BJID 916 1–6

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The Brazilian Journal of

INFECTIOUS DISEASES
www.elsevier.com/locate/bjid

1 Original article

2 Evaluation of emerging infectious disease and the

3 importance of SINAN for epidemiological
4 surveillance of Venezuelans immigrants in Brazil
a,∗
5 Q2 Mário Maciel de Lima Junior , Gabbrielle Almeida Rodrigues b ,
6 Maysa Ruiz de Lima c
7 Q3 a Departamento de Medicina Interna, Universidade do Estado de Roraima, Universidade da Boa Vista, Boa Vista, RR, Brazil
8
b Universidade Federal de Roraima, Boa Vista, RR, Brazil
9
c Prefeitura de Pacaraima, Boa Vista, RR, Brazil
10

11 a r t i c l e i n f o a b s t r a c t
12

13 Article history: Background: Following socio-economic turmoil in Venezuela, millions of the Venezuelan peo-
14 Received 24 April 2019 ple are migrating to the neighboring Latin American countries including Brazil. Besides the
15 Accepted 20 July 2019 social and economic burden of these migrants, Brazil must manage the health-related issues
16 Available online xxx arising as consequence of these Venezuelan migrants.
17 Poor health services in Venezuela along with unhygienic travelling conditions, lack of
18 Keywords: food (malnutrition) and potable water, unhealthy and overcrowded refugee camps or shel-
19 Venezuela ters, poor availability of medical services have made the migrant Venezuelan population
20 Brazil susceptible to various diseases, especially infectious diseases.
21 SINAN SINAN system is a health-related system in Brazil that keeps track of different health
22 Epidemiological surveillance occurrences in the society and allows health care workers and policymakers free access to
these data.
Objectives: To evaluate the emergence of infectious diseases as a consequence of the arrival
of Venezuelans immigrants in Brazil and to assess the importance of SINAN for epidemio-
logical surveillance.
Methods: Observational retrospective study. Data were collected from the SINAN system
between 2015 and 2017 and was analyzed using descriptive statistics, and Mann-Whitney
test (using SPSS tool version 12). Evaluated infectious diseases in this study were tuberculo-
sis, sexually transmitted infections (STIs), HIV/AIDS, syphilis, viral hepatitis, leishmaniasis,
and malaria.
Results: STIs were the most commonly reported diseases. Compared to Brazilians, Venezue-
lan migrants reported significantly higher number of HIV/Aids (p < 0.046) and leishmaniasis
cases (p < 0.049), while Brazilians reported significantly higher number of hepatitis cases
(p < 0.046). Malaria was also more prevalent among Venezuelan migrants than native Brazil-
ians.

∗
Corresponding author at: Rua Levindo, Inácio de Oliveira, 1547, Paraviana, Boa Vista, RR CEP: 69307-272, Brazil.
E-mail addresses: mmljr2@gmail.com (M.M. Junior), gabrielle.enf@hotmail.com (G.A. Rodrigues), maysaruiz@homail.com (M.R. Lima).
https://doi.org/10.1016/j.bjid.2019.07.006
1413-8670/© 2019 Published by Elsevier España, S.L.U. on behalf of Sociedade Brasileira de Infectologia. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Junior MM, et al. Evaluation of emerging infectious disease and the importance of SINAN for epidemiological
surveillance of Venezuelans immigrants in Brazil. Braz J Infect Dis. 2019. https://doi.org/10.1016/j.bjid.2019.07.006 BJID 916 1–6
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23 Conclusion: Increased incidence of infectious diseases among the migrant population should
24 be considered seriously as lack of adequate control of these diseases might lead to outbreaks.
© 2019 Published by Elsevier España, S.L.U. on behalf of Sociedade Brasileira de
Infectologia. This is an open access article under the CC BY-NC-ND license (http://
25 creativecommons.org/licenses/by-nc-nd/4.0/).

