Abstract
BACKGROUND:
Low calorie diets are often poorly sustainable in the long term. Soluble Fiber (SF) slows gastric emptying, diminishes meal energy content and increases satiety. Adding SF to popular foods as pasta could be a good solution to improve diet adherence and metabolic parameters of obese patients.
OBJECTIVE:
to evaluate the effects of low – calorie diets including SF-enriched pasta in obese subjects on self-referred satiety, weight and metabolic parameters (glucose, insulin, glycated haemoglobin- HbA1c, plasma lipids) in a 3-months follow up.
METHODS:
30 obese patients (6M/24F, aged 43,4±10.3 years; BMI 33.4±1.56) were randomized into 2 groups; two isocaloric diets were prescribed: a diet with a serving of SF (chicory inulin 2%) enriched and lignin extruded pasta was given to the 1st group (A) every day; the 2nd group (B) had common semolina pasta. Five follow up visits with anthropometric and metabolic measurements were planned. Plasma OGTT (glucose, insulin), HbA1c, total cholesterol, HDL-cholesterol, triglycerides were determined at baseline (T0) and at the end of the study (T1, after 3 months). Overall weight loss and drop out were evaluated. Subjects were asked to report their feeling of satiety and appetite at every visit using a Visual Analogue Scale (VAS 10 CM). Treatment satisfaction had been evaluated by a questionnaire about the characteristics of SF pasta (appearance, colour, texture, stickiness, flavour and taste) with another VAS.
RESULTS:
The weight loss was kg 6.29±3.62 in group A and kg 1.87±1.66 in group B (p < 0.0002); one patient dropped out in group A, 3 in group B. The satiety and appetite VAS score were 7.6±1.1 (t1) in group A and 5.0±1.0 in group B. Group A was more satisfied of the diet plan taste (score of 8,66±0,97 vs. 1.09 (p < 0.01); 9,14±0.86 of patients of the A group and 6.07±2.05 (p < 0.01) of the B group declared they have eaten “enough”. HbA1c (p < 0.0001) and insulin level after glucose load (at 120’) decreased significantly more in the group A than in group B (p < 0.002). The diet did not affect lipid profile either in Group A and Group B after three months.
CONCLUSION:
SF enrichment and lignine extrusion of pasta increase satiety and diet adherence, and improve metabolic parameters.
Introduction
Obesity has a multifactorial etiology [1]; although it is widespread and associated with serious complications, effective prevention and treatment are still unsatisfactory. Among the currently available therapeutic approaches, the first step is represented by lifestyle changes to induce a negative energy balance. Low calorie diet and physical activity are the first line treatments for their efficacy, safety and low costs [2]. However, long-term compliance is not easily achievable because, generally, it is difficult for most obese subjects to change eating habits, increase physical activity, control stressing events or manage special meals.
A multidimensional approach including educational strategies is recommended but it is expensive and requires long-term follow up and skilled professionals. Conventional dietetic plans are a first line approach to the management of obesity [3–5]: unfortunately they are often monotonous, obese dieters hardly reach a feeling of satiety, or loose it easily.
The role of specific nutrients, foods and food groups in inducing satiety has been extensively studied [6, 7].
Soluble fiber (SF: psyllium, guar, pectine, inuline, glucomannan, oat and barley fiber) fractions are recommended as nutraceutical supplements administered before the meal. Their viscous properties delay gastric emptying and slow glucose and cholesterol absorption [8–13].
A diet that exploits the satiating properties of SF and satisfies the taste at the same time may help to increase long-term compliance and enhance weight loss in obese subjects [6].
Pasta is a typical course of traditional Italian cuisine: it is tasty, easy to cook and healthy, if planning fish or vegetable-based recipes [14]. Pasta is a popular food not only in Italy: approximately 14.3 million tons of pasta are produced every year worldwide [15]. Furthermore, some sizes of pastas (spaghetti, e.g.) have low Glycaemic Index and, consequently, induce low postprandial blood glucose and insulin responses [16, 17]. Adding SF to pasta could be a useful way to increase satiety by slowing the gastric emptying and diminishing the meal energy content.
