Tolerance and nutritional therapy of dietary fibre from konjac glucomannan hydrolysates for patients with inflammatory bowel disease (IBD)

Bioactive Carbohydrates and Dietary Fibre 2 (2013) 93–98

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Tolerance and nutritional therapy of dietary fibre from konjac glucomannan hydrolysates for patients with inflammatory bowel disease (IBD) P. Suwannaporna, K. Thepwongb, R. Testerc, F. Al-Ghazzewic,n, J. Piggottd, N. Shene, Z. Chene, F. Chene, J. Yange, D. Zhange, M. Tangc a

Department of Food Science and Technology, Faculty of Agro-Industry, Kasetsart University, 50 Ngam Wong Wan Road, Lat Yao, Chatuchak, Bangkok 10900, Thailand b Nopparat Rajathanee Hospital, 679 Ram-intra Road, Bangkok 10230, Thailand c Glycologic Ltd., 70 Cowcaddens Road, Glasgow G4 0BA, UK d Departamento de Alimentos e Nutrição, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista, Rodovia Araraquara, Jaú Km 1, 14801-902 Araraquara, SP, Brasil e Suining Chinese Medicine Hospital, 629000 Suining City, Sichuan Province, PR China

art i cle i nfo

ab st rac t

Article history:

Carbohydrates may provide an alternative therapeutic approach for a number of digestive

Received 4 July 2013

health disorders such as inflammatory bowel disease (IBD). The aim of this work was to

Received in revised form

characterise the tolerance and efficacy of low and high molecular weight konjac gluco-

30 August 2013

mannan hydrolysates within healthy volunteers and patients suffering from IBD and

Accepted 10 September 2013

associated gut conditions. These conditions included constipation, Crohn's disease and ulcerative colitis. For general tolerance, fourteen patients participated whilst for the

Keywords:

digestive disorder trial, there were twenty. Scores of taste/texture of the product, bowel

Konjac glucomannan hydrolysates

movement, stool consistency, diarrhoea, existence/absence of blood in the faeces,

Inflammatory bowel disease (IBD) Dietary fibre Nutritional therapy

abdominal pains, flatulence, vomiting, fever, improvement of life style after use, willingness to use in the future and clinician's statements about each patient's conditions before and after use were recorded. The results showed that the hydrolysates were tolerated well for patients with diarrhoea and had a significant improvement on bowel movement, stool consistency, abdominal pain and flatulence after ten days. With respect to effects on IBD, there was a significant health benefit after fourteen days of consumption for bowel movement, stool consistency, diarrhoea, existence/absence of blood in the faeces, abdominal pain, flatulence and vomiting. Most patients declared an improvement of their life style after consuming the hydrolysates. The use of konjac glucomannan hydrolysates as a therapeutic agent or adjunct to standard treatments could prove a successful tool for the treatment of a range of disorders; although large scale studies are required to characterise further the role of the carbohydrates. & 2013 Elsevier Ltd. All rights reserved.

n

Corresponding author. Tel.: þ44 141 331 3054; fax: þ44 141 331 8079. E-mail address: [email protected] (F. Al-Ghazzewi).

2212-6198/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.bcdf.2013.09.005

94

1.

