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MINI REVIEW article

Front. Cardiovasc. Med., 11 August 2023
Sec. Hypertension
This article is part of the Research Topic Global Excellence in Cardiovascular Medicine: Central and South America View all 10 articles

Seasonal variation in blood pressure: what is still missing?

  • 1Hypertension League of Porto Alegre, Porto Alegre, Brazil
  • 2Department of Internal Medicine, School of Medical Sciences, State University of Campinas, Campinas, Brazil
  • 3Department of Hypertension and Cardiometabolism, São Francisco Hospital, Santa Casa de Misericórdia de Porto Alegre, Feevale University, Porto Alegre, Brazil
  • 4Center for Clinical Research and Management Education, Division of Health Care Sciences, Dresden International University, Dresden, Germany
  • 5School of Medicine, Lutheran University of Brazil, Canoas, Brazil
  • 6Hypertension and Vascular Risk Unit, Hospital Clínic (IDIBAPS), Department of Internal Medicine, University of Barcelona, Barcelona, Spain
  • 7Centro de Investigación Biomédica en Red-Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, Spain

Seasonal variation of blood pressure (BP) is a topic in cardiology that has gained more attention throughout the years. Although it is extensively documented that BP increases in seasons coupled with lower temperatures, there are still many gaps in this knowledge field that need to be explored. Notably, seasonal variation of BP phenotypes, such as masked and white coat hypertension, and the impact of air pollution, latitude, and altitude on seasonal variation of BP are still poorly described in the literature, and the levels of the existing evidence are low. Therefore, further investigations on these topics are needed to provide robust evidence that can be used in clinical practice.

1. Introduction

Seasonal variation of blood pressure (BP) is an important topic in cardiology that has gained more relevance throughout the years. In the treatise titled “On Airs, Waters, and Places” (1) Hippocrates had already suggested in 400 BC that to investigate medicine properly, physicians should “in the first place to consider the seasons of the year, and what effects each of them produces”. Rose (2) reported in 1961 the first analysis evidencing the influence of BP fluctuations within the seasons. Since then, several epidemiological studies have shown that cold air stimulation can promote an increase in BP (35). Additionally, clinical trials indicated an association between seasons with lower temperature and greater cardiovascular mortality (6, 7). In 2020, the ESH Working Group on Blood Pressure Monitoring and Cardiovascular Variability published a consensus statement on seasonal variation of BP (8) summarizing the main evidence on this topic so far. They described several interesting aspects of the pathophysiological mechanisms involving temperature and BP, different strategies for measuring the seasonal variation of BP, the prognostic relevance of seasonal BP changes, clinical implications of this association, and final recommendations for clinical practice. However, we would like to raise some other important gaps that still need further investigation and may contribute to a better understanding of seasonal BP variation. In this review, we will discuss the existing knowledge and the gaps about the association of seasonal variation of BP with different hypertension phenotypes, air pollution, latitude, and altitude.

2. Masked hypertension and white-coat hypertension

Hypertension is a major risk factor for cardiovascular events (9, 10) and is usually diagnosed based on office BP measurements. However, due to BP variability, current guidelines have recommended the performance of out-of-office BP measurements besides office BP measurements for a more accurate diagnosis of hypertension (11). The evaluation of office and out-of-office BP in the same subject has revealed that different hypertension phenotypes may exist (11). Sustained hypertension (SH) is usually the most common hypertension phenotype and is coupled with elevated cardiovascular risk (11). Masked hypertension (MH) and white-coat hypertension (WCH) must be also considered, given their high frequency in the population and clinical relevance. MH and WCH may have heterogeneous prevalence in diverse clinical settings and populations, reaching 7%–52% and 9%–54% respectively (12, 13). In this regard, a recent study by Barroso et al. (14) evidenced an expressive rate of misdiagnosis when solely regarding on office BP levels. The authors identified that 20.6% of the participants with an office prehypertension diagnosis had MH, while 27.8% of individuals with office stage-1 hypertension had WCH. Importantly, both MH and WCH are also associated with higher cardiovascular morbidity and mortality when compared with normotension (15).