In particular, SF inulin (IN) is an interesting adjunctive component of pasta.
IN [18] is a non-digested, fully soluble, and fermentable fiber with known prebiotic properties, which is naturally found in chicory, wheat, onion, garlic. It is a mix of linear fructose polymers with β (2 ⟶1) linkages. IN was originally proposed as functional food capable of improving parameters of the metabolic syndrome, i.e. blood glucose concentration and lipid metabolism [19–24]. More recently, it has been hypothesized that IN may have a favourable effect on body mass index (BMI). The exact mechanism by which IN acts remains unclear: experimental studies have shown that IN modulates gastrointestinal hormones secretion, increasing glucagon-like peptide-1 and glucagon-like peptide-2, that promote satiety, and decreasing ghrelin, which stimulates food intake and leads to lower weight gain [25–27]; furthermore, IN influences gut microbiota composition with its prebiotic properties, increasing bifidobacteria population. The link between gut microbiota, obesity and metabolic syndrome by increasing the energy harvest from undigested food was largely investigated [28–30] but it is still impossible to recognize an “obesogenic” microbiota composition. Limited data [31] suggest that long-term administration of IN may contribute to weight reduction in adolescents and in overweight and obese adults. The mechanisms by which IN influences BMI are still unclear and the next step is to find which way IN operate. Further studies are also warranted to determine the dose (minimal, optimal, and dose-response effect), and the duration of intervention to achieve weight reduction.
An independent role may be attributed to resistant starch (RS) that in vivo works as a functional fiber. By definition, RS is a food starch fraction resistant to enzymatic digestion and absorption in the human small intestine. This property is due to high amounts of retrograded amylose, physically inaccessible starch, digestion-resistant starch granules, and fragments of chemically and thermally modified starches [32, 33]. RS has been somewhat arbitrarily divided into subcategories based on analytical chemical tests rather than on research of physiological benefits in vivo [34]. The resistance to enzymatic digestion can take benefits by reducing the caloric value of the food, providing energy to the gut bacteria and enhancing fermentation. RS is not the only starch that reaches the colon to supply energy for fermentation.
Also, other fractions of starch reach the colon: their amount depends on the composition of the diet. Furthermore, the relative quantity of RS in foods changes with the exception of the chemically or thermally treated starches.
The consumption of RS instead of digestible starch has several favorable metabolic effects as the improvement of postprandial glucose and insulin response, the reduction of cholesterol and triglyceride levels, the increase in insulin sensitivity, satiety and reduction of fat deposits [35]. These properties make RS an attractive dietary tool for the prevention of metabolic diseases as well as for nutritional therapy for Type 2 diabetes and cardiovascular disease [36].
Aim of the study
The aim of this study is to evaluate the short time (3 months) effects of low-calories diet plans for obese subjects that include SF (chicory inulin 2%) –enriched pasta on: 1) weight loss 2) self-referred satiety 3) follow up adherence 4) metabolic parameters (glucose and insulin levels, HbA1c, lipid plasma profile).
Subjects
Thirty obese outpatients (6M/24F, age 4.4±10.3 years) were recruited. They were selected from San Camillo Forlanini Hospital Diabetic Unit database (MyStar Connect ® MeTeDa, S.Benedetto del Tronto, AP). The overall BMI of the enrolled obese was 33.4±1.56 kg/m2. The subjects were screened with the following exclusion criteria: diagnosed psychiatric and eating disorders, active drug addiction, pregnancy and comorbidities and drugs that can interfere with nutritional assessment.
The patients were divided into two randomized groups, A and B (Table 1); there was no difference regarding age, sex distribution, weight, BMI at start (T0).
Proximate composition of raw materials Nutritive content (g), energy value and glycemic index per 100 g edible portion
Proximate composition of raw materials Nutritive content (g), energy value and glycemic index per 100 g edible portion
The study was performed according to the Declaration of Helsinki on the human trial performance and informed consent was provided by participants.
