Adherence to Low-Carbohydrate Diets in Patients with Diabetes: A Narrative Review

Introduction

The number of people with type 2 diabetes has nearly quadrupled from 1980 to 2014 with the prevalence now estimated to be 8.5% of the global population.¹ Diabetes is associated with increased morbidity and mortality, but the development and progression of weight-related type 2 diabetes can be delayed with exercise, diet, and weight loss of 5–10%.^2–5 Guidelines from the American Diabetes Association and Academy of Nutrition and Dietetics therefore recommend that overweight adults with type 2 diabetes reduce energy intake to promote weight loss.^6–9 However, the optimal dietary approach to weight loss is widely debated, among both health professionals and the lay public. A preponderance of data suggests that low carbohydrate diets (LCD) and very low carbohydrate, ketogenic diets (VLCKD) can be effective tools for weight loss, A1c reduction, blood pressure lowering, and improving triglycerides and HDL-C in trial settings.^7,10 An emerging body of evidence, however, suggests that better adherence to a weight-reducing diet, rather than the diet composition itself is an important factor for weight loss success.^11,12

Dietary predictors of adherence vary based on the type of diet. In one study examining both qualitative and quantitative methods among adults following a restrictive dietary pattern, adherence varied significantly between dietary groups, with those following a vegan and vegetarian-based diet demonstrating particularly high adherence and gluten-free and weight loss dieters being comparably low. Four consistent predictors of adherence were noted. Self-efficacy and social identification with one’s dietary group positively predicting adherence, whereas mood or weight control as motivation for dietary choice had negative effects.¹³ Personality characteristics have also been linked to dietary adherence, with conscientiousness, lower levels of emotional eating, and openness to experience being associated with better adherence in weight-loss intervention programs.^13–15 Mental health is known to play an important role as well. For those with celiac disease, depression and anxiety were associated with poor adherence to a gluten-free diet.¹³

There is no consensus on the amount of carbohydrates permitted for a LCD or VLCKD. Whether carbohydrates should include total carbohydrates versus net carbohydrates also remains debatable Net carbohydrates are calculated as total carbohydrates after excluding fiber and sugar alcohols (if applicable). For this review, studies were eligible for inclusion if they were randomized control trials including adults diagnosed with Type 2 diabetes, had a minimum intervention duration of 24 weeks, and if the intervention restricted the proportion or quantity of dietary carbohydrate to at least less than 50 grams of carbohydrate per day. Studies using active control diets were included. All forms of comparison diet that did not include carbohydrate restriction were permitted, including low-fat, high-carbohydrate, low-glycemic index, high-protein, Mediterranean and “healthy eating”. Included studies also needed to report actual (self-reported or measured) carbohydrate intake during or at the end of the intervention. All countries were eligible but language was restricted to English. Studies that did not meet these criteria were excluded. Included studies did not differentiate between total versus net carbohydrates. This article seeks to review the literature related to adherence to LCD and VLCKD in people with type 2 diabetes based on the aforementioned criteria.

A Brief History of Low Carbohydrate and Very Low Carbohydrate Diets

The development of the VLCKD as a treatment for diabetes mirrors its use as a treatment for epilepsy. VLCKD was the standard of care for both diabetes and epilepsy prior to the development antidiabetic and antiepileptic drugs, respectively^16–18 After the development of pharmacologic treatments, interest in dietary modification waned. However, medications failed to yield a universal cure, prompting a resurgence in research and clinical interest in LCD and VLCKD for the management of diabetes and epilepsy.

In 1921, the Mayo Clinic treated a series of epilepsy patients with a ketone-producing diet. This “ketogenic diet” was an effective alternative to fasting.¹⁸ First reported in 1925, the macronutrient distribution of the ketogenic diet for pediatric epilepsy consisted of 1 g protein per kilogram of body weight, 10–15 g of carbohydrates per day, and the remainder of the calories from fat.¹⁹ In these earliest reports of the diet in the treatment of epilepsy, dietary adherence played a significant role in seizure control.¹⁹

