0315/2024 - Relationship between salt and blood pressure in indigenous and non-indigenous populations
Relação entre sal e pressão arterial em populações indígenas e não indígenas
Autor:
• Aline Silva Porto - Porto, A.S - <alineportonutri@gmail.com>ORCID: https://orcid.org/0000-0002-4780-3228
Coautor(es):
• Ludimila Forechi - Forechi, L. - <ludimilaforechi@yahoo.com.br>ORCID: https://orcid.org/0000-0002-6657-0503
• Maria Del Carmen Bisi Molina - Molina, M.D.C.B - <mdcarmen2007@gmail.com>
ORCID: https://orcid.org/0000-0002-8614-988X
• José Geraldo Mill - Mill, J.G - <josegmill@gmail.com, polyanaromano@hotmail.com>
ORCID: http://orcid.org/0000-0002-0987-368X
Resumo:
Objective: Was to compare the impact of salt consumption on blood pressure of an indigenous and of a non-indigenous population in Brazil. Design: The studies were carried out in a racial mixed (white, black and brown) urban population of Vitória (n=1.663), the capital of Espírito Santo State, and in the indigenous population settled in the indigenous reserve of Aracruz (n=663), in the same state. Salt consumption was evaluated by a 12-hour overnight urine collect and BP was measured in visit to University Hospital (in the Vitória study) or in a visit to health facility attending to the indigenous population of the reserve. Results: Salt consumption mean ± sd was very high (13.4 ± 5.9 g/day vs.11.8 ± 5.9 g/day; P<0.001), respectively, in indigenous and non-indigenous population. Even considering that BP levels were lower in the indigenous group (118/75 mmHg) the BP response to the salt consumption was almost the five times higher in non-indigenous group, that is, the slope of the systolic BP in the non-indigenous was higher than in the indigenous (?=0.49 ± 3.42) vs. non-indigenous: (?=1.0 ±3.97; P=0.01). The same was observed for diastolic BP (0.58 ± 2.18 vs. non-indigenous: 0.81 ± 2.72; P=0.1). Conclusion: The low sensitivity to salt consumption could partly explain the higher values of salt consumption by the indigenous population.
Palavras-chave:
salt, urine, blood pressure, indigenous population, urban populationAbstract:
Objetivo: Comparar o impacto do consumo de sal na pressão arterial de uma população indígena e não indígena no Brasil. Metodologia: Os estudos foram realizados em uma população urbana mestiça (branca, preta e parda) de Vitória (n=1.663), capital do estado do Espírito Santo, e na população indígena assentada na reserva indígena de Aracruz (n= 663), no mesmo estado. O consumo de sal foi avaliado por meio de coleta de urina noturna de 12 horas e aferição da PA em visita ao Hospital Universitário (no estudo Vitória) ou em visita a unidade de saúde que atende a população indígena da reserva. Resultados: A média ± dp do consumo de sal foi muito alta (13,4 ± 5,9 g/dia vs. 11,8 ± 5,9 g/dia; P<0,001), respectivamente, na população indígena e não indígena. Mesmo considerando que os níveis pressóricos foram menores no grupo indígena (118/75 mmHg), a resposta da PA ao consumo de sal foi quase cinco vezes maior no grupo não indígena, ou seja, a inclinação da PA sistólica nos não indígenas foi maior que nos indígenas (β=0,49 ± 3,42) vs. não indígenas: (β=1,0 ±3,97; P=0,01). O mesmo foi observado para PA diastólica (0,58 ± 2,18 vs. não indígenas: 0,81 ± 2,72; P=0,1). Conclusão: A baixa sensibilidade ao consumo de sal pode explicar em parte os valores mais elevados de consumo de sal pela população indígena.Keywords:
sal, urina, pressão arterial, população indígena, população urbanaConteúdo:
Introduction
Chronic Non-comunicable Diseases (NCDs) are the leading causes of morbidity and mortality worldwide burden, accounting with 63% of deaths globally and 72% in Brazil1.Cardiovascular diseases are the leading cause of mortality around the world and arterial hypertension (AH) is the most important risk factor for cardiovascular deaths2. The development of high blood pressure depends of a large number of factors, including non-modifiable (genetic traits, sex and age) and modifiable lifestyle-related risk factors such as smoking, excessive consumption of alcoholic beverages, and high sodium intake3-5.
