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Regional incidence of venous thromboembolism in Brazil

Abstract

Background

Several studies conducted in areas with temperate climates have suggested that the incidence of venous thromboembolism (VTE) varies depending on seasonal climatic fluctuations. However, no studies have been conducted comparing areas with semi-arid climate with areas with temperate climates.

Objectives

To analyze whether there is a correlation between the incidence of VTE in areas with semi-arid climates and areas with temperate climates in Brazil.

Methods

Retrospective data were acquired for patients diagnosed with VTE from January 2011 to December 2014 from the Brazilian National Health Service for the following Brazilian states that have semi-arid climates: Alagoas, Ceará, Maranhão, Paraíba, Pernambuco, Piauí, and Rio Grande do Norte (all located in the Northeast Region of Brazil); and the following states with temperate climates: Paraná, Santa Catarina, and Rio Grande do Sul (all located in the South Region of Brazil). Data on climatic variation were obtained from the National Meteorological Institute and population data were obtained from the Brazilian Institute of Geography and Statistics.

Results

There was a significant correlation in the incidence of VTE cases in areas with lower temperatures (p < 0.001). The South Region exhibited significantly lower temperatures than the Northeast Region (p < 0.001) and had a significantly higher number of cases of VTE than the Northeast Region (p < 0.001).

Conclusions

There are more cases of VTE in areas with temperate climates, where temperatures are lower. However, there is still little information in the literature on seasonal fluctuations and incidence of VTE. More studies of this subject are needed.

Keywords:
venous thromboembolism; venous thrombosis; seasonality; climate

Resumo

Contexto

Vários estudos realizados em climas temperados sugerem que há uma variação na incidência de tromboembolismo venoso (TEV) de acordo com as estações climáticas. Entretanto, nenhum estudo foi feito comparando áreas de clima semiárido com áreas de clima temperado.

Objetivos

Analisar se existe correlação entre a incidência do TEV em áreas de clima semiárido e de clima temperado no Brasil.

Métodos

Foi feito um levantamento de dados retrospectivos de pacientes com diagnóstico de TEV no Sistema Único de Saúde de janeiro de 2011 a dezembro de 2014 provenientes dos seguintes estados com clima semiáridos: Alagoas, Ceará, Maranhão, Paraíba, Pernambuco, Piauí e Rio Grande do Norte, localizados na Região Nordeste do Brasil; e dos seguintes estados com clima temperado: Paraná, Santa Catarina e Rio Grande do Sul, localizados na Região Sul do Brasil. Os dados de variação climática foram obtidos do Instituto Nacional de Meteorologia e os dados populacionais do Instituto Brasileiro de Geografia e Estatística.

Resultados

Houve correlação significativa na incidência de casos de TEV em regiões de temperaturas mais baixas (p < 0,001). A Região Sul apresentou temperaturas significativamente menores que as da Região Nordeste (p < 0,001) e apresentou número significativamente maior de casos de TEV do que a Região Nordeste (p < 0,001).

Conclusão

Há mais casos de TEV em regiões de clima temperado, onde as temperaturas são mais baixas. No entanto, pouco ainda é conhecido na literatura sobre a flutuação sazonal e a incidência de TEV. Sendo assim, mais estudos são necessários nessa área.

Palavras-chave:
tromboembolismo venoso; trombose venosa; sazonalidade; clima

INTRODUCTION

The global prevalence of venous thromboembolism (VTE) is very high, ranging from 50 to 200 cases per 100,000 inhabitants per year.11 Silverstein MD, Heit JA, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ 3rd. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population-based study. Arch Intern Med. 1998;158(6):585-93. PMid:9521222. http://dx.doi.org/10.1001/archinte.158.6.585.
http://dx.doi.org/10.1001/archinte.158.6...

2 Maffei FH. Epidemiologia da trombose venosa profunda e de suas complicações no Brasil. Cir Vasc Angiol. 1998;14:5-8.

3 Fowkes FJ, Price JF, Fowkes FG. Incidence of diagnosed deep vein thrombosis in the general population: systematic review. Eur J Vasc Endovasc Surg. 2003;25(1):1-5. PMid:12525804. http://dx.doi.org/10.1053/ejvs.2002.1778.
http://dx.doi.org/10.1053/ejvs.2002.1778...
-44 Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrøm J. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost. 2007;5(4):692-9. PMid:17367492. http://dx.doi.org/10.1111/j.1538-7836.2007.02450.x.
http://dx.doi.org/10.1111/j.1538-7836.20...
Seasonality of VTE incidence has been reported in various studies conducted in areas with temperate climates.11 Silverstein MD, Heit JA, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ 3rd. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population-based study. Arch Intern Med. 1998;158(6):585-93. PMid:9521222. http://dx.doi.org/10.1001/archinte.158.6.585.
http://dx.doi.org/10.1001/archinte.158.6...