Because both office BP and out-of-office BP increase in colder seasons, the prevalence of SH is markedly greater in the winter when compared to the summer (8, 16, 17). Conversely, little is known regarding the impact of the seasons on MH and WCH. A post-hoc analysis of the Japan Morning Surge Home Blood Pressure (J-HOP) Study (16) evaluating 4,267 individuals found that MH prevalence was lower in the summer compared to the other seasons [MH odds ratio (OR) winter/summer = 2.36 [95% Confidence Interval (CI) = 1.79–3.10], p < 0.001] while WCH prevalence was higher in the summer, with an OR winter/summer = 0.55 (95% CI = 0.42–0.72; p < 0.001). Likewise, an ambulatory BP monitoring study (18) including 1,075 Japanese patients with chronic kidney disease evidenced that MH was more common in the winter, while WCH was more prevalent in the summer. By contrast, a Chinese study evaluating 649 adolescents assessed by ambulatory BP monitoring reported that both WCH and MH were more frequently detected in the summer (17). Furthermore, Narita et al. (19) found a higher prevalence of nocturnal masked hypertension in the summer among 2,544 Japanese individuals assessed by home BP monitoring. The discrepancies regarding the seasonal variation of hypertension phenotypes reported by the aforementioned studies underscore the need of further studies addressing this topic. In addition, available studies were conducted in Eastern countries and it is not known whether their results may be reproducible in other populations.

3. Air pollution

Another important topic is the impact of air pollution on the seasonal variation of BP (20). Both in- and outdoor air pollution are harmful to the cardiovascular system and may increase the BP (20, 21). However, most of the studies on this topic have focused on the short-term effects of air pollution on BP (22, 23). Air pollutants concentration may vary seasonally, depending on the region (24). Thus, some studies reported seasonal differences in the association of air pollution with all-cause and cardiovascular mortality (2528). Recently, Jin et al. (29) found that environmental ozone was associated with an increased risk of cardiovascular diseases (hazard ratio = 1.0035; 95% CI = 1.0033–1.0037) during the warm months in older Americans.

Air pollutants have been also associated with hospital admissions for hypertension, depending on the climate conditions. Tsai et al. (30) and Chen and Yang (31) found that different air pollutant types were associated with hospitalizations on warm and cool days. Wu et al. (32) conducted a cohort study with young adults and found significant interactions between temperature and air pollution on BP, especially for high air pollution concentrations. The average systolic BP (SBP) change related to a 10°C decrease in temperature for high concentrations of particulate matter with a diameter ≤2.5 μm was 3.6 mmHg (95% CI = 1.9–5.2 mmHg). Similar results were found for organic carbon and nitrogen dioxide, being the average SBP change of 3.3 mmHg (95% CI = 2.0–4.6 mmHg) and 2.8 mmHg (95% CI = 1.6–4.1 mmHg), respectively. A cross-sectional study by Choi et al. (33) also found that summer and winter seasons present correlations of different air pollutants with increased SBP and diastolic BP (DBP) in each season. Fine particulate matter and nitrogen dioxide were associated with BP increase in the warm-weather seasons, while sulfur dioxide and ozone were associated with BP increase in the cold-weather seasons. It is important to note that most of the aforementioned studies were restricted to Easter Asia, which could also limit the external validity of results for other geographical areas with different ethnicities and cultural characteristics. Therefore, further studies about the role and impact of air pollution on BP and its seasonal variability are needed (34).