Salt consumption is high all over the world, including the indigenous populations that adopted nutrition habits similar to those occurring in the general population6. The Intersalt Cooperative Research Group, showed that the range of salt consumption varied widely from 0.2 mmol/day (that is, less than 1 g/day of salt) to 234 mmol/day (equivalent to 14 g/day of salt). Additionally, the INTERSALT study demonstrated the existence of a linear relationship between the mean salt intake of each population and mean values of blood pressure7. The World Health Organization suggests a daily intake of sodium of 2 g, equivalent to 5 g of table salt8. Several studies have investigated salt consumption in Brazilians, showing values almost twice this recommendation. In a representative sample of the adult Brazilian population, salt consumption was estimated to be around 9.34 g/day9. Studies in specific groups such as in a quilombola populations, 11.5 g/day consumption was measured10 while in a indigenous group established in an indigenous reserve in Espírito Santo State a mean consumption of 13.7 ± 7.1 g/day was observed from an overnight 12 hours (12-h) urine collect6. Native Brazilian populations did not use salt in the cooking process and the prevalence of AH was almost absent11. Over the years, westernization of the eating habits of the several indigenous populations living in Brazil may have influenced the progressive increase of blood pressure levels and development of AH. However, the relationship between salt intake and blood pressure seem to show some differences among indigenous group since in the study of Meyerfreund et al.6 (2009) the prevalence AH was quite different in two indigenous populations living in the north coast of Espírito Santo State despite similar salt intake according to an overnight urine collect.
The Intersalt Study showed a positive and linear relationship between 24-hour sodium excretion and systolic blood pressure (SBP) across different populations of five continents7. The indigenous populations included in this study did not add salt in the food preparing process and showed a flattened relationship between age, and blood pressure suggesting that the age-dependent SBP increase would be dependent of the excessive sodium intake. However, comparative studies of high salt diets on blood pressure levels of indigenous and non indigenous populations with similar dietary habits related to salt consumption remains to be determined. Therefore, the aim of this study was to compare the relationship between salt consumption and blood pressure in an indigenous population living in a reserve with an urban and racially mixed population.
Material and Methods
Populations and samples
Data were collected in two cross-sectional studies. The first, in a representative sample of the urban population (25-64 years old) of Vitória, the capital of Espírito Santo State and the second in adults (>20 years old) of an indigenous population living in a reserve in Aracruz, north coast of the same state. In Vitória, the data were collected in a representative sample of households (N = 1.663; 1999-2001), selected by a random sample of domiciles12. In the indigenous reserve, all subjects (>20 years) were invited. From an eligible population of 834 subjects, 663 (79.5%) attended to the project for data collection (2003-2004)6. Both studies were designed to investigate the prevalence and severity of cardiovascular risk factors and were approved by the national and institutional ethics committees. All data were collected following international rules in according with the Declaration of Helsinki.
Research protocols were similar in both studies and participants were invited to attend to the University Hospital (urban population of Vitória) or to the Health Unit of the indigenous reserve in a pre-scheduled day. Sociodemographic characteristics (sex, age, schooling, self reported race/ethnicity) and habits (smoking and alcohol intake) were collected by questionnaires during the visit. Blood sample was collected in fasting condition. All other data were obtained by specific exams during the same visit. All participants were asked to avoid strenuous physical exercise and to not to drink alcohol in the 24 h previous to exams.
Anthropometry
Body weight (kg), and height (cm) were collected while the participants were fasting, barefoot and in light clothes using an electronic scale (precision of 0.1 kg) and a wall mounted stadiometer (precision of 0.5 cm). Weight classification was based on body mass index (BMI), calculated as the ratio between weight (Kg) to the squared height (m). Subjects were classified as eutrophic (BMI < 25kg/m2), overweight (BMI ? 25.0 - 29.9 kg/m2) or obese (BMI ? 30 kg/m2).
Blood pressure
Resting systolic and diastolic blood pressures (SBP, DBP) were measured in the left arm in sitting position after a rest period of 5 min. Three readings with 5-10 min intervals were obtained in each subject by using an oscilometric automatic device (Onrom 705CP, Japan). Clinical blood pressure was determined as the mean of the last two measurements. Subjects were classified as hypertensive if blood pressure was ?140/90 mmHg or in use of anti-hipertensive drugs, including diuretics.