2 Maffei FH. Epidemiologia da trombose venosa profunda e de suas complicações no Brasil. Cir Vasc Angiol. 1998;14:5-8.

3 Fowkes FJ, Price JF, Fowkes FG. Incidence of diagnosed deep vein thrombosis in the general population: systematic review. Eur J Vasc Endovasc Surg. 2003;25(1):1-5. PMid:12525804. http://dx.doi.org/10.1053/ejvs.2002.1778.
http://dx.doi.org/10.1053/ejvs.2002.1778...

4 Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrøm J. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost. 2007;5(4):692-9. PMid:17367492. http://dx.doi.org/10.1111/j.1538-7836.2007.02450.x.
http://dx.doi.org/10.1111/j.1538-7836.20...

5 Stein PD, Kayali F, Olson RE. Analysis of occurrence of venous thromboembolic disease in the four seasons. Am J Cardiol. 2004;93(4):511-3. PMid:14969640. http://dx.doi.org/10.1016/j.amjcard.2003.10.061.
http://dx.doi.org/10.1016/j.amjcard.2003...

6 Kleinfelder D, Andrade JL, Schlaad SW, Carvalho FC, Bellen BV. A sazonalidade do tromboembolismo venoso no clima subtropical de São Paulo. J Vasc Bras. 2009;8(1):29-32. http://dx.doi.org/10.1590/S1677-54492009005000005.
http://dx.doi.org/10.1590/S1677-54492009...

7 Brown HK, Simpson AJ, Murchison JT. The influence of meteorological variables on the development of deep venous thrombosis. Thromb Haemost. 2009;102(4):676-82. PMid:19806252.

8 Gallerani M, Boari B, Toma D, Salmi R, Manfredini R. Seasonal variation in the occurrence of deep vein thrombosis. Med Sci Monit. 2004;10(5):CR191-6. PMid:15114268.

9 Ribeiro DD, Bucciarelli P, Braekkan SK, et al. Seasonal variation of venous thrombosis: a consecutive case series within studies from Leiden, Milan and Tromsø. J Thromb Haemost. 2012;10(8):1704-7. PMid:22681473. http://dx.doi.org/10.1111/j.1538-7836.2012.04811.x.
http://dx.doi.org/10.1111/j.1538-7836.20...

10 Fink AM, Mayer W, Steiner A. Seasonal variations of deep vein thrombosis and its influence on the location of the thrombus. Thromb Res. 2002;106(2):97-100. PMid:12182906. http://dx.doi.org/10.1016/S0049-3848(02)00094-4.
http://dx.doi.org/10.1016/S0049-3848(02)...

11 Boulay F, Berthier F, Schoukroun G, Raybaut C, Gendreike Y, Blaive B. Seasonal variations in hospital admission for deep vein thrombosis and pulmonary embolism: analysis of discharge data. BMJ. 2001;323(7313):601-2. PMid:11557707. http://dx.doi.org/10.1136/bmj.323.7313.601.
http://dx.doi.org/10.1136/bmj.323.7313.6...
-1212 Dentali F, Ageno W, Rancan E, et al. Seasonal and monthly variability in the incidence of venous thromboembolism. A systematic review and a meta-analysis of the literature. Thromb Haemost. 2011;106(3):439-47. PMid:21725580. http://dx.doi.org/10.1160/TH11-02-0116.
http://dx.doi.org/10.1160/TH11-02-0116...
The majority of them show that prevalence is higher during periods of lower temperatures.

However, no studies have been conducted that compare areas with semi-arid tropical climates with areas that have temperate climates. The objective of this study was to analyze whether there is a correlation between the incidence of VTE in areas with semi-arid climates and areas with temperate climates in Brazil.

METHODS

Retrospective data were acquired for patients diagnosed with VTE from the Brazilian National Health Service (SUS - Sistema Único de Saúde).1313 Datasus [site na Internet]. Brasília, DF: Ministério da Saúde; 2016 [citado 2016 jun 1]. http://www2.datasus.gov.br.
http://www2.datasus.gov.br...
Patients were selected who had been diagnosed between January 2011 and December 2014 in the following Brazilian states that have semi-arid climates: Alagoas, Ceará, Maranhão, Paraíba, Pernambuco, Piauí, and Rio Grande do Norte (all located in the Northeast Region of Brazil); and the following states with temperate climates: Paraná, Santa Catarina, and Rio Grande do Sul (all located in the South Region of Brazil).

