Original Article | Published:

Interventions and public health nutrition

Long-term effects of a Palaeolithic-type diet in obese postmenopausal women: a 2-year randomized trial

European Journal of Clinical Nutrition volume 68, pages 350357 (2014) | Download Citation

Contributors: Study concept and design; acquisition of data; and drafting the manuscript: CM, SS, MR, CL, TO, and BL. Analysis and interpretation of data and critical revision of the manuscript for important intellectual content: all the authors. Statistical analysis: CM, SS. ME, and BL. Obtained funding: TO, BL, and MR. Administrative, technical or material support: SB, CL, TO, and BL. Study supervision: MR, CL, TO, and BL.

Subjects

Abstract

Background/Objectives:

Short-term studies have suggested beneficial effects of a Palaeolithic-type diet (PD) on body weight and metabolic balance. We now report the long-term effects of a PD on anthropometric measurements and metabolic balance in obese postmenopausal women, in comparison with a diet according to the Nordic Nutrition Recommendations (NNR).

Subjects/Methods:

Seventy obese postmenopausal women (mean age 60 years, body mass index 33 kg/m2) were assigned to an ad libitum PD or NNR diet in a 2-year randomized controlled trial. The primary outcome was change in fat mass as measured by dual-energy X-ray absorptiometry.

Results:

Both groups significantly decreased total fat mass at 6 months (−6.5 and−2.6 kg) and 24 months (−4.6 and−2.9 kg), with a more pronounced fat loss in the PD group at 6 months (P<0.001) but not at 24 months (P=0.095). Waist circumference and sagittal diameter also decreased in both the groups, with a more pronounced decrease in the PD group at 6 months (−11.1 vs−5.8 cm, P=0.001 and−3.7 vs−2.0 cm, P<0.001, respectively). Triglyceride levels decreased significantly more at 6 and 24 months in the PD group than in the NNR group (P<0.001 and P=0.004). Nitrogen excretion did not differ between the groups.

Conclusions:

A PD has greater beneficial effects vs an NNR diet regarding fat mass, abdominal obesity and triglyceride levels in obese postmenopausal women; effects not sustained for anthropometric measurements at 24 months. Adherence to protein intake was poor in the PD group. The long-term consequences of these changes remain to be studied.

Introduction

The incidence of obesity has increased substantially since the early 1980s, resulting in major public health challenges.1, 2 Related to this, dietary risk factors and physical inactivity collectively accounted for 10% of global deaths and disability-adjusted life years in a recent comparative risk assessment of the burden of disease and injury.2 Central fat accumulation, that is, the accumulation of visceral adipose tissue, is clearly associated with an increased risk of type 2 diabetes mellitus (T2DM) and cardiovascular disease (CVD).3 In menopause, fat is redistributed from peripheral to central depots, which is associated with an increased incidence of diabetes and CVD among postmenopausal women.4

Diets moderately high in protein (25–30% of energy intake) have been suggested to be beneficial for weight loss when used ad libitum, at least up to 12 months.5 This includes a more pronounced reduction in body fat and blood pressure and improved lipid profile when compared with high-carbohydrate diets. However, it is not clear if an increased protein intake is sustainable during long-term diet interventions. An increased intake of monounsaturated fats (MUFA) and omega-3 fatty acids and moderately decreased intake of carbohydrates (40% of energy intake) may also be beneficial with regard to weight loss as well as have protective effects on CVD.6, 7

Such dietary properties are possible with a Palaeolithic-type diet (PD), making it seem worthy of randomized controlled trials. Short-term studies with this type of diet have suggested beneficial effects on energy intake, weight, waist circumference, body mass index (BMI), and metabolic balance, including insulin sensitivity, as well as cardiovascular risk markers, even when administered ad libitum in comparison with other types of diets.8, 9, 10, 11 Our hypothesis was that a PD would be more efficient than a conventional low-fat/high-fibre diet12 at reducing fat mass during a 2-year randomized dietary intervention trial in obese postmenopausal women. Furthermore, we wanted to analyze if a PD would have beneficial effects on cardiovascular risk markers.