Salt consumption
Participants in both studies received previous instructions for an overnight 12-h overnight urine collection in the evening of the clinic visit. Individuals were asked to void as nearly as possible of 7:00 pm in the night before exams. From this moment they were orientated to collect all urine in a plastic bottle (2 liters volume) and to proceed the last collect around 7:00 am next day. The exact time of the last urine void and last collect in the bottle should be annotated in a form in order to calculate the exact interval of urine collect. In the indigenous community the urine collect was guided by trained health professionals attending local health facilities. When arriving at the local of exams (University Hospital in Vitória or the local health facility in the indigenous reserve) the bottle was delivered to a research assistant to determine the period of urine collect and to measure urine volume in a graduated cylinder with 10 mL precision. A sample (5 mL) was separated and sent to a central laboratory (SESC-Vitória) to sodium and potassium dosage. Urinary flow (mL/min) was measured by dividing total urinary volume by the period of urinary collect. Urine collect was considered valid if the volume was ?250 mL and with no report of urine lost13. The daily sodium intake was estimated from the 12-h urinary sodium excretion according to a validation study of our group showing that nearly 47% of the 24-h sodium excretion is found in the 12-h overnight urine sample14. Salt consumption (g/day) was calculated considering that all urinary sodium comes from NaCl ingestion.
Statistical analysis
Data were shown as means and standard deviations or in absolute frequencies and percentages. The goodness-to-fit to a Gaussian distribution was verified by the Kolmogorov-Smirnov test. Differences between groups were assessed using the students t test for independent samples. The chi-square test was applied for categorical variables. The association between blood pressure and urinary sodium excretion (Ur-Na) was performed using Pearson's coefficient, and a multivariate linear regression model was used to test the dependence of blood pressure on sodium excretion, adjustment by two covariates in this order: age and BMI. All statistical analyses were performed using SPSS 22.0 Statistical Package (SPSS, Chicago, IL). Statistical significance was set at P < 0.05.
Results
From the indigenous population (N=663) we removed from this analysis 33 who did not collected 12-h urine, 17 with 12-h urine <250 mL, 18 with implausible salt consumption (? 30g/day), and 15 without data of blood pressure, serum creatinine, or body weight. Others 61 were removed because they were in use of anti-hypertensive drugs, remaining 526 participants in the analysis.
From the 1.663 non indigenous participants recruited in the Vitória, we removed from the analysis 10 without urine collect, 45 with 12-h urine volume <250 mL 50 with implausible salt consumption (? 30g/day) and others 25 without data of blood pressure, creatinine or body weight. Others 254 were removed because they were in use of antihipertensive drugs, remaining 1.279 participants in the analysis.
The socio-demographic characteristics of the two samples are shown in Table 1.
[Table 1 near here]
The sex distribution was similar in both groups and the indigenous group showed lower schooling levels and excessive fat accumulation (overweight and obesity was less prevalent: (51.9% vs 44.7%; p<0.05). Regular smoking was similar in the two groups. Hypertension, however, was less frequent in the indigenous population (18.1% vs 29.3%; p<0.01).
[Table 2 near here]
Table 2 shows anthropometric, clinical and biochemical characteristics of the groups. The indigenous group was around seven years younger than the urban one. BMI was slightly lower in indigenous, while blood pressure, cholesterol, triglicerydes, glycemia, creatinine and uric acid also showed lower values in indigenous as compared to the non-indigenous. High density lipoprotein showed an opposite picture being higher in indigenous, however.
[Table 3 near here]
The general characteristics of the 12-h urine are shown in Table 3. The indigenous group produced a urine with smaller volume (around 14% less) but with higher sodium concentration (154 vs 128 mmol/L; p<0.001). Concentration of creatinine was similar in both groups, so that the ratio of sodium to creatinine was also higher in indigenous. The sodium to potassium ratio was higher in indigenous group (6.7 vs 4.9 mmol/mmol) and much above the actual recommendations (~1) in the two groups. The calculated 12-h sodium excretion as well as the estimated salt consumption were both higher in the indigenous group as compared the non-indigenous one (13.4 ± 5.9 vs 11.8 ±5.9 g/day; p<0.01).
[Table 4 near here]
The relationship between systolic and diastolic blood pressure as a function of salt consumption is shown in Table 4. The scatter plots show that indigenous with a very high salt intake (>15 g/day) showed lower systolic and diastolic blood pressure values as compared with the non-indigenous subjects with similar salt consumption. Linear trends between salt intake and blood pressures (systolic and diastolic) were moderate (r=0.41 and r=0.39 but significant (p<0.01) in non-indigenous and the same was found for indigenous groups (r=0.52 and r=0.45; (p<0.01).