The study protocol was approved by the Ethical Committee of the San Camillo Forlanini Hospital in Rome (prot. 1690/CE Lazio 1, Sept. 12th , 2018).
In the first visit (T0) all the obese patients underwent to anthropometric assessment (Height, Weight, BMI) and nutritional counseling. After randomization two isocaloric-low calorie diets (17 kcal/kg; carbohydrates ∼45%, fat ∼30%, proteins ∼1.1 g/kg/day) was given to the two groups (A) and (B). The 1st group (A) a meal per die with fiber enriched pasta and the 2nd group (B; control group) a meal with ordinary semolina pasta were given, respectively. All the subjects were encouraged to drink an adequate water amount (1500–2000 ml/day). 5 fortnightly follow-up visits were programmed (anthropometry; counseling) for three months (T1).
Metabolic parameters (blood glucose and insulin after oral glucose tolerance test-OGTT (0, 60’, 120’), Glycated Haemoglobin – HbA1c, Total Cholesterol – T-Chol, HDL cholesterol – HDL-C, Triglycerides -TGs) have been checked at the beginning and at the end of the dietetic intervention (3 months).
Treatment efficacy and patients diet adherence have been evaluated considering overall weight loss and drop out in the two groups.
Study subjects were asked to report their feelings of satiety and appetite – as felt in the week before the evaluation – at T0 and at T1 using a visual analogue scale (VAS 10 CM).
Furthermore, feeling of satiety, pasta tastiness and treatment satisfaction have been evaluated by means of questionnaires about various sensory attributes (appearance, colour, texture, stickiness, flavour and taste) with another VAS, administered to the patients of both groups at the end of treatment.
One patient (6.6%) dropped out after the first check-up; in control group 3 patients did.
Pasta
Either dietetic pasta “FiberPasta” ® and common pasta were supplied by the manufacturer Polverini mill, Monte S.Severo, Ancona, Italy. Table 1 shows the bromathological composition per 100 grams of the two raw type of pasta as reported by the manufacturer.
The percent composition of FiberPasta is as follows: 1381/330 kj/kcal, 15 g/100 g proteins, 1,3 g/100 g fat, 58 g/100 g carbohydrates; total dietary fiber is 15 g/100 g, chicory-extracted inulin is 2 g/100 g. The Glycemic Index value of the two types of pasta come from the Institute of Food Science and Nutrition of the University of Piacenza.
In addition, the same product has a higher RS content than common pasta one. It is obtained with a technological process of warming/cooling of starch in controlled environment. The RS percentage is 4.5%.
The lignin extrusion gives light amber colour to “Fiberpasta”, that looks similarly to the common semolina pasta. The size and package of the single servings were anonymous and blinded for investigators and patients. Pasta was cooked in domestic ordinary recipes (about 6’ in 2 liters of salty water), with seasonal vegetables and dressing in accordance with the prescribed amounts (olive oil, tomato, spices, cheese, fish).
Methods
Anthropometric measurements including body weight and height were assessed in accordance with the techniques described [37] Fasting blood sample were collected in the morning; OGTT was performed as recommended by OMS [38].
Statistics
The results are presented as average±standard deviation; paired T test was performed (significance p = 0.05).
Results
The characteristics of all the patients (Group A and Group B) are showed in Table 2.
Description of the studied subjects (mean values±SD; ns = not significant)
Description of the studied subjects (mean values±SD; ns = not significant)
The results are reported in Table 3a, 3c.
Results. The values (weight, BMI) at T0 and T1 of the two studied groups are reported as average±standard deviation and as Δ 0–T1. The significance level is p = 0.05. Abbreviations are in the text
Results. The values (TG, T-Chol, HDL-C) at T0 and T1 of the two studied groups are reported as average±standard deviation and as Δ T0–T1. The significance level is p = 0.05. Abbreviations are in the text
Results. The values (insulin, glucose, HbA1c) at T0 and T1 of the two studied groups are reported as average±standard deviation and as Δ T0–T1. The significance level is p = 0.05. Abbreviations are in the text
The overall weight loss at the end of the study (3 months) was 6.29±3.62 kg and 1.87±1.66 kg (p < 0.0002) in Group A and Group B, respectively; BMI decrease was 2.39±1.32 in group A and 0.63±0.62 in group B (p < 0.0001).
