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Home , Dietary fiber

Aaron I. Vinik, MD Dietary in David J.A. Jenkins, MD Management of

Current evidence suggests that high-fiber diets, elderly, or growing children, may require supplements especially of the soluble variety, and soluble fiber of and trace . People with upper supplements may offer some improvement in gastrointestinal dysfunction are at risk of bezoar , lower total and formation and cautioned against a high in fiber of low-density lipoprotein (LDL) cholesterol, and have the leafy type. Careful attention must be paid other beneficial effects in patients with non-- to insulin dose because hypoglycemia can result if there dependent diabetes mellitus (NIDDM). Diets enriched is a radical change in fiber intake and insulin dose is not with and induce 10-20% reduced appropriately. Care must be exercised in the reductions in serum cholesterol and LDL in both normo- use of "novel" , including the wood , and hypercholesterolemic subjects and have the ability because little is known of their safety and efficacy. to blunt the hypertriglyceridemic effects of diets high in Diabetes Care 11:160-73,1988 carbohydrate and low in fiber. In insulin-dependent diabetes mellitus (IDDM) the situation is less clear, but a decrement of the circadian profile has been shown. Americans, in general, consume too little fiber. With the need to restrict fat and reduce protein, an increase in is mandatory. A practical goal he diabetic diet has undergone considerable re- would be to establish the present level of fiber intake (15-30 g/day) and to gradually increase it. An intake of vision, often without scientific basis, yet a num- up to 40 g of fiber per day or 25 g/1000 kcal of ber of highly controversial issues remain. Central intake appears beneficial; in many individuals on Tto these issues is the liberalization of carbo- weight-reducing diets higher levels may be unacceptable hydrate intake and the recommended increases in because of gastrointestinal side effects. The level of consumption of fiber. In the 1971 guidelines of the maximum benefit has not been determined. Fiber American Diabetes Association (ADA), a liberalized supplementation appears beneficial only if given with carbohydrate intake was recommended but no specific a diet comprising approximately half of the calories as mention of the fiber content was made (1). In the 1979 carbohydrate. should be selected with moderate policy statement, the ADA recommended reducing the to high amounts of dietary fiber from a wide variety of intake of fat and increasing that of complex carbohy- choices to include both soluble and insoluble types of fiber. Insufficient data are available on the long-term drates to -50% of the total calories with the ingestion safety of high-fiber supplements. People at risk for of foods high in fiber as desirable (2). Dietary advice to deficiencies, such as postmenopausal women, the patients with diabetes continues to emphasize the vir- tues of complex carbohydrates rich in fiber, but the dogma is coming under closer scrutiny and remains a controversial issue (3-6). These diets are substantially different from the average American diet, and it has been From the Departments of Internal Medicine and Surgery, The University of Michigan, Ann Arbor, Michigan, and the Departments of Medicine and Nutri- suggested that they may not be effective if the insulin tional Sciences, St. Michael's Hospital, University of Toronto, Toronto, Canada. secretory capacity is compromised. These diets may prove Address correspondence and reprint requests to Aaron I. Vinik, MD, Univer- sity of Michigan Medical Center, 2922 B. Taubman Health Center, 1500 E. unacceptable in certain people and may have untoward Medical Center Drive, Ann Arbor, Ml 48109. effects in patients with autonomic neuropathy (7,8). In

160 DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 A.I. VINIK AND D.J.A. JENKINS

addition, they have not been tested adequately in spe- These epidemiological leads and the evidence that cial subsets of patients whose and status has accumulated on use of fiber in treatment of diabetes may in the long term be at risk. have led to recommendations by the American (2), Ca- We briefly review the history of dietary vicissitudes in nadian (32), and British (33) Diabetes Associations to diabetes, including what the term fiber means and its increase fiber as a means of reducing the postprandial possible mode of action. More recent studies will be blood glucose rise. In fact, the American College of reviewed that have shed light on the value of fiber man- Cardiology has now adopted these recommendations. agement of diabetes, , , and the However, diabetes is a complex disease in which the special needs of subsets of patients with diabetes. Rec- exact relevance of postprandial hyperglycemia is not ommendations will be made that are based on the evi- always clear, and the issue of reducing the fasting or dence adduced. basal blood glucose appears more important. Also obes- ity and hyperlipidemia may be of greater consequence in the long term than postprandial hyperglycemia. Be- HISTORICAL NOTE fore embarking on an examination of the different stud- ies and their implications, the definition of the term fiber High-carbohydrate diets are not new to diabetes. More and its proposed mechanism of action must be dis- than 2000 years ago, physicians in India were treating cussed. type II (non-insulin-dependent) obese diabetic patients with high-carbohydrate diets containing grains and . Some 1900 years ago, Aretaeus of Cap- DEFINITION OF DIETARY FIBER padocia (9) advised people with the symptoms of dia- betes to eat a diet consisting of milk, , and . Many terms have been used interchangeably to refer to Other famous protagonists of high-carbohydrate diets fiber. It has most recently been defined as "endogenous were von Duering (10), who in 1868 introduced the components of material in the diet which are re- diet, Mosse (11), who developed the diet in 1903, sistant to digestive enzymes produced by man. They are and van Noorden (12), who in 1912 recommended - predominantly nonstarch and and as a cure. It took almost a quarter of a century for may include, in addition, associated substances" (34,35). these suggestions to be examined seriously, and Hims- Dietary fiber should not be confused with crude fiber, worth in 1935 (13) showed that in normal healthy sub- which is a term referring to the residue of plant food jects the ingestion of a diet high in carbohydrate im- remaining after the sequential extraction with a solvent, proved glucose tolerance. This he attributed to increased dilute acid, and alkali (36) and eliminates hemicel- insulin sensitivity. lulose and soluble fiber fractions, giving a value that The first suggestion that dietary fiber may be involved may be one-fifth that of the true dietary-fiber value (37). with diabetes was made by Trowell (14). Diabetes was Several other terms are loosely used interchangeably rare in the ancient empires of Rome and Greece. It was as "fiber" but do not necessarily mean the same. Resi- also rare in primitive people living in rural East Africa due or bulk refers to the indigestible content of food who had high-fiber intakes but became prevalent with such as is found in plant fiber but is also used to refer the processing of food. Trowell also noted that the di- to increases in fecal output regardless of whether any abetes mortality during World War II closely followed portion of the food being referred to remains in the colon the use of low-extraction, low-fiber white flour in place after digestion. Roughage describes certain types of foods of the high-extraction, high-fiber natural flour (15). In in the diet and includes high-fiber foods. Bulk simply 1976, Trowell hypothesized that fiber-depleted diets are refers to that component of foods that has the capacity conducive to diabetes in susceptible human genotypes. to retain water and thereby to increase the weight of the This hypothesis is supported by the relative rarity of di- stool, such as wheat bran, which is a by-product of the abetes in adult African men (1%), who consume 10-25 milling process and comprises the outer layers of the g of crude fiber per day, and the frequency of diabetes wheat grain including the aleurone layer. in American and British men (>3%), who eat 3.5-11 g The quantitation of total dietary fiber has proved dif- of crude fiber per day (16-18). ficult until recently because of the lack of appropriate In the mid to late 1970s, Anderson and colleagues methodology. The Association of Official Analytical (19-22) showed that diabetic subjects fed a diet high in Chemists (AOAC), after conducting an extensive study carbohydrate and fiber had reduced blood glucose lev- (36), agreed to accept a standard method (37,38) for els and diminished insulin requirements. At the same measuring total dietary fiber in food based on the en- time, Jenkins and colleagues (23,24) demonstrated that zymatic degradation and gravimetric determination of purified viscous fiber without alteration in the carbo- the residue. The needs of physiologists, however, differ hydrate intake reduced postprandial glucose and insulin from those of the analytical chemists. A standardized responses to test in both diabetic and nondiabetic method is needed to quantify the content of the water- volunteers. Addition of purified viscous fiber to meta- soluble and -insoluble components and identify the bolic diets resulted in reduced urinary losses of glucose individual , polygalacturonic acids, ga- and ketone bodies (25). The results of these studies have lactomannans, (3-, rhamnogalacturans, arabi- been confirmed by others (26-31). nogalactans, and others that may contribute to the ef-

DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 161 DIETARY FIBER

fects observed. Among the methods currently available addition, the safety and efficacy of these fibers have not to measure these various subfractions, the Southgate been evaluated; the mechanism of action of these fibers chemical fractionation procedure (37) coupled with gas- will be reviewed in more detail. liquid chromatography (38) appears to be the best avail- able standard; it has been used by Anderson (39) to derive an extensive list of the fiber content of various PHYSIOLOGIC EFFECTS OF FIBER foodstuffs in common usage. For convenience, fibers may be divided into two broad The suggested benefits of increased intake of fiber in- classes: the so-called soluble and the insoluble. The sol- clude not only the reduction in postprandial rise in blood uble consist of the gums, gels, mucillages, pectic sub- glucose concentration but also lower basal glucose con- stances, and a portion of what used to be called the centration, enhanced sensitivity to insulin, and lower . The insoluble consist of the noncarbo- cholesterol level. Any theories of the mechanism of ac- hydrate fiber component, lignin, , and some of tion of fiber should therefore address all these obser- the hemicelluloses, especially those combined with lig- vations. nin. In general, it is the soluble fibers that have been Altered transit time. Early studies indicated that fiber demonstrated to have effects on carbohydrate and lipid of the gelling variety was capable of reducing the rate metabolism. They are fermented to gas and short-chain of bulk-phase diffusion in a model for fatty acids in the colon and contribute little to fecal bulk absorption (40). However, subsequent studies focused because the acids are rapidly cleared. The insoluble fi- on the effect of viscous fiber to delay gastric emptying bers, on the other hand, are largely responsible for in- time (41). It was thought that the slowing of gastric emp- creasing the bulk of the but have little metabolic tying was the most important mechanism for the ob- effect. The effects of the soluble fibers may relate to their served effects of fiber coupled with the information that, ability to reduce the rate of absorption of from when added to meals, postprandial hyperglycemia was the bulk phase in the lumen of the small intestine (40). reduced. However, the results of gastric emptying stud- In addition, soluble fibers appear to prolong the rate of ies depend on the conditions at the time of testing. Much gastric emptying and intestinal transit time (41). The in- of the work relating to the slowing of gastric emptying soluble fibers have the opposite effects, reducing gastric by guar gum and used hypertonic liquid test meals emptying and intestinal and colonic transit times (42). (41,47,48) and the results may not be relevant to the There have been several attempts to determine whether emptying of solid meals of dry matter (49,50). Harju et the effects of fiber can be predicted on the basis of its al. (51,52) have used pectin and guar gum to relieve physiochemical properties. The specific symptoms of patients with dumping syndrome. In the composition of each plant food may contribute to its latter study, prolongation of the gastric emptying time biologic effects. The more in a plant food, the for solids was noted with guar (52). Blackburn et al. (53) greater its ability to increase fecal bulk. There is also have shown that in diabetic subjects, although there is evidence that particle size may be critical and the mill- a delay in gastric emptying and glucose levels are re- ing process may yield particles that are coarse, which duced, there is no correlation between the two, sug- have been shown to normalize intestinal transit time gesting that this mechanism might contribute but cannot (43), whereas fine bran may have much less effect on be the sole mechanism contributing to the reduced post- fecal bulk and may even induce (44). prandial responses. and drying, boiling, or pureeing of cereals, len- Effects within small intestine. The soluble fibers, e.g., tils, or may disrupt the fiber structure or other as- guar and pectin, increase intestinal transit time (41), pects of the food and result in the loss of capacity to whereas the insoluble fibers such as wheat bran and normalize metabolism with lower postprandial levels of decrease the intestinal transit time and in- glucose and insulin (45). Nevertheless, an exact quan- crease intestinal bulk. Studies with D- have shown titation of the effects of fiber on homeostasis based on that the glucose-lowering effects may be a consequence the physiochemical properties is difficult. of decreased rate of carbohydrate absorption rather than The claim of "high-fiber food" by various manufac- increased total glucose utilization or suppression of he- turers needs to be viewed with caution if the nature of patic glucose production (40). The possible effects of the fiber and its effect on the food have not been dem- fiber within the small intestine include changes in mix- onstrated. There are a number of "novel" fibers that do ing, motility, and convection; intraluminal digestion not occur naturally. In addition, nonabsorbable carbo- rates; thickness of the unstirred layer; inhibition of max- hydrates are generated in the food preparation process, imum transport capacity; altered pH profile; and, with and even the physiochemical properties of the endog- long-term treatment, altered intestinal morphology. enous fiber are altered. Purified cellulose preparations Blackburn et al. (53), on the basis of small intestine are being used as a means of fortifying foods commer- perfusion studies in normal individuals, suggested that cially (46) and wood cellulose has been used on the fiber inhibited intestinal motility and thus decreased assumption that it represents natural fiber. Evidence is convection. There is also some evidence from in vitro lacking that these fibers will produce the effects asso- studies that the thickness of the unstirred layer may be ciated with the ingestion of fiber-containing foods. In increased by the tendency of the soluble fibers to form

162 DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 A.I. VINIK AND D.J.A. JENKINS

gels and thus to effectively create a gel-filtration system izable groups such as the uronic acid residues of the with the gut (42). However, studies in humans showed and hemicelluloses. This property enables some that only with pectin was there evidence of an increase fibers to bind minerals (64) such as calcium, , and in the thickness of the unstirred water layer. With guar and to bind organic substances as well (65,66). this was not found and here the weight of evidence Insoluble fibers such as cellulose have been shown to points to a reduced rate of bulk diffusion (53). There is bind Ca2+, and the presence of phytin foods, rich in also speculation that fiber may package carbohydrate insoluble fiber, have been associated with minimal de- molecules and insulate them from the digestive enzymes ficiency. It has been suggested from in vitro studies that in the intestine and decrease access to the intestinal wall fiber in the diet may bind cholesterol and bile salts in (50). Certain high fibers may have antienzyme activity the gut, thus interfering in the enterohepatic circulation (50). Fiber has been shown to reduce pancreatic en- of cholesterol (67,68). Changes in lipid metabolism sug- zyme activity and decrease pancreatic enzyme secretion gest that fiber may exert actions in the intestine that (54,55). facilitate the lipid- and cholesterol-lowering effects of Gut hormone effects. As might be expected from its fiber (69,70). These include effects on low-density chy- ability to alter the rate and site of absorption in lomicra synthesis and the site of absorption of lipids the gut, dietary fiber has been shown to influence the (69-79). Alternative mechanisms embrace the altered release of gut hormones. The response of gastric inhib- very-low-density lipoprotein (VLDL) turnover discussed itory polypeptide (GIP), a stimulus for insulin secretion, elsewhere in this issue. was more attenuated in healthy diabetic subjects and in Effects in large bowel. Bacterial of fiber patients with postgastrectomy dumping syndrome after in the colon generates short-chain fatty acids that may ingesting fiber-supplemented meals than after control inhibit mobilization and intestinal synthesis meals (56,57). With smaller amounts of fiber, Levitt et and decrease gluconeogenesis (45,53). Indeed, this has al. (7) found no reduction in GIP response to a mixed been the basis of the development of a number of pu- meal but did record distinctly lower plasma glucagon tative oral hypoglycemic agents. The role of the short- responses, an observation confirmed by others (58). Al- chain fatty acids in enhanced glucose utilization, insulin though this may have contributed to the lesser hyper- secretion, and hepatic glucose utilization needs further glycemia, it may be due to reduction in elaboration. absorption with the fiber-supplemented meal. An inter- esting observation has been the demonstration of an en- hanced release of plasma somatostatin with fiber (59). Somatostatin delays the absorption of carbohydrate and EFFECTS OF HIGH-FIBER DIETS ON PATIENTS glucose from the small intestine and could be partly WITH DIABETES mediating the effects of fiber. Further studies are clearly needed. Two major approaches have been used to study the ef- Peripheral metabolic effects. Numerous studies have fects of fiber on carbohydrate metabolism in diabetes: demonstrated that the lowered blood glucose levels seen the first uses purified fiber such as guar and pectin, and after fiber consumption are associated with either un- the second increases the fiber content of the diet with changed or lowered insulin levels (49,56). These acute normally available fibers. There are many papers in the effects cannot be ascribed to increased insulin sensitivity literature dealing with the role of dietary fiber in man- but may be due to the slowed rate of intestinal transit agement of diabetes. All have made important contri- and an attenuated stimulus; however, the observation butions to understanding the possible role of fiber; how- in some studies that chronic ingestion of fiber is asso- ever, it has been difficult to arrive at a consensus opinion ciated with lower basal glucose levels and decreased because of the widely different strategies used to study urinary excretion of C-peptide (60,61) suggest an in- the problem. Studies have used different types of fiber crease in insulin sensitivity or a decreased demand for that may have very different effects, and the dose of fiber insulin. Indeed, in the studies where this has been ex- used has varied among studies. Soluble and insoluble amined (62-64), an increase in insulin binding to mon- fibers whose effects may counteract each other have ocyte receptors for insulin has been found. This effect been used in combination. Studies that examined acute may clearly have some importance in the obese patient. effects or studies carried out for only short periods in a The changes in binding, however, must be separated metabolic ward may not necessarily apply in the home from those of weight reduction and improvement in di- or natural environment. Altering fiber and macronutrient abetes control. content of the diet has led to difficulty in ascribing the Using an artifical pancreas (Biostator), Christiansen et effects to fiber alone. Separation of the effects of fiber al. (65a) endeavored to measure the effect of guar on from those of weight reduction, , car- insulin requirements in seven patients with insulin-de- bohydrate restriction, and the initial level of diabetes pendent diabetes mellitus (IDDM). They found that the control have all made interpretation difficult. Testing the mean 24-h requirements were reduced by 12.4%. effects of fiber on plasma lipids and lipoproteins has Absorption of organic substances. The cation-ex- been inconsistent. The evaluation of responses based on change capacity of fibers relates to their content of ion- the different reports with fasting blood glucose, post-