[Figure 1 near here]
The slopes of the curves were five times higher na systolic blood pressure in indigenous as compared to the non-indigenous group (p=0.01), as shown in Figure 2. The values for indigenous people are as follows: (?=0.49 ± 3.42 sd) vs. non-indigenous: (?=1.0 ±3.97 sd); P=0.01). The same was observed for diastolic BP (?=0.58 ± 2.18 sd vs. non-indigenous: ?=0.81 ± 2.72; p=0.1, although not statistically significant.
Discussion
In this study, we observed that salt consumption was quite high in almost all subjects where this variable was investigated, independent of the group, that is, either the urban population as the indigenous population showed a very high sodium content in their diet, irrespective to ethnicity. Regarding to blood pressure, we observed a linear trend between the estimated salt consumption and SBP. The degree of associated, however, was weak for both groups despite a lower increment (mmHg/g of daily salt intake) observed in indigenous people. The lower influence of salt intake in blood pressure may partially explain lower blood pressure levels in indigenous subject as well as the lower prevalence of hypertension, even after age adjustment. In both groups, the influence of salt intake in DBP was more evident than for SBP.
Assessment of sodium intake, however, is not easy when tested in large number subjects. The gold standard method is the 24-h urine collect. However, there are serious inconveniences of this procedure when used in the general population because subjects are generally outside their homes along the day. Therefore, our group developed several studies to validate the overnight 12-h urine collect to estimate salt consumption and our studies to validate the 12-h overnight urine collect as an alternative method to estimate salt intake. In one of these studies14 the overnight 12-h urine comprised 47% of the 24-h urine, a value that was confirmed in a larger study in the general population of Vitória15. In this noteworthy that 12-h overnight urine collect has been currently being used in other studies in different populations16,17. Several criteria were used to consider a timed urine collect as 'valid', causing a loss of about 10% participants in the two studies presente in this study, a value lower that it was usual when other methods to evaluate salt consumption, such as 24-h recall and food diary) are used17-19.
To investigate the relationship between salt consumption and blood pressure we also removed from the analysis all subjects in use of antihipertensive drugs, including diuretics, because these drugs would be an important confounder to determinate the association between these two variables. More important, we used the same methods to collect and process the urine and blood pressure data. Therefore, data of these two populations can be compared without important bias interfering in the results.
We observed that in both populations the salt consumption is high and quite above the WHO-recommendations of 5 g/day. Similar results have been obtained in other studies in Brazil as well in populations of other countries. In a previous analysis of the data of this same study, Meyerfreund et al.6 (2009), related that the salt intake was similar in the three different groups (Guarani, Tupinikin and non-indigenous (11.7 ± 5.3 g/day; 13.7 ± 7.2 g/day and 14.2±7.2 g/day; P>0.05, respectively.
The relationship between salt intake and blood pressure is well established in the literature20-23. However, to date this is the first study to compare the impact of sodium intake with blood pressure in two populations with a high and similar pattern of salt intake but with different ancestry. We discuss here some possible causes for the lower impact of sodium on the blood pressure of the indigenous, even with the high salt intake observed in this group.
First point should be the Pulse Wave Velocity (PWV), a physiological hypothesis could be a lower pressure reactivity, thus resulting in lower blood pressure, this fact was seen in the study evaluating an association between PWV, blood pressure reactivity and ethnicity in the Brazilian population of African descent thats is this structural modification of the vessel could be caused by low blood pressure levels in African descent individuals24.
Another point to considerer seems to be the issue of salt sensibility in indians when to compare non-indigenous populations. A possible explanation go this finding may be related to the pressoric diuresis phenomenon which may be more effective in indigenous than in the non indigenous people25-27. However, experimental studies should be performed to confirm this hypothesis.
Other aspect to be considered is the impact of overweight/obesity on blood pressure. Recent population studies have demonstrated the relationship between high salt intake in adults, obesity and arterial hypertension28-29, but this fact does not seem to be supported in our study, since the prevalence of diabetes is low in this population and seems to be unrelated to arterial hypertension.
Our study has some limitations. First, point is that the 24-hour urinary excretion was not used, which is considered the gold standard, despite that, the 12-hour urinary collection was used, which has high reproducibility and sensitivity, and can be used in populations of Vitória, Espírito Santo, because it has a formula validated here in Brazil14,19.