In the 1910s, Drs. Frederick Madison Allen and Elliot Proctor Joslin studied low carbohydrate, high-fat diets for the treatment of diabetes mellitus.¹⁷ Decreased urinary glucose output was a marker of efficacy. These diets consisted roughly of 70% fat and 10% carbohydrates.¹⁷ Prior to 1920, poor dietary adherence in patients with diabetes was noted to result in recurrent admission and poor outcomes.²⁰

The Atkins’ diet, popularized in 1972, was the first ketogenic diet to gain widespread appeal for obesity management. Variants of the classical ketogenic diet (CKD) were developed to improve tolerability. These include the modified Atkins’ diet (MAD)^21,22 the medium-chain triglyceride diet, and the low glycemic index treatment.²³ The MAD does not require an initial fasting period and is meant to be easy to follow. Fats are encouraged and carbohydrates limited to less than 20 grams per day.^22,24 A meta-analysis evaluated the 15 studies of ketogenic diets for epilepsy in adults.²³ The studies had a combined dropout rate of 45%, with fewer patients completing the trials of the CKD (38%) and better completion rates with the MAD (56%).²³ Of the patients who dropped out of the classical ketogenic diet studies, about 60% did so due to inability to adhere which was attributed to psychosocial reasons, fatigue and weight loss.^25–28 Among the participants who failed to complete the MAD studies, about half discontinued the diet due to inability to adhere. When ketogenic diets are used to control epilepsy, adherence appears to be inversely related to the degree of dietary restriction. Side effects and psychosocial stressors also appear to impact dietary adherence in this setting.

Defining Low Carbohydrate and Very Low Carbohydrate Diets and Their Clinical Benefits

Dietary approaches for weight loss typically emphasize either decreasing carbohydrate intake, decreasing fat intake or decreasing calories/portions.²⁹ A typical American diet consists of 2200 calories per day, with roughly 36–40% from fat, 16–18% from protein, and 45% from carbohydrates.^30–32 Traditional dietary guidelines for people with diabetes recommended that individuals consume 45–65% of daily energy intake from carbohydrates high in fiber.³³ Randomized control trials generally define low carbohydrate diets as <40–45% of calories from carbohydrate.⁷ However, more recently, studies have examined carbohydrate restricted eating patterns and found them to be safe. Some studies have also demonstrated metabolic benefits with LCDs and VLCKDs including weight loss,^34,35 improved lipid profiles,^7,36 better glycemic control,³⁶ and reduced medication dependence in persons with diabetes.^34,37

Although there are no accepted definitions for LCD or VLCKD, a selection of these eating patterns is reviewed herein based on the aforementioned criteria.

Low Carbohydrate Diets (LCDs)

These diets typically limit carbohydrate intake to 26–45% of daily caloric intake but do not seek to promote ketosis.^7,38 These eating plans emphasize vegetables low in carbohydrate, fat from plant and animal foods, and protein from meat, poultry, fish, shellfish, eggs, cheese, plant-based sources like tofu and tempeh, and nuts. They avoid starchy and sugary foods such as pasta, rice, potatoes, bread, couscous, barley, polenta, cereal, crackers, and sweets. Popular LCDs include the South Beach and the Zone Diets.^39,40 A meta-analysis of 9 studies showed significant weight loss in patients with type 2 diabetes on LCDs (less than 130g/day of carbohydrate) compared to control groups over long durations, and greater weight loss than control diets (typically low fat diets) at 6 months but not statistically greater at 12 months, possibly due to declining adherence over time.^41,42 LCDs are associated with an increase in serum HDL-cholesterol and a decrease in fasting triglycerides when compared to low fat eating patterns.^7,36 In an analysis of nine studies of dietary patterns each using a <130 g/day from three months to two years, triglycerides were reduced and HDL was increased. LDL and total cholesterol changes were not statistically significant.⁴¹ Kirkpatrick analyzed eight meta-analyses of studies involving LCD and VLKCD in overweight or obese patients with prediabetes or type 2 diabetes and found a reduction in triglyceride levels, but no consistent changes in HDL, LDL, or total cholesterol though this was thought to be likely due to low adherence in all but one of the studies included.⁴³ Fechner’s meta-analysis compared the effects of varying degrees of carbohydrate reduction in LCDs on metabolic markers. Though only four of 37 included trials involved those with type 2 diabetes, the authors found that the degree of carbohydrate restriction was proportional to triglyceride reduction.⁴⁴