Subjects and methods

Subjects

The subjects were recruited in 2007 through advertisements in local newspapers. In total, 210 women expressed an interest in participating in the study (Figure 1) out of which 70 postmenopausal non-smoking women with a BMI27 kg/m2 fulfilled the inclusion criteria. Exclusion criteria included consumption of a restricted or vegetarian diet, allergy to key components in the intervention diets, history of heart disease, kidney disease, hyperthyreosis or hypothyreosis, osteoporosis or diabetes. Other exclusion criteria were abnormal fasting plasma glucose levels (7 mmol/l), blood pressure exceeding 150/90 mm Hg, hormone replacement therapy, statins, beta-blockers or any medication for psychiatric disorders. Three women on monotherapy with an angiotensin-converting enzyme inhibitor for mild hypertension were included in the study. Each woman met a physician for clinical assessment, followed by a series of baseline tests at the Clinical Research Center at Umeå University Hospital, Umeå, Sweden.

Figure 1
Figure 1

Flow diagram of subjects’ participation in the trial. Participants were prescribed to eat either a PD or a diet according to the NNR.

Diet intervention

After baseline measurements, the women were randomized to a PD or a Nordic Nutrition Recommendations (NNR) diet for 24 months. All study personnel (except the dieticians) were blinded to the dietary allocation of the participants. Both diets were consumed ad libitum. The PD provided 30% of energy intake (E%) from protein, 40 E% fat and 30 E% carbohydrates and included a recommendation for a high intake of MUFA and polyunsaturated fatty acids (PUFA). The diet was based on lean meat, fish, eggs, vegetables, fruits, berries and nuts. Additional fat sources were avocado and oils (rapeseed and olive oil) used in food preparation and dressing. Dairy products, cereals, added salt and refined fats and sugar were excluded. The NNR diet12 was aiming at a daily intake of 15 E% protein, 25–30 E% fat and 55–60 E% carbohydrates, with emphasis on low-fat dairy products and high-fibre products. Each group took part in a total of 12 group sessions held by a trained study dietician (one dietician per diet) throughout the 24-month study period. The group sessions consisted of information on and cooking of the intervention diets, dietary effects on health, behavioral changes and group discussions. The subjects were given recipes and written instructions to facilitate the preparation of meals at home. Eight group sessions (four cooking classes and four follow-up sessions) were held during the first 6 months of the intervention. Additional group meetings were held at 9, 12, 18 and 24 months. The protocol was in accordance with the Helsinki declaration and approved by the Regional Ethical Review Board at Umeå University, Umeå, Sweden. This trial was registered at clinicaltrials.gov as NCT00692536.

Anthropometry and metabolic parameters

Anthropometric measurements were made at baseline and after 6, 12, 18 and 24 months, as described earlier.13 The sagittal abdominal diameter was recorded at the umbilical level as the height of the abdomen measured when lying down on the examination couch with the legs straight. Body composition, including an estimation of the total percentage of body fat, was measured by dual-energy X-ray absorptiometry (GE Medical Systems, Lunar Prodigy X-ray Tube Housing Assembly, Brand BX-1L, Model 8743, Madison, WI, USA). Systolic and diastolic blood pressure was measured twice at 2-min intervals in the sitting position after 5 min rest, using an automatic blood pressure meter (Boso-medicus, Bosch, Germany). Fasting blood samples were drawn from the antecubital vein after a resting period. Aliquots were frozen immediately at −20 °C until analyzed for plasma glucose, plasma insulin, serum cholesterol, triglycerides, high-density lipoprotein (HDL) cholesterol, tissue plasminogen activator activity, plasminogen activator inhibitor type 1 (PAI-1) activity and high-sensitivity C-reactive protein (hsCRP). Serum low-density lipoprotein (LDL) was calculated as (serum cholesterol−serum HDL−serum triglycerides)/2.2.

Dietary assessment

Dietary intake was assessed using the 4-day estimated self-reported food records conducted at baseline (2 × 4 days) and monthly until 6 months, thereafter at 9, 12, 18 and 24 months. Subjects were instructed to keep a record of all food items consumed over 4 consecutive days (three weekdays and one weekend day) and to describe and estimate the amount of food eaten by using coloured food-portion photographs representing known weights and household measuring utensils (for example, cup, spoon and standard weight of food items). The reported food intake was converted to estimates of energy and nutrient intake using the nutritional analysis package Dietist XP (version 3.0, Kost och Näringsdata AB, Bromma, Sweden) based on the food composition database of the Swedish National Food Administration (2008-03-06).