Second, the use of hypertensive or lipidlowering drugs could bring some confusion, since we do not know if the the diagnosis was correctly made before the study or if the use of such medications. Nevertheless, the non-indigenous and indigenous group, diastolic and Systolic blood pressure was not influenced by the use of antihypertensive group drugs. In addition, data collection was performed at different times, but this in no way invalidates the study, as the urine data collections were similar to each other and followed reliable urine losses. Finally, even though statistical adjustments have been made, the population samples were nor matched for age, salt and IMC important variables that could affect blood pressure and potentially confound our observations.
This is a pioneering population study with the aim of verifying the relationship between salt level and blood pressure in both populations. It should be noted that in all verifications, possible collection errors were eliminated from the sample, and urine collection seems to be quite robust given the minimum percentage of collection losses (20.3 and 23% of urinary losses in the indigenous and urban population); In addition, all researchers who participated in the studies were duly trained and certified to administer the questionnaires, instruction urine handling, storage in an adequate and safe place and blood pressure equipment were calibrated according to the season.
It is noteworthy that the collection of urine from the indigenous population was collected in loco in order to preserve the characteristics of the sample. Finally, this is a population-based community observational study, with a cross-sectional approach being obtained and it is not possible to establish a causal relationship, only an inference relationship, which is expected for cross-sectional studies.
Conclusion
There was a linear trend of a 5-fold increase in systolic blood pressure, and salt and almost 2-fold for diastolic blood pressure and salt, both observed for the indigenous population versus non-indigenous. Low sensitivity to salt consumption could partially explain the lower blood pressure values in the indigenous population as compared to the racially mixed population of Vitória.
Acknowledgments
We thank, first of all, all study participants who were willing to perform the 12-hour urine collection and voluntarily participate in the research. This study was funded by a scholarship from the Higher Education Personnel Improvement Coordination (CAPES) with the aid of a research grant from FEST Federal University of Espírito Santo (UFES).
Disclosure statement
No potential conflict of interest was reported by the author(s).
Funding
This work was supported by Fapes-CNPq/PRONEX (No. 24/2018) and CNPq (No. 302518/2019-3).
References
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Chronic Non-comunicable Diseases (NCDs) are the leading causes of morbidity and mortality worldwide burden, accounting with 63% of deaths globally and 72% in Brazil1.Cardiovascular diseases are the leading cause of mortality around the world and arterial hypertension (AH) is the most important risk factor for cardiovascular deaths2. The development of high blood pressure depends of a large number of factors, including non-modifiable (genetic traits, sex and age) and modifiable lifestyle-related risk factors such as smoking, excessive consumption of alcoholic beverages, and high sodium intake3-5.
Salt consumption is high all over the world, including the indigenous populations that adopted nutrition habits similar to those occurring in the general population6. The Intersalt Cooperative Research Group, showed that the range of salt consumption varied widely from 0.2 mmol/day (that is, less than 1 g/day of salt) to 234 mmol/day (equivalent to 14 g/day of salt). Additionally, the INTERSALT study demonstrated the existence of a linear relationship between the mean salt intake of each population and mean values of blood pressure7. The World Health Organization suggests a daily intake of sodium of 2 g, equivalent to 5 g of table salt8. Several studies have investigated salt consumption in Brazilians, showing values almost twice this recommendation. In a representative sample of the adult Brazilian population, salt consumption was estimated to be around 9.34 g/day9. Studies in specific groups such as in a quilombola populations, 11.5 g/day consumption was measured10 while in a indigenous group established in an indigenous reserve in Espírito Santo State a mean consumption of 13.7 ± 7.1 g/day was observed from an overnight 12 hours (12-h) urine collect6. Native Brazilian populations did not use salt in the cooking process and the prevalence of AH was almost absent11. Over the years, westernization of the eating habits of the several indigenous populations living in Brazil may have influenced the progressive increase of blood pressure levels and development of AH. However, the relationship between salt intake and blood pressure seem to show some differences among indigenous group since in the study of Meyerfreund et al.6 (2009) the prevalence AH was quite different in two indigenous populations living in the north coast of Espírito Santo State despite similar salt intake according to an overnight urine collect.
The Intersalt Study showed a positive and linear relationship between 24-hour sodium excretion and systolic blood pressure (SBP) across different populations of five continents7. The indigenous populations included in this study did not add salt in the food preparing process and showed a flattened relationship between age, and blood pressure suggesting that the age-dependent SBP increase would be dependent of the excessive sodium intake. However, comparative studies of high salt diets on blood pressure levels of indigenous and non indigenous populations with similar dietary habits related to salt consumption remains to be determined. Therefore, the aim of this study was to compare the relationship between salt consumption and blood pressure in an indigenous population living in a reserve with an urban and racially mixed population.