concern for international organizations.15 The black death 75

Introduction
(bubonic plague) in Europe most likely occurred due to con- 76

flict with Asia minor and then it spread rapidly through trade 77
26 Reliable information is of paramount importance towards ade-
routes. 78
27 quate monitoring and delivery of health care services.1 It is
The close association between migration and emergence 79
28 already established that the backbone of a successful disease
of diseases, both in the host and the migrant population, 80
29 control program is a strong disease information system as it
can be explained by several factors. Firstly, the unfavourable 81
30 not only provides the information essential to run the program
environmental or social conditions which led to migration of 82
31 satisfactorily but also lends support to different decision-
the population in the first place like poverty, overcrowded 83
32 making including allocation and rational use of resources.2
settlements, poor economic infrastructure, and collapse of 84
33 Failure of disease control programs has been mainly
health care, scarcity facilities, lack of sanitation, safe and Q4 85
34 attributed to lack of credible and evidence-based decision
potable water, and education, etc. Secondly, the entire pro- 86
35 making in health sectors.2,3 Other obstacles were outdated,
cess of migration from one country to another might make 87
36 incomplete and incomprehensible health related data.
the migrating population susceptible to diseases, as the risk 88
37 To overcome all these hindrances, in 1994 the Brazilian
of emergence of infectious diseases care increases because of 89
38 Government introduced a nationwide disease information
lack of proper sanitation, availability of safe drinking water, 90
39 system for notifiable diseases, the SINAN (“Sistema Nacional
scarcity of food leading to malnutrition, overcrowding, etc. 91
40 de Agravos de Notificaçäo”).2,4
Even after reaching the host countries, the migrant popula- 92
41 In the year 2004, the Brazilian Ministry of Health stated the
tion might remain susceptible to various infectious diseases 93
42 objectives of SINAN as to diagnose any health-related occur-
especially due to overcrowded shelters or refugee camps, and 94
43 rences in a population, to assess the associated risk factors,
poor availability of food, potable, water, and health care facil- 95
44 and to provide information to identify specific epidemiolog-
ities. 96
45 ical situations in a given geographic area.2,5 The systematic
According to a 1994 report of the US Centers for Dis- 97
46 information provided by SINAN is stated to be decentralized
ease Control and Prevention around 50,000 people died due 98
47 so that all health professionals and the community may have
to cholera when leaving Rwanda migrating to Zaire. Simi- 99
48 access to it. Thus, it plays a pivotal role in not only plan-
larly, incidences of malaria outbreaks in the refugee camps 100
49 ning, and prioritizing of objectives but also in successfully
of Afghanistan and Pakistan are well documented.16 In 1999 101
50 implement, monitor and evaluate health related interven-
Rowland et al. described the occurrence of cutaneous leishma- 102
51 tions.2,5
niasis among one third of the Afghan refugees in Pakistan.17 103
52 According to a 2008 WHO report, in developing countries
Sometimes contact with newer populations (host), newer 104
53 of all diseases infectious diseases such as HIV/Aids (5.2%),
microbes, vectors, cultural changes, behavioural and lifestyle 105
54 malaria (4%) and tuberculosis (2.7%) were are the prevail-
changes might again increase the risk of infection in 106
55 ing ones.2,6 The report also mentioned that the so-called
the already vulnerable migrant population. Several atypical 107
56 neglected tropical diseases (NTDs) were also quite common.7,8
vector-borne infections especially louse-borne diseases like 108
57 According to a report published by the International Orga-
epidemic typhus and relapsing fever are commonly prevalent 109
58 nization for Migration in 2009, around 3% of the global
in refugee camps and are associated with high fatality rate. 110
59 population are migrants of which 200 million people are doc-
Moreover, overcrowding in poor sanitary conditions might 111
60 umented as international migrants and around 26 million
lead to emergence of atypical infections and multidrug resis- 112
61 people are estimated to be internally displaced in 52 coun-
tant strains of common microbes. 113
62 tries.9 Especially in the past 50 years, huge number of people
Currently, the poor socioeconomic status of Venezuela 114
63 have been forced to migrate from their own countries to
has driven thousands of its citizens to migrate to differ- 115
64 other countries due to various causes (especially due to socio-
ent countries including Brazil. Incessant entry of Venezuelan 116
65 economic unrest, war, etc.).10–12
migrants to Brazil has led to several socio-economic issues 117
66 In 2004 Saker et al. published in their report that popu-
including health related issues. Thus, regular epidemiological 118
67 lation mobility might lead to several health-related negative
surveillance, especially for infectious diseases, of the migrant 119
68 consequences affecting the migrant population, the host pop-
Venezuelan and the local host population is essential to pre- 120
69 ulation, or both.13 The most significant impact of migration
vent outbreaks. 121
70 is the spread of infectious diseases. Most of the epidemics in
The objective of this study was to evaluate the emerging 122
71 human history occurred due to population migration either
infectious diseases among Venezuelans immigrants in Brazil 123
72 as consequence of war or of a complete change in the
and to assess the importance of SINAN for epidemiological 124
73 whole society.14 Thus, the spread of infectious disease from
surveillance in the same population. 125
74 one country to other countries remains the most important