Climatic data for the capital cities of each of the states listed were obtained from the official National Meteorological Institute (Inmet - Instituto Nacional de Meteorologia),1414 Inmet [site na Internet]. Brasília, DF: Ministério da Agricultura, Pecuária e Abastecimento; 2016 [citado 2016 jun 1]. http://www.inmet.gov.br.
http://www.inmet.gov.br...
covering the same period. Population data were obtained from the official Brazilian Institute of Geography and Statistics’ (IBGE - Instituto Brasileiro de Geografia e Estatística).1515 Ibge [site na Internet]. Rio de Janeiro: Ministério do Planejamento, Orçamento e Gestão; 2016 [citado 2016 jun 1]. www.ibge.gov.br.

Data were subjected to statistical analysis using the Spearman and Mann-Whitney tests.

RESULTS

Table 1 lists descriptive statistics for the temperatures of the states investigated, showing that the median temperatures in the Southern states were lower than the temperatures recorded in the states in the Northeast. Data for some months were not included in the table because official figures were not available (Table 1).

Table 1
Descriptive statistics for temperatures by state, in degrees Celsius.

Table 2 lists descriptive statistics for the number of cases of VTE per 100,000 inhabitants in the states investigated. This table shows that the highest median values were for the states in the South Region.

Table 2
Descriptive statistics for number of cases of venous thromboembolism per 100,000 inhabitants of the states investigated.

Table 3 lists descriptive statistics for average temperature in each Region (Northeast or South), showing that the states in the South had a lower mean temperature than the states in the Northeast.

Table 3
Descriptive statistics for mean temperatures of each Region, in degrees Celsius.

The Mann-Whitney nonparametric test revealed a significant difference in temperature between the two regions. The South Region had significantly lower temperatures than the Northeast Region (p < 0.001) (Figure 1).

Figure 1
Variation in mean temperature in the Northeast Region and the South Region, in degrees Celsius.

Population data for the states investigated were obtained from IBGE. The total population of the South Region was 27,384,815 people and the total for the Northeast Region was 36,988,674 people.

Table 4 lists descriptive statistics for the number of cases of VTE per 100,000 inhabitants by Region. This table shows that the median is higher in the South Region than in the Northeast Region.

Table 4
Descriptive statistics for number of cases of venous thromboembolism per 100,000 inhabitants in each Region.

The Mann-Whitney nonparametric test revealed a significant difference between the Regions in terms of the number of cases of VTE. The South Region had a significantly higher number than the Northeast Region (p < 0.001) (Figure 2).

Figure 2
Cases of venous thromboembolism per 100,000 inhabitants in the Northeast and South Regions.

The Spearman’s correlation coefficient revealed a negative and significant correlation between temperature and rate of VTE per 100,000 inhabitants (r = -0.652; p < 0.001) (Figure 3).

Figure 3
Correlation between incidence of cases of venous thromboembolism per 100,000 inhabitants and temperature in degrees Celsius.

DISCUSSION

Several studies in the literature correlate VTE cases with climatic variation. Stein et al.55 Stein PD, Kayali F, Olson RE. Analysis of occurrence of venous thromboembolic disease in the four seasons. Am J Cardiol. 2004;93(4):511-3. PMid:14969640. http://dx.doi.org/10.1016/j.amjcard.2003.10.061.
http://dx.doi.org/10.1016/j.amjcard.2003...
conducted a study analyzing data from the National Hospital Discharge Survey database covering the period from 1979 to 1999. They analyzed 7,682,000 cases of patients with VTE, 2,457,000 with pulmonary thromboembolism, and 5,767,000 with DVT, but did not find any correlation between seasonal variation and incidence of VTE.55 Stein PD, Kayali F, Olson RE. Analysis of occurrence of venous thromboembolic disease in the four seasons. Am J Cardiol. 2004;93(4):511-3. PMid:14969640. http://dx.doi.org/10.1016/j.amjcard.2003.10.061.
http://dx.doi.org/10.1016/j.amjcard.2003...

