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Effect of a high-protein diet on maintenance of blood pressure levels achieved after initial weight loss: the DiOGenes randomized study

Abstract

Randomized trials have shown significant blood pressure (BP) reductions after increased protein compared with carbohydrate intake, but the effect on BP maintenance after initial weight loss is unclear. We examined the effect of a high-protein diet on the maintenance of reduced BP after weight loss in 420 overweight adults from the Diet, Obesity and Genes study. After an 8-week weight-loss period (>8% BW), subjects (42±6 years) were randomized to either a high-protein diet (23–28 en% protein) or a lower-protein control diet (10–15 en% protein) for 26 weeks. BMI after weight loss was 30.3±4.3 kg m−2, BP was 118/73 mm Hg and 28 subjects (6.5%) used antihypertensive agents. Systolic BP during 26 weeks of weight maintenance dietary intervention increased in both treatment groups, but it was 2.2 mm Hg less (95% CI: −4.6 to 0.2 mm Hg, P=0.08) in the high-protein group than in the lower-protein control group. In 191 (pre)hypertensive subjects (baseline systolic BP120 mm Hg), a larger difference was observed (−4.2 mm Hg (−7.7, −0.7), P=0.02). The effect was attenuated after adjustment for initial BP (−3.4 mm Hg (−6.9, −0.03), P=0.048), and after additional adjustment for weight change (−2.7 mm Hg (−6.1, 0.4), P=0.11). Adjustment for 24-h urinary excretion of sodium and potassium did not change the results. Diastolic BP yielded similar results. These findings suggest that a BP reduction after weight loss is better maintained when the intake of protein is increased at the expense of carbohydrates. This effect is partly mediated by body weight.

Introduction

Hypertension is the leading risk factor worldwide for total and cardiovascular mortality.1 Diet and lifestyle have an important role in blood pressure (BP) control. Established dietary measures to lower BP are weight reduction in overweight and obese individuals, reduced sodium intake, moderation of alcohol intake (among those who drink) and an increased potassium intake.2, 3 More recently, interest has grown in diet composition and macronutrient intake, including protein. In the OmniHeart study, a randomized cross-over trial among 164 US adults with untreated (pre)hypertension, a 6-week protein-rich diet reduced BP by 1.6/1.4 mm Hg when compared with a carbohydrate-rich diet.4 When compared with a diet rich in monounsaturated fat, however, no effect of dietary protein on BP was observed.4 Subsequent randomized controlled trials that investigated the BP-lowering effect of diets with a higher protein content at the expense of carbohydrates showed inconsistent results.5, 6, 7, 8, 9 These trials primarily focussed on weight loss8, 9 or weight maintenance after initial weight loss.5, 6, 7 In these trials, sample size was relatively small, and no adjustments were made for (imbalances in) baseline BP, other potential confounding factors or change in body weight, which may partly explain the variable findings.

In the pan-European Diet, Obesity and Genes (DiOGenes) study, the effect of diets differing in protein content and glycaemic index on body weight was studied in 773 overweight adults aged <65 years.10, 11 Within the DiOGenes study, Gogebakan et al.12 explored whether weight-loss-induced improvements in cardiovascular risk factors were subsequently affected by ad libitum diets differing in protein content and glycaemic index. They showed a beneficial effect of a low-glycaemic index diet and/or low-protein diet on high-sensitive C-reactive protein, whereas lipid profiles and BP were not differentially affected. Initial BP levels and weight change, however, were not taken into account in their analysis, and no adjustments were made for salt intake. We therefore examined the effect of the high-protein diet on maintenance of reduced BP after weight loss in the DiOGenes study, with stratification for (pre)hypertensive status and adjustment for potential confounders such as body weight changes.

Subjects and methods

The DiOGenes study design

The present analysis used data from the pan-European DiOGenes study, a randomized controlled trial on the effects of diets varying in protein content and glycaemic index on weight-loss maintenance conducted between November 2005 and April 2007 (http://www.diogenes-eu.org). The DiOGenes study was approved by the local ethics committees of each European centre, and has been described in more detail elsewhere.10 In brief, the design of the multicentre DiOGenes study imposed an initial low calorie diet-induced weight loss of at least 8% of body weight in overweight and obese subjects, followed by a 26-week dietary intervention period serving as a weight maintenance phase. During this weight maintenance phase, four different ad libitum diets were compared with either high or low glycaemic index and/or protein content for the maintenance of body weight.11 BP was also monitored during this intervention period.

