests were performed to detect other arbovirus species, or at least discussing the performance data from the kit used in the study.

In line 90, the authors should clearly provide the exact number of samples discarded.

Reviewer #2: The methodology of this ancillary study is well described; however, it is necessary to state the sampling strategy. Also, I suggest clarifying the term “stratified” in line 44: does it refer to stratification in the context of a complex sampling design of the PAI study or to the three exposure groups? The exposure and control groups were adequately selected in terms not only of ethnicity but also of a gradient of urbanization, which allowed the evaluation of the contrasts of main interest; however, it is not clear the reason(s) behind testing a hypothesis of association between body mass index (BMI) and seroprevalence (lines 40-41): I suggest to provide evidence in support of the biological plausibility and/or clinical relevance of such relationship. The statistical approach seems to be consistent with the aim of the study, however, it is not clear whether the PAI study (and the ancillary) had a complex sampling design and, therefore, whether or not point and uncertainty estimates should account for it: Please provide further details.

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #1: In table 1, there is a typing error in the "Mean DP", perhaps it might be "SD- standard deviation".

Reviewer #2: Results from descriptive statistics and univariate analysis are clear and correspond to the analysis plan, under de assumption that PAI (and the ancillary) study did not followed a complex sampling design (i.e., simple random sampling): Please, consider to change the title of table 1 (“Description of anthropometric parameters (n = 433)”) as it shows more than anthropometric parameters for which there is a high proportion of missing data (22.2%). I have the following concerns about the multivariate analysis: 1. What was the control group? If this group was the “urbanized control community” as its denomination suggests, then is incorrect to present a prevalence ratio for that group (Table 3: APR=0.966), furthermore, an APR lower than the unity (0.608) for the Fulni-ô is not plausible since prevalence in this group is 78.3% (213/272) as compared to 5.8% (3/52) in the “urbanized control community”; 2. Alternatively, if the “control” group was the Truká, then there would be a zero prevalence in the denominator of any PR (or APR); and 3. There is no indication of which variables the prevalence ratio was adjusted for or what were the reasons behind selecting them to be included in a multivariate model (the univariate analysis does not support a relationship to prevalence for any covariate).

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #1: The authors claim that the "less urbanized Indigenous community might be the most endangered for new viral outbreaks". This sound a very strong statement, since the authors provide information about only one arbovirus species, and the prevalence of CHIKV infections in the indigenous populations analyzed indicated that this population likely presents herd immunity to CHIKV. The authors should reformulate the sentence.

Reviewer #2: In general, the validity of a conclusion regarding prevalence is contingent upon the sampling design, something that the authors did not describe in the manuscript and cannot be traced from the references to the main study (PAI). Furthermore, there are concerns about the analysis itself that must be clarified before attempting an interpretation of the results.

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #1: (No Response)

Reviewer #2: N.A.

--------------------

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #1: The authors recruited patients from indigenous Populations in the São Francisco Valley, Brazil between August 2016 and June 2017, to collect clinical data and blood samples that underwent serology testing for anti-CHIKV IgG by ELISA. By analyzing the data from 433 patients, the authors argues that there is a high prevalence of Chikungunya virus infection in the Fulni-ô indigenous population between 2016 and 2017. The study found 78·3% of the samples from Fulni-ô group tested positive for anti-CHIKV IgG. Authors' conclusions are consistent with the results presented in the study, they provide a discussion about limitations of the study as well as on previously published related literature.

In line 13 from the introduction section, the authors should provide a reference for the claim: "in the semi-arid region of the Brazilian Northeast (the poorest region in the country) and in the Amazon Forest region. "

Reviewer #2: Nicacio et al., conducted a Chikungunya serosurvey in two indigenous groups and in an urbanized control community (30-70 years old) in Northeast Brazil, as an ancillary study of the Project of Atherosclerosis among Indigenous Populations (PAI). This is a relevant research question because of the particularities and vulnerability of the target populations; however, the absence of a detailed description of the methodological approach – specifically, the sampling design – of both the principal and the ancillary studies precludes to reach meaningful inferences regarding the burden of the infection as determined by estimates of seroprevalence.

--------------------

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Reviewer #2: No

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PLoS Negl Trop Dis. 2021 Jun 28;15(6):e0009468. doi: 10.1371/journal.pntd.0009468.r002

Author response to Decision Letter 0

28 Jan 2021

Attachment

Submitted filename: Rebuttal LetterPLOS1 DEFINITIVOdocx.docx

Click here for additional data file.^{(40.8KB, docx)}

PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0009468.r003

Decision Letter 1

Brett M Forshey, Eugenia Corrales-Aguilar

9 Mar 2021

Dear Dr Nicacio,

When you are ready to resubmit, please upload the following:

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Sincerely,

Brett M. Forshey

Associate Editor

PLOS Neglected Tropical Diseases

Eugenia Corrales-Aguilar

Deputy Editor

PLOS Neglected Tropical Diseases

***********************

The authors made a number of improvements to the manuscript in response to the reviews. However, there are still significant issues to address, as indicated by the reviewer and by my comments below. I'm also attaching a track changes version of the manuscript with a number of other comments.