Material and Methods
Populations and samples
Data were collected in two cross-sectional studies. The first, in a representative sample of the urban population (25-64 years old) of Vitória, the capital of Espírito Santo State and the second in adults (>20 years old) of an indigenous population living in a reserve in Aracruz, north coast of the same state. In Vitória, the data were collected in a representative sample of households (N = 1.663; 1999-2001), selected by a random sample of domiciles12. In the indigenous reserve, all subjects (>20 years) were invited. From an eligible population of 834 subjects, 663 (79.5%) attended to the project for data collection (2003-2004)6. Both studies were designed to investigate the prevalence and severity of cardiovascular risk factors and were approved by the national and institutional ethics committees. All data were collected following international rules in according with the Declaration of Helsinki.
Research protocols were similar in both studies and participants were invited to attend to the University Hospital (urban population of Vitória) or to the Health Unit of the indigenous reserve in a pre-scheduled day. Sociodemographic characteristics (sex, age, schooling, self reported race/ethnicity) and habits (smoking and alcohol intake) were collected by questionnaires during the visit. Blood sample was collected in fasting condition. All other data were obtained by specific exams during the same visit. All participants were asked to avoid strenuous physical exercise and to not to drink alcohol in the 24 h previous to exams.
Anthropometry
Body weight (kg), and height (cm) were collected while the participants were fasting, barefoot and in light clothes using an electronic scale (precision of 0.1 kg) and a wall mounted stadiometer (precision of 0.5 cm). Weight classification was based on body mass index (BMI), calculated as the ratio between weight (Kg) to the squared height (m). Subjects were classified as eutrophic (BMI < 25kg/m2), overweight (BMI ? 25.0 - 29.9 kg/m2) or obese (BMI ? 30 kg/m2).
Blood pressure
Resting systolic and diastolic blood pressures (SBP, DBP) were measured in the left arm in sitting position after a rest period of 5 min. Three readings with 5-10 min intervals were obtained in each subject by using an oscilometric automatic device (Onrom 705CP, Japan). Clinical blood pressure was determined as the mean of the last two measurements. Subjects were classified as hypertensive if blood pressure was ?140/90 mmHg or in use of anti-hipertensive drugs, including diuretics.
Salt consumption
Participants in both studies received previous instructions for an overnight 12-h overnight urine collection in the evening of the clinic visit. Individuals were asked to void as nearly as possible of 7:00 pm in the night before exams. From this moment they were orientated to collect all urine in a plastic bottle (2 liters volume) and to proceed the last collect around 7:00 am next day. The exact time of the last urine void and last collect in the bottle should be annotated in a form in order to calculate the exact interval of urine collect. In the indigenous community the urine collect was guided by trained health professionals attending local health facilities. When arriving at the local of exams (University Hospital in Vitória or the local health facility in the indigenous reserve) the bottle was delivered to a research assistant to determine the period of urine collect and to measure urine volume in a graduated cylinder with 10 mL precision. A sample (5 mL) was separated and sent to a central laboratory (SESC-Vitória) to sodium and potassium dosage. Urinary flow (mL/min) was measured by dividing total urinary volume by the period of urinary collect. Urine collect was considered valid if the volume was ?250 mL and with no report of urine lost13. The daily sodium intake was estimated from the 12-h urinary sodium excretion according to a validation study of our group showing that nearly 47% of the 24-h sodium excretion is found in the 12-h overnight urine sample14. Salt consumption (g/day) was calculated considering that all urinary sodium comes from NaCl ingestion.
Statistical analysis
Data were shown as means and standard deviations or in absolute frequencies and percentages. The goodness-to-fit to a Gaussian distribution was verified by the Kolmogorov-Smirnov test. Differences between groups were assessed using the students t test for independent samples. The chi-square test was applied for categorical variables. The association between blood pressure and urinary sodium excretion (Ur-Na) was performed using Pearson's coefficient, and a multivariate linear regression model was used to test the dependence of blood pressure on sodium excretion, adjustment by two covariates in this order: age and BMI. All statistical analyses were performed using SPSS 22.0 Statistical Package (SPSS, Chicago, IL). Statistical significance was set at P < 0.05.
Results
From the indigenous population (N=663) we removed from this analysis 33 who did not collected 12-h urine, 17 with 12-h urine <250 mL, 18 with implausible salt consumption (? 30g/day), and 15 without data of blood pressure, serum creatinine, or body weight. Others 61 were removed because they were in use of anti-hypertensive drugs, remaining 526 participants in the analysis.