4. Latitude and altitude

BP may vary differently from geographical areas because of differences in latitude and altitude, given that Earth is a geoid. Few studies evaluated differences in seasonal variation of BP according to latitudes, and most of them assessed the effects of temperature and ultraviolet light (35, 36), as well summarized by Weller et al. (37). Of note, Duranton et al. (35) conducted a study in patients undergoing haemodialysis in different latitudes in Europe and found that individuals on northern latitudes had an attenuated seasonal variation of the BP. Interestingly, the same group (38) found no interaction of different latitudes in the seasonal variation of BP when analysing a different cohort of haemodialysis patients, suggesting that knowledge on this topic is far from be established. It is also noteworthy that a substantial part of the evidence evaluating the impact of latitude on seasonal variation of BP was derived from a specific group of patients (hemodialysis patients) and was conducted in Europe. Furthermore, there is a lack of evidence regarding the effects of geomagnetic activity and gravity on the different latitudes and how they could affect BP in the different seasons.

Altitude is also known to interfere with BP. Tsao et al. (39) conducted a cohort study in Taiwan with a small sample of subjects comparing BP in different altitudes in winter and summer. SBP showed a significant variation between altitudes in winter (120.4 ± 17.6 mmHg at 298 m vs. 136.1 ± 19.3 mmHg at 2,610 m; p < 0.0001), but not in summer (120.7 ± 13.2 mmHg at 298 m vs. 123.6 ± 17.0 mmHg at 2,610 m p = 0.0786). However, DBP variation was significant in both seasons (78.1 ± 11.6 mmHg at 298 m vs. 82.6 ± 10.9 mmHg at 2,610 m p = 0.0096, and 78.9 ± 8.9 mmHg at 298 m vs. 76.2 ± 8.9 mmHg at 2,610 m p = 0.0022, respectively). To our knowledge, this is the only study we found assessing the effects of altitude on the seasonal variation of BP. Therefore, further studies are necessary to establish the impact of altitude on seasonal BP variation.

5. Conclusion

Further investigations are still needed to establish the real impact of seasonal variation of BP on hypertension phenotypes and the role of air pollution, latitude, and altitude on this regard. For all topics, there is an urge for studies with more robust designs—preferably cohorts, using primary datasets (not post-hoc analyses), with larger sample sizes, and evaluating broader populations with different ethnicities and cultural characteristics. Hypertension and BP involve the individual’s intrinsic and extrinsic characteristics. Genetic propensity combined with behavioral and environmental factors may result in a predisposition to developing hypertension (40). For that reason, it is important to assess different ethnicities (genetic pools), cultures (dietary intake and other behavioral factors), and geographical areas in studies evaluating BP, especially seasonal variations of BP.

As Hippocrates has written in “On Airs, Waters, and Places” (1), it is crucial to understand the environmental factors underlying and associated with diseases. In the case of BP and hypertension, the environment plays a very important role, and, once physicians understand better these aspects, patients will be benefited from more individualized treatments and management.

Author contributions

EB conceived the manuscript idea. EB, GF and CB reviewed the literature and wrote the manuscript. WN, AC and MC participated in the design and reviewed the manuscript for intellectual content. All authors contributed to the article and approved the submitted version.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The handling editor PL-J declared a past co-authorship with the authors MC, AC.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

1. Hippocrates of Kos. On airs, waters, and places (classics revisited—400 BCE). Hygeia—Revista Brasileira de Geografia Médica e da Saúde. (2006) 2:1–14. doi: 10.14393/Hygeia2168602

CrossRef Full Text | Google Scholar

2. Rose G. Seasonal variation in blood pressure in man. Nature. (1961) 189:235. doi: 10.1038/189235a0

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Brennan PJ, Greenberg G, Miall WE, Thompson SG. Seasonal variation in arterial blood pressure. Br Med J (Clin Res Ed). (1982) 285:919–23. doi: 10.1136/bmj.285.6346.919

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Alpérovitch A, Lacombe J-M, Hanon O, Dartigues J-F, Ritchie K, Ducimetière P, et al. Relationship between blood pressure and outdoor temperature in a large sample of elderly individuals: the three-city study. Arch Intern Med. (2009) 169:75–80. doi: 10.1001/archinternmed.2008.512

CrossRef Full Text | Google Scholar

5. Chen R, Lu J, Yu Q, Peng L, Yang D, Wang C, et al. The acute effects of outdoor temperature on blood pressure in a panel of elderly hypertensive patients. Int J Biometeorol. (2015) 59:1791–7. doi: 10.1007/s00484-015-0987-9