In meta-analyses, there is a significant A1c reduction in people adhering to LCD compared to a high carb (fat restricted) diet with 2 years of follow-up.^36,45 However, the A1c reduction appears to be due to the studies with carbohydrate restriction to less than 26% of energy, so this may not be generalizable.⁴⁵ LCDs are associated with greater reductions in the number and dose of diabetes medications compared to other diets.^45,46

Very Low Carbohydrate Ketogenic Diets (VLCKDs)

Ketogenic diets adapted for weight management and general wellness differ from those used to treat epilepsy. Although there is no standardized definition, these eating patterns are typically characterized by reducing dietary carbohydrates to 20–50 g per day but sometimes are defined for study purposes as <26% of daily calories.^7,47 This goal is based on the level of carbohydrate reduction required to produce ketosis, which is typically <50 g/day.⁴⁸ Many of these eating plans consist of an induction phase and most do not advocate for calorie restriction, based on the premise that the higher protein and fat in the diet, and potentially the circulating ketones, promote satiety.^48–50 In research and clinical practice, ketosis can be measured as BHB in blood on fingerstick or acetoacetate in urine⁵¹ Ketone meters are available to monitor for home use and have also been used to follow adherence in studies.^52,53

These eating patterns have been shown in meta-analysis to cause greater A1c reduction and weight loss than diets without carbohydrate restriction at 3 and 6 months, but this advantage is no longer seen at 12 months.⁴⁵ VLCKDs have shown superior weight loss to other eating plans in some studies^54,55 and no difference in others.^56,57 Guldbrand’s study compared a low fat diet to a VLCKD and weight loss was similar for the two groups (LFD −3.99±4.1 kg; LCD −4.31±3.6 kg).⁵⁸

Lipid profile changes induced by LCDs can occur in a relatively short time. Additionally, Choi’s meta-analysis found that the VLCKD has cardiovascular disease risk reducing effects in patients with diabetes and obesity or overweight, with serum HDL significantly increased and serum triglycerides decreased in those on VLCKD.⁵⁹ Similarly, Westman’s 6-month trial showed that VLCKD reduced triglycerides and increased HDL, with improvements significantly more than those seen with LFD.⁶⁰

VLCKDs have an immediate impact on glycemic control. Over 3–6 month study periods, Yancy, Saslow, and Westman demonstrated HbA1c improvements in patients on VLCKDs compared to other dietary interventions.^34,61,62 The success of longer-term interventions has been more modest, but also more difficult to interpret as adherence wanes over time and most studies relied on dietary recall and self-reporting to monitor adherence.

Medication reductions are a prominent benefit of very low carbohydrate eating patterns. A majority of patients in three to six month VLCKD studies by Yancy and Westman were able to either eliminate or reduce their diabetes medications.^34,62 Though HbA1c reductions were often modest in studies more than a year in duration, many of these studies still demonstrated significant reductions in insulin and diabetes medication requirements, and it is likely that medication reduction blunted the A1c response.^53,54,63,64

Diabetes remission has been defined as achieving an HbA1c of 6.5% or less in the context of either complete medication cessation or cessation of all medications except metformin.⁶⁵ A systematic review and meta-analysis of studies comparing LCDs to other diets or control arms by Goldenberg identified studies that reported on diabetes remission rates at 6 months (8 studies) and 12 months (3 studies). When complete medication independence was not factored in, LCDs achieved greater remission compared to controls at 6 months (an additional 32 per 100 subjects) and more modest remission rates at 12 months (an additional 10 per 100 subjects). When complete medication cessation was used as the definition for diabetes remission, rates were reduced and results were no longer statistically significant. Subgroup analyses showed more significant remission rates at six months among patients on non-insulin agents.⁴²

Dietary Adherence Methods and Results in Low Carbohydrate Diet Trials

Adherence is defined by the World Health Organization as “the extent to which a person’s behavior – taking medication, following a diet and/or executing lifestyle changes – corresponds with agreed recommendations from a health care provider”.⁶⁶ Assessing dietary adherence remains a challenge due to inconsistencies in how it is measured in studies. One common method is self-reporting using tools such as food records, food frequency questionnaires, or 24-hour dietary recalls. Other measurements include biomarkers, attendance at counseling sessions, and completion rates of the study intervention.