Study population

The population of the present analysis included overweight and obese adults from eight European countries (that is, The Netherlands, Denmark, United Kingdom, Greece, Spain, Germany, Bulgaria and the Czech Republic) who successfully lost weight. Mean reduction in body weight during 8 weeks was 11.0±3.3 kg, which was accompanied by a BP decrease of 7.8±11.1 mm Hg systolic and 5.0±8.0 mm Hg diastolic (all P<0.001). In the present analysis, we examined the effect of dietary protein on maintaining a reduced BP during 26 weeks of follow-up. Changes in glycaemic index were not taken into account because there was no significant interaction with protein intake in relation to BP (P interaction=0.61). Of the 773 adults who were randomized, 619 subjects were assigned to either a high-protein diet or a diet with a lower protein content (that is, lower-protein control diet). The original DiOGenes study also included a group of 154 subjects who consumed a regular ‘background diet’, but this group was not included in the present analysis. In addition, 185 subjects (30%) dropped out during the 26-week dietary intervention period, and 13 subjects were excluded because of missing BP data, leaving 420 subjects for the present analysis (Figure 1).

Figure 1
figure1

Flow diagram of subjects from the DiOGenes randomized study included in the present analyses on the effect of dietary protein content on maintaining achieved blood pressure level. BP denotes blood pressure.

Dietary intervention

Subjects were advised to maintain their achieved weight during the intervention. All subjects completed a 3-day dietary record at weeks 4 and 26 of the dietary intervention period. During the intervention period, subjects received careful and intensive dietary and behavioural guidance on macronutrient intake (and glycaemic index) every two weeks up to week 6, and once a month thereafter. In addition to dietary guidance, participants from The Netherlands and Denmark could choose free foods with prespecified protein content from a shop, resulting in a more controlled intervention (that is, ‘trial shop’ intervention).10

The target protein content was 23–28 energy percent (en%) for the high-protein diet and 10–15 en% for the lower-protein control group. The study was ad libitum for total energy intake, but was carefully controlled for macronutrient composition based on a points system.13

Body weight and BP

Height was measured using a stadiometer to the nearest 0.5 cm. Body weight was measured at randomization, after 4 weeks of intervention and after 26 weeks of intervention using a calibrated digital balance to the nearest 0.1 kg. BMI was calculated by dividing the subject’s weight (in kg) by the square of height (in m). Systolic and diastolic BP were measured three times at randomization and after 26 weeks of intervention by the same trained research staff in the morning after an overnight fast with an automatic device after at least 5 min while resting in a supine position according to WHO criteria. The mean value of the last two measurements was recorded. All measurements were performed according to the same standardized operating procedures in all participating centres. Hypertension was defined as systolic BP140 mm Hg or diastolic BP90 mm Hg or use of antihypertensive agents.

Other measurements

Information on current health status, medical history, medication use and lifestyle factors was obtained by questionnaires. Participants were classified as current smokers, former smokers or never smokers. Alcohol intake was assessed in grams of ethanol per day. Physical activity was assessed with the Baecke questionnaire14 consisting of 16 items from which three indexes were calculated: work index referring to physical activity at work, sport index referring to sports participation during leisure time and leisure-time index referring to physical activity during leisure time excluding sport activities.

A 24-h urine collection was performed after 4, 14 and 26 weeks of intervention. Completeness of urinary collection was checked by recovery rate of para amino benzoic acid, which was determined by spectrophotometry (Stasar, Gilford Instruments Laboratories, Oberlin, OH, USA). Urinary nitrogen to assess adherence to the diet was determined by Dumas combustion methodology using a VarioMax CN analyzer (Elementar, Hanau, Germany). In addition, 24-h urine samples were used for analysis of sodium and potassium (Roche Modular, Roche, Germany).

Statistical analysis

All analyses were performed with the SPSS software (SPSS Inc., Chicago, IL, USA). Two-sided P-values <0.05 were considered statistically significant. Values in text and tables are reported as means±s.d. or as means (95% CI), unless stated otherwise. Diet composition was tested with an independent sample t-test for between-group differences. Response to treatment was defined as change in BP from randomization. BP values were not available for subjects who dropped out during the intervention period (that is, 185 subjects (30%)). Between-group differences were analysed using analysis of variance based on the completers-only population. The analyses were repeated with adjustment for baseline BP. To examine a potential intermediary role for body weight, we additionally adjusted our analyses for change in body weight. In addition, we examined a potential intermediary role for excretion of sodium and potassium by including 24-h urinary excretion during intervention (mean of week 4, 14 and 26) as covariates.