From the 1.663 non indigenous participants recruited in the Vitória, we removed from the analysis 10 without urine collect, 45 with 12-h urine volume <250 mL 50 with implausible salt consumption (? 30g/day) and others 25 without data of blood pressure, creatinine or body weight. Others 254 were removed because they were in use of antihipertensive drugs, remaining 1.279 participants in the analysis.
The socio-demographic characteristics of the two samples are shown in Table 1.
[Table 1 near here]
The sex distribution was similar in both groups and the indigenous group showed lower schooling levels and excessive fat accumulation (overweight and obesity was less prevalent: (51.9% vs 44.7%; p<0.05). Regular smoking was similar in the two groups. Hypertension, however, was less frequent in the indigenous population (18.1% vs 29.3%; p<0.01).
[Table 2 near here]
Table 2 shows anthropometric, clinical and biochemical characteristics of the groups. The indigenous group was around seven years younger than the urban one. BMI was slightly lower in indigenous, while blood pressure, cholesterol, triglicerydes, glycemia, creatinine and uric acid also showed lower values in indigenous as compared to the non-indigenous. High density lipoprotein showed an opposite picture being higher in indigenous, however.
[Table 3 near here]
The general characteristics of the 12-h urine are shown in Table 3. The indigenous group produced a urine with smaller volume (around 14% less) but with higher sodium concentration (154 vs 128 mmol/L; p<0.001). Concentration of creatinine was similar in both groups, so that the ratio of sodium to creatinine was also higher in indigenous. The sodium to potassium ratio was higher in indigenous group (6.7 vs 4.9 mmol/mmol) and much above the actual recommendations (~1) in the two groups. The calculated 12-h sodium excretion as well as the estimated salt consumption were both higher in the indigenous group as compared the non-indigenous one (13.4 ± 5.9 vs 11.8 ±5.9 g/day; p<0.01).
[Table 4 near here]
The relationship between systolic and diastolic blood pressure as a function of salt consumption is shown in Table 4. The scatter plots show that indigenous with a very high salt intake (>15 g/day) showed lower systolic and diastolic blood pressure values as compared with the non-indigenous subjects with similar salt consumption. Linear trends between salt intake and blood pressures (systolic and diastolic) were moderate (r=0.41 and r=0.39 but significant (p<0.01) in non-indigenous and the same was found for indigenous groups (r=0.52 and r=0.45; (p<0.01).
[Figure 1 near here]
The slopes of the curves were five times higher na systolic blood pressure in indigenous as compared to the non-indigenous group (p=0.01), as shown in Figure 2. The values for indigenous people are as follows: (?=0.49 ± 3.42 sd) vs. non-indigenous: (?=1.0 ±3.97 sd); P=0.01). The same was observed for diastolic BP (?=0.58 ± 2.18 sd vs. non-indigenous: ?=0.81 ± 2.72; p=0.1, although not statistically significant.
Discussion
In this study, we observed that salt consumption was quite high in almost all subjects where this variable was investigated, independent of the group, that is, either the urban population as the indigenous population showed a very high sodium content in their diet, irrespective to ethnicity. Regarding to blood pressure, we observed a linear trend between the estimated salt consumption and SBP. The degree of associated, however, was weak for both groups despite a lower increment (mmHg/g of daily salt intake) observed in indigenous people. The lower influence of salt intake in blood pressure may partially explain lower blood pressure levels in indigenous subject as well as the lower prevalence of hypertension, even after age adjustment. In both groups, the influence of salt intake in DBP was more evident than for SBP.
Assessment of sodium intake, however, is not easy when tested in large number subjects. The gold standard method is the 24-h urine collect. However, there are serious inconveniences of this procedure when used in the general population because subjects are generally outside their homes along the day. Therefore, our group developed several studies to validate the overnight 12-h urine collect to estimate salt consumption and our studies to validate the 12-h overnight urine collect as an alternative method to estimate salt intake. In one of these studies14 the overnight 12-h urine comprised 47% of the 24-h urine, a value that was confirmed in a larger study in the general population of Vitória15. In this noteworthy that 12-h overnight urine collect has been currently being used in other studies in different populations16,17. Several criteria were used to consider a timed urine collect as 'valid', causing a loss of about 10% participants in the two studies presente in this study, a value lower that it was usual when other methods to evaluate salt consumption, such as 24-h recall and food diary) are used17-19.