Dietary Recall

Though dietary recall is commonly used to assess adherence in LCD studies, the validity of self-reported food diaries is widely debated. Kipnis compared biomarkers with dietary recall using Food Frequency Questionnaires and showed that relying on dietary recall can dramatically underestimate intake.⁶⁷ It is not surprising that underreporting is common given that food records are reactive by nature, 24h dietary recall relies on memory, and food frequency questionnaires have a finite list of foods. In addition to this, a societal stigma against obesity often creates a social desirability bias that potentially exacerbates underreporting. Still, self-reported data can be useful in understanding food behaviors and eating patterns beyond the information provided by biomarkers alone.⁶⁸

Some of the studies already reviewed relied on dietary records to assess adherence. Guldbrand’s randomized two-year intervention compared a LFD to VLCKD (Table 1). Diet records were conducted during three consecutive days including one weekend day at 3, 6, 12, and 24 months, and participants were given dedicated scales to weigh foods. During the first 6 months, adherence to their respective diet was similar between the groups based on mean macronutrient intake, with an increase in energy from fat in the LCD group. The study was unable to conclude that VLCKD caused greater weight reduction. This finding differs from many other studies, but the authors also noted that they used fewer resources to achieve adherence.⁵⁸ Iqbal’s randomized two year study of patients with obesity and type 2 diabetes compared an LCD of <30g/day with an LFD. Participants were given educational nutrition sessions carbohydrate counting applications to help maintain their target intake, which was estimated using 24-hour recall. These were group sessions conducted as frequently as weekly in the first month and then gradually decreased to monthly for the study duration. Despite these interventions, adherence was low based on these metrics. Additionally, the VLCKD group had a 60% attrition rate and participants in both groups appeared to consume similar diets with moderate restriction in carbohydrates at the study’s conclusion.⁶⁹ Hu’s clinical trial compared a VLCKD with a LFD (<30% fat, <7% saturated fat) over 12-months (Table 1). Overall adherence was measured using a composite score composed of attendance at counselling sessions, deviation from nutrient goals, and urinary ketone presence. Four weekly one-on-one dietician sessions were held in the first month, followed by 10 group sessions every other week for 5 months and 6 monthly group sessions thereafter. Attendance between groups did not vary significantly with over 50% participating. The study also had a relatively low attrition rate of 21% in the VLCKD group. However, composite scores for adherence were similar between the groups. A one-interquartile-range increase in composite score suggested better adherence to VLCKD and was associated with greater weight loss and improved body composition with increased lean mass. Indicators of adherence in the LFD were not associated with weight loss.⁷⁰

Table 1 Summary of Trials on Adherence to LCKD in Patients with Type 2 Diabetes

The results of these studies demonstrate the challenges of dietary adherence and of measuring adherence with dietary recall.

Biomarkers

Other studies have used a combination of biomarkers with self-reporting to address these limitations. Tay assessed dietary intake using daily weighed food records with software to calculate average quarterly nutrient intake between VLCKD and LFD (Table 1). Biomarkers were used to confirm adherence: protein intake was measured using 24-hour urinary urea to creatinine ratio and carbohydrate reduction by using monthly plasma BHB concentrations. Plasma BHB concentrations and the ratio of urinary urea to creatinine excretion increased and remained higher over the 52-week period than with the high carbohydrate diet, consistent with lower carbohydrate and higher protein intake in LCD patients. In addition to individualized dietary plans, this study involved one-on-one sessions with a dietician for dietary instruction and support every 2 weeks for the first 12 weeks and monthly thereafter. The use of individualized dietary sessions may have played a part in the high adherence rate noted.⁷¹ Yancy’s unblinded study compared VLCKD versus orlistat plus LFD (Table 1). As participants approached their goal weight or if cravings threatened dietary adherence, 5g of carbohydrates were added to their daily intake each week until weight was maintained or cravings diminished.⁵⁵ Dietary adherence was measured using urinary ketones in combination with 4-day food records at baseline and at 2, 12, 24, 36, and 48 weeks. The proportion of VLCKD participants with urinary ketones present (≥5 mg/dL [≥0.9 mmol/L]) at two weeks was 72%. This declined to a low of 13% at 48 weeks; the decline could have been due to decreased adherence, increased carbohydrate intake for weight maintenance or increased use of ketones for energy leading to lower urinary levels. Participants had one-hour group meetings for dietary instruction and counseling twice monthly for 3 months then monthly for 3 months. The frequency of these sessions may have contributed to the relatively low attrition rate of 24% in the VLCKD group.⁶³