Adherence to protein intake

Nitrogen excretion in urine (NU) was used as a biomarker for protein intake, with three 24-h urine samples collected at baseline and after 6 and 24 months. The para-aminobenzoic acid method14 was used to verify the completeness of the urine collections. NU was determined using the Kjeldahl technique with a Kjeltec analyser (model NMKL nr 6, Eurofins Food & Agro AB, Lidköping, Sweden). Duplicates for 10% of the samples were included for quality control. The analytical precision was±10%.

Measurement of energy expenditure

Resting energy expenditure (REE) was measured at baseline and after 6 and 24 months using indirect calorimetry (Datex-Ohmeda Deltatrac II, Datex-Ohmeda Inc, Madison, WI, USA) with breath-by-breath sampling. Free-living physical activity energy expenditure (PAEE) was estimated at the same time points using data collected over a 7-day period using a combined accelerometer and heart rate monitor (Actiheart, CamNtech Ltd, Cambridge, UK) as described previously.15, 16, 17 Diet-induced thermogenesis, that is the production of heat after eating, was fixed at 10% of the total energy expenditure (TEE) for all individuals in the study. TEE was calculated for each participant as the sum of the PAEE and REE, divided by 0.9 and expressed as kcal or MJ per 24-h day.

Statistical methods and randomization

The primary outcome of the study was the change in fat mass over a period of 2 years, which was also used to calculate power. Thirty-five subjects were estimated to be needed in each diet arm to achieve a significant outcome (P<0.05) with 80% power. Block randomization with a block size of four and an allocation ratio of 1:1 was done by a statistician blinded to the study. Most variables were normally distributed, but serum insulin, serum TG, PAI-1, hsCRP, total lean mass and PUFA (g) required logarithmic transformation. Differences between groups at baseline were tested by independent sample t-tests. We used generalized estimating equations to evaluate repeated measurements over time. A two-sided P-value <0.05 was considered significant. Statistical analyses were performed using the SPSS for Windows (version 20.0, IBM Corporation, Armonk, NY, USA). The primary analysis in this trial was an intention-to-treat analysis.

Results

Subject characteristics

No differences were found in the baseline characteristics between the diet groups, except for higher HDL cholesterol in the PD group (Tables 1 and 3). A total of 30% (n=21) of the participants were lost to follow-up (Figure 1). A higher proportion of participants completed the PD arm than the NNR arm (77% PD, 63% NNR). Medication use did not change during the study period.

Table 1: Baseline characteristics of the study participantsa

Energy expenditure and dietary intake

REE, PAEE and TEE did not change or differ between the groups during the study period (Table 2), with the exception of a decrease in REE at 6 months in the study population as a whole. The change in reported nutrient intake between baseline, 6 and 24 months and the difference between the groups at each time point is presented in Table 2. No difference was found between the diet groups regarding nutrient intake at baseline. Reported daily energy intake decreased over time, without significant differences between groups (Table 2). The PD group had a 19% and 20% lower reported energy intake and the NNR group 18% and 12% lower reported energy intake at 6 and 24 months, respectively.

Table 2: Changes in energy expenditure, dietary intake and biomarker of protein intake during 2 years of intervention among obese postmenopausal womena

The PD group reported a significantly lower intake (E% and g/day) of carbohydrates, higher intake (E% and g/day) of protein, MUFA, PUFA, cholesterol and higher total fat (E%), MUFA:SFA (saturated fatty acid) and PUFA:SFA ratios compared with the NNR group (Table 2). The PD group reported a more pronounced change in the ratio (E%) protein:carbohydrates:total fat from baseline to 6 and 24 months (17:46:33, 23:29:44 and 22:34:40, respectively) compared with the NNR group (17:45:35, 19:48:32 and 17:43:34, respectively). Target intakes were not fully achieved; the PD did not reach the target amounts of percentage energy of protein (30 E%) at 6 and 24 months, and the NNR group did not reach the target amounts of carbohydrates (55–60%).

Adherence to protein intake

A total of 406 urine collections from 65 subjects (34 PD, 31 NNR) at baseline, 51 subjects (30 PD, 21 NNR) at 6 months and 39 subjects (21 PD, 18 NNR) at 24 months were available for comparison of reported protein intake and NU. Mean NU were 13 g/day in both the groups at baseline (Table 2). There was no difference in NU within or between groups at 6 or 24 months follow-up, indicating poor adherence to the target protein intake (30 E%) in the PD group.

