Assessment of a 4-Week Starch- and Sucrose-Reduced Diet and Its
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nutrients Article Assessment of a 4-Week Starch- and Sucrose-Reduced Diet and Its Effects on Gastrointestinal Symptoms and Inflammatory Parameters among Patients with Irritable Bowel Syndrome Clara Nilholm 1,* , Ewa Larsson 1, Emily Sonestedt 2 , Bodil Roth 1 and Bodil Ohlsson 1 1 Department of Internal Medicine, Skåne University Hospital, SE-20502 Malmö, Sweden; [email protected] (E.L.); [email protected] (B.R.); [email protected] (B.O.) 2 Department of Clinical Sciences, Lund University, SE-20502 Malmö, Sweden; [email protected] * Correspondence: [email protected] Abstract: Dietary advice constitutes a treatment strategy for irritable bowel syndrome (IBS). We aimed to examine the effect of a starch- and sucrose-reduced diet (SSRD) on gastrointestinal symptoms in IBS patients, in relation to dietary intake and systemic inflammatory parameters. IBS patients (n = 105) were randomized to a 4-week SSRD intervention (n = 80) receiving written and verbal dietary advice focused on starch and sucrose reduction and increased intake of protein, fat and dairy, or control group (n = 25; habitual diet). At baseline and 4 weeks, blood was sampled, and participants filled out IBS-SSS, VAS-IBS, and Rome IV questionnaires and dietary registrations. C-reactive protein and cytokines TNF-α, IFN-γ, IL-6, IL-8, IL-10, and IL-18 were analyzed from plasma. At 4 weeks, the intervention group displayed lower total IBS-SSS, ‘abdominal pain’, ‘bloating/flatulence’ and ‘intestinal symptoms´ influence on daily life’ scores (p ≤ 0.001 for all) compared to controls, and a 74%, responder rate (RR = DTotal IBS-SSS ≥ −50; RRcontrols = 24%). Median values of sucrose Citation: Nilholm, C.; Larsson, E.; (5.4 vs. 20 g), disaccharides (16 vs. 28 g), starch (22 vs. 82 g) and carbohydrates (88 vs. 182 g) were Sonestedt, E.; Roth, B.; Ohlsson, B. lower for the intervention group compared to controls (p ≤ 0.002 for all), and energy percentages Assessment of a 4-Week Starch- and Sucrose-Reduced Diet and Its Effects (E%) of protein (21 vs. 17 E%, p = 0.006) and fat (47 vs. 38 E%, p = 0.002) were higher. Sugar-, on Gastrointestinal Symptoms and starch- and carbohydrate-reductions correlated weakly-moderately with total IBS-SSS decrease for Inflammatory Parameters among all participants. Inflammatory parameters were unaffected. IBS patients display high compliance Patients with Irritable Bowel to the SSRD, with improved gastrointestinal symptoms but unaltered inflammatory parameters. Syndrome. Nutrients 2021, 13, 416. In conclusion, the SSRD constitutes a promising dietary treatment for IBS, but needs to be further https://doi.org/10.3390/nu13020416 researched and compared to established dietary treatments before it could be used in a clinical setting. Academic Editor: Giacomo Caio Keywords: dietary intervention; IBS; inflammation; starch; sucrose Received: 12 December 2020 Accepted: 26 January 2021 Published: 28 January 2021 1. Introduction Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Irritable bowel syndrome (IBS) is a functional gastrointestinal (GI) disorder with published maps and institutional affil- varying prevalence estimates of 4–11% depending on geography and the diagnostic cri- iations. teria used [1,2]. It is characterized by abdominal pain and altered bowel habits, in the absence of identifiable organic disease. Of IBS patients, 62–90% attribute aggravation of GI symptoms to intake of specific foods [3]. Accordingly, diet modification is employed as a primary treatment strategy. The National Institute for Health and Care Excellence (NICE) guidelines, which recommend regular meal patterns and decreased intake of mineral water, Copyright: © 2021 by the authors. caffeine, fat and spicy foods, are used as a first-line treatment for IBS [4]. As a second-line Licensee MDPI, Basel, Switzerland. treatment, the low FODMAP diet, which advocates exclusion of fermentable oligo-, di- and This article is an open access article distributed under the terms and monosaccharides and polyols, is an evidence-based dietary treatment commonly used in conditions of the Creative Commons the clinical setting [5]. Still, 20–50% of IBS patients do not experience reduced GI symptom Attribution (CC BY) license (https:// burden following NICE guidelines and/or a low FODMAP diet [6]. As such, research creativecommons.org/licenses/by/ is needed to identify symptom-inducing foods in IBS, in order to develop alternative, 4.0/). individualized dietary treatments. Nutrients 2021, 13, 416. https://doi.org/10.3390/nu13020416 https://www.mdpi.com/journal/nutrients Nutrients 2021, 13, 416 2 of 19 After initial digestion by mastication and salivary amylase, starch and sucrose are primarily digested by the