However, Kleinfelder et al.66 Kleinfelder D, Andrade JL, Schlaad SW, Carvalho FC, Bellen BV. A sazonalidade do tromboembolismo venoso no clima subtropical de São Paulo. J Vasc Bras. 2009;8(1):29-32. http://dx.doi.org/10.1590/S1677-54492009005000005.
http://dx.doi.org/10.1590/S1677-54492009...
analyzed 955 cases of VTE from 1996 to 2003 and detected a higher incidence during hot months. In contrast, Brown et al.77 Brown HK, Simpson AJ, Murchison JT. The influence of meteorological variables on the development of deep venous thrombosis. Thromb Haemost. 2009;102(4):676-82. PMid:19806252. performed a retrospective analysis of 37,336 cases over 20 years in Scotland, reporting a higher incidence of VTE during the coldest month (p < 0.0001). Similar results were observed by Gallerani et al.88 Gallerani M, Boari B, Toma D, Salmi R, Manfredini R. Seasonal variation in the occurrence of deep vein thrombosis. Med Sci Monit. 2004;10(5):CR191-6. PMid:15114268. in a prospective study of 1166 cases at the Hospital Geral de Ferrara, in Italy, where VTE incidence was higher in the winter (p < 0.0001). Other researchers, such as Ribeiro et al.,99 Ribeiro DD, Bucciarelli P, Braekkan SK, et al. Seasonal variation of venous thrombosis: a consecutive case series within studies from Leiden, Milan and Tromsø. J Thromb Haemost. 2012;10(8):1704-7. PMid:22681473. http://dx.doi.org/10.1111/j.1538-7836.2012.04811.x.
http://dx.doi.org/10.1111/j.1538-7836.20...
Fink et al.,1010 Fink AM, Mayer W, Steiner A. Seasonal variations of deep vein thrombosis and its influence on the location of the thrombus. Thromb Res. 2002;106(2):97-100. PMid:12182906. http://dx.doi.org/10.1016/S0049-3848(02)00094-4.
http://dx.doi.org/10.1016/S0049-3848(02)...
Boulay et al.,1111 Boulay F, Berthier F, Schoukroun G, Raybaut C, Gendreike Y, Blaive B. Seasonal variations in hospital admission for deep vein thrombosis and pulmonary embolism: analysis of discharge data. BMJ. 2001;323(7313):601-2. PMid:11557707. http://dx.doi.org/10.1136/bmj.323.7313.601.
http://dx.doi.org/10.1136/bmj.323.7313.6...
and Dentali et al.,1212 Dentali F, Ageno W, Rancan E, et al. Seasonal and monthly variability in the incidence of venous thromboembolism. A systematic review and a meta-analysis of the literature. Thromb Haemost. 2011;106(3):439-47. PMid:21725580. http://dx.doi.org/10.1160/TH11-02-0116.
http://dx.doi.org/10.1160/TH11-02-0116...
also reported higher incidence rates of VTE cases in the winter.

There are certain factors and hypotheses that can be considered with relation to these observations. During hotter periods, people tend to be more sedentary because of excess heat, increasing immobility.1616 Mora-Rodriguez R, Ortega JF, Fernandez-Elias VE, et al. Influence of Physical Activity and Ambient Temperature on Hydration: The European Hydration Research Study (EHRS). Nutrients. 2016;8(5):252. PMid:27128938. http://dx.doi.org/10.3390/nu8050252.
http://dx.doi.org/10.3390/nu8050252...
During colder months, development of VTE may also be related to reduced physical activity and to vasoconstriction induced by low temperatures, which reduces blood flow in the lower limbs.66 Kleinfelder D, Andrade JL, Schlaad SW, Carvalho FC, Bellen BV. A sazonalidade do tromboembolismo venoso no clima subtropical de São Paulo. J Vasc Bras. 2009;8(1):29-32. http://dx.doi.org/10.1590/S1677-54492009005000005.
http://dx.doi.org/10.1590/S1677-54492009...