In an additional analysis, we classified subjects in two strata on the basis of their systolic BP level (treated or untreated) 120 mm Hg or <120 mm Hg. The analyses were also repeated in the subgroup of participants from Denmark and The Netherlands who had followed the ‘trial shop’ intervention that was more controlled, which resulted in larger contrasts in protein intake.

Results

Baseline characteristics

Participants’ characteristics at the start of the intervention period (that is, baseline) according to diet are shown in Table 1. Mean age of the study population was 42±6 years and mean BMI was 30.3±4.3 kg m−2. Mean BP was 118.0±13.6 mm Hg systolic and 72.9±9.6 mm Hg diastolic (including subjects using antihypertensive agents), and 13.6% of the participants were hypertensive. There were no significant differences between groups. There were also no significant differences with subjects who dropped out during intervention (that is, mean BP 118.2/72.0 mm Hg, mean age 40±6 years and mean BMI was 31.3±4.4 kg m−2).

Table 1 Characteristics of 420 subjects from the DiOGenes study in the high-protein diet group and the lower-protein control group after initial weight loss

Protein intake

Self-reported mean dietary intakes during intervention are presented in Table 2. Mean (±s.d.) dietary protein intake was 3.2±0.5 en% (15.7±2.6 g per day) higher in the high-protein diet group compared with the lower-protein control group (P<0.001), which originated mainly from animal sources. This difference in self-reported protein intake was confirmed by a 2.1±0.5 g higher 24-h urinary excretion of nitrogen in the high-protein diet group (P<0.001). The proportion of total energy consumed from carbohydrates was 5.9±0.8% lower in the high-protein diet group (P<0.001), whereas glycaemic index was similar for the two diets (P=0.30).

Table 2 Dietary intake and urinary markers during intervention in 420 subjects of the DiOGenes study, according to high-protein and lower-protein control diet

In participants with a BP120 mm Hg (n=191), self-reported protein intake was 2.6±0.7 en% (13.7±3.7 g per day) higher in the high-protein diet group compared with the lower-protein control group (P<0.001). The difference in 24-h urinary nitrogen excretion was 1.9±0.7 g per day (P<0.001). Detailed data on self-reported dietary intake and urinary markers of this subgroup are tabulated in the online supplement to this paper (Supplementary Table 1).

In participants from Denmark and The Netherlands (n=158) who had followed the ‘trial shop’ intervention that was more controlled, we observed a larger contrast in protein intake. Self-reported protein intake was 6.1±0.6 en% (23.1±3.7 g per day) higher in the high-protein group, which was confirmed by a 2.9±0.6 g higher 24-h urinary nitrogen excretion (all P<0.001). Detailed data on self-reported dietary intake and urinary markers of this subgroup are tabulated in the online supplement to this paper (Supplementary Table 2).

Effects of protein intake on BP

BP increased in both groups during the weight maintenance dietary intervention, but less in the high-protein diet group than in the lower-protein control group (Table 3). The treatment effect was −2.2 (95% CI: −4.6, 0.2) mm Hg for systolic BP (P=0.08) and −0.9 (−2.5, 0.6) mm Hg for diastolic BP (P=0.24). After adjustment for baseline BP, the treatment effect for systolic BP was attenuated to −1.3 (−3.8, 0.8) mm Hg (P=0.22).

Table 3 Blood pressure during intervention in 420 subjects from the DiOGenes study, according to high-protein and lower-protein control diet

Mean change in body weight was 0.02±0.4 kg in the high-protein diet group versus 1.0±0.4 kg in the lower-protein control group (P=0.07). The difference in systolic BP response (adjusted for initial systolic BP) independent of weight change was −0.9 (−3.1, 1.2) mm Hg. Mean 24-h urinary excretion of sodium during intervention did not significantly differ between the high-protein diet and lower-protein control diet (182.3 versus 173.7 mmol per 24 h, respectively, P=0.30, Table 2), whereas potassium excretion was significantly higher in the high-protein group (82.3 versus 76.5 mmol per 24 h, respectively, P=0.03). Adjusting our analysis for sodium and potassium excretion did not change the results (that is, BP effect: −1.1 (−3.3, 1.1) mm Hg systolic).