The VAS score about satiety and appetite were 5.1±1.0 (T0) and 7.6±1.1 (T1) and 3.0±1.2 and 5.0±1.0, respectively in Group A and Group B. The analysis of the administered question sheets revealed that group A was satisfied with the diet plan with a score of 8,66±0,97, group B showed a score of 1.09 (p < 0.01). 9,14±0.86 of patients of the group A and 6.07±2.05 (p < 0.01) of patients of the group B declared they have eaten “enough”. Referring to their palatability both dietetic and common pasta got the maximum score (10) without any difference in the groups.
Only one patient in group A declared “weakness” and one in group B “irritability” subjectively referable to the diet. All the patients of both groups agreed that nutritional counselling every 15 days helped them to change their lifestyle. In the short time no difference in blood glucose (fasting and after oral challenge), total cholesterol HDL-cholesterol and triglycerides in the two groups was observed; HbA1c and insulin level after glucose load (T1 –120’) decreased more significantly in the group A vs. group B (respectively p < 0.0001 and p < 0.002).
Traditional low calorie dietetic plans are often monotonous and hardly sustainable in the long term by most of the obese [1, 5]. Food choices enlargement is an important opportunity to preserve dietary adherence: pasta is an accepted, tasty and pleasant food for dieters. The enrichment with an adequate dietary fiber amount helps to increase satiety but can modify the appearance of pasta. Pasta made from durum semolina maintains a desirable firm texture during cooking, and it has a natural amber color that is perceived by the consumers as a good quality marker; generally fiber addition gives to pasta a particular texture, taste and brown color that make it different from common pasta one, and possibly less appealing for many.
It was necessary to make pasta more attractive to ensure and increase consumer acceptance [39]: the SF enriched pasta (FiberPasta®) is very similar to common pasta for the lignin extrusion: so that it was possible for us to blind the subjects of the two groups and investigators. The technological processes to which the tested fiber enriched pasta underwent maintain the organoleptic characteristics of the common semolina pasta and represent an appealing claim for the customer. None of the blinded participants to the study noted a difference of the administered fiber enriched pasta as texture, color, and taste.
The studied subjects reported increase of satiety and reduction of appetite, as demonstrated by the VAS score; they also referred a good taste and satisfaction for fiber enriched dietetic pasta, similar to common semolina pasta eaten in Italy, in a short time setting (3 months).
It is likely that these organoleptic characteristics could be useful to maintain the adherence to the diet also in the long term. It is our aim to evaluate this kind of diet in a longer setting with a daily choice of pasta.
The significant weight reduction (6,29±3,62 kg whereas the one of group B was 1,87±1,66 kg) (p < 0,0002) has been appreciated immediately, reinforcing compliance to the overall dietetic plan.
Our results confirm also the efficacy of including popular food choices in diets. A recent systematic review concluded that most of the short time studies on fiber supplementation did not enhance satiety (61%), did not reduce food intake (78%) and neither fiber fraction type nor fiber total dose were related to satiety response or food intake [40].
In other reports short- and long-term effects of dietary fibers are conflicting; the multiple mechanisms of action related to their different physico-chemical properties probably play specific effects: e.g. fiber fractions characterized as being more viscous (pectins, β-glucans and guar gum) reduce appetite more than the less viscous ones (59% vs. 14%) [41, 42].
The stool frequency and characteristics were normal; all the studied subjects consumed an adequate water amount; no significant gastrointestinal discomfort (e.g. diarrhoea, bloating, nausea, constipation) has been reported by the studied subjects, probably because the added fiber was a soluble one, with a low impact on colonic microflora and motility.