- Abstract: The confidence interval for the Fulni-o group does not include the point estimate.

- Abstract and elsewhere: It's not clear what makes one tribe more "urbanized" than another - that term is never defined, and the population density of the two tribes seems similar.

- Introduction: The first paragraph of the Introduction about pandemics is too generic and does not add to the manuscript -recommend deleting.

- Introduction line 10-11: States that South and Central America had 1.5 million chikungunya cases in 2013, but that does not seem to be correct.

- Figure 1: the 'control' area should be shown on the map as well.

- Methods, line 102: States that "Peripheral blood collections were also performed in EW 22/2017" which is confusing. Since the section is titled Collection of biological material, all collections should be mentioned here.

- Methods, lines 125-128: The sample size calculation needs to be explained better. What hypothesis was being tested - was this to compare populations? Estimate the overall prevalence? With what precision? Etc.

- Table 2: This table should show the breakdown of CHIKV seropositivity by variable (eg by age group), not just the overall percentage of participants by age group. So, what percentage of females were seropositive and what percentage of males were seropositive? Also please include confidence intervals.

- Discussion: in multiple places the authors refer to "official data indicate a markedly lower prevalence of CHIKV in the non-indigenous areas" - but no seroprevalence data is shown to compare. Please clarify and provide a reference to the data.

There are other comments and recommendations to consider in the word version of the submission, attached.

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #2: In this revised version of the manucript the authors clarified most of the issues raised before, for example, the reason behind the selection of the control group and the sampling of the ancillary study. Noticebly, the authors acknowledged the error made in estimating prevalence ratios (PR); however, it is not clear to me why didn't they re-estimate the PR (at least for the group with non zero prevalence). I suggest to provide additional information about participation rates by group and if possible, also to include a contrast between the samples of the ancillary (n=433) and main (n=1061) studies. This information might help the authors to account for the non expected results as declared in the discussion section.

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #2: The results correctly reflect the analysis plan and are clearly presented.

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #2: The conclusions are supported by the data, however, as I pointed out before (methods), providing further description of the sample that participated in the study might shed light to the interpretation of some unexpected findings, as declared by the authors, or at least to rule out the effect of selection bias due to diferential participation rates across groups.

--------------------

Editorial and Data Presentation Modifications?

Reviewer #2: N.A.

--------------------

Summary and General Comments

Reviewer #2: N.A.

--------------------

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Reviewer #2: No

Figure Files:

Data Requirements:

Reproducibility:

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PLoS Negl Trop Dis. 2021 Jun 28;15(6):e0009468. doi: 10.1371/journal.pntd.0009468.r004

Author response to Decision Letter 1

31 Mar 2021

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PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0009468.r005

Decision Letter 2

Brett M Forshey, Eugenia Corrales-Aguilar

14 Apr 2021

Dear MD Nicacio,

Thank you very much for submitting your manuscript "Anti- chikungunya virus seroprevalence in indigenous groups in the São Francisco Valley, Brazil" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. The reviewers appreciated the attention to an important topic. Based on the reviews, we are likely to accept this manuscript for publication, providing that you modify the manuscript according to the review recommendations.

Please prepare and submit your revised manuscript within 30 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email.

When you are ready to resubmit, please upload the following:

[1] A letter containing a detailed list of your responses to all review comments, and a description of the changes you have made in the manuscript.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Thank you again for your submission to our journal. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Brett M. Forshey

Associate Editor

PLOS Neglected Tropical Diseases

Eugenia Corrales-Aguilar

Deputy Editor

PLOS Neglected Tropical Diseases

***********************

The authors have done a good job of addressing the reviewers concerns, with one major exception: Table 2 still does not show the data necessary for this publication. This should be the breakdown of participants and seropositivity, by subpopulation, by region. For example, it should show of the number of males from the control region, how many were positive and what percentage. Same for females from the control region, same for males from the indigenous regions, etc; the same breakdown should be shown for other variables such as age, etc. I've tried to demonstrate one way of displaying this data in track changes in the word document the authors had provided (attached). Also, here are other publications showing the data along the lines of what is needed for this manuscript - it doesn't have to be this format exactly, but hopefully will give you the idea of the data needed.

Table 1 in this manuscript: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0008355

Table 1 in this manuscript: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0006163

Please also clarify what the data at the bottom of Table 2, for age and BMI, represent - is that the mean age and BMI for positive individuals from those regions? How do those numbers compare with negative individuals from the same regions?

Figure Files:

Data Requirements:

Reproducibility:

To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option to publish peer-reviewed clinical study protocols. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

References

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article's retracted status in the References list and also include a citation and full reference for the retraction notice.