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prandial glucose, urinary glucose, and HbA, has been sulin requirements were sustained for studies lasting up highly varied. to 1 yr. Several early investigators, including Jenkins et al. in Until recently, however, no acceptable purified fiber Oxford (79,80), Levitt et al. in South Africa (7), and preparation was commercially available for clinical use. Goulder and colleagues in Britain (57,81), have dem- Currently, several preparations are available, and these onstrated that the addition of the unabsorbable polysac- have been employed in studies in Europe and more re- charides guar and pectin reduced postprandial glycemia cently in the United States and elsewhere. in both normal and diabetic subjects, often with a re- Several new studies from England, Ireland, and Fin- duced need for insulin secretion. The fibers that were land were described at a Guar Symposium held in Lon- most effective were those with the highest (40), don in December 1985. Most studies showed beneficial which may be related to an effect on the slowing of effects of adding varying amounts of guar to the regular gastric emptying (40,41), or limited diffusion of diges- meal plan but were short term and not well controlled tive products (40,42). To be effective, the fiber had to (88). be incorporated into the food (82), because fiber that was given in capsule (83), sprinkled on food (84), or taken before a meal (85) was found to be ineffective. INCREASING FIBER IN ORDINARY FOODS The ingestion of fiber with one meal was found to retard the hyperglycemia with a second meal (60). Nonviscous Rather than supplementing diets with purified fibers, fibers such as those found in wheat bran had less marked many investigators have studied the relationship of diet effects than the viscous fibers that were reported to be to diabetes control by modifying the traditional diabetic successful (27,69,86,87). The acute effects of fiber may diet by use of ordinary foods high in fiber content. These be dose dependent. Both glucose and insulin responses diets generally contain substantial amounts of foods in were lowered in diabetic subjects given test meals sup- which the carbohydrate is slowly digested and absorbed plemented with a total of 26 g guar and pectin. Glucose and could also be described as lente carbohydrate (89). response fell 30% in IDDM and from 30 to 60% in non- Legumes such as and produce the least rise insulin-dependent diabetes mellitus (NIDDM) with a 42 in blood glucose (90). Anderson et al. (20-22,77,91) to 60% decrease in the insulin response (56,79). In the devised high-fiber diets that have been very successful studies carried out by others, the reduction in the insulin in improving diabetic control. These diets contain 70% response was not found with 9-18 g but did occur with carbohydrate and 35 g dietary fiber/1000 kcal. Both 26 g, suggesting a dose-dependent effect (Fig. 1). IDDM and NIDDM patients on this regimen for 16-18 Test-meal studies were followed up with short-term days showed significant decreases in both fasting and metabolic studies in which 14-26 g guar given daily, postprandial glucose concentrations. A majority of pa- mixed with the food, reduced the urinary glucose and tients had decreased or discontinued insulin or sulfo- 3-hydroxybutyrate losses by 40% compared with the nylurea therapy (77,91). Those patients who followed control period. In further studies with guar crispbread, high-fiber maintenance diets with 60% carbohydrate for relative reductions in fasting blood glucose were seen. up to 15-21 mo have shown additional reduction in Such findings were confirmed in longer-term studies with fasting blood glucose levels that enabled further de- a guar granulate that demonstrated, in addition, im- crease or discontinuation of the hyperglycemic medi- proved postprandial blood glucose levels and lower in- cation. Many obese subjects were able to decrease their sulin responses. Reduced urinary glucose levels and in- insulin dose or discontinue sulfonylurea on the high- carbohydrate high-fiber diet. The greatest reduction in EFFECTS OF FIBERS ON CHOLESTEROL AND GLUCOSE glucose levels and insulin doses, however, occurred in those who had the greatest degree of weight reduction (92). In a 6-wk study, Simpson et al. (26) reported a modest reduction in fasting and postprandial glucose concentrations but a significant reduction in 24-h urine glucose on a diet containing large amounts of legumes. In this study and others, however, it was difficult to determine whether the improved glucose control was due to the high-carbohydrate content of the diet or the o rate of digestion of the starch or the fiber (93). Q HI oc 0 10 20 30 LONG-TERM EFFECTS % REDUCTION OF FASTING BLOOD GLUCOSE

FIG. 1. Compilation of data in literature showing bene- Contrasting with these observations are those of an 8- ficial effects of soluble fibers on cholesterol and glucose wk metabolic study in which the amount and source of and relatively weak or negative effects of insoluble and the carbohydrate were kept constant and the fiber was fruit fibers. either low (11 g/1000 kcal) or high (27 g/1000 kcal)

164 DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 A.I. VINIK AND D.).A. JENKINS

(94,95). No significant effects were found in glucose cemic control between the two diets. Almost identical control, postprandial , or HbA, or in the insulin findings have been reported by Riccardi et al. (74). Thus, requirements in adult patients with NIDDM. whereas digestible carbohydrate may have a small effect The problems in interpreting findings is further illus- on fasting blood glucose levels or basal blood glucose trated by the impact of the associated carbohydrate con- levels, the predominant effect of high-carbohydrate high- tent of the diet on the effects of fiber. Studies with guar fiber diets results from the increase in dietary fiber. Fur- had only demonstrated consistent effects in reducing thermore, increasing carbohydrate but not dietary fiber urinary glucose levels where patients were on higher results in a significant decrease in HDL cholesterol. For carbohydrate intakes. Riccardi et al. (74) studied the fiber to exert its optimum effect, it may have to be given effects of three outpatient diets (low CHO, 42%, low as a part of a high-carbohydrate diet. Viscous fiber added fiber, 20 g; high CHO, 53%, low fiber, 16 g; and high to a low-carbohydrate diet of diabetic patients appears CHO, 53%, high fiber, 54 g) over a 10-day period and to have little effect (50) in contrast to the same fiber found that improved glucose tolerance was observed added to high-carbohydrate diets, where consistent im- only with the high-carbohydrate high-fiber diet. provements were seen. Mann (61) examined 18 patients with NIDDM on a low-carbohydrate diet in a crossover design with a high- carbohydrate diet rich in cereal, vegetable, and fruit fiber. Each diet was carried out for a period of 6 wk FIBER ENRICHMENT OF and, after a metabolic profile, the diets were reversed HIGH-CARBOHYDRATE FOODS for a further 6 wk, after which the volunteers were ad- mitted for a final 24-h profile. Carbohydrate comprised Perhaps an ideal way to achieve the maximum fiber 59% of the total energy, with 44 g total dietary fiber. In effect is to incorporate the most effective soluble fiber patients with IDDM as well as those with NIDDM a forms into starchy foods. The mixing that seems impor- significant improvement was seen in fasting and pre- tant to ensure maximum effectiveness of fiber is thereby prandial blood glucose levels as well as in the HbA!. achieved, and the higher carbohydrate content of the No significant change was found, however, in post- diet is also ensured. This was achieved early with guar- prandial glucose levels. In a further series of experi- enriched crispbread, and long-term studies became pos- ments, the incorporation of substantial quantities of sible that had not been possible previously due to poor cooked dried beans into ordinary meals (e.g., haricot, palatability of purified guar and pectin. red kidney beans, and ) as a source of soluble fiber Gatti et al. (96) in Italy produced guar-enriched was examined in both IDDM and NIDDM patients (93). that was fed in chronic studies to normal, diabetic, and Significant reduction was found in the basal, prepran- hypercholesterolemic patients. A significant improve- dial, 2-h postprandial, daily mean, and 24-h urine glu- ment in plasma glucose, daily glucose profile, and gly- cose excretion on this high-carbohydrate diet. In addi- cosuria was observed. In hyperlipidemic subjects a tion, total and low-density lipoprotein (LDL) cholesterol reduction of and a significant hypocho- levels fell without any associated increase in lesterolemic effect were demonstrated. levels. High-density lipoprotein (HDL) cholesterol and Thompson and colleagues (97) compared the acute HDL/LDL ratio tended to increase (28). response in 19 IDDM and NIDDM diabetic subjects to These findings have been confirmed and appear to three test meals (white , control pasta, and guar- apply equally well to diabetic children (24). These stud- enriched pasta), each containing 50 g available carbo- ies, however, were done in both NIDDM and IDDM hydrate. They found the least postprandial rise in the patients who were relatively well controlled. Patients group receiving guar pasta (4.4 ± 0.5 vs. 5.4 ± 0.4 mM who had NIDDM were more prone to significant de- in control pasta). Furthermore, guar significantly re- grees of hypoglycemia; 6 wk of this high-carbohydrate duced the incremental glucose area under the 3-h glu- diet caused a significant reduction in HbA, (from 10.6 cose-response curve. Urinary C-peptide and urinary glu- to 8.5%), fasting glucose dropped from 9.6 to 6.8 mM, cose were also significantly reduced by guar. No preprandial glucose from 9.9 to 7.5 mM, and the 2-h difference was seen between IDDM and NIDDM pa- postprandial glucose from 12.1 to 10.8 mM. Mean tients. The authors concluded that enriching commonly 24-h blood glucose profile was also markedly improved, eaten foods with guar appears an effective method of with a reduction from 11.6 to 9.3 mM (21). reducing blood glucose levels and urinary glucose levels In the 1970s, Brunzell et al. (95) showed that in non- in diabetic patients. diabetic subjects, patients with mild diabetes, and dia- betic patients established on treatment, a high-carbo- hydrate formula feed containing principally dextrose was associated with lower blood glucose levels and insulin FIBER AND HYPERLIPIDEMIA requirements than a low-carbohydrate high-fat formula. Simpson et al. (27) found that, on a diet of this nature, Of major concern in NIDDM and more recently IDDM the postprandial glucose levels were significantly higher, is the increased risk of atherosclerotic heart disease, a and overall there appeared to be no difference in gly- major cause of death (98). The possible effects of fiber

DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 165 DIETARY FIBER

on metabolism have been alluded to above Fiber and obesity. The suggestion that the replacement (99,100). Of the supplemental fibers, only the soluble of fiber-rich foods by those depleted in fiber was a factor fibers such as pectin, oat bran, and guar appear to have in the obesity of Western countries stimulated interest a cholesterol-lowering effect; 12-40 g of guar or pectin in the use of fiber for treatment of obesity (14). How- (19,72) or 50-100 g of oat bran (75) have been found ever, the potential role of fiber in preventing or treating to consistently lower cholesterol in patients with hyper- obesity has remained an open question (115-126). At cholesterolemia by —6—15%. These fibers have also been a recent symposium on fiber and obesity, investigators shown to lower LDL cholesterol without a rise in tri- reported on the effects of fiber on weight reduction, glycerides (19,69,70,72). In studies with natural foods satiety, and compliance with complex dietary restric- rather than supplements, a lipid-lowering effect can also tions (127). These studies were in general carried out in be demonstrated if the diet is high in legumes (101,102). large numbers of patients attending weight-loss clinics The rise in fasting triglyceride levels that accompany an or in people on diets for various reasons. Although the early increase in carbohydrate intake can often be pre- results appear to be conflicting, they may be related to vented by a simultaneous increase in fiber intake (103). the dose of guar used. In one study in IDDM patients, addition of fiber signif- In addition, where dietary advice is already being fol- icantly reduced serum cholesterol levels from 206 to lowed and in well-controlled studies, the effect of fiber 147 mg/dl without a change in triglyceride level (16). supplementation may have been masked by adher- In obese diabetic outpatients after high-carbohydrate high- ence to a hypocaloric diet with weight loss in both test fiber diets, serum cholesterol and triglycerides were and control situations. Most agreed that fiber-treated pa- lowered, which may have been due partly to weight tients were more compliant and experienced less loss (92). and greater satiety with their meals. Forster (128) sug- Where diets high in legumes (76) or where increased gested that fiber should be used in conjunction with diet proportions of soluble fiber in a variety of food sources and should not be relied on as the sole means of at- (e.g., and ) have been incorporated into the tempting weight reduction. diet, levels of both serum cholesterol and triglycerides There are therefore some encouraging data to support have fallen (79). Decreases in serum triglycerides in di- the continued need to carry out long-term studies in a abetic patients on increased-carbohydrate high-fiber diets controlled manner to determine the safety and efficacy were also reported by Anderson and Ward {77), who of fiber supplementation as a form of treatment of the measured the lipid responses in diabetic patients after a obese diabetic patient. diet containing 60% carbohydrate and high fiber for 15 Fiber and pregnancy. There are few data available on mo. When fiber intakes were increased, serum triglyc- the use of fiber in pregnancy. This is mainly due to the eride levels also fell from —250 to 126 mg/dl, and total prevailing attitude in the United States that it is inap- LDL cholesterol and VLDL triglycerides decreased sig- propriate to starve women during pregnancy. In the few nificantly in another group of patients on a high-fiber studies that have been reported, fiber seems to be rel- diet with 42% carbohydrate (78). atively safe. Paired oral glucose tolerance tests were per- Long-term studies by Anderson and Ward {77) showed formed during the third trimester of pregnancy in four that home maintenance diets containing 55-60% car- gestational diabetic patients. Guar produced a signifi- bohydrate, 20-25% fat, and 50 g plant fiber signifi- cant reduction in mean serum glucose at 1, 2, and 3 h, cantly reduced triglyceride concentrations while de- and each of the four patients showed a normal glucose creasing insulin requirements in insulin-requiring NIDDM tolerance curve. The authors concluded "the improve- patients. These diets were maintained for up to 4 yr ment is sufficient to suggest a potential clinical value in (104). The exact contribution to the lipid changes of the the treatment of gestational diabetes" (129). decrease in insulin requirement, the weight loss, or the Fiber and the elderly. Age ranges of NIDDM patients decrease in caloric intake is unknown. in many of the studies described above frequently in- cluded patients ^65 yr of age. Kyllastinen and Lahikai- nen (130) supplemented the diet of 14 elderly (67- to 75-yr-old) diabetic patients on oral hypoglycemics with fIBER SUPPLEMENTS 16 g guar daily. They found a reduction (12.7%) in serum cholesterol, whereas serum calcium, , iron, The international medical literature from 1975 to 1985 and zinc were unchanged. The authors concluded that contains over 100 clinical studies on the therapeutic use "in some elderly diabetics guar supplementation im- of guar gum, primarily in the treatment of diabetes and proved glycemic control" (130). Patient-to-patient re- hypercholesterolemia, and the vast majority confirm the sponse was variable. Uusitupa et al. (108) similarly con- promise shown in the earlier studies of Jenkins and col- cluded a study in seven elderly patients (aged 65-81 leagues. The only findings to contrast with these obser- yr), one on diet therapy, the others on oral hypoglycem- vations are those in which the fiber derived from natural ics. The results showed that adding guar to the diet (5 foods or where a significant portion of the fiber was g/meal) significantly reduced postprandial blood glu- insoluble. In these cases, studies have been unable to cose levels in fairly well controlled subjects. Studies car- show a reduction in serum lipids (4,5,74,94,105-114). ried out in Toronto by Kay (131) also concluded that

166 DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 A.I. VINIK AND D.J.A. JENKINS

increasing the fiber intake from some foods was bene- ficial if well tolerated by elderly diabetic patients. SIDE EFFECTS OF HIGH FIBER DIETS

Concerns have been raised about the vitamin and min- eral status of people who change from a habitually low FACTORS TO CONSIDER IN ADDITION TO FIBER fiber diet to one rich in fiber. Studies of vitamin and mineral status in adults on high-fiber diets have not found High-fiber diets that contain substantial amounts of fi- evidence of deficiency (72,140). ber-rich starchy foods have been successfully used by In terms of soluble fiber supplements, Mclvor and col- several investigators (19-30). Whereas the effects were leagues (141) gave at least 30 g of guar daily for 16 wk attributed to fiber, other studies indicated that the action to 8 NIDDM patients, resulting in no significant changes may be complex and related to the physical form of the in hematologic or hepatorenal function. Serologic food, the ingestion of the previous meal, the type of food screening did not reveal a change in protein or mineral eaten, and the rate of release of carbohydrate from the metabolism or in electrolyte balance. Jenkins et al. (25) food (40,45,50,90,115). administered 14-26 g of guar daily for 6 mo to 8 dia- The fact that not all carbohydrate foods produce the betic patients. Biochemical tests of blood showed that same glycemic response has long been recognized, es- guar produced no evidence of serum zinc, , or pecially in the German literature. Recently, attention calcium changes. Tuomilehto et al. (67) gave 15 g of has been drawn to this by several studies (132-135) guar daily for 3 mo to 12 obese hypercholesterolemic noting the very different glycemic responses generated patients and at the end of this time, noted no significant by the starchy foods, potato, bread, rice, and corn. Most changes in 24-h urinary , , calcium, interesting was the fact that potatoes elicit a glycemic or magnesium. Aro et al. (142) and James et al. (65) response similar to that of an equivalent amount of glu- have found no effects on serum calcium, magnesium, cose, whereas elicits a much flatter re- phosphate, iron, or urinary calcium excretion. Har- sponse (132). Further studies emphasized that the form muth-Hoene (66) added 22.5 g of guar daily to a mixed of the food is important; i.e., parboiled rice produces a diet for 12 days and found that this did not significantly much flatter response than regular rice, and ground rice influence nitrogen balance, mineral absorption, or di- a much greater elevation of glucose and insulin levels gestible energy. These findings support similar obser- than whole rice (135). Presumably, grinding the rice has vations in normal volunteers on metabolic diets. the effect of making the starch more available to amyl- A number of studies have been carried out to examine olytic digestion. This effect is also seen with other ce- the absorption of important drugs such as digoxin, par- reals such as oats, wheat, and . Pureed also acetamol, glipizide, and penicillin. Huupponen et al. induce a much greater rise than whole (136). As (143,144) have shown a reduction in peak levels of di- discussed elsewhere in this issue, studies on a variety of goxin and penicillin but glipizide absorption was un- foods of equivalent carbohydrate content showed the changed. glycemic response varied from 15 to 98%. Of special Nevertheless, it is possible, especially with diets rich interest was the finding that, as a class, the legumes in phytate and insoluble fiber, that absorption of cal- produce the lowest glycemic response (76), which may cium, iron, and zinc could be impaired and result in be due to the slow release of carbohydrate during diges- deficiencies if used for a long time in susceptible indi- tion rather than to carbohydrate malabsorption (50,103). viduals (114), although these deficiencies may have lit- Jenkins and colleagues (45,90) have demonstrated in tle significance in terms of energy balance. High-fiber vitro, with human digestive juices, that some starchy diets have also been reported to cause small increases foods release their products of carbohydrate digestion in fecal loss oi in the form of nitrogen and more slowly than others. There appears to be a good fat (114). Theoretically, vitamin B12 and iron deficiency relationship between the rate of digestion of foods in could result if the high-fiber diets are low in ani- vitro and the glycemic response elicited by the foods in mal protein, but the abundance of epidemiological both nondiabetic and diabetic people (137,138). The data points against this in traditional normal fiber di- differences in responses to different foods may be related ets. to many other components in foods that alter their di- Although there is no incontrovertible evidence that gestibility, such as fiber, enzyme inhibitors, lectins, tan- soluble fiber supplements or moderate increases in fiber nins, phytates, , fats, proteins, and (89). intake from mixed sources causes malabsorption of Interactions between different macronutrients (81) and macro- or micronutrients, it is prudent to caution against the structure of food may alter the digestibility and pro- the unmonitored long-term use of fiber in individuals at duce very different glycemic responses. The effects of risk, such as the elderly. Deleterious effects of recom- fat, especially in large amounts, on the rate of gastric mended levels of fiber in pregnant or growing children emptying may certainly alter the glycemic response. Thus, are not known. No data are available on the effects on analysis of the dietary fiber intake and even fiber type trace minerals such as , , and chro- may not be sufficient to determine the response in any mium, which may have further ramifications for insulin given situation (139). sensitivity in NIDDM.