Subgroup analysis

In subjects with a systolic BP120 mm Hg (n=191), the treatment effect was −4.2 (−7.7, −0.7) mm Hg systolic (P=0.02, Table 4). After adjustment for initial BP, the treatment effect was attenuated to −3.4 (−6.9, −0.03) mm Hg (P=0.048). Further adjustment for change in body weight (that is, 0.7±5.1 kg for the lower-protein group and −1.1±7.1 kg for the high-protein group, P=0.045) resulted in a BP response of −2.7 (−6.1, 0.6) mm Hg (P=0.11), whereas adjustment for sodium and potassium excretion (in addition to baseline BP) resulted in a BP response of −3.1 (−6.5, 0.4) mm Hg systolic (P=0.08). We observed no significant effect of protein intake on BP in subjects with systolic BP<120 mm Hg (Table 4). Diastolic BP showed similar results (Table 4).

Table 4 Blood pressure during intervention in subjects from the DiOGenes study, stratified by initial blood pressure levela

In participants from Denmark and The Netherlands (n=158), the treatment effect was −3.3 (−7.0, 0.4) mm Hg for systolic BP (P=0.08). After adjustment for initial BP, the treatment effect was attenuated to −2.5 (−6.0, 0.9) mm Hg (P=0.15). Adjustment for both systolic BP and weight change (that is, 2.5±3.7 kg for the lower-protein group and 0.7±5.2 kg for the high-protein group, P<0.05) yielded a systolic BP effect of −1.6 mm Hg (P=0.40), whereas adjustment for sodium and potassium excretion did not change the results, that is, treatment effect −2.5 (−6.0, 1.0) mm Hg systolic. Diastolic BP showed similar results (data not shown).

Discussion

In the present study, based on data from the DiOGenes study, we examined the effect of protein intake on maintaining a reduced BP after 8 weeks of energy restriction. During the 26 weeks of intervention (aiming at maintaining body weight), BP increased in most participants, but this increase was 2.2 mm Hg less in (pre)hypertensive participants who increased protein intake to 22 en% at the expense of carbohydrates. The effect of protein on BP was attenuated and was no longer statistically significant after adjustment for weight change, suggesting that the effect was partly mediated by body weight.

Strengths of the DiOGenes study include its prospective large-scale, randomized controlled design. BP was measured according to strict and standardized protocols in all participating centers. Compliance to the protein manipulation was confirmed by urinary excretion of nitrogen. Body weight, an important BP determinant, was carefully monitored because it was the primary outcome of the DiOGenes study. We were able to examine the effect of protein intake on the BP response independent of changes in body weight, in contrast to other studies of protein intake and BP after weight loss.6, 11 Moreover, we examined a potential intermediary role for salt intake and performed stratification by (pre)hypertensive status.

The present study also had limitations. First, because of missing BP values, we excluded subjects who dropped out during the intervention (30%). However, baseline characteristics were similar to those subjects included in the analysis, making it unlikely that this non-differential drop-out has influenced our findings. Second, the difference in protein intake was lower (3.3 en%) than targeted (12.0 en%11), which may partly explain why the observed overall BP response was relatively small and non-significant. We observed larger BP effects in subgroups with a larger contrast in protein intake, that is, −3.3 mm Hg systolic in participants who followed the ‘trial shop’ intervention (protein difference 6 en%). Third, initial BP (118 mm Hg systolic) may have been too low to find a significant effect. The effect was larger and statistically significant in participants with BP120 mm Hg. Finally, participants in the high-protein group increased their intake of protein-rich foods and reduced their intake of carbohydrate-rich foods. Because dietary intakes were not fully controlled, other nutrients that could influence BP may also have changed, including fiber, fatty acids and polyphenols. We adjusted our analyses for sodium and potassium excretion during intervention, but we cannot exclude residual confounding by unmeasured nutrients (for example, polyphenols).