Similarly, Goldstein’s study comparing a VLCKD with the calorie restricted ADA diet used urinary ketones measured at 6 weeks and 3, 6, and 12 months to compliment the information obtained by 3 day dietary recall. The authors noted that mean carbohydrate intake at 3, 6 and 12 months was more than double the goal. This correlated with urinary ketone elevation in 61% of the VLCKD diet at 6 week after diet initiation, but in only 7% at the conclusion of the study 12 months later (Goldstein et al, 2011).

Westman’s study randomized individuals with obesity and type 2 diabetes to either a VLCKD or a low-glycemic, reduced calorie diet (500 kcal/day deficit from weight maintenance diet) (Table 1). Adherence to diet and exercise was measured using a combination of self-report, food records, and urinary ketones. All participants completed food records (on 5 consecutive days, including a weekend) at baseline and at weeks 4, 12, and 24. Though group rather than individual meetings were held, these were conducted as frequently as weekly for 3 months and included a physician. After that, regular meetings were held every other week for 3 months. Though only 58% of participants completed the study, both groups had good adherence based on self reported dietary intake and interventions led to improvements in hemoglobin A_1c, fasting glucose, fasting insulin, and weight loss, though the VLCKD group had greater improvements in hemoglobin A_1c, body weight, and HDL.³⁷

Challenges Affecting LCD Adherence in Patients with Diabetes

Cultural Barriers

Although it is well-established that genetics influences the development and degree of complications associated with type 2 diabetes, it is also known that behavioral factors including diet and physical activity are directly associated with diabetes diagnosis and progression. Dietary habits are shaped early in life and are influenced by an individual’s knowledge and experiences which are often shaped by their culture.⁷² Today, there is increased recognition for the impact of culture on health.⁷³ Culture refers to shared values, beliefs and social behaviors that collectively shape a group’s identity and interaction in and with their environment.⁷³ When prescribing diabetes management plans, it is important that clinicians are sensitive to their patients’ cultural traditions so that counseling and interventions are appropriate and more likely to have meaningful outcomes.⁷⁴

East Asian diets are typically white rice-based with less consumption of whole grains and fat. Excess consumption of white rice has been associated with higher risk of type 2 diabetes due to its⁷⁵ high glycemic index and load, leading to postprandial blood glucose excursions and hyperinsulinemia.⁷⁶ Zhao et al recently analyzed gender difference in dietary energy of Chinese adults and found that the intake of carbohydrates was 282.4g/day in males and 242 g/day in females, respectively.⁷⁷ Data from the 2013–2015 Korean National Health and Nutrition Examination Survey found that a significant part of the population exceeded recommended ranges of carbohydrates. A higher carbohydrate diet was associated with lower intake of energy and saturated fats, including more grains and fruit but less meat, fish, eggs, beans, and dairy.⁷⁸ Noodles are often used as the main ingredient in Korean meals and are additionally noted to have high glycemic loads and are usually eaten in larger than recommend serving sizes⁷⁹ Similarly, a typical Thai meal involves many complementary dishes, which are served together with rice.⁸⁰ The importance of rice is reflected by one of the most common greetings, “kin khaao reuu yang?” (Have you consumed rice yet?).⁸¹