In the study of Emilien et al. [41] the reduction of total daily energy intake was 179 kcal replacing standard wheat flour with resistant wheat starch, but there was no effect on subjective appetite. Instead, in the study of Wanders [42] the attention was focused on differences depending on fiber chemical structure: despite effects on energy intake and body weight were relatively small, fiber characterized as being more viscous reduced appetite more often than those less viscous ones. Also, Kristensens [8] agrees that role of viscosity in mediating appetite regulation is not firmly established but effect on digesta viscosity induced by solid vs. liquid meals needs to be addressed in the future.
Higher amount of enriched fiber (up to 25 per cent) could significantly reduce the overall acceptability; in our study the tested pasta had the maximum acceptability level – 15 per cent – reported for pastas enriched with cereal bran: cereal bran can be added up to 15 per cent levels (wheat, rice and oat bran) and 10 per cent levels (barley bran) without adversely affecting the physicochemical, cooking and sensory quality of pasta [39, 43]: there are no data on pasta enriched with the particular soluble fiber (chicory inulin) and functional fiber (resistant starch) used in our study.
The inclusion of this fiber enriched pasta in low calorie diet plans for obese patients brought a higher weight loss and a lower drop out during a 3-month follow up in Group A in comparison with controls (isocaloric portions of common pasta). This result may be likely attributed to the increased volume/calories ratio which enabled patients in the Group A to eat a greater volume of pasta servings, with subsequent increased feeling of satiety after meals.
The added soluble fiber may contribute to increase satiety also by reducing insulin response after meal, as suggested by the OGTT results at T1: also, in group B reduction at 120’ at T1 was observed but to a significantly lesser extent. This finding could be related to the slower digestion of the dietetic pasta for viscous properties of fiber. Also, the reduction of insulin-resistance subsequent to weight loss plays an important role.
Average blood glucose levels are reduced, as suggested by the significant decrease of HbA1c (Δ HbA1c group A – 6±3 mmol/mol (–0.335±0.63%); group B – 1±2 mmol/mol (– 0.11±0.20%); p < 0.0001 and by the reduction trend of blood glucose 120’ after challenge (not significant). These results may be due to the increased insulin sensitivity related to the weight loss.
Finally, the lipid values were not affected by diet neither in Group A nor in Group B. These data can be explained by the short term of the study (3 months). A longer period could be able to show any effect on lipid metabolism.
Conclusions
Strenght of this study is the demonstration that specific technological processes (SF enrichment and lignin extrusion) have positive effects on the appeal and the acceptance of fiber-enriched pasta. They increase satiety and consequently diet adherence. Our study also shows metabolic parameter improvement. These results may encourage to include this type of pasta in hypocaloric diets, enlarging food choices and subsequently increasing adherence in obese subjects. Limitations of the study are the small size of the sample and the short follow up. Further observation is needed to study the long-term effects of this kind of diet.
In conclusion, satiating agents as SF are neither the only nor the most important way to lose weight: the overall control of food intake, the increase of physical activity and the pharmacological and surgical therapy play a specific and complementary role in obtaining and maintaining an acceptable weight in the long time. Total fiber ability to increase satiety is poorly significant but choosing selected soluble and functional fractions, as inulin, to enrich pasta seems to induce favorable results enhancing adherence to dietetic low-calorie plans in obese subjects, inducing a higher weight loss, reducing postprandial insulinaemia; it represents a useful tool in the overall management of obesity.
Further studies are necessary to demonstrate if these favorable results can be obtained also in overweight/obese type 2 diabetic subjects [21].
It could be interesting to study the effects of the regular consumption of the regular use of fiber enriched pasta on gastrointestinal microbiota composition: in fact, rapid variations of bacterial populations is a significant factor in weight reduction and glucose metabolism improvement (28–30).
Finally, it is remarkable that fiber enriched pasta inclusion in the diet can help to target the required allowances of dietary fiber in large groups of populations and increase their comprehensive health benefits and protection against chronic noncommunicable diseases.
Conflict of interest
The authors declare to have no conflict of economical interest with the sponsor of the present study in the last five years.
Author disclosure statement
This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. The authors have no competing interests to declare.
Footnotes
Acknowledgements
Dr. Antonio Vivenzio for linguistic support.