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bohydrate. Foods should be selected with moderate to ADHERENCE TO MEAL-PLANNING REGIMENS high amounts of dietary fiber. The 1986/1987 exchange lists compiled by the American Diabetes Association in McCulloch and colleagues (145) studied 178 IDDM pa- conjunction with the American Dietetic Association use tients focusing on their understanding of, and compli- a symbol to indicate foods with a fiber content of at ance with, a controlled carbohydrate diet. They found least 3 g per serving. These foods include legumes, roots, that 40% could not remember their dietary prescription , green leafy , all types of whole-grain and 35% did not estimate carbohydrate and scored badly cereals (including wheat, barley, oats, corn, and rye), on a quiz on carbohydrate content of common foods. and . Fruits and vegetables should be eaten raw Quiz scores were significantly associated with HbA, lev- and not pureed, which causes loss or reduction of the els. The authors concluded that "adequate dietary com- fiber effect. Abdominal cramping, discomfort, and fla- pliance is rare." To assess patients' perception of ad- tulence can be minimized by starting with small servings vice, Cantrill and Wright (146) interviewed 56 diabetic and increasing gradually. Insufficient data are available patients managed at diabetic clinics and a matched group on the long-term safety of very high fiber diets or fiber of 58 diabetic patients managed in general practice. supplements, although, to date, there are no deleterious Thirty-one percent of the general practice group and 7% reports. People at risk of deficiencies, e.g., postmeno- of the hospital group claimed to have received no die- pausal women, the elderly, and growing children, may tary advice from any source since diagnosis. Of the 18 require supplements of calcium and trace minerals. Sub- patients who monitored their blood glucose, all were jects with upper gastrointestinal dysfunction are at risk insulin dependent. Fifteen of the general practice group of bezoar formation and should be cautioned against a and 16 of the hospital group did not monitor blood or diet high in leafy vegetables such as . Careful urinary glucose. Of those who monitored urinary glu- attention must be paid to insulin dose, because hypo- cose, only 44% recorded the results, hospital patients glycemia can result if the dose is not reduced appropri- recording most frequently. Of 11 patients for whom a ately. Children may also benefit from an increase in the high-carbohydrate high-fiber diet was prescribed, ad- fiber content of their diets but may not tolerate large herence was evaluated over a 4-yr period. Nine patients amounts. Pregnant diabetic women appear to tolerate had good to excellent adherence, one had fair adher- fiber well, but there are too few studies to advise for or ence, and one had poor adherence. In the studies re- against its use in pregnancy. Care must be exercised in ported on fiber in the management of obesity, 67% of the use of novel fibers, because little is known of their patients on fiber adhered to the weight-reduction pro- safety or efficacy. gram and could satisfy their hunger and satiety needs, whereas only 27% on the weight-reduction program without fiber adhered to the program and lost weight. It SUMMARY does seem that availability of a low-calorie, guar-en- riched supplement may help individuals adhere to a se- Whereas there is still considerable controversy over use verely calorie-restricted meal plan. of the high-fiber diet in treatment of diabetes and some feel that it is premature to impose these diets on the diabetic population, others have strong convictions about RECOMMENDATIONS FOR THE USE OF FIBER the benefits to be obtained. These diets appear to have been most effective in patients taking fewer than 30 U With the recommendation of restricting fat intake to of insulin daily or in NIDDM patients who are being <30% and a protein intake of 0.8 g/kg (12-20% of treated with a diet or a sulfonylurea agent. Hyperlipid- total kcal) there is a need to increase carbohydrate to emia has clearly shown benefit in some patients taking 50-60% of the caloric intake. This amount of refined large quantities of fiber. In obese subjects, dietary fiber carbohydrate can have deleterious effects on glucose may aid in weight control by slowing the rate of food and lipoproteins. Evidence suggests that fiber may offer ingestion, inducing satiety, and decreasing the caloric some improvement in carbohydrate metabolism and density of the diet. However, these options should be lower total cholesterol, LDL cholesterol, and triglycer- made available to patients with diabetes only after de- ides. Fiber may also contribute to lower blood pressure tailed discussion with the health-care providers, includ- and enhance weight loss in obese subjects on hypoca- ing the physician and the nutritionist, to determine loric diets. Estimates of the current dietary fiber intake whether individuals can comply with the diet day to of adults in the United States range from 13 to 30 day. A thorough discussion of the data, the possible g/day, with men averaging 19.1 g/day and women 13.4 benefits, and untoward effects of the diet is essential. g/day. A practical goal would be to establish the current In-depth counseling and individualizing meal plans for intake and gradually increase it toward a goal of dou- each patient's need, with the provision of extensive rec- bling the intake. Fiber should be taken in a range of ipes and information on the dietary content of foods as foods to include both soluble and insoluble forms. Fiber well as what is known of their physiologic effects, are supplementation appears to provide benefit only if given essential for successful use of this dietary approach to with a diet comprising at least 50% of calories as car- treatment.