Traditional South Asian diets are often high in starchy foods such as potatoes, flatbread (roti and chapati), rice and fried snacks.^82,83 The STARCH study, a cross-sectional multicenter survey of 796 patients, demonstrated carbohydrates made up over 60% of energy intake for Indian patients with T2DM.⁸⁴ Due to globalization, industrialization and socioeconomic changes, dietary patterns in South Asia have generally shifted to consumption of high fat, less nutrient-dense foods with increased intake of sugar and dairy, particularly among urban and higher income rural dwellers.⁸⁵ Both the traditional eating patterns and modern eating patterns can make adherence to dietary patterns difficult in South Asian countries. This is of particular importance given that South Asians develop type 2 diabetes at younger ages and at lower BMI and have increased rates of complications.⁸² A systematic review noted that for individuals of South Asian descent, food plays a key role in maintaining relationships. This often resulted in⁷⁴ social pressure to not adhere to diabetic diets when at social events.⁷⁴

Traditional Hispanic diets among Dominican, Mexican and Puerto Rican communities include staples such as rice, beans and tortillas.⁸⁶ As seen in other cultures, migration is associated with changes in dietary habits. Mexican Americans are one of the largest growing minority groups in the USA. Higher acculturation among adults of Mexican descent living in the USA has been associated with lower intake of the healthy foods in a traditional Mexican diet, including fruits, vegetables, legumes, and whole grains. Instead, adoption of a Western diet is common, which is usually low in fruits and vegetables and high in refined grains and added sugar.^87–89 The 2017–2018 prevalence of diagnosed diabetes in adults aged 18 years or older living in the US was highest among people of Hispanic origin (12.5%), and non-Hispanic blacks (11.7%). Among adults of Hispanic origin, Mexicans (14.4%) and Puerto Ricans (12.4%) had the highest prevalence, followed by Central/South Americans (8.3%) and Cubans (6.5%) (Prevalence of Diagnosed Diabetes | Diabetes | CDC).

In the US, non-Hispanic blacks (NHBs) are comprised of heterogeneous groups including those from African and Caribbean ancestry. Despite differences in ethnicity, both groups of NHBs in the US are more likely to be diagnosed with diabetes and experience higher rates of complications and mortality compared to their Caucasian counterparts.⁹⁰ Eating patterns of NHBs are shaped by historical factors such as the transatlantic slave trade, and the common social belief that “more shapely” body types are deemed more desirable compared to other cultures’ value of “ideal thinness”.⁹¹ Traditional African America cuisine, often referred to as “soul food” includes starchy vegetables and legumes (black-eyed peas, pinto beans, lima beans), grains (rice, grits, cornbread, biscuits), a variety of green leafy vegetables (collards, mustard and turnip greens) in addition to meats that are often breaded and fried. It is not uncommon to see combinations of foods such as rice paired with black eyed peas (“hopping john”) or red beans and rice. It is also common to see smoked meats added to vegetables to increase flavor.⁸⁶ A common theme of qualitative and ethnographic studies investigating eating practices of African Americans is the importance of taste and concerns that healthier options did not taste as satisfying as traditional foods.^92–95 Social events with more attendees usually translated to more traditional cultural foods being present and increased the likelihood of choosing less healthy options and overeating.⁹²

Because of vast similarities in culture such as religion and language, the Middle Eastern and North African (MENA) Region are often grouped together when describing health outcomes. Traditionally, this region’s diet was felt to be one of the healthiest as it is the basis of the well-studied “Mediterranean diet” that is high in vegetable proteins, fibers, minerals and vitamins. The cultural emphasis on these foods makes it challenging for patients to adhere to ketogenic diets. The authors of the Goldstein study noted difficulty involved in prescribing the Atkins diet over an extended period in the Mediterranean area, where fruit and vegetable intake is high. Patients were able to avoid eating “pure carbohydrates” (bread, rice, etc.), but continued to consume vegetables and dairy products.⁹⁶ Over the past few decades,⁹⁷ many countries in this region continue to experience a socioeconomic transition due to urbanization, and this has impacted nutritional choices. There has been a shift away from tradition to a diet heavier in processed foods,⁹⁸ sugar sweetened beverages, and often lacking in vegetables, fruits, and whole grains.⁹⁹ Mean energy intake in most countries in this region is higher than the global average, with Turkey and Yemen ranking among the highest.⁹⁸ In countries like Saudi Arabia, female gender is believed to be a barrier to optimal diabetes management due to limitations of health education. Women also have lower levels of physical activity compared to men due to time-consuming domestic responsibilities as well as a lack of culturally appropriate outdoor facilities.¹⁰⁰