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Marti-Soler H, Gonseth S, Gubelmann C, Stringhini S, Bovet P, Chen PC, et al. Seasonal variation of overall and cardiovascular mortality: a study in 19 countries from different geographic locations. PLoS One. (2014) 9:e113500. doi: 10.1371/journal.pone.0113500

PubMed Abstract | CrossRef Full Text | Google Scholar

7. Yang L, Li L, Lewington S, Guo Y, Sherliker P, Bian Z, et al. Outdoor temperature, blood pressure, and cardiovascular disease mortality among 23 000 individuals with diagnosed cardiovascular diseases from China. Eur Heart J. (2015) 36:1178–85. doi: 10.1093/eurheartj/ehv023

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Stergiou GS, Palatini P, Modesti PA, Asayama K, Asmar R, Bilo G, et al. Seasonal variation in blood pressure: evidence, consensus and recommendations for clinical practice. Consensus statement by the European society of hypertension working group on blood pressure monitoring and cardiovascular variability. J Hypertens. (2020) 38:1235–43. doi: 10.1097/HJH.0000000000002341

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Nadruz W Jr, Claggett B, Henglin M, Shah AM, Skali H, Rosamond WD, et al. Racial disparities in risks of stroke. N Engl J Med. (2017) 376:2089–90. doi: 10.1056/NEJMc1616085

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Nadruz W Jr, Claggett B, Henglin M, Shah AM, Skali H, Rosamond WD, et al. Widening racial differences in risks for coronary heart disease. Circulation. (2018) 137:1195–7. doi: 10.1161/CIRCULATIONAHA.117.030564

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 practice guidelines for the management of arterial hypertension of the European society of hypertension and the European society of cardiology: ESH/ESC task force for the management of arterial hypertension. J Hypertens. (2018) 36:2284–309. doi: 10.1097/HJH.0000000000001961

PubMed Abstract | CrossRef Full Text | Google Scholar

12. Feitosa ADM, Mota-Gomes MA, Barroso WS, Miranda RD, Barbosa ECD, Brandão AA, et al. The impact of changing home blood pressure monitoring cutoff from 135/85 to 130/80 mmHg on hypertension phenotypes. J Clin Hypertens. (2021) 23:1447–51. doi: 10.1111/jch.14261

CrossRef Full Text | Google Scholar

13. Gorostidi M, Vinyoles E, Banegas JR, De La Sierra A. Prevalence of white-coat and masked hypertension in national and international registries. Hyperten Res. (2015) 38:1–7. doi: 10.1038/hr.2014.149

CrossRef Full Text | Google Scholar

14. Barroso WKS, Feitosa ADM, Barbosa ECD, Miranda RD, Brandão AA, Vitorino PVO, et al. Prevalence of masked and white-coat hypertension in pre-hypertensive and stage 1 hypertensive patients with the use of TeleMRPA. Arq Bras Cardiol. (2019) 113:970–5. doi: 10.5935/abc.20190147

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Stergiou GS, Asayama K, Thijs L, Kollias A, Niiranen TJ, Hozawa A, et al. Prognosis of White-Coat and masked hypertension. Hypertension. (2014) 63:675–82. doi: 10.1161/HYPERTENSIONAHA.113.02741

PubMed Abstract | CrossRef Full Text | Google Scholar

16. Narita K, Hoshide S, Fujiwara T, Kanegae H, Kario K. Seasonal variation of home blood pressure and its association with target organ damage: the J-hop study (Japan morning surge-home blood pressure). Am J Hypertens. (2020) 33:620–8. doi: 10.1093/ajh/hpaa02

PubMed Abstract | CrossRef Full Text | Google Scholar

17. Zhou Y, Zhao L, Meng X, Cai QJ, Zhao XL, Zhou XL, et al. Seasonal variation of ambulatory blood pressure in Chinese hypertensive adolescents. Front Pediatr. (2022) 10:1022865. doi: 10.3389/fped.2022.1022865