Please cite this article in press as: Junior MM, et al. Evaluation of emerging infectious disease and the importance of SINAN for epidemiological
surveillance of Venezuelans immigrants in Brazil. Braz J Infect Dis. 2019. https://doi.org/10.1016/j.bjid.2019.07.006 BJID 916 1–6
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Table 1 – Demand for health related interventions by Brazilians

Q1 and Venezuelan migrants in the municipality of
Pacaraima, Roraima state, Brazil, 2015–2017.
Brazilians and Brazilians and Brazilians and Brazilians and Brazilians and
foreigners seeking foreigners seeking foreigners seeking foreigners requiring foreigners requiring
medical attention dental appointments appointments for nebulization in 2017 injectable drugs in
from 2015–2017 in 2017 dressing in 2017 2017

Brazilians Foreigners Brazilians Foreigners Brazilians Foreigners Brazilians Foreigners Brazilians Foreigners

January 315 128 80 20 315 128 0 0 0 0

February 297 122 127 23 297 122 1 0 1 0
March 364 179 158 58 364 179 0 0 0 0
April 226 130 100 92 226 130 1 1 1 1
May 369 284 136 80 369 284 2 0 2 0
June 321 262 182 70 321 262 0 0 0 0
July 242 262 130 80 242 262 5 17 5 17
August 291 344 151 59 291 344 3 63 3 63
September 256 268 45 20 256 268 2 42 2 42
October 349 306 114 47 349 306 2 86 2 86
November 269 240 186 52 269 240 4 106 4 106
December 254 174 116 45 254 174 3 63 3 63

All the data available in the SINAN system regarding 158

Materials and methods infectious diseases reported between 2015 and 2017 for the 159

municipality of Pacaraima were abstracted and analyzed. For 160

126 The study was a three-year retrospective observational study
the purpose of analysis the infectious diseases tuberculo- 161
127 covering all infectious diseases reports between 2015 and 2017.
sis, sexually transmitted infections, HIV/Aids, syphilis, viral 162

hepatitis, leishmaniasis, and malaria were considered. In 163

addition, data available on medical consultation, dental con- 164

128 Study site
sultation, nursing services, and other health related services 165

were also taken into account. 166

129 Place of study
Country of origin (Brazil or Venezuela) of study subjects 167
130 The study analyzes data available from the municipality of
was also considered to assess the specific health conditions 168
131 Pacaraima, Brazil during the study period (2015–2017). The
(infectious diseases) among the different groups of people. 169
132 municipality of Pacaraima is located in the North of the State
133 of Roraima, in the North mesoregion, Boa Vista microregion,
134 located at the geographical coordinates 61◦ 09 15 West lon- Statistical analysis 170

135 gitude and 04◦ 29 33 North latitude. It is limited to the
136 North by the Bolivarian Republic of Venezuela, to the South Data of all the three years (2015, 2016, and 2017) were com- 171

137 by Municipalities of Boa Vista and Amajari, to the East by piled and analyzed. Descriptive statistics were used to analyze 172

138 Municipalities of Normandy and Uiramutã, and to the West the data initially. Specific infectious diseases rates reported 173

139 by Municipality of Amajari (Ministry of Defense, 2004). It has among Brazilians and Venezuelans were compared with the 174

140 a territorial area of 8,028,483 km2 which corresponds to 3.58% nonparametric Mann-Whitney test. Any p-value <0.05 was 175

141 of the territory of Roraima (SEPLAN, 2014). According to data considered to be statistically significant. All analyses were 176

142 from the IBGE/Demographic Census, in 2017 the municipality conducted using the software STATA v12. 177

143 had a population of 12,375 people (IBGE, 2017). In relation to

144 basic health care, the municipality has five teams of family
145 health strategy (ESF), four oral health teams and 28 commu- Results
146 nity health agents (ACS). Of these five ESF teams, three are
147 serving in the municipality headquarters and two in indige- Total number of medical appointments in the three years 178

148 nous communities (São Marcos and Raposa Serra do Sol). In (2015–17) was 6252, of which 3553 (56.8%) were sought by 179

149 addition to the ESF teams, the municipality has implemented Brazilians and remaining by Venezuelans (Table 1 and Fig. 1). 180

150 the Family Health Support Nucleus (NASF), modality 1, which No prominent pattern was observed for Brazilian residents; 181

151 are multiprofessional teams that has an integrated work with however, the number of Venezuelans seeking medical care 182

152 the Family Health teams (eSF), the Primary Care teams for increased over the time from January to August followed by 183

153 specific populations (Offices in the Street - eCR) and with the small drop during the later months of the year. 184