Traditional Italian cuisine is that of the Mediterranean diet, including controlled quantities of fats, a low percentage of carbohydrates, a low glycemic index and a high content in dietary fiber.¹⁰¹ Pasta, traditionally an Italian dish, has expanded to many countries and has become a major dietary source of energy globally. Somewhat counterintuitively, several studies have found the glycemic index of pasta to be low to moderate compared to other starchy foods such as white bread and potatoes. Cross sectional analysis demonstrated that higher pasta intake was associated with better adherence to the Mediterranean diet.¹⁰² However, over the years there has been a decrease in adherence to the Mediterranean dietary pattern. This is thought to be secondary to several factors, including changes in socio-cultural, intergenerational, and economic factors, such as increased income. Poor adherence is also believed to be a consequence of the evolving female gender role, different organization of working hours, urbanization and globalization.¹⁰³

Religious Barriers

Similar to cultural traditions, dietary patterns and adherence to specific diets can be influenced by religion. For example, studies have shown a short-term increase in caloric intake with corresponding weight increase and an increase in glycemic and lipid markers due to Christmas festivities.¹⁰⁴

Several recent publications have shown that the nutritional changes observed during Ramadan are associated with unhealthy dietary changes. During observance, individuals will consume a predawn meal, to obtain requirements of water, carbohydrates and energy needed for daytime hours. This meal varies slightly by region but typically consists of bread/cereal, couscous, eggs, cheese, and/or rice. The sunset meal that breaks the fast can average up to 150 g of carbohydrates and over 1200 kcal and usually includes dates, meat or cheese pastries and rice.^105,106 This is traditionally followed by an additional meal eaten a few hours later or nocturnal grazing.¹⁰⁶ One food survey of 340 Moroccan households found significant increases in energy intake, carbohydrate intake, sucrose intake, sodium intake, and calcium intake and a significant decrease in protein and lipid intake. Carbohydrates increased from 312 g/day before Ramadan to 360 g/day during Ramadan. This was possibly due to increased consumption of cereal products, which are popular in this period. An atmosphere of festive solidarity and family grouping is also thought to contribute to the changes in dietary habits.¹⁰⁷

Yom Kippur (Jewish Day of Atonement) is considered the holiest day of the Jewish calendar and is one of two times of the year that people of Jewish faith abstain from food and water for 25 hours (from sunset on day 1 to one hour after sunset the following day). The other day long fast is Tish B’Av, also known as Ninth of Av, but there are 4 additional periods of potential fasting of shorter duration within the Jewish faith.¹⁰⁸

The religious group Seventh-day Adventists promotes vegetarianism, which may be advantageous as several studies have shown that vegetarianism is associated with lower prevalence of type 2 diabetes.¹⁰⁹ However, the diet of Seventh-day Adventists is characterized by a large intake of carbohydrates in the form of fruits and vegetables, as well as high content of fatty acids, dietary fiber, folic acid, vitamin C, vitamin E and Mg¹¹⁰ Vegetarianism is also practiced in Hinduism and Buddhism.^111,112 Though dietary practices vary, the traditional diets of Hindu families include carbohydrates as a staple, usually rice and or chapatis (form of bread).¹¹³ Lin et al investigated vegetarian practices of Hindus and Buddhist in Malaysia and found that rice was a major dietary staple and was consumed daily by majority of participants. Other carbohydrates consumed included porridge, rice noodles and bread. Buddhism participants consumed higher daily intake of carbs compared to Hindu ones with a carbohydrate intake of 67.7% of total energy intake and 63.55%, respectively.¹¹⁴

Economic Barriers

People of lower socioeconomic status often face unique challenges in adhering to planned dietary changes. One barrier unique to people with lower economic security is food insecurity – the disruption of food intake or eating patterns due to the cost of food items exceeding an individual’s or family’s financial circumstances.¹¹⁵ Food insecurity is associated with a higher hemoglobin A1c.¹¹⁶ Low carbohydrate eating patterns are potentially more expensive than higher carbohydrate plans, although one study regarded the potential increased cost as negligible.^117,118 This could potentially limit access (or perceived access) to this eating pattern for people with inadequate financial resources.