sucrase-isomaltase (SI) enzyme in the ileum [7]. Previous re- search has identified an increased prevalence of rare SI gene variants in IBS patients [8,9], which confer reduced enzymatic activity and subsequent insufficient starch and sucrose digestion [10]. Unabsorbed carbohydrates may induce digestive symptoms through colonic fermentation or osmotic activity, resulting in bloating, flatulence, abdominal pain, and diarrhea [3,5]. Historically, clinical investigation of IBS patients has focused on identifying fructose and/or lactose intolerance, conditions identified in up to 70% of IBS patients [11]. In a recent study by Kim et al. [12], SI deficiency (SID) was identified through intestinal biopsy in 35% of patients with presumed IBS-D/M. These data warrant further study of the relevance of starch and sucrose intolerance in IBS. High dietary sugar intake has been proposed to increase subclinical inflammation, as shown by elevated C-reactive protein (CRP) in some previous studies [13]. Additionally, in- take of added sugar and sugar-sweetened beverages is associated with increased expression of proteins involved in inflammatory response signaling [14]. Diets rich in sugar, starch and saturated fats could activate the innate immune system through increased production of pro-inflammatory cytokines [15]. An association between IBS and elevated amounts of circulating cytokines, such as IL-6, IL-8, TNF-α, and IL 1β has been documented, although these results were not reproducible in other studies [3]. We have previously reported that IBS patients markedly improve their GI symptoms following a starch- and sucrose-reduced diet (SSRD) for 2 weeks [16]. Two hypotheses were raised: (1) the SSRD has continued positive effects on GI symptoms in IBS patients after 4 weeks and (2) improvements are related to a quantifiable decrease in starch and sucrose intake and reduced plasma CRP and cytokine levels. The primary aim of the present study was to evaluate the effect of the SSRD on IBS patients after 4 weeks. Secondary aims were to quantify and correlate significant changes in nutrient intakes and systemic inflammatory CRP and cytokine levels with GI symptom changes. 2. Materials and Methods 2.1. Study Design and Subjects The study was a randomized, open clinical trial with a 4-week dietary intervention in IBS patients. Patients with an IBS diagnosis, 18–70 years, with Northern European ancestry, were recruited from registries from Primary Healthcare Centers (PCC) (2015–2017) and the Department of Gastroenterology (2016–2017), Skåne University Hospital, according to the International Statistical Classification of Diseases and Related Health Problems–ICD-10. The recruitment process (Figure1 and Supplementary Figure S1) is described in a previous publication [16]. Initially, 2034 IBS patients from PCC and 789 IBS patients from the Department of Gastroenterology were identified. After exclusion of 1144 duplicates, 1679 patients remained. Invitation letters were sent to 528 randomly selected patients from the PCC and 151 patients from the tertiary healthcare center after exclusion of patients who had moved from the area or who had no available phone number. In a random order, patients were contacted via regular mail with information about the study. After- wards, follow-up calls were made to contacted patients and 145 were willing to participate (33 patients [23%] from the tertiary healthcare center; 111 women [77%]). Questionnaires covering sociodemographic and lifestyle factors, the Rome IV ques- tionnaire, the irritable bowel syndrome-severity scoring system (IBS-SSS), the visual analog scale for irritable bowel syndrome (VAS-IBS), the Bristol stool form scale (BSFS), and food diaries were sent to the 145 patients for completion during the run-in period, before an appointment at the Department of Internal Medicine. At the appointment, all patients were thoroughly examined by a physician and a medical history was taken. Anthropometric measurements of weight (kg) and height (m) in light in-door clothing, and systolic and diastolic blood pressures (mmHg) (Omron® automatic reading, Omron Electronics AB, Malmö, Sweden) in supine position were performed at study start, as well as after the study completion. The inclusion period lasted from January 2018 to February 2019. Nutrients 2021, 13, x FOR PEER REVIEW 4 of 21 Nutrients 2021, 13, 416 3 of 19 Assessed for eligibility (n=145) Excluded (n=40) ♦ Not meeting inclusion criteria (n=22) ♦ Declined to participate (n=18) ♦ Other reasons (n=0) Randomized (n=105) Allocation Allocated to intervention (n=80) Allocated to control (n=25) ♦ Received allocated intervention (n=80) ♦ Received allocated intervention (n=25) ♦ Did not receive allocated intervention ♦ Did not receive allocated intervention (n=0) (n=0) Follow-up Lost to follow-up