To investigate the relationship between salt consumption and blood pressure we also removed from the analysis all subjects in use of antihipertensive drugs, including diuretics, because these drugs would be an important confounder to determinate the association between these two variables. More important, we used the same methods to collect and process the urine and blood pressure data. Therefore, data of these two populations can be compared without important bias interfering in the results.
We observed that in both populations the salt consumption is high and quite above the WHO-recommendations of 5 g/day. Similar results have been obtained in other studies in Brazil as well in populations of other countries. In a previous analysis of the data of this same study, Meyerfreund et al.6 (2009), related that the salt intake was similar in the three different groups (Guarani, Tupinikin and non-indigenous (11.7 ± 5.3 g/day; 13.7 ± 7.2 g/day and 14.2±7.2 g/day; P>0.05, respectively.
The relationship between salt intake and blood pressure is well established in the literature20-23. However, to date this is the first study to compare the impact of sodium intake with blood pressure in two populations with a high and similar pattern of salt intake but with different ancestry. We discuss here some possible causes for the lower impact of sodium on the blood pressure of the indigenous, even with the high salt intake observed in this group.
First point should be the Pulse Wave Velocity (PWV), a physiological hypothesis could be a lower pressure reactivity, thus resulting in lower blood pressure, this fact was seen in the study evaluating an association between PWV, blood pressure reactivity and ethnicity in the Brazilian population of African descent thats is this structural modification of the vessel could be caused by low blood pressure levels in African descent individuals24.
Another point to considerer seems to be the issue of salt sensibility in indians when to compare non-indigenous populations. A possible explanation go this finding may be related to the pressoric diuresis phenomenon which may be more effective in indigenous than in the non indigenous people25-27. However, experimental studies should be performed to confirm this hypothesis.
Other aspect to be considered is the impact of overweight/obesity on blood pressure. Recent population studies have demonstrated the relationship between high salt intake in adults, obesity and arterial hypertension28-29, but this fact does not seem to be supported in our study, since the prevalence of diabetes is low in this population and seems to be unrelated to arterial hypertension.
Our study has some limitations. First, point is that the 24-hour urinary excretion was not used, which is considered the gold standard, despite that, the 12-hour urinary collection was used, which has high reproducibility and sensitivity, and can be used in populations of Vitória, Espírito Santo, because it has a formula validated here in Brazil14,19.
Second, the use of hypertensive or lipidlowering drugs could bring some confusion, since we do not know if the the diagnosis was correctly made before the study or if the use of such medications. Nevertheless, the non-indigenous and indigenous group, diastolic and Systolic blood pressure was not influenced by the use of antihypertensive group drugs. In addition, data collection was performed at different times, but this in no way invalidates the study, as the urine data collections were similar to each other and followed reliable urine losses. Finally, even though statistical adjustments have been made, the population samples were nor matched for age, salt and IMC important variables that could affect blood pressure and potentially confound our observations.
This is a pioneering population study with the aim of verifying the relationship between salt level and blood pressure in both populations. It should be noted that in all verifications, possible collection errors were eliminated from the sample, and urine collection seems to be quite robust given the minimum percentage of collection losses (20.3 and 23% of urinary losses in the indigenous and urban population); In addition, all researchers who participated in the studies were duly trained and certified to administer the questionnaires, instruction urine handling, storage in an adequate and safe place and blood pressure equipment were calibrated according to the season.
It is noteworthy that the collection of urine from the indigenous population was collected in loco in order to preserve the characteristics of the sample. Finally, this is a population-based community observational study, with a cross-sectional approach being obtained and it is not possible to establish a causal relationship, only an inference relationship, which is expected for cross-sectional studies.
Conclusion
There was a linear trend of a 5-fold increase in systolic blood pressure, and salt and almost 2-fold for diastolic blood pressure and salt, both observed for the indigenous population versus non-indigenous. Low sensitivity to salt consumption could partially explain the lower blood pressure values in the indigenous population as compared to the racially mixed population of Vitória.
Acknowledgments
We thank, first of all, all study participants who were willing to perform the 12-hour urine collection and voluntarily participate in the research. This study was funded by a scholarship from the Higher Education Personnel Improvement Coordination (CAPES) with the aid of a research grant from FEST Federal University of Espírito Santo (UFES).
Disclosure statement
No potential conflict of interest was reported by the author(s).
Funding
This work was supported by Fapes-CNPq/PRONEX (No. 24/2018) and CNPq (No. 302518/2019-3).
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