Additionally, respiratory tract infections during the winter may induce a hypercoagulable state due to increased fibrinogen levels, which was also observed by Brown et al.,77 Brown HK, Simpson AJ, Murchison JT. The influence of meteorological variables on the development of deep venous thrombosis. Thromb Haemost. 2009;102(4):676-82. PMid:19806252. Boulay et al.,1212 Dentali F, Ageno W, Rancan E, et al. Seasonal and monthly variability in the incidence of venous thromboembolism. A systematic review and a meta-analysis of the literature. Thromb Haemost. 2011;106(3):439-47. PMid:21725580. http://dx.doi.org/10.1160/TH11-02-0116.
http://dx.doi.org/10.1160/TH11-02-0116...
and Gallerani et al.88 Gallerani M, Boari B, Toma D, Salmi R, Manfredini R. Seasonal variation in the occurrence of deep vein thrombosis. Med Sci Monit. 2004;10(5):CR191-6. PMid:15114268. Furthermore, less time exposed to sunlight causes reduced melatonin production and increases coagulability.66 Kleinfelder D, Andrade JL, Schlaad SW, Carvalho FC, Bellen BV. A sazonalidade do tromboembolismo venoso no clima subtropical de São Paulo. J Vasc Bras. 2009;8(1):29-32. http://dx.doi.org/10.1590/S1677-54492009005000005.
http://dx.doi.org/10.1590/S1677-54492009...

In cold conditions, some coagulation factors are elevated in vitro, such as platelet counts and platelet aggregation rates, while there is also a reduction in plasma volume, which increases the viscosity of the blood and of fibrinogen, providing conditions that increase the number of thrombosis cases.1111 Boulay F, Berthier F, Schoukroun G, Raybaut C, Gendreike Y, Blaive B. Seasonal variations in hospital admission for deep vein thrombosis and pulmonary embolism: analysis of discharge data. BMJ. 2001;323(7313):601-2. PMid:11557707. http://dx.doi.org/10.1136/bmj.323.7313.601.
http://dx.doi.org/10.1136/bmj.323.7313.6...

With regard to liquid consumption, there is no difference in fluid equilibrium between hotter and cooler temperatures. Liquid consumption is higher in hotter temperatures, but liquid losses are also proportionally higher.1717 Malisova O, Bountziouka V, Panagiotakos DB, Zampelas A, Kapsokefalou M. Evaluation of seasonality on total water intake, water loss and water balance in the general population in Greece. J Hum Nutr Diet. 2013;26(Suppl. 1):90-6. PMid:23521514. http://dx.doi.org/10.1111/jhn.12077.
http://dx.doi.org/10.1111/jhn.12077...

In our study, states in the North Region of Brazil were excluded from the analysis because of a lack of sample data. Sampling rates are higher in the Northeast Region, but it does appear that there is still a higher rate of under-notification of cases than in the data for the South Region, where there are more resources available for health care. Data on the incidence of VTE were obtained from the SUS, which is Brazil’s official public health system.

After statistical analysis, there was a significant correlation between incidence of VTE cases and lower temperatures (p < 0.001). Specifically, the colder the temperature, the higher the incidence of VTE. The South Region has significantly lower temperatures than the Northeast Region (p < 0.001) and had a significantly higher number of cases of VTE than the Northeast Region (p < 0.001).

CONCLUSIONS

The incidence of VTE is higher in the states in the South of Brazil, where temperatures are lower. However, there is still little information in the literature on the correlation between seasonal fluctuation and incidence of VTE. More studies of this subject are therefore needed.

  • Financial support: None.
  • The study was carried out at Integrated Vascular Surgery Service, Hospital Beneficência Portuguesa (BP), São Paulo, SP, Brazil.