PubMed Abstract | CrossRef Full Text | Google Scholar

18. Iimuro S, Imai E, Watanabe T, Nitta K, Akizawa T, Matsuo S, et al. Clinical correlates of ambulatory BP monitoring among patients with CKD. Clin J Am Soc Nephrol. (2013) 8:721–30. doi: 10.2215/CJN.06470612

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Narita K, Hoshide S, Kanegae H, Kario K. Seasonal variation in masked nocturnal hypertension: the J-HOP nocturnal blood pressure study. Am J Hypertens. (2021) 34:609–18. doi: 10.1093/ajh/hpaa193

PubMed Abstract | CrossRef Full Text | Google Scholar

20. van de Borne P. Airborne pollution: a ubiquitous and growing cardiovascular risk factor. e-J Cardiol Pract. (2022) 22:19.

Google Scholar

21. Ramos PM. Air pollution: a new risk factor for cardiovascular disease. e-J Cardiol Pract. (2022) 22:20.

Google Scholar

22. Choi Y-J, Kim S-H, Kang S-H, Kim S-Y, Kim O-J, Yoon C-H, et al. Short-term effects of air pollution on blood pressure. Sci Rep. (2019) 9:20298. doi: 10.1038/s41598-019-56413-y

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Huang W, Wang L, Li J, Liu M, Xu H, Liu S, et al. Short-term blood pressure responses to ambient fine particulate matter exposures at the extremes of global air pollution concentrations. Am J Hypertens. (2018) 31:590–9. doi: 10.1093/ajh/hpx216

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Brook RD, Rajagopalan S, Pope CA, Brook JR, Bhatnagar A, Diez-Roux AV, et al. Particulate matter air pollution and cardiovascular disease. Circulation. (2010) 121:2331–78. doi: 10.1161/CIR.0b013e3181dbece1

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Peng RD, Dominici F, Pastor-Barriuso R, Zeger SL, Samet JM. Seasonal analyses of air pollution and mortality in 100 US cities. Am J Epidemiol. (2005) 161:585–94. doi: 10.1093/aje/kwi075

PubMed Abstract | CrossRef Full Text | Google Scholar

26. Bell ML, Ebisu K, Peng RD, Walker J, Samet JM, Zeger SL, et al. Seasonal and regional short-term effects of fine particles on hospital admissions in 202 US counties, 1999–2005. Am J Epidemiol. (2008) 168:1301–10. doi: 10.1093/aje/kwn252

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Kettunen J, Lanki T, Tiittanen P, Aalto PP, Koskentalo T, Kulmala M, et al. Associations of fine and ultrafine particulate air pollution with stroke mortality in an area of low air pollution levels. Stroke. (2007) 38:918–22. doi: 10.1161/01.STR.0000257999.49706.3b

PubMed Abstract | CrossRef Full Text | Google Scholar

28. Rajagopalan S, Al-Kindi SG, Brook RD. Air pollution and cardiovascular disease: JACC state-of-the-art review. J Am Coll Cardiol. (2018) 72:2054–70. doi: 10.1016/j.jacc.2018.07.099

PubMed Abstract | CrossRef Full Text | Google Scholar

29. Jin T, Di Q, Réquia WJ, Danesh Yazdi M, Castro E, Ma T, et al. Associations between long-term air pollution exposure and the incidence of cardiovascular diseases among American older adults. Environ Int. (2022) 170:107594. doi: 10.1016/j.envint.2022.107594

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Tsai S-S, Tsai C-Y, Yang C-Y. Fine particulate air pollution associated with increased risk of hospital admissions for hypertension in a tropical city, Kaohsiung, Taiwan. J Toxicol Environ Health A. (2018) 81:567–75. doi: 10.1080/15287394.2018.1460788