154 Health Academy Program. In 2017, out of those who sought dental care 1525 (70.24%) 185

were Brazilians and the remaining were Venezuelan migrants 186

(n = 646) (Table 1). Still in 2017, the number of dressings pro- 187

155 Data collection vided was higher for Venezuelans (n = 518) than for Brazilians 188

(n = 60) (Table 1). In addition, 378 Venezuelans required neb- 189

156 Data collection was carried out through consultation with ulization and 384 required injectable drugs, numbers much 190

157 SINAN and through the software DATASUS. higher than the 23 and 62 Brazilians, respectively (Table 1). 191

Please cite this article in press as: Junior MM, et al. Evaluation of emerging infectious disease and the importance of SINAN for epidemiological
surveillance of Venezuelans immigrants in Brazil. Braz J Infect Dis. 2019. https://doi.org/10.1016/j.bjid.2019.07.006 BJID 916 1–6
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400
350
300

Numbers
250
200
150
100
50
0

t
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Month

Brazilians Foreigners

Fig. 1 – Number of medical appointments sought each month from 2015 to 2017.

Table 2 – Reported infectious diseases among Brazilians and Venezuelan migrants in the municipality of Pacaraima,
Roraima state, Brazil, 2015–2017.
Disease Brazil (number) Venezuela (number) Total (number) p-value

Tuberculosis 7 9 16 0.658
Sexually transmitted disease 396 333 729 0.275
HIV/AIDS 08 25 33 0.046*
Syphilis 4 4 8 1.00
Hepatitis 39 1 40 0.046*
Leishmaniasis 65 207 267 0.049*

∗
p-value <0.05 (Mann-Whitney test).

2500

2000

1500

1000

500

0
ry

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r
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e
y

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2015 2016 2017

Fig. 2 – Number of people tested for malaria each month from 2015 to 2017.

192 Both Brazilians and Venezuelan migrants reported all Malaria screening for residents was usually done during 210

193 the evaluated infectious diseases namely tuberculosis, STIs, the period of March–June, but there was an increase in the 211

194 HIV/Aids, syphilis, hepatitis, and leishmaniasis. Majority of number of screening in August 2016 (Fig. 2). In 2016, a higher 212

195 the reports were for STIs and of the 729 STI cases 396 proportion of screened people for malaria was positive during 213

196 were reported by Brazilians and 333 by Venezuelan migrants first half of the year, whereas in 2017 there were more malaria 214

197 in Brazil. However, the numbers of reporting for each dis- cases reported at the end of the year (October–December) 215

198 ease varied between the two groups (Table 2). There were (Fig. 3). 216

199 more cases of tuberculosis, HIV/Aids, and leishmaniasis

200 among Venezuelan migrants (tuberculosis = 9; HIV/Aids = 25;
201 lesishmaniasis = 207) than among Brazilians (tuberculosis = 7; Discussion
202 HIV/Aids = 8; for lesishmaniasis = 65) (Table 2). Nonetheless,
203 there were reports of STIs and hepatitis (STIs = 396; hepati- Venezuela was once considered among the leading countries 217

204 tis = 39) among Brazilians than among Venezuelan migrants of the Latin America regarding vector borne diseases and 218

205 in Brazil (STIs = 333; hepatitis = 1) (Table 2). Despite the differ- strong and efficient public health related policies.18,19 It was 219

206 ences in the numbers of reporting between the two groups considered the first country to eradicate malaria following 220

207 for each infection (except for syphilis; four in both groups), a very successful insecticide spraying campaign.19 However, 221

208 only for hepatitis and HIV/Aids the differences were signifi- there has been a rise of vector borne diseases in Venezuela. 222

209 cant (p = 0.046 for both infections). Among the many attributing factors for this crisis, short- 223

Please cite this article in press as: Junior MM, et al. Evaluation of emerging infectious disease and the importance of SINAN for epidemiological
surveillance of Venezuelans immigrants in Brazil. Braz J Infect Dis. 2019. https://doi.org/10.1016/j.bjid.2019.07.006 BJID 916 1–6
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2015 2016 2017

Fig. 3 – Percentage of malaria positive case each month from 2015 to 2017.