Bioactive Carbohydrates and Dietary Fibre 2 (2013) 93 –98

Introduction

Inflammatory bowel disease (IBD) describes a number of multifactorial disorders which occur in the digestive system (Steed, Macfarlane, & Macfarlane, 2008) and are characterised by chronic inflammation of the gastrointestinal tract (Gentschew & Ferguson, 2012) due to abnormal immune responses (Chassaing et al., 2011). These intestinal disorders include Crohn's disease (CD) and ulcerative colitis (UC). Recent studies have reported that IBD conditions are initiated by genetic, environmental and abnormal immunological factors (Leenen & Dieleman, 2007). The disease development is affected by the diet, life style and other susceptible endogenous factors including the gut microflora (Gentschew & Ferguson, 2012). It has been suggested in recent years that the human bowel microbiota produce antigenic factors which initiate the chronic immune inflammation of the bowel mucosa defined as CD and UC (Sartor, 2003, 2008; Tannock, 2010). Interactions between a host and a microbial community represents a symbiotic relationship which have been shown to be favourable with respect to ‘prebiotic’ carbohydrates in the: mouth to protect against dental caries (Maitra, Rollins, Tran, Al-Ghazzewi, & Tester, 2013); gut (Chen, Cheng, Wu, Liu, & Liu, 2008; Connolly, Lovegrove, & Tuohy, 2010; Van Zyl, Rose, Trollope, & Görgens, 2010); vagina (Tester et al., 2012) and; skin (Bateni et al., 2013). According to the most recent definition of a prebiotic (Roberfroid et al., 2010), it is ‘a selectively fermented ingredient that results in specific changes, in the composition and/or activity of the gastrointestinal microbiota, thus conferring benefit(s) upon host health’. With respect to IBD, prebiotics change the composition of the intestinal microbiota toward more protective species and thus alters the systemic and mucosal immune responses of the host (Looijer-van Langen & Dieleman, 2009). The authors proposed that in addition to the changes in the intestinal microbiota, protective mechanisms of prebiotics include improving intestinal barrier integrity, regulating the mucosal and systemic immune response and the production of short chain fatty acids (SCFAs). One approach for the treatment of IBD involves using antibiotics (Table 1), although they often have side-effects and have limited success, especially for UC (Rahimi, Nikfar, Rezaie, & Abdollahi, 2007). This has led researchers to focus on finding alternative therapies for IBD-such as prebiotics, probiotics or a combination of the two (synbiotics). Introducing prebiotics as a therapeutic agent or adjunct to standard treatment could prove a successful tool for the treatment of a range of physiological disorders. Conflicting data from limited animal and human studies have reported on the impact of carbohydrates, especially prebiotics, on inflammatory bowel disease (IBD). In fact, nutritional management is considered to be an integral part of patients care in order to induce remission of CD (Russell, 1991; Smith, 2008; Basson, 2012). It has been found that fibre-rich unrefined carbohydrates have a positive effect on the treatment of CD (Heaton, Thornton, & Emmett, 1979) although Russell (1991) reported that diet does not alter the course of the disease. Videla et al. (2001) investigated dextran sodium sulphateinduced colitis in ninety five rats, by ‘treating’ the animals with

Table 1 – Overview of the current therapy regime for IBD. Therapeutic agent

Conditions of disease

Delivery method

5-Aminosalicylate (5-ASA) Corticosteroids

Mild to moderate

Oral, topical

Moderate to severe

Oral, topical, intravenous

Immunomodulators: e.g. – Azathioprine – 6-Mercaptopurine – Cyclosporine A – Tacrolimus – Methotrexateen

Moderate to severe steroid –dependent and steroid-refractory disease fistulising

Oral, topical, injection

Antibiotics: e.g. – Metronidazole – Ciprofloxacin

Active

Oral, intravenous

Biological therapies: e.g. – Adalimumab – Certolizumab pegol – Infliximab

Modern to severe fistulising

Intravenous infusion, injection

Probiotics and prebiotics e.g. – Escherichia coli Nissle 1917 – Fructooligosaccharide – Glucomannan hydrolysates

Remission maintenance

Ingestion

400 mg/day of inulin. This showed an improvement in the animals’ health. Work involving combinations of FOS with inulin has also shown a reduction in the inflammation (Hoentjen et al., 2005). In contrast, galacto-oligosaccharides fed to rats increased the amount of faecal bifidobacteria but had no effect on the reduction of inflammation for induced colitis (Holma, Juvonen, Asmawi, Vapaatalo, & Korpela, 2002). Furthermore, Cherbut, Michel, & Lecannu (2003) found that fructo-oligosaccharide (FOS) reduced the extent of tri-nitrobenzene sulphonic acid— induced colitis in rats. However, FOS had no effect on dextran sulphate sodium induced colitis in rats according to others (Moreau et al., 2003). Limited human trials focused on the treatment of both CD and UC have indicated a positive response to some carbohydrates (Calafiore et al., 2012; Lindsay et al., 2006; Casellas et al., 2007; Hussey, Issenman, Persad, Oiley, & Christensen, 2003; Hallert, Kaldma, & Petersson, 1991). Konjac glucomannan is a plant derived polysaccharide and has a long history of use as a traditional food source in Asia with interesting physical properties (Thomas, 1997; Zhang, Xie, & Gan, 2005). Native konjac glucomannan swells many times its (native) volume when hydrated. The rigid gel formed (which may cause choking) is used as a gelling agent, thickener, emulsifier and stabiliser in foods (Imeson, 2009).