168 DIABETES CARE, VOL. 11, NO. 2, FEBRUARY 1988 A.I. VINIK AND D.J.A. JENKINS

Although much has been learned in the last few years 10. Von Duering AN: Ursache und Heilung des Diabetes about the role of fiber in the management of the patient Mellitus. Hanover, Schmorlund Seefeld, 1868 with diabetes, much has yet to be learned. Central to 11. Mosse A: Le diabete et I'alimentation aux pommes de the whole issue is the long-term safety of high-fiber diets. terre. Paris, Alcan, 1903 12. Von Noorden C: New Aspects of Diabetes. Pathology The impact on calcium, trace mineral metabolism, and and Treatment. Bristol, UK, Wright, 1912, p. 100-10 needs to be defined. Because patients with di- 13. Himsworth HP: Dietetic factor determining glucose tol- abetes may be at risk for osteopenia, it seems prudent erance and sensitivity to insulin of healthy men. Clin Sci to avoid an additional risk of negative calcium balance. 2:67-94, 1935 Information on the interactions of different fibers with 14. Trowell HC: Dietary-fiber hypothesis of the etiology of each other and the macronutrients of the diet is sorely diabetes mellitus. Diabetes 24:762-65, 1975 needed. Comparisons are needed of the effects of die- 15. Trowell HC: Definition of dietary fiber and hypothesis tary supplements of fiber and natural selection of high- that it is a protective factor in certain diseases. Am} Clin fiber foods with measurement of standardized variables, Nutr 29:417-27, 1976 e.g., HbA,, glucose profiles, C-peptide, cholesterol (LDL 16. Trowell HC: Diabetes mellitus and dietary fiber of starchy foods. Am I Clin Nutr 31 :S53-57, 1978 and HDL), and triglycerides. 17. Ahrens EH Jr, Boucher CA: The composition of a sim- New insights into the physiologic effects of fiber in ulated American diet. J Am Diet Assoc 73:613-20, 1978 the small intestine and the colon and the role of the 18. MarlettJA, Bokram RL: Relationship between calculated short-chain fatty acids that are generated will help in the dietary and crude fiber intakes of 200 college students. understanding of their mechanism of action. Am 1 Clin Nutr 34:335-42, 1981 For the guidance of the individual and the general 19. Kiehm TG, Anderson JW, Ward K: Beneficial effects of public, honest labeling of food products should be en- a high carbohydrate, high fiber diet on hyperglycemic couraged. Guidelines should be established for the diabetic men. Am ) Clin Nutr 29:895-99, 1976 standardization of the techniques for measurements and 20. Anderson JW, Midgley WR, Wedman B: Fiber and dia- for validation of physiologic effects claimed for high- betes. Diabetes Care 2:369-79, 1979 21. Anderson JW, Chen WL: Plant fiber: carbohydrate and fiber products. The novel fibers that are appearing need lipid metabolism. Am J Clin Nutr 32:346-63, 1979 to undergo as close and circumspect a scrutiny as was 22. Anderson JW: The role of dietary carbohydrate and fiber directed at the naturally occurring fibers. in the control of diabetes. Adv Intern Med 26:67-96, 1980 23. Jenkins DJA, Wolever TMS, Haworth R, Leeds AR, REFERENCES Hockaday TDR: Guar gum in diabetes. Lancet 2:1086- 87, 1976 1. American Diabetes Association: Special report: princi- 24. Kinmouth AL, Angus RM, Jenkins PA, Smith MA, Baum ples of and dietary recommendations for pa- JD: Whole foods and increased dietary fibre improve tients with diabetes mellitus: 1971. Diabetes 20:633- blood glucose control in diabetic children. Arch Dis Child 34, 1971 57:187-94, 1982 2. American Diabetes Association: Special report: princi- 25. Jenkins DJA, Wolever TMS, Bacon S, Nineham R, Lees ples of nutrition and dietary recommendations for indi- R, Rowden R, Lover M, Hockaday TD: Diabetic diets: viduals with diabetes mellitus: 1979. Diabetes Care high carbohydrate combined with high fiber. Am J Clin 2:520-23, 1979 Nutr 33:1729-33, 1980 3. Reaven GM: How high the carbohydrate? Diabetologia 26. Simpson HCR, Simpson RW, Lousley S, Carter RD, Geekie 19:409-13, 1980 M, Hockaday TD, Mann Jl: A high carbohydrate le- 4. Coulston A, Greenfield M, Kraemer F, Tobery T, Reaven guminous fibre diet improves all aspects of diabetic con- G: Effect of source of dietary carbohydrate on plasma trol. Lancet 1:1-5, 1981 glucose and insulin responses to test meals in normal 27. Simpson RW, Mann Jl, Eaton J, Moore RA, Carter R, subjects. Am ) Clin Nutr 33:1279-82, 1980 Hockaday TDR: Improved glucose control in maturity- 5. Coulston A, Greenfield MS, Kraemer FB, Tobery TA, onset diabetes treated with high-carbohydrate modified Reaven GM: Effect of differences in source of dietary fat diet. Br Med ] 1:1753-56, 1979 carbohydrate on plasma glucose and insulin responses 28. Simpson RW, Mann Jl, Eaton J, Carter RD, Hockaday to meals in patients with impaired carbohydrate toler- TDR: High-carbohydrate diets and insulin-dependent di- ance. Am } Clin Nutr 34:2716-20, 1981 abetics. Br Med J 2:523-25, 1979 6. Jarrett RJ: More about carbohydrates. Diabetologia 21: 29. Simpson HCR, Carter RD, Lousley S, Mann Jl: Digestible 427-28, 1981 carbohydrate—an independent effect on diabetic con- 7. Levitt NS, Vinik Al, Sive AA, Child PT, Jackson WPU: trol in type 2 (non-insulin dependent) diabetic patients? The effect of dietary fiber on glucose and hormone re- Diabetologia 23:235-39, 1982 sponses to a mixed meal in normal subjects and in di- 30. Rivellese A, Riccardi G, Giacco A, Pacioni D, Genovese abetic subjects with and without autonomic neuropathy. S, Mattioli PL, Mancini M: Effect of dietary fibre on glu- Diabetes Care 4:515-19, 1980 cose control and serum lipoproteins in diabetic patients. 8. Vinik Al, Glowniak J: Hormonal secretion in diabetic Lancet 2:447-50, 1980 autonomic neuropathy. NY State} Med 82:871-86, 1982 31. Munoz JM, Sandstead HH, Jacob RA, Logan GM Jr, Reck 9. Aretaeus: On the Causes, Symptoms and Cure of Acute SJ, Klevay LM, Dintzis FR, Inglett GE, Shuey WC: Effects and Chronic Diseases. Moffat J, Trans. London, Rich- of some cereal brans and textured vegetable protein on ardson, 1785 plasma lipids. Am I Clin Nutr 32:580-92, 1979

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32. Special Report Committee of the Canadian Diabetes As- kins AL, Barker H, Jenkins MJ: Rate of digestion of foods sociation: 1980 guidelines for the nutritional manage- and postprandial glycaemia in normal and diabetic sub- ment of diabetes mellitus. J Can Diabetes Assoc 42:110- jects, fir Med jf 281:14-17, 1980 18, 1981 51. Harju E, Larmi TK: Efficacy of guar gum in preventing 33. Nutrition Sub-Committee of the British Diabetic Asso- the dumping syndrome. ) Parenter Enterol Nutr 7:470- ciation Medical Advisory Committee: Dietary recom- 72, 1983 mendations for the 1980s—a policy statement by the 52. Harju E, Heikkila J, Larmi TK: Effect of guar gum on British Diabetic Association. Hum Nutr Appl Nutr 36:378- gastric emptying after gastric resection.) Parenter Enterol 86, 1982 Nutr 8:18-20, 1984 34. Report of the Expert Advisory Committee on Dietary Fiber 53. Blackburn NA, Redfern JS, Jarjis H, Holgate AM, Han- to the Health Protection Branch. Ontario, Canada, Natl. ning I, ScarpelloJHB, Johnson IT, Read NW: The mech- Health and Welfare, 1985 anism of action of guar gum in improving glucose tol- 35. Prosky L: Analysis of total dietary fiber: the collaborative erance in man. Clin Sci 66:329-36, 1984 study. In Dietary Fiber. Vahouny GV, Kritchevsky D, 54. Sommer H, Kasper H: The effect of dietary fiber on the Eds. New York, Plenum, 1985, p. 1-16 pancreatic excretory function. Hepato-Gastroenterology 36. Deutsch MJ: Vitamins and other nutrients. General Ref- 27:477-83, 1980 eree Reports, Committee on Foods II. / Assoc Off Anal 55. Dunaif G, Schneeman BO: The effect of dietary fiber on Chem 69:259, 1986 human pancreatic enzyme activity in vitro. Am ) Clin 37. Southgate DAT: Determination of carbohydrates in foods. Nutr 34:1034-35, 1981 II. Unavailable carbohydrates, j Sci Food Agric 20:331- 56. Kay RM, Grobin W, Track NS: Diets rich in natural fiber 35, 1969 improve carbohydrate tolerance in maturity-onset, non- 38. Southgate DAT: The measurement and characterisation insulin dependent diabetics. Diabetologia 20:18-21, of cereal dietary fiber. In Proc Brood and Gezondheid, 1981 Brussels, September 10, 1985, p. 17-27 57. Morgan LM, Goulder TJ, Tsiolakis D, Marks V, Alberti 39. Anderson JW: Plant Fiber in Foods. Lexington, KY, HCF KGMM: The effect of unabsorbable carbohydrate on gut Diabetes Res. Found., 1986 hormones: modification of post-prandial GIP secretion 40. Jenkins DJA, Wolever TMS, Leeds AR, Gassull MA, by guar. Diabetologia 17:85-89, 1979 Haisman P, Dilawarie JB, Goff DV, Metz GL, Alberti 58. Jenkins DJA, Wolever TMS, Nineham R, Bacon S, Smith KGMM: Dietary fibres, fibre analogues and glucose tol- R, Hockaday TD: Dietary fiber and diabetic therapy: a erance: importance of viscosity. Br Med J 1:1392-94, progressive effect with time. Adv Exp Med Biol 119:275- 1978 79, 1979 41. Holt S, Heading RC, Carter DC, Prescott LF, Tothill P: 59. Shimoyama R, Uehara S, Itagaki Y, Izumiyama S, Hir- Effect of gel fibre on gastric emptying and absorption of ayama A: Effects of guar intake on plasma somatostatin- glucose and paracetamol. Lancet 1:636-39, 1979 like immunoreactivity in diabetic patients. Hokkaido 42. Eisenhans B, Sufke U, Blume R, Caspary WF: The influ- Igaku Zasshi 57:727-32, 1982 ence of carbohydrate gelling agents on rat intestinal 60. Jenkins DJA, Wolever TMS, Nineham R, Sarson DL, Bloom transport of and neutral amino acids SR, Ahern J, Albert KGMM, Hockaday TDR: Improved in vitro. Clin Sci 59:373-80, 1980 glucose tolerance four hours after taking guar with glu- 43. Payler DK, Pomare EW, Heaton KW, Harvery RF: The cose. Diabetologia 19:21-24, 1980 effect of wheat bran on intestinal transit. Gut 16:209- 61. Mann Jl: Lines to legumes: changing concepts of dia- 13, 1975 betic diets. Diabetic Med 1:191-98, 1984 44. Wrick KL: The influence of dietary fiber source on hu- 62. Pederson O, Hjollund E, Lindskov HO, Helms P, Soren- man intestinal transit and stool output, j Nutr 29:1474- sen NS, Ditzel J: Increased insulin receptor binding to 79, 1976 monocytes from insulin-dependent diabetic patients after 45. Jenkins DJA, Thorne MJ, Camelon K, Jenkins A, Rao AV, a low-fat, high-starch, high-fiber diet. Diabetes Care Taylor RH, Thompson LU, Kalmusky J, Reichert R, Fran- 5:284-91, 1982 cis T: Effect of processing on digestibility and the blood 63. Hjollund E, Pedersen O, Richelsen B, Beck-Nielsen H, glucose response: a study of lentils. Am ) Clin Nutr Sorensen NS: Increased insulin binding to adipocytes 36:1093-101, 1982 and monocytes and increased insulin sensitivity of glu- 46. Wrick KL, Robertson JB, Van Soest PJ, Lewis BA, Rivers cose transport and metabolism in adipocytes from non- JM, Roe DA, Hackler LR: The influence of dietary fiber insulin-dependent diabetics after a low-fat/high-starch/ source on human intestinal transit and stool output. J high-fiber diet. Metabolism 32:1067-75, 1983 Nutr 113:1464-79, 1983 64. Ward GM, Simpson RW, Simpson HCR, Naylor BA, Mann 47. Wilmshurst P, Crawley JCW: The measurement of gastric Jl, Turner RC: Insulin receptor binding increased by high transit time in obese subjects using 24Na and the effects carbohydrate low fat diet in non-insulin-dependent di- of energy content and guar gum on gastric emptying and abetics. Eur) Clin Invest 12:93-96, 1982 satiety. Br j Nutr 44:1-6, 1980 65. James WPT, Branch WJ, Southgate DA: Calcium binding 48. Leeds AR, Ralphs DNL, Ebied F, Metz G, Dilawari JB: by dietary fibre. Lancet 1:638-39, 1978 Pectin in the dumping syndrome: reduction of symptoms 65a.Christiansen JS, Bonnevie-Neilsen V, Svendsen PA, Rubin and plasma volume changes. Lancet 1:1075-78, 1981 P, R0nn B, NerupJ: Effect of guar gum on 24-hour insulin 49. Jenkins DJA, Leeds AR, Gassull MA, Cochet B, Alberti requirements of insulin-dependent diabetic subjects as KGMM: Decrease in postprandial insulin and glucose assessed by an artificial pancreas. Diabetes Care 3:659- concentrations by guar and pectin. Ann Intern Med 86:20- 62, 1980 23, 1977 66. Harmuth-Hoene AE: Der Einfluss von Guar auf die Stick- 50. Jenkins DJA, Wolever TMS, Taylor RH, Ghafari H, Jen- stoffbilanz, die Resorption von Mineralstoffen und Spu-