PubMed Abstract | CrossRef Full Text | Google Scholar

31. Chen C-C, Yang C-Y. Association between gaseous air pollution and hospital admissions for hypertension in Taipei, Taiwan. J Toxicol Environ Health A. (2018) 81:53–9. doi: 10.1080/15287394.2017.1395573

PubMed Abstract | CrossRef Full Text | Google Scholar

32. Wu S, Deng F, Huang J, Wang X, Qin Y, Zheng C, et al. Does ambient temperature interact with air pollution to alter blood pressure? A repeated-measure study in healthy adults. J Hypertens. (2015) 33:2414–21. doi: 10.1097/HJH.0000000000000738

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Choi J-H, Xu Q-S, Park S-Y, Kim J-H, Hwang S-S, Lee K-H, et al. Seasonal variation of effect of air pollution on blood pressure. J Epidemiol Community Health. (1978). (2007) 61:314–8. doi: 10.1136/jech.2006.049205

CrossRef Full Text | Google Scholar

34. Brauer M, Casadei B, Harrington RA, Kovacs R, Sliwa K, Group the WHFAPE. Taking a stand against air pollution—the impact on cardiovascular disease: a joint opinion from the world heart federation, American college of cardiology, American heart association, and the European society of cardiology. Eur Heart J. (2021) 42:1460–3. doi: 10.1093/eurheartj/ehaa1025

PubMed Abstract | CrossRef Full Text | Google Scholar

35. Duranton F, Kramer A, Szwarc I, Bieber B, Gayrard N, Jover B, et al. Geographical variations in blood pressure level and seasonality in hemodialysis patients. Hypertension. (2018) 71:289–96. doi: 10.1161/HYPERTENSIONAHA.117.10274

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Rostand SG. Ultraviolet light may contribute to geographic and racial blood pressure differences. Hypertension. (1997) 30:150–6. doi: 10.1161/01.HYP.30.2.150

PubMed Abstract | CrossRef Full Text | Google Scholar

37. Weller RB, Feelisch M, Kotanko P. Correspondence on ‘seasonal variation in blood pressure: evidence, consensus and recommendations for clinical practice. Consensus statement by the ESH working group on blood pressure monitoring and cardiovascular variability’. J Hypertens. (2020) 38:2077–9. doi: 10.1097/HJH.0000000000002593

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Duranton F, Palma A, Stegmayr B, Wauthier M, Torres A, Argilés A. Blood pressure seasonality in hemodialysis patients from five European cities of different latitudes. Kidney Blood Press Res. (2018) 43:1529–38. doi: 10.1159/000494019

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Tsao T-M, Hwang J-S, Tsai M-J, Lin S-T, Wu C, Su T-C. Seasonal effects of high-altitude forest travel on cardiovascular function: an overlooked cardiovascular risk of forest activity. Int J Environ Res Public Health. (2021) 18:9472. doi: 10.3390/ijerph18189472

PubMed Abstract | CrossRef Full Text | Google Scholar

40. Brook RD, Weder AB, Rajagopalan S. “Environmental hypertensionology” the effects of environmental factors on blood pressure in clinical practice and research. J Clin Hypertens. (2011) 13:836–42. doi: 10.1111/j.1751-7176.2011.00543.x

CrossRef Full Text | Google Scholar

Keywords: blood pressure, seasonal variation, masked hypertension, white coat hypertension, air pollution, altitude, environment

Citation: Barbosa ECD, Farina GS, Basso CS, Camafort M, Coca A and Nadruz W (2023) Seasonal variation in blood pressure: what is still missing?. Front. Cardiovasc. Med. 10:1233325. doi: 10.3389/fcvm.2023.1233325

Received: 1 June 2023; Accepted: 1 August 2023;
Published: 11 August 2023.

Edited by:

Patricio López-Jaramillo Universidad de Santander (UDES), Colombia

Reviewed by:

Diego Chemello, Federal University of Santa Maria, Brazil

© 2023 Barbosa, Farina, Basso, Camafort, Coca and Nadruz. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Eduardo Costa Duarte Barbosa edubarbosa@terra.com.br

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.