Bioactive Carbohydrates and Dietary Fibre 2 (2013) 93 –98

The swelling limits its applications; particularly in nutritional and pharmaceutical products. These functional limitations can be resolved by depolymerising the native polymer (Khanna, 2003; Al-Ghazzewi, Khanna, Tester, & Piggott, 2007). This hydrolysis makes readily available prebiotic molecules for gut friendly bacteria to utilise effectively (Connolly et al., 2010). Human studies have indicated that konjac glucomannan hydrolysates may function as prebiotics in man (Huang, Liu, Yang, & Huang, 2007; Connolly et al., 2010). The depolymerisation removes the glucomannans ability to swell and thus make a strong indigestible bolus. The use of konjac glucomannan for the treatment of a range of physiological disorders including diarrhoea and IBD has been discussed elsewhere (Tester & Al-Ghazzewi, 2013). The aim of the present study was to characterise the tolerance and efficacy of konjac glucomannan hydrolysates for promoting bowel health within a range of digestive conditions. These include constipation, UC and CD.

2.

Glucomannan hydrolysates from konjac flour with different molecular weights (o10,000 Da, ‘GMH’) and (410,000 Da, ‘AMH’) were prepared by Glycologic Limited as reported elsewhere (Al-Ghazzewi & Tester, 2004). These hydrolysates were used to study the tolerance and nutritional effects on IBD at the Suining Chinese Medicine Hospital, 629000 Suining City, Sichuan Province, China with ethical approval (Ref. 200903) and the Nopparat Rajathanee Hospital, 679 Ram-Intra Road, Bangkok 10230, Thailand (Ref. 027/55), respectively.

2.1.

abdominal pain, flatulence and vomiting were recorded at days zero and ten.

2.2.

Tolerance

A total of fourteen male and female participants aged 20 to 78 suffering from diarrhoea for different reasons, including food poisoning were included in this study. Participants’ consents were obtained prior to the study then assigned to receive 3.3 g per day GMH dissolved/dispersed in 150 ml water for ten days. Scores of the effects of the hydrolysates including average number of bowel movements, stool consistency,

Nutritional effects on IBD

A total of twenty patients were selected according to their IBD symptoms which were constipation/diarrhoea, CD and/or UC. Symptoms recorded were from inpatient, outpatient and chronic patient gastrointestinal hospital departments. Participants’ consents were obtained prior to the study and they received 3.3 g per day AMH dissolved/dispersed in 150 ml water for fourteen consecutive days. Scores (Table 2) of taste/ texture, bowel movements, stool consistency, diarrhoea, existence/absence of faecal blood, abdominal pain, flatulence, vomiting, fever and any improvement of life style after use were recorded at days zero, seven and fourteen. Patients’ willingness to use the product in the future and the clinician's statements about the patients’ bowel disorders before and after use were also recorded.

2.3.

Materials and methods

Statistical analysis

Statistical differences were determined by Friedman Test and Wilcoxon Matched Pairs Test using Minitab 15 (Minitab Inc., State College, PA). The results were considered significant when P-values were nPo0.05, nnPo0.01, nnnPo0.001.

3.

Results and discussion

Konjac glucomannan hydrolysates were well tolerated when ingested. Statistical analysis using Wilcoxon Matched Pairs Test between day zero and ten for consumption of the material showed significant benefits for bowel movement (Po0.005), stool consistency (Po0.005), abdominal pain and flatulence (Po0.01) but no-significant effect on vomiting (Fig. 1). Regarding the nutritional effects on IBD, there was a significant difference between days zero and fourteen for bowel movement (Po0.05), stool consistency, diarrhoea, absence/existence of blood in faeces, abdominal pain, flatulence and vomiting (Po0.001). Scores for fever symptoms showed no-significant difference (Fig. 2). A significant number (Po0.001) of patients adapted to

Table 2 – Measurements scores used to record the symptoms of patients. Symptoms

95

Score 0

1

2

3

4

Numbers of bowel movements Diarrhoea Stool consistency Abdominal pain

None

Present

Present

Present

Present

– – –

Absent Formed None

Flatulence

–

None

Vomiting Fever Improvement of life style Use again

– – –

Absent Absent None

Slight Loose Slight but well tolerated Slight but well tolerated Slight Slight Slight

Often Watery Moderate and interfering with but not preventing daily activities Moderate and interfering with but not preventing daily activities Often Moderate Moderate

Very often Bloody Severe and preventing normal daily activities Severe and preventing normal daily activities Very often Severe Too much

–

No

Possible

May be

Definitely

96

Bioactive Carbohydrates and Dietary Fibre 2 (2013) 93 –98

Fig. 1 – Effects of konjac glucomannan hydrolysates (GMH) on bowel movement, stool consistency, abdominal pain, flatulence and vomiting for patients suffering from diarrhoea after ten days of treatment. GMH¼ Molecular weighto10,000 Daltons, nnPo0.01, NS¼not significant.