Patient Preference

A potential component of adherence that is difficult to quantify is patient buy in. In studies of low carbohydrate dietary interventions, randomized trials such as those by Guldbrand and Iqbal,^58,69 tend to have poorer rates of adherence than non-randomized trials such as those by Hussein and Hallberg.^35,53 In a 24-week study by Hussain in which obese participants chose between a VLCKD and a low-calorie diet, participants with diabetes who chose a VLCKD lost 12% of their body weight, whereas those who chose a low-calorie eating plan lost 7%.³⁵ In a year-long intervention, Hallberg found that patients with type 2 diabetes on a VLCKD experienced a 12% mean weight loss and 17% reduction in hemoglobin A1c. Health coaches monitored ketones and adjusted diet as needed to achieve ketosis. Participants received education either on-site or via web-based recorded content and also received remote care from health coaches. The study had a very low attrition rate of 16.8% from the VLCKD group.⁵³ Two-year follow-up showed more modest improvements in glycemic control with HbA1c reductions of 0.6–0.9% observed in those on VLCKDs, which may be in part due to the higher attrition rate over longer observation periods.^64,119,120 This suggests that there may be an element of patient “buy-in” to the dietary strategy that promotes adherence.

Potential Solutions

Overcoming barriers to dietary adherence in patients with diabetes is critical to reducing disease burden and preventing its progression. Objective self-monitoring of carbohydrate intake can help maintain dietary adherence. Validated examples include the use of home biomarkers such as urinary ketone levels and blood or breath ketone meters.^121–123 Urbain et al examined serum and urine ketones during the 6th week of a VLCKD. Urine ketones were measured using over-the-counter reagent strips that determined the presence of acetoacetate. The levels of blood and urine ketone bodies correlated throughout the 24-hour period. The best time for urine testing for ketosis was early morning and several hours after dinner.⁵¹ Hand-held ketone sensors using a fingerstick obtained capillary blood sample accurately measure BHB in starvation-induced ketonemia when compared with the gold standard, venous whole blood by an enzymatic laboratory reference method.¹²⁴ More affordable meters have also shown good correlation. Moore compared the Precision Xtra meter with the more affordable Meter 2- Keto-Mojo in a double-blind cross-over study. Ketone and glucose levels were measured before and twice after ingesting racemic ketone, natural ketone, or maltodextrin supplement. Both meters had excellent agreement between each other for measuring ketone measurement, including the more affordable Meter 2.¹²⁵

In office monitoring of other biochemical markers is also helpful. As described above, significant improvements in blood glucose, HbA1c, HDL cholesterol and triglyceride levels are consistently noted in those who following a VLCKD and therefore could be used as markers of adherence. Weight loss and improvements in blood pressure have also been noted but are less specific to an LCD.

Accuracy issues notwithstanding, another potential tool to improve adherence may be through self-monitoring of food intake, eg, using a food diary. Burke’s systematic review of self-monitoring in weight management found significant associations between monitoring frequency and weight loss consistently in the 15 studies assessing dietary self-monitoring. However, the level of evidence was weak due to methodologic limitations.¹²⁶ Though a food diary has the limitations previously discussed, when used as the sole tool for assessing adherence, it may play a role in improving the mindfulness of the types and amounts of foods consumed, thereby indirectly helping adherence.

Educational interventions may also be a means of improving adherence. In a Swedish study, an educational course on carbohydrate restricted diet (75 g/day or less) and corresponding insulin dose reduction was used to enhance adherence among patients with type 1 diabetes over four years. After 2 years, about 50% achieved stable lowering of HbA1c.¹²⁷ In addition, continuous care models integrating telemedicine are a novel approach that has been effective at guiding nutritional ketosis and assisting with adherence.¹²⁰

Future Research Directions

Research has identified multiple methods to measure and improve dietary adherence to LCD. Given the bias associated with self-reported dietary intake, studies comparing various objective measures of dietary adherence are needed to determine the optimal metric. More research is also needed to better understand the potential role for weight loss medications as adjunct therapy to assist adherence to an LCD, as well as the myriad of cultural, psychological, and economic factors that play a role in adherence. Additionally, the long-term effects of VLCKD on biochemical parameters requires further investigation to help individualize therapy.