Anthropometry and cardiometabolic risk markers

Both the diet groups decreased their total fat mass: −6.5 and−2.6 kg at 6 months; and−4.6 and−2.9 kg at 24 months for the PD and NNR group, respectively, with a significant difference between the groups at 6 months but not at 24 months (P<0.001 and P=0.095 respectively; Figure 2). The PD group also lost more total lean mass (−1.3 vs−0.4 kg; P=0.005) during the first 6 months. Both the diet groups had a significant weight loss during the whole study period, with significantly greater weight loss in the PD group at all follow-up time points except at 24 months (Figure 2). The largest weight loss was measured at the 12-month follow-up;−8.7 kg in the PD group and−4.4 kg in the NNR group. BMI (mean (±s.e.m.)) decreased 3.0 (±0.30), 3.3 (±0.36) and 2.4 (±0.41) kg/m2 in the PD group and 1.2 (±0.27), 1.7 (±0.38) and 1.4 (±0.34) kg/m2 in the NNR group at 6, 12 and 24 months, respectively. The loss in BMI was more pronounced in the PD group at 6 months (P<0.001) and 12 months (P=0.002) but not at 24 months (P=0.059). In both the diet groups, waist circumference decreased significantly during the whole study period, with a significantly more pronounced decrease in the PD group at 6 months (−11.1 vs −5.8 cm; P=0.001; Figure 2). In addition, the sagittal diameter decreased significantly over time in a similar manner in both the groups, with a larger decline in the PD group at 6 months (−3.7 vs−2.0 cm; P<0.001; Figure 2). Concomitantly, hip circumference decreased over time with a significant difference between the groups at 6 months (−6.8 with PD vs−2.7 cm with NNR at 6 months; P<0.001).

Figure 2
Figure 2

The effect of diet intervention on different anthropometric measurements. Generalized estimated equations were used, with the Palaeolithic diet group as a reference group. P-values for the diet × time interaction for (a) fat mass<0.001, (b) weight<0.001, (c) waist=0.001 and (d) sagittal diameter<0.001. Data are presented as mean±s.e., *P<0.05, **P<0.01 and ***P<0.001 for differences between diet groups at respective time points based on estimated marginal means. NS, not significant.

Triglyceride levels decreased significantly in the PD group over time with a 0.26 and 0.22 mmol/l difference between the diet groups at 6 and 24 months (P<0.001 and P=0.004), respectively (Table 3). Other beneficial cardiometabolic changes occurred in the study population as a whole over time (Table 3). At both 6 and 24 months, diastolic blood pressure, heart rate, CRP, LDL cholesterol and PAI-1 activity decreased, as well as systolic blood pressure and total cholesterol at 6 months, and HDL cholesterol increased at 24 months. No differences were measured over time or between groups with regard to fasting glucose, fasting insulin concentrations and tissue plasminogen activator activity.

Table 3: Changes in bioindicators during 2 years of intervention among obese postmenopausal womena

Discussion

We found that a diet with reduced carbohydrate and SFA intake and a relative increase in the intake of protein, MUFA and PUFA has strong and long-lasting effects on fat mass, body weight and abdominal obesity in postmenopausal women, but there were no significant differences in anthropometric measurements at 24 months between the groups. Notably, triglyceride levels decreased significantly more in the PD group than in the control group based on the NNR diet. However, adherence to the target intake of protein was poor in the PD group.

Increased visceral fat mass, associated with liver fat (that is, ectopic fat accumulation), may contribute to increased risk for the metabolic and cardiovascular complications after the menopause.18 Triglyceride elevations are an essential part of the metabolic dysfunction seen with ectopic fat accumulation. Of interest is that we recently showed a 5-week PD to be associated with a 49% decrease in liver fat and increased insulin sensitivity linked to a 41% decrease in serum triglycerides.13 A diet with a similar macronutrient composition as the present study was also shown previously to reduce visceral fat more than total fat on a long-term basis, albeit with a high dropout from the study after 2 years.19 Further studies on the putative effect by a PD on visceral fat and ectopic fat seem therefore warranted.