Fig. 2 – Effects of konjac glucomannan hydrolysates (AMH) on bowel movement, stool consistency, diarrhoea, blood in faeces, abdominal pain, flatulence, vomiting and fever for patients with inflammatory bowel disease (IBD) symptoms after zero, seven and fourteen days of treatment. AMH¼ Molecular weight 410,000 Daltons, nPo0.05, nnn P o0.001, NS¼ not significant.

the taste and texture of the material and favoured using it by the end of the trial. Also, a significant (Po0.001) number of patients participating in the trial declared there was an improvement of their life style after consuming the hydrolysates and would use the material again. Overall these data are very positive with respect to tolerance and health. The discomfort and symptoms associated with IBD appear to have been eased due to the hydrolysed glucomannan—probably as a consequence of many of the biological benefits it can deliver (Tester & AlGhazzewi, 2009, 2013; Tizard, Carpenter, McAnalley, & Kemp, 1989). These properties/roles include (i) soluble dietary fibre; (ii) prebiotic; (iii) capacity to bind pathogens and prevent them from binding to epithelial cells (e.g. in gut); (iv) capacity to stimulate topical healing and immune responses; and (v) capacity to generate systemic immune responses.

It is likely that the glucomannans play a broad role of activities in the gut that are highlighted within IBD suffers (as studied here) although applicable to broader aspects of gut health. The effects relate to creating a healthy gut microbiota and binding (Hickey, 2012) to pathogens (facilitating removal from the body) in parallel with direct effects on the gut mucosa to help counter the underlying cause of inflammation etc. These effects may be mediated by components of the local or systemic immune system. Konjac glucomannan is used as a gelling agent, thickener, emulsifier and stabiliser in foods (Imeson, 2009). Interestingly, it has a number of desirable nutritional characteristics which include: providing dietary fibre (Chiu & Stewart, 2012); as an aid to avoid constipation (Chen et al., 2008); a laxative (Chen, Cheng, Liu, Liu, & Wu, 2006); help with the management of diverticulitis (Latella et al. 2003; Frieri, Pimpo, & Scarpignato, 2006; Petruzziello, Iacopini, Bulajic, Shah, & Costamagna, 2006); satiety (Keithley & Swanson, 2005); a fermentable substrate (Chen, Fan, Chen, & Chan, 2005) in the colon (prebiotic); restricting the growth of pathogens in the gut (Elamir et al., 2008) plus; control of cholesterol and glucose absorption (Arvill & Bodin, 1995; Gallaher et al., 2002; Sood, Baker, & Coleman, 2008). It has been reported that both native and hydrolysed konjac glucomannans have positive health benefits in the gut (Elamir et al., 2008; Pan, Chen, Wu, Tang, & Zhao, 2009; Tester, & Al-Ghazzewi, 2009, 2013). Chen et al., (2008) reported that native konjac flour can promote bowel movement by thirty percent and improve colonic ecology in constipated adults. Human faecal gut models have indicated that hydrolysed konjac glucomannan may function as a prebiotic in man (Connolly et al., 2010). In human consumption trials, Huang et al. (2007) reported that konjac glucomannan hydrolysates promote the growth selectively of probiotic bacteria (both lactobacilli and bifidobacteria). According to some authors, it is in fact a more effective prebiotic than native konjac glucomannan (Chen et al., 2005). The ability of konjac glucomannan hydrolysates to function as a prebiotic and to their capacity to inhibit certain bacteria (especially Escherichia coli) from attaching to epithelial cells (Becker & Galletti, 2008; Al-Ghazzewi & Tester, 2013) in the gut may reduce pathogen bacterial colonisation. Hence, this may prevent pathogen ability to initiate and induce chronic immune inflammation of the bowel mucosa, especially chronic inflammations observed in Crohn's disease (Eaves-Pyles et al., 2008). In total, there are many nutritional benefits of consuming glucomannans in the diet. The possibility that these carbohydrates may have a positive impact on IBD is intriguing and may be due to a number of factors. These include a prebiotic role, pathogen binding, tissue regeneration and topical or systemic immune role.

4.

Conclusions

The hydrolysed konjac glucomannan was well tolerated and the symptoms associated with IBD appear to have been eased due to the biological effects of the hydrolysates. Introducing such carbohydrates as a therapeutic agent or adjunct to standard treatment could prove a successful tool for the

Bioactive Carbohydrates and Dietary Fibre 2 (2013) 93 –98

treatment of a range of physiological disorders although large scale studies in humans are required to characterise further the specific role of these carbohydrates.

Acknowledgements The authors would like to thank all staff from the Suining Chinese Medicine Hospital, China and the Nopparat Rajathanee Hospital, Thailand.

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