REFERÊNCIAS

  • 1
    Silverstein MD, Heit JA, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ 3rd. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population-based study. Arch Intern Med. 1998;158(6):585-93. PMid:9521222. http://dx.doi.org/10.1001/archinte.158.6.585
    » http://dx.doi.org/10.1001/archinte.158.6.585
  • 2
    Maffei FH. Epidemiologia da trombose venosa profunda e de suas complicações no Brasil. Cir Vasc Angiol. 1998;14:5-8.
  • 3
    Fowkes FJ, Price JF, Fowkes FG. Incidence of diagnosed deep vein thrombosis in the general population: systematic review. Eur J Vasc Endovasc Surg. 2003;25(1):1-5. PMid:12525804. http://dx.doi.org/10.1053/ejvs.2002.1778
    » http://dx.doi.org/10.1053/ejvs.2002.1778
  • 4
    Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrøm J. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost. 2007;5(4):692-9. PMid:17367492. http://dx.doi.org/10.1111/j.1538-7836.2007.02450.x
    » http://dx.doi.org/10.1111/j.1538-7836.2007.02450.x
  • 5
    Stein PD, Kayali F, Olson RE. Analysis of occurrence of venous thromboembolic disease in the four seasons. Am J Cardiol. 2004;93(4):511-3. PMid:14969640. http://dx.doi.org/10.1016/j.amjcard.2003.10.061
    » http://dx.doi.org/10.1016/j.amjcard.2003.10.061
  • 6
    Kleinfelder D, Andrade JL, Schlaad SW, Carvalho FC, Bellen BV. A sazonalidade do tromboembolismo venoso no clima subtropical de São Paulo. J Vasc Bras. 2009;8(1):29-32. http://dx.doi.org/10.1590/S1677-54492009005000005
    » http://dx.doi.org/10.1590/S1677-54492009005000005
  • 7
    Brown HK, Simpson AJ, Murchison JT. The influence of meteorological variables on the development of deep venous thrombosis. Thromb Haemost. 2009;102(4):676-82. PMid:19806252.
  • 8
    Gallerani M, Boari B, Toma D, Salmi R, Manfredini R. Seasonal variation in the occurrence of deep vein thrombosis. Med Sci Monit. 2004;10(5):CR191-6. PMid:15114268.
  • 9
    Ribeiro DD, Bucciarelli P, Braekkan SK, et al. Seasonal variation of venous thrombosis: a consecutive case series within studies from Leiden, Milan and Tromsø. J Thromb Haemost. 2012;10(8):1704-7. PMid:22681473. http://dx.doi.org/10.1111/j.1538-7836.2012.04811.x
    » http://dx.doi.org/10.1111/j.1538-7836.2012.04811.x
  • 10
    Fink AM, Mayer W, Steiner A. Seasonal variations of deep vein thrombosis and its influence on the location of the thrombus. Thromb Res. 2002;106(2):97-100. PMid:12182906. http://dx.doi.org/10.1016/S0049-3848(02)00094-4
    » http://dx.doi.org/10.1016/S0049-3848(02)00094-4
  • 11
    Boulay F, Berthier F, Schoukroun G, Raybaut C, Gendreike Y, Blaive B. Seasonal variations in hospital admission for deep vein thrombosis and pulmonary embolism: analysis of discharge data. BMJ. 2001;323(7313):601-2. PMid:11557707. http://dx.doi.org/10.1136/bmj.323.7313.601
    » http://dx.doi.org/10.1136/bmj.323.7313.601
  • 12
    Dentali F, Ageno W, Rancan E, et al. Seasonal and monthly variability in the incidence of venous thromboembolism. A systematic review and a meta-analysis of the literature. Thromb Haemost. 2011;106(3):439-47. PMid:21725580. http://dx.doi.org/10.1160/TH11-02-0116
    » http://dx.doi.org/10.1160/TH11-02-0116
  • 13
    Datasus [site na Internet]. Brasília, DF: Ministério da Saúde; 2016 [citado 2016 jun 1]. http://www2.datasus.gov.br
    » http://www2.datasus.gov.br
  • 14
    Inmet [site na Internet]. Brasília, DF: Ministério da Agricultura, Pecuária e Abastecimento; 2016 [citado 2016 jun 1]. http://www.inmet.gov.br
    » http://www.inmet.gov.br
  • 15
    Ibge [site na Internet]. Rio de Janeiro: Ministério do Planejamento, Orçamento e Gestão; 2016 [citado 2016 jun 1]. www.ibge.gov.br.
  • 16
    Mora-Rodriguez R, Ortega JF, Fernandez-Elias VE, et al. Influence of Physical Activity and Ambient Temperature on Hydration: The European Hydration Research Study (EHRS). Nutrients. 2016;8(5):252. PMid:27128938. http://dx.doi.org/10.3390/nu8050252
    » http://dx.doi.org/10.3390/nu8050252
  • 17
    Malisova O, Bountziouka V, Panagiotakos DB, Zampelas A, Kapsokefalou M. Evaluation of seasonality on total water intake, water loss and water balance in the general population in Greece. J Hum Nutr Diet. 2013;26(Suppl. 1):90-6. PMid:23521514. http://dx.doi.org/10.1111/jhn.12077
    » http://dx.doi.org/10.1111/jhn.12077

Publication Dates

  • Publication in this collection
    Sept 2017

History

  • Received
    03 May 2017
  • Accepted
    04 July 2017
Sociedade Brasileira de Angiologia e de Cirurgia Vascular (SBACV) Rua Estela, 515, bloco E, conj. 21, Vila Mariana, CEP04011-002 - São Paulo, SP, Tel.: (11) 5084.3482 / 5084.2853 - Porto Alegre - RS - Brazil
E-mail: secretaria@sbacv.org.br