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renelementen und die verdauliche Energie bei 6 wei- dependent diabetes mellitus. Diabetes Care 3:520-25, blichen Versuchspersonen. Beitr Infusionther Klin Ernaehr 1980 Forsch Prax 12:68-80, 1983 83. Cohen M, Leong VW, Salmon E, Martin FIR: The role 67. Tuomilehto J, Karttunen P, Vinni S, Kostiainen E, Uusi- of guar and dietary fibre in the management of diabetes tupa M: A double-blind evaluation of guar gum in pa- mellitus. Med J Aust 1:59-61, 1980 tients with dyslipidaemia. Hum Nutr Appl Nutr 37:109- 84. Williams DRR, James WPT, Evans IE: Dietary fibre sup- 16, 1983 plementation of a "normal" breakfast administered to 68. Simpson HCR, Simpson RW, Lousley S, Carter RD, Geekie diabetics. Diabetologia 18:379-83, 1980 M, Hockaday TDR, Mann Jl: A high carbohydrate le- 85. Jenkins DJA, Nineham R, Craddock C, Craig-McFeely P, guminous fibre diet improves all aspects of diabetic con- Donaldson K, Leigh T, Snook J: Fibre and diabetes. Lan- trol. Lancet 1:1-5, 1981 cet 1:434-35, 1979 69. Bosello O, Ostuzzi R, Armellini F, Micciolo R, Scuro 86. Miranda PM, Horwitz DL: High-fiber diets in the treat- LA: Glucose tolerance and in bran-fed pa- ment of diabetes mellitus. Ann Intern Med 88:482-86, tients with impaired glucose tolerance. Diabetes Care 1978 3:46-49, 1980 87. Monnier LH, Blotman MJ, Colette C, Monnier MP, Mir- 70. Gatti E, Catenazzo G, Camisasca E, Torri A, Denegri E, ouse J: Effects of dietary fibre supplementation in stable Sirtori CR: Effects of guar-enriched pasta in the treatment and labile insulin-independent diabetics. Diabetologia of diabetes and hyperlipidemia. Ann Nutr Metab 28:1 — 20:12-17, 1981 10, 1984 88. Fuessl H, Adrian TE, Bacarese-Hamilton AJ, Bloom SR: 71. Munoz JM, Sandstead HH, Jacob RA, Logan GM Jr, Effects of guar on plasma glucose and gut hormone re- Reck SJ, Klevay LM, Dintzis FR, Inglett GE, Shuey WC: sponse in type II diabetics. Br Diabetes Assoc Spring Effects of some cereal brans and textured vegetable Meeting, Oxford, UK, 1985, p. 59 protein on plasma lipids. Am j Clin Nutr 32:580-92, 89. Jenkins DJA: Lente carbohydrate: a newer approach to 1979 the dietary management of diabetes. Diabetes Care 5: 72. Jenkins DJA, Wolever TM, Taylor RH, Reynolds LK, 634-41, 1982 Nineham R, Hockaday TD: Diabetic glucose control, 90. Jenkins DJA, Wolever TMS, Taylor RH, Barker H, Fiel- lipids and trace elements on long term guar. Br Med J den H, Baldwin JM, Bowling AC, Newman HC, Jenkins 280:1353-54, 1980 AL, Goff DV: of foods: a physiological 73. MahalkoJR, Sandstead HH, Johnson LK, Inman LF, Milne basis for carbohydrate exchange. Am) Clin Nutr 34:362- DB, Warner RC, Haung EA: Effect of consuming fiber 66, 1981 from corn bran, soy hulls, or apple powder on glucose 91. Anderson JW, Sieling B: High fiber diets for obese tolerance and plasma lipids in type II diabetes. Am I Clin diabetic patients. Obesity Bariatric Med 9:109-17, Nutr 39:25-34, 1984 1980 74. Riccardi G, Rivellese A, Pacioni D, Genovese D, Mas- 92. Nuttall FQ: Diet and the diabetic patient. Diabetes Care tranzo P, Mancini M: Separate influence of dietary car- 6:197-207, 1983 bohydrate and fibre on the metabolic control in diabe- 93. Hollenbeck CB, Coulston AM, Donner CC, Williams tes. Diabetologia 26:116-21, 1984 RA, Reaven GM: The effects of variations in percent of 75. Anderson JW: Hypocholesterolemic effects of oat-bran naturally occurring complex and simple carbohydrates or intake for hypercholesterolemic men. Am \ Clin on plasma glucose and insulin response in individuals Nutr 40:1146-55, 1984 with non-insulin-dependent diabetes mellitus. Diabetes 76. Jenkins DJA: Leguminous in the dietary manage- 34:151-55, 1985 ment of hyperlipidemia. Am ) Clin Nutr 38:567-73, 94. Hollenbeck CB, Coulston AM, Reaven GM: To what 1983 extent does increased dietary fiber improve glucose and 77. Anderson JW, Ward K: Long-term effects of high-car- lipid metabolism in patients with noninsulin-dependent bohydrate, high-fiber diets on glucose and lipid metab- diabetes mellitus (NIDDM)? Am ) Clin Nutr 43:16-24, olism: a preliminary report on patients with diabetes. 1986 Diabetes Care 1:77-82, 1978 95. Brunzell JD, Lerner RL, Hazzard WR, Porte D, Bierman 78. Rivellese A, Riccardi G, Giacco A, Postiglione A, Mas- EL: Improved glucose tolerance with high carbohydrate tranzo P, Mattioli PL: Reduction of risk factors for ath- feeding in mild diabetes. N Engl I Med 284:521-24, erosclerosis in diabetic patients treated with high fiber 1974 diets. Prev Med 12:128-32, 1983 96. Gatti E, Catenazzo G, Camisasca E, Torri A, Denegri E, 79. Jenkins DJA, Leeds AR, Gassull MA, Cochet B, Alberti Sirtori CR: Effects of guar-enriched pasta in the treatment KGMM: Decrease in postprandial insulin and glucose of diabetes and hyperlipidemia. Ann Nutr Metab 28:1- concentrations for guar and pectin. Ann Intern Med 10, 1984 86:20-23, 1977 97. Thompson LU, Ferrari F, Bosello O, Rao AV, Wong G: 80. Jenkins DJA, Goff DV, Leeds AR, Alberti KGMM, Wol- Effect of guar-enriched pasta on blood glucose control ever TMS, Gassull MA, Hockaday TDR: Unabsorbable in diabetics (Abstract). Diabetes 34:205A, 1985 carbohydrates and diabetes: decreased post-prandial hy- 98. Lipid Research Clinics Program: Lipid research clinics perglycemia. Lancet 2:172-74, 1976 coronary primary prevention trial results. I. Reduction 81. Goulder TJ, Alberti KGMM, Jenkins DA: Effect of added in incidence of coronary heart disease. II. The relation- fiber on the glucose and metabolic response to a mixed ship of reduction in incidence coronary heart disease to meal in normal and diabetic subjects. Diabetes Care cholesterol lowering. JAMA 3:351-74, 1984 1:351-55, 1978 99. Kritchevsky D, Story J: Binding of bile salts in vitro by 82. Hall SEH, Bolton TM, Hetenyi G Jr: The effect of bran nonnutritive fiber. I Nutr 104:458-62, 1974 on glucose kinetics and plasma insulin in non-insulin- 100. Story J, Kritchevsky D: Comparison of the binding of