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PLoS Negl Trop Dis. 2021 Jun 28;15(6):e0009468. doi: 10.1371/journal.pntd.0009468.r006

Author response to Decision Letter 2

30 Apr 2021

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PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0009468.r007

Decision Letter 3

Brett M Forshey, Eugenia Corrales-Aguilar

11 May 2021

Dear MD Nicacio,

We are pleased to inform you that your manuscript 'Anti- chikungunya virus seroprevalence in Indigenous groups in the São Francisco Valley, Brazil' has been provisionally accepted for publication in PLOS Neglected Tropical Diseases.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

Should you, your institution's press office or the journal office choose to press release your paper, you will automatically be opted out of early publication. We ask that you notify us now if you or your institution is planning to press release the article. All press must be co-ordinated with PLOS.

Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Brett M. Forshey

Associate Editor

PLOS Neglected Tropical Diseases

Eugenia Corrales-Aguilar

Deputy Editor

PLOS Neglected Tropical Diseases

***********************************************************

PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0009468.r008

Acceptance letter

Brett M Forshey, Eugenia Corrales-Aguilar

14 Jun 2021

Dear MD Nicacio,

We are delighted to inform you that your manuscript, "Anti- chikungunya virus seroprevalence in Indigenous groups in the São Francisco Valley, Brazil," has been formally accepted for publication in PLOS Neglected Tropical Diseases.

We have now passed your article onto the PLOS Production Department who will complete the rest of the publication process. All authors will receive a confirmation email upon publication.

The corresponding author will soon be receiving a typeset proof for review, to ensure errors have not been introduced during production. Please review the PDF proof of your manuscript carefully, as this is the last chance to correct any scientific or type-setting errors. Please note that major changes, or those which affect the scientific understanding of the work, will likely cause delays to the publication date of your manuscript. Note: Proofs for Front Matter articles (Editorial, Viewpoint, Symposium, Review, etc...) are generated on a different schedule and may not be made available as quickly.

Soon after your final files are uploaded, the early version of your manuscript will be published online unless you opted out of this process. The date of the early version will be your article's publication date. The final article will be published to the same URL, and all versions of the paper will be accessible to readers.

Thank you again for supporting open-access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Shaden Kamhawi

co-Editor-in-Chief

PLOS Neglected Tropical Diseases

Paul Brindley

co-Editor-in-Chief

PLOS Neglected Tropical Diseases

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Appendix. Notification of suspected cases of chikungunya fever in Águas Belas municipality, from 2016 to 2020.

(XLSX)

Click here for additional data file.^{(13.1KB, xlsx)}

S2 Appendix. Notification of suspected cases of chikungunya fever in Itaíba municipality, from 2015 to 2017.

(XLSX)

Click here for additional data file.^{(11.4KB, xlsx)}

S1 Table. Analysis of median values of age and BMI with anti-chikungunya virus seroprevalence.

(DOCX)

Click here for additional data file.^{(15.3KB, docx)}

Attachment

Submitted filename: Rebuttal LetterPLOS1 DEFINITIVOdocx.docx

Click here for additional data file.^{(40.8KB, docx)}

Attachment

Submitted filename: Revised Article with Changes H - bmf.docx

Click here for additional data file.^{(68.3KB, docx)}

Attachment

Submitted filename: Rebuttal Letter Second Revision PLOS.docx

Click here for additional data file.^{(36.1KB, docx)}

Attachment

Submitted filename: Revised Article with Changes Highlighted (2) bmf.docx

Click here for additional data file.^{(74.8KB, docx)}

Attachment

Submitted filename: Rebuttal Letter Second Revision_update PLOS.docx

Click here for additional data file.^{(32.8KB, docx)}

Data Availability Statement

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Anti-chikungunya virus seroprevalence in Indigenous groups in the São Francisco Valley, Brazil

Jandir Mendonça Nicacio

Ricardo Khouri

Antônio Marconi Leandro da Silva

Manoel Barral-Netto

João Augusto Costa Lima

Ana Marice Teixeira Ladeia

Rodrigo Feliciano do Carmo

Anderson da Costa Armstrong

Roles

Abstract

Background

Objective

Methodology/Principal findings

Conclusions/Significance

Author summary

Introduction

Methods

Ethics statement

Study design and sample selection

Indigenous groups

Fig 1. Geographic locations of the Truká, Fulni-ô, and control group.

Anthropometric data collection

Collection of biological material

Serological tests

Statistical analysis

Results

Table 1. Description of characteristics of the total sample studied (n = 433).

Table 2. Prevalence of CHIKV IgG antibodies in population groups (control, Fulni-ô, and Truká) and association with age, sex, and anthropometric data.

Discussion

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Brett M Forshey

Eugenia Corrales-Aguilar

Roles

Author response to Decision Letter 0

Decision Letter 1

Brett M Forshey

Eugenia Corrales-Aguilar

Roles

Author response to Decision Letter 1

Decision Letter 2

Brett M Forshey

Eugenia Corrales-Aguilar

Roles

Author response to Decision Letter 2

Decision Letter 3

Brett M Forshey

Eugenia Corrales-Aguilar

Roles

Acceptance letter

Brett M Forshey

Eugenia Corrales-Aguilar

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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