The lack of a significant decrease in fasting glucose and insulin levels in our study may be explained in part by the fact that the subjects had normal glucose tolerance at baseline (that is, ‘obese but healthy’), thereby reducing the possibility of improving the metabolic status and these cardiovascular risk markers. In contrast, we found significant effects over time, but not between the groups, of PAI-1 and CRP levels, with a mean decrease in the PD group that was approximately twice that of the NNR group. Analyses of the putative effects of a PD in subjects with a more pronounced metabolic dysfunction are encouraged by short-term studies indicating an improvement in the glucose tolerance and cardiovascular risk markers of patients with T2DM and CVD.9, 10, 20

The profound decrease in energy intake (20% vs 12% for the PD and NNR groups at 24 months) is in line with earlier short-term studies from us and others.9, 10, 11, 13, 20 This may be due to effects on satiety by increased intake of protein and low energy-dense foods, as well as PUFAs.21, 22, 23, 24, 25, 26, 27, 28 Notably, no significant differences were found in urinary nitrogen excretion between the diet groups at any time point, which may have limited the differences between the groups. Adherence to the target protein intake was thus poor in the PD group, in line with earlier studies with the aim of increasing protein intake.29, 30 There could be several reasons for this, such as protein-rich food being more expensive, social influences on women’s food choices or a lower food preference for protein-rich food among women.31, 32, 33 Importantly, this suggests that other factors than protein content contributes to the beneficial effects of the PD diet. One possibility is the higher intake of PUFAs in the PD group. In line with this, increased satiety after intake of long chain omega-3 fatty acids has been demonstrated.25

The magnitude of effects on body composition and triglyceride levels do, however, suggest that larger randomized trials are done regarding putative differences between a PD and other types of diet with different macronutrient compositions. The reductions in fat mass, weight and abdominal obesity were thus profound but less different between groups than expected from our power analysis.

Despite the stratification for BMI, the PD group had a more beneficial metabolic profile at baseline, including higher HDL cholesterol levels. The NNR study group also had higher variability in some of the study variables, which may have influenced our ability to detect differences between the groups. Therefore, we may have underestimated the effects of the intervention on various outcome variables. In addition, the dropout rate from the study was larger than expected (37% and 23%, respectively, for the NNR and PD group); the latter in line with recent data from Jonsson et al.22

We did not include an observational study group. Therefore, we cannot conclude whether the changes observed in these intervention groups differ from the natural course regarding the study parameters in this population. However, our aim was to investigate the possible effect of a diet regimen in comparison with the low-fat, high-fibre diet in Nordic countries generally recommended when the study started.

In conclusion, a PD during 2 years with ad libitum intake of macronutrients, including an increased intake of PUFAs and MUFAs, reduces fat mass and abdominal obesity with significantly better long-term effect on triglyceride levels vs an NNR diet. Adherence to the prescribed protein intake was poor in the PD group, suggesting that other components of the PD diet are of greater importance. The putative long-term beneficial effects of different components of the PD on obesity-related diseases, notably T2DM, need to be explored.

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Acknowledgements

We thank all of the women who participated in this study for their invaluable patience and cooperation. Erik Hägg, Jonas Andersson, Lars-Göran Sjöström, Göran Ericsson, Inger Arnesjö, Katarina Iselid and Monica Holmgren made important contributions to screening the health of study subjects and technical assistance. Johanna Larsson helped process food records. Kate Westgate and Stefanie Mayle (MRC Epidemiology Unit, University of Cambridge, Cambridge, UK) assisted with processing physical activity data. Paul Franks contributed important views on planning the study. This study was supported by grants from The Swedish Council for Working Life and Social Research (2006-0699 and 2010-0398), the Swedish Research Council (K2011-12237-15-6), the Swedish Heart and Lung Foundation, the County Council of Västerbotten and Umeå University, Sweden.

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Author notes

    • C Mellberg
    • , S Sandberg
    •  & M Ryberg

    These authors share first authorship.

    • T Olsson
    •  & B Lindahl

    These authors share senior authorship.

Affiliations

  1. Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden

    • C Mellberg
    • , M Ryberg
    •  & T Olsson
  2. Department of Public Health and Clinical Medicine, Occupational and Environmental Medicine, Umeå University, Umeå, Sweden

    • S Sandberg
    •  & B Lindahl
  3. Department of Statistics, USBE, Umeå University, Umeå, Sweden

    • M Eriksson
  4. MRC Epidemiology Unit, University of Cambridge, Cambridge, UK

    • S Brage
  5. Department of Food and Nutrition, and Sport Science, University of Gothenburg, Gothenburg, Sweden

    • C Larsson
  6. Department of Food and Nutrition, Umeå University, Umeå, Sweden

    • C Larsson

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The authors declare no conflict of interest.

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Correspondence to C Mellberg.

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DOI

https://doi.org/10.1038/ejcn.2013.290

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