224 age/poor supply of insecticides, antiparasitic drugs, and fuel

Table 3 – Number of cases positive for malaria among
225 are the major factors along with widespread malnutrition, Brazilians and Venezuelan migrants in the municipality
226 collapse of the existing health system, poor epidemiological of Pacaraima, Roraima state, Brazil, 2015–2017.
227 surveillance and almost no reporting of infectious diseases
Year Local dwellers From other states Venezuelans Total
228 cases.20,21 Besides vector borne diseases, viral infections espe-
229 cially arboviral diseases like dengue, chikungunya, and Zika 2015 170 10 340 520
2016 169 13 1262 1444
230 are on the rise.22 One of the most important reemerging
2017 285 22 943 1250
231 parasitic diseases in Venezuela is malaria; there is almost
Total 624 966 2545 3214
232 three-fold increase in the incidence of malaria cases since
233 2014.18,23 Besides malaria, Chagas disease and leishmania-
234 sis are the other two vector borne diseases which are posing Venezuelan migrants in Brazil (p = 0.046) and those of hepatitis 266
235 severe threat to Venezuela.24,25 was significantly higher among Brazilians (p = 0.046) (Table 2). 267
236 Currently, with political unrest and collapse of once thriv- The number of malaria positive cases were far greater 268
237 ing economic system, the health care system of this country among the Venezuelan migrants in Brazil (n = 340, 1262, and 269
238 has also collapsed. Lack of jobs, economic stagnation, high 943 in 2015, 2016, and 2017, respectively) compared to Brazil- 270
239 inflation, high rate of crime, poor availability of day–day ians (n = 170, 169, and 285 in 2015, 2016, and 2017, respectively) 271
240 amenities have led millions of Venezuelan citizens to migrate (Table 3). 272
241 from their own land to other Latin American countries includ- Thus, it is evident that the incidence of infectious dis- 273
242 ing Brazil.18 eases especially malaria is significantly higher in Venezuelan 274
243 Migrant populations as such usually suffer from differ- migrants. 275
244 ent health related problems due to travelling in unhygienic In line with the present study, Tuite et al. have also shown 276
245 conditions, lack of food, potable water, overcrowding, poor the implication of Venezuelan migrants on emergence and 277
246 medical care, etc. In addition, settlement in the new country re-emergence of previously controlled infectious diseases like 278
247 might prove very difficult especially if the number of migrants tuberculosis, malaria, diphtheria, measles, etc. and on subse- 279
248 exceeds the capacity of the hosting country. The number of quent outbreaks of these diseases in host as well as migrant 280
249 Venezuelan migrants to Brazil had a striking increase each populations.26 281
250 passing day and Brazil has started to take humanitarian steps Pavli et al. published a systematic review including all 282
251 for the Venezuelan migrants. Among all the other issues, the published articles (using PubMed search and published 283
252 health related issues are of immense importance as there are between 2003 and 2016) on health problems (both communica- 284
253 possibilities that many of the infectious diseases might spread ble and noncommunicable) in migrants and refugees coming 285
254 from these Venezuelan migrants to the locals. to Europe. Like our study, they also noted that the burden 286
255 In this retrospective observational study we have assessed of diseases due to population migration cannot be ignored 287
256 the importance of the Brazilian health-related information and underscored the need for a multidisciplinary integrated 288
257 system (SINAN) regarding surveillance of certain infectious approach would be best for both the migrant and the host 289
258 diseases in the municipality of Pacaraima between 2015 and population.27 290
259 2017 where huge numbers of Venezuelan migrants have taken Another interesting finding of this study is the num- 291
260 shelter by collecting data. ber of live births reported among Brazilians and Venezuelan 292
261 Data analysis revealed that about equal number of migrants in Brazil (Table 4). The number of live births among 293
262 Brazilians and Venezuelan migrants were seeking medical Brazilians (80, 91, and 77, in 2015, 2016, and 2017, respectively) 294
263 attention, but Venezuelan migrants seeking treatment (both were quite high compared to those among the Venezuelan 295
264 medical and dental) seemed to be on the rise (Table 1). migrants to Brazil (17, 32, and 45, in 2015, 2016, and 2017, 296
265 Reporting of HIV/Aids cases were significantly higher among respectively) (Table 4). This suggests probable lack of proper 297

Please cite this article in press as: Junior MM, et al. Evaluation of emerging infectious disease and the importance of SINAN for epidemiological
surveillance of Venezuelans immigrants in Brazil. Braz J Infect Dis. 2019. https://doi.org/10.1016/j.bjid.2019.07.006 BJID 916 1–6
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8. Hotez PJ, Molyneux D, Fenwick A, et al. Control of neglected 338

Table 4 – Number of live births among Brazilians and
tropical diseases. N Engl J Med. 2007;357:1018–27. 339
Venezuelan migrants in the municipality of Pacaraima,
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a key factor in the epidemiology of neglected tropical 341
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Please cite this article in press as: Junior MM, et al. Evaluation of emerging infectious disease and the importance of SINAN for epidemiological
surveillance of Venezuelans immigrants in Brazil. Braz J Infect Dis. 2019. https://doi.org/10.1016/j.bjid.2019.07.006 BJID 916 1–6