Previous BP trials in which protein intake was increased (at the expense of carbohydrates) during weight loss or weight maintenance showed conflicting results.5, 6, 7, 8, 9 Our results in (pre)hypertensive participants were in line with those from Delbridge et al.6 who showed that a high-protein diet was more successful compared with a carbohydrate-rich diet in maintaining BP in participants with systolic BP130 mm Hg (that is, −6.6 mm Hg, P<0.05). Larssen et al.7 reported a 4.3 mm Hg lower systolic BP for participants on a high-protein diet, which was borderline significant (P=0.05). In both studies, despite randomization, baseline BP was 4–5 mm Hg higher in the intervention group than in the control group.6, 7 This difference was not accounted for in the analyses and, as a result, BP effects may have been overestimated. Other weight loss8, 9 or weight maintenance5 studies found no significant effect for BP in favour of a high-protein diet. In these trials,5, 8, 9 BP was not the primary outcome, sample size was relatively small (n<20 per intervention group)5, 9 or baseline BP was low (110 mm Hg systolic),8 which may (partly) explain the absence of an effect on BP. Finally, the BP effect in these trials was not adjusted for weight change.

The BP effect of protein without (initial) weight loss has also been investigated in observational studies and several trials, suggesting a small beneficial effect of protein on BP.15 In the Omniheart trial, the modest reduction in BP that was observed for the high-protein diet compared with the diet high in carbohydrates was more pronounced in hypertensives compared with prehypertensives (−3.5 versus −0.9 mm Hg for systolic BP),4 which is comparable to our findings. Our results are also in agreement with findings from two recently published isoenergetic trials on the effect of protein supplementation on BP.16, 17 In a 4-week randomized, double-blind study in 94 Dutch adults with elevated BP (mean systolic BP149 mm Hg), systolic BP was 4.9 mm Hg (P<0.01) lower after supplementation with 60 g per day protein (20% pea, 20% soy, 30% egg and 30% milk-protein isolate) compared with 60 g per day maltodextrin.17 Another large randomized, double-blind cross-over trial in 352 adults with prehypertension or stage 1 hypertension (mean systolic BP126 mm Hg) that was recently published indicated that 8 weeks of supplementation with 40 g per day soy protein or milk protein reduced systolic BP (−2.0 mm Hg for soy protein and −2.3 mm Hg for milk protein) compared with carbohydrates.16

The mechanism through which protein might reduce BP remains unclear. Several hypotheses have been put forward. First, protein content of the diet has been suggested to favourably influence body weight (maintenance).18, 19 Body weight is a well-established BP determinant, that is, 1 kg reduction in body weight results in a 1 mm Hg lower systolic BP.20 When we adjusted our analysis for change in body weight, the BP effect was attenuated (with 0.6 mm Hg) and no longer statistically significant. This suggests that the effect of protein on BP may (at least partly) be explained by its effect on body weight. Second, dietary protein has been proposed to increase renal sodium excretion.21 Cirillo et al.21 examined urea excretion in an overnight urine sample in 3705 Italians, and found an inverse association with BP only in subjects with a high sodium excretion. They hypothesized that a high-protein intake could counteract the sodium-dependent BP rise via stimulation of renal sodium excretion. In the present study, protein intake did not affect urinary sodium excretion during intervention. This makes a potential intermediary role for renal sodium excretion unlikely, although the sodium content of the diet was not available to confirm this finding. Finally, it cannot be excluded that a reduced intake of carbohydrates instead, rather than a higher intake of protein, is responsible for a beneficial effect on BP.

In conclusion, the present analyses within the multicentre DiOGenes study shows that reduced BP after initial weight loss may be better maintained by increasing the protein content of the diet at the expense of carbohydrates, especially in (pre)hypertensive subjects. This effect may be partly mediated via body weight.

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Acknowledgements

The DiOGenes project (http://www.diogenes-eu.org) is funded by a grant from the European Union Food Quality and Safety Priority of the Sixth Framework Program (contract no. FP6-2005-513946). DiOGenes is supported by the European Community (contract no. FOOD-CT-2005-513946). The writing of this report and the determination of 24-h urinary sodium and potassium excretion was funded by Top Institute (TI) Food and Nutrition (project number A-1003), Wageningen, The Netherlands. TI Food and Nutrition is a public/private partnership that generates vision on scientific breakthroughs in food and nutrition, resulting in the development of innovative products and technologies (www.tifn.nl). Partners are major food companies and Dutch research organizations.

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Correspondence to M A van Baak.

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Engberink, M., Geleijnse, J., Bakker, S. et al. Effect of a high-protein diet on maintenance of blood pressure levels achieved after initial weight loss: the DiOGenes randomized study. J Hum Hypertens 29, 58–63 (2015). https://doi.org/10.1038/jhh.2014.30

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