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various bile acids and salts in vitro by several types of Developments of Importance to Health. Heaton KW, Ed. fiber. J Nutr 106:1292-94, 1976 London, Newman, 1978, p. 141-49 101. Anderson JW: Hypocholesterolemic effects of oat-bran 120. Haber GB, Heaton KW, Murphy D, Burroughs LF: De- or bean intake for hypercholesterolemic men. Am ) Clin pletion and disruption of dietary fibre: effects on satiety, Nutr 40:1146-55, 1984 plasma-glucose, and serum-insulin. Lancet 2:679-82, 102. Jenkins DJA, Wolever TMS, Taylor RH, Barker H, Fiel- 1977 den H: Exceptionally low blood glucose response to dried 121. Grimes DS, Gordon C: Satiety value of wholemeal and beans: comparison with other carbohydrate foods. Br . Lancet 2:106, 1978 Medy 281:578-80, 1980 122. Duncan KH, Bacon JA, Weinsier RL: The effects of high 103. Anderson JW: High-fibre diets for diabetic and hyper- and low energy density diets on satiety, energy intake triglyceridemic patients. Can Med Assoc j 123:975-79, and eating time of obese and nonobese subjects. Am / 1980 Clin Nutr 37:763-67, 1983 104. Story L, Anderson JW, Chen WJ, Karounos D, Jefferson 123. Krotkiewski M: Effect of guar gum on body weight, hun- B: Adherence to high carbohydrate, high fiber diets: long- ger ratings and metabolism in obese subjects. Br j Nutr term studies of non-obese diabetic men. / Am Diet Assoc 52:97-105, 1984 85:1105-10, 1985 124. Arsenio L, Cavalli Sforza LT, Magnati G, Strata A: Ri- 105. Wirth A, Middelhoff G, Braeuning C, Schlierf G: Treat- cerca clinica sull' impiego di una farina deproteinizzata ment of familial hypercholesterolemia with a combina- di guar nel trattamento dell' obesita. Ada Bio-Med Ate- tion of bezafibrate and guar. 45:291-97, neo Parmense 52:149-57, 1981 1982 125. Evans E, Miller DS: Bulking agents in the treatment of 106. Najemnik C, Kritz H, Irsliger K, Laube H, Knick B, Klimm obesity. Nutr Metab 18:199-203, 1975 HD, Wahl P, Vollmar J, Brauning C: Guar and its met- 126. Leeds AR, Judd PA: Dietary fiber and weight manage- abolic effects in type II diabetic subjects. Diabetes Care ment. In Dietary Fiber. Basic and Clinical Aspects. Va- 7:215-20, 1984 houny GV, Kritchevsky D, Eds. New York, Plenum, 1986, 108. Uusitupa M, Tuomilehto J, Karttunen P, Wolf E: Long- p. 335-42. term effects of guar gum on metabolic control, serum 127. Bjorntorp P, Vahouny GV, Kritchevsky D (Eds.): Dietary cholesterol and blood pressure levels in type 2 (non- fiber and obesity. In Proc Satellite Symp to the Second insulin-dependent) diabetic patients with high blood Washington Symposium on Dietary Fiber, Washington, pressure. Ann Clin Res Suppl 43:126-31, 1984 DC, April 28, 1984. New York, Liss, 1985 109. Virtanen V, Maenpaa J, Pitkanen L: Problem cases in 128. Forster H: Treatment of obesity with low energy diet and screening for congenital hypothyroidism. Pediatr Res fiber. In Dietary Fiber in Health and Disease. Vahouny 18:119, 1984 GV, Kirtchevsky, Eds. New York, Plenum, 1985 110. Farrell R, Owens D, Tyrrell D, Thompkins GH: Is guar 129. Gabbe SG, Cohen AW, Herman GO, Schwartz S: Effect useful in type II diabetics? Br Diabetes Assoc Spring of dietary fiber on the oral glucose tolerance test in preg- Meeting, Oxford, UK, 1985, p. 60 nancy. Am j Obstet Cynecol 143:514-17, 1982 111. Bosello O, Cominacini L, Zocca I, Garbin U, Ferrari F, 130. Kyllastinen M, Lahikainen T: Long-term dietary supple- Davoli A: Effects of guar gum on plasma lipoproteins mentation with a fiber product (guar gum) in elderly and apolipoproteins C-ll and C-lll in patients affected by diabetics. Curr Ther Res Clin Exp 30:872-79, 1981 familial combined hyperlipoproteinemia. Am) Clin Nutr 131. Kay RM: Dietary fiber. / Lipid Res 23:221-42, 1982 40:1165-74, 1984 132. Crapo PA, Reaven G, Olefsky J: Postprandial plasma 112. Dalzell GW, MacNeil AJ, Hadden DR, Atkinson AB, glucose and insulin responses to different complex car- Weaver JA, Kennedy AL, Holmes J: Effects of guar on bohydrates. Diabetes 26:1178-83, 1977 poorly controlled non-insulin dependent diabetes mel- 133. Crapo PA, Kolterman OG, Waldeck N, Reaven GM, litus. Br Diabetes Assoc Meeting, Belfast, UK, 1985, p. Olefsky JM: Postprandial hormone responses to different 34 types of complex carbohydrates in individuals with im- 113. Jenkins DJA: Dietary fiber, diabetes and hyperlipidemia: paired glucose tolerance. Am ) Clin Nutr 33:1723-28, progress and prospects. Lancet 2:1287-90, 1979 1980 114. Jenkins DJA, Wolever TMS, Jenkins AL, Lee R, Wong 134. Schauberger G, Brinck UC, GuldnerG, Spaethe R, Nik- GS, Josse R: Glycemic response to wheat products: re- las L, Otto H: Exchange of carbohydrates according to duced response to pasta but no effect of fiber. Diabetes their effect on blood glucose (Abstract). Diabetes 26 Care 6:155-59, 1983 (Suppl. 1):415, 1977 115. Heaton KW: Food intake regulation and fibre. In Med- 135. O'Dea K, Nestel PJ, Antonoff L: Physical factors influ- ical Aspects of Dietary Fiber. Spiller GA, Kays RM, Eds. encing postprandial glucose and insulin responses to New York, Plenum, 1980, p. 223-38 starch. Am I Clin Nutr 33:760-65, 1980 116. Van Itallie TB: Dietary fiber and obesity. Am J Clin Nutr 136. Haber GB, Heaton KW, Murphy D, Burroughs LF: De- 31:S43-52, 1978 pletion and disruption of dietary fibre: effects on satiety, 117. AM R, Staub H, Leveille GA, Boyle PC: Dietary fiber and plasma-glucose, and serum-insulin. Lancet 2:679-82, obesity: a review. In Dietary Fibre in Health and Disease. 1977 Vahouny GV, Kritchevsky D, Eds. New York, Plenum, 137. Jenkins DJA, Ghafari H, Wolever TMS, Taylor RH, Bar- 1982, p. 139-49 ker HM, Fielden H, Jenkins AL, Bowling AC: Relation- 118. Heaton KW: Food fibre as an obstacle to energy intake. ship between the rate of digestion of foods and post- Lancet 2:1418-21, 1973 prandial glycaemia. Diabetologia 22:450-55, 1982 119. Heaton KW: Fibre, satiety and insulin—a new approach 138. Eno J: A new approach to diet for diabetes. / Can Diet to overnutrition and obesity. In Dietary Fibre: Current Assoc 40:118-22, 1979

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139. Collings P, Williams C, MacDonald I: Effect of cooking 143. Huupponen R, Seppala P, lisalo E: Effect of guar gum, on serum glucose and insulin responses to starch. Br a fibre preparation, on digoxin and penicillin absorption Medy 282:1032, 1981 in man. Eur) Pharm 26:279-81, 1984 140. Anderson JW, Ferguson SK, Karounos D, O'Malley L, 144. Huupponen R, Karhuvaara S, Seppala P: Effect of guar Sieling B, Chen W-JL: Mineral and vitamin status on gum on glipizide absorption in man. Eur J Clin Phar- high-fiber diets: long-term studies of diabetic patients. macol 28:717-19, 1985 Diabetes Care 3:38-40, 1980 145. McCulloch DK, Young RJ, Steel JM, Wilson EM, Prescott 141. Mclvor ME, Cummings CC, Leo TA, Mendeloff Al: Flat- RJ, Duncan LJ: Effectof dietary compliance on metabolic tening postprandial blood glucose responses with guar control in insulin-dependent diabetics. Hum Nutr Appl gum: acute effects. Diabetes Care 8:274-78, 1985 Nutr 37A:287-92, 1983 142. Aro A, Uusitupa M, Voutilainen E, Korhonen T: Effects 146. Cantrill JA, Wright C: Community pharmacists and the of guar gum in male subjects with hypercholesterolemia. health education of diabetic patients. Pharm I 235:449, Am J Clin Nutr 39:911-16, 1984 1985

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