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Peer-reviewed | Manuscript received: March 23, 2017 | Revision accepted: November 28, 2017 in different varieties

Implications for apple consumption in persons affected by fructose intolerance

Katharina Hermann, Ursula Bordewick-Dell

Fructose malabsorption is often er- Abstract roneously referred to in the media as (FM) and hereditary fructose intolerance (HFI) are path­ fructose intolerance, which means ological diseases that should be clearly distinguished from one another, but for that it can be easily confused with both of which fructose is a relevant substrate. The treatment for both diseases the metabolic disease hereditary consists of fructose restriction, but with a completely different focus for each. In fructose intolerance [2]. The diffe- the case of HFI, consumption of fructose must be avoided completely, but in the rent forms of fructose intolerance case of FM, a desensitization strategy can be adopted. This strategy exploits the should be clearly distinguished mechanism of -induced fructose transport. Thus, for FM (unlike for HFI) from one another [3]. • Table 1 pro- it is not necessary to abstain from consuming containing fructose comple- vides a comparison of HFI and FM tely. with regard to their pathomecha- have a high fructose content, and also have an unfavorable fructose/glu- nisms, symptoms, diagnosis, and cose ratio of > 1, which means that at first glance, they appear unsuitable for treatment. In both of these diseases, patients with FM. treatment­ is based on nutritional therapy with fructose restriction Our investigations have shown that depending on the variety, the fructose con- playing a key role, but the focus of tent of apples can vary considerably. Although in every variety of apple, the fruc- the treat­ment is completely different tose content is higher than the glucose content, it is still not necessary to abstain for each. from the consumption of apples completely in the case of FM. In addition to The main reason for the current selecting an apple variety with the lowest possible fructose content, other re- trend of increasing fructose intake commendations that can help to improve fructose absorption can also be taken is (in addition to general nutritional into account. The extent to which glucose promotes the absorption of fructose or recommendations promoting a high improves the symptoms of FM by doing so requires further investigation. and vegetable intake), the wide Keywords: intolerances, fructose malabsorption, hereditary fructose intol­ range of foods available [2]. How­ erance, fructose/glucose ratio, fructose content, apples, fruit ever, the increasing use of high fruc- tose corn (HFCS) in the food industry has had a particular impact in terms of increased intake of fruc- tose from non-natural sources [1]. This sweet syrup made of Introduction consists of up to 90% fructose. It is a cheap alternative to that Fructose intake has increased signi- is used for sweetening [4]. HFCS ficantly in recent years [1] and this is often used to make soft drinks, Citation: trend is partly responsible for the in- bread products, , and Hermann K, Bordewick-Dell U creasing prevalence of fructose mal- ketchup [5]. Fructose naturally oc- (2018) Fructose in different apple absorption (FM) [2]. Fructose is also curs mainly in fruit, vegetables, and varieties. Implications for apple the substrate involved in diseases of [3]. consumption in persons affected fructose , such as here- Foods with added HFCS, as well as by fructose intolerance. Ernah- ditary fructose intolerance (HFI). fructose-rich are key concerns rungs Umschau 65(3): 48–52 Therefore, fructose content in food for patients with diseases of fructose This article is available online: is an important issue for patients metabolism and impaired fructose DOI: 10.4455/eu.2018.010 who have diseases in which fructose absorption. While HFI treatment fo- is a key factor. cuses solely on strict abstinence from

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fructose malabsorption (FM) hereditary fructose intolerance (HFI) general description impairment of intestinal disease of fructose metabolism [11] fructose absorption [10] genetic defect unknown [3] mutation of the ALDOB gene [12] heredity unknown [13] autosomal recessive [14] prevalence approx. 1:3 [13] 1:20 000 [14] pathophysiology altered activity of the relevant transporters in deficiency of the fructose-1-- the intestinal wall [15], incomplete absorption aldolase () of genetic origin [14] of fructose with subsequent in the toxic accumulation of fructose-1-phosphate, colon [3] especially in the cells of the liver, the intestines, and the proximal tubule [16], and disorder of fructose metabolism with blocking of and glucogenesis [14] symptoms gastrointestinal symptoms [3, 10] symptoms of persistent hypoglycemia, liver and kidney damage, failure to thrive, reduced blood coagulation, edema, and ascites [14] diagnosis after oral intake of fructose [3] genetic analysis using DNA sequencing [14]

treatment three-step model [17]: strict restriction of fructose, sucrose, - significantly reduced fructose intake on a tem- and [3] porary basis, especially free fructose (abstinence phase) [3], - followed by gradual reintroduction of fructose in order to increase fructose tolerance and to determine individual fructose tolerance (testing phase), - then, transition to long-term nutrition that is adapted to the patient’s needs and require- ments [17] prognosis can be treated successfully through changes to if the dietary recommendations are adhered to the diet; taking account of individual preferences in a consistent manner, there is no reduction in and avoiding deficiencies ensures preser- life expectancy; if hereditary fructose intoler­ vation of quality of life [17] ance is present but not detected, this can lead to death [3]

Tab. 1: Comparison of fructose malabsorption with hereditary fructose intolerance FODMAPs = fermentable oligo-, di-, and polyols [1]

fructose as a treatment method, die- high fructose content and an imba- the individual variety is taken into tetic modification of FM aims to in- lance between fructose and glucose account, the free fructose content crease fructose tolerance. If glucose [7]. Therefore, at first glance, it ap- and free glucose content of the apple intake is increased at the same time that people with FM should varieties , , and Jo- as fructose intake, fructose can also be advised against eating this fruit. nagored was determined and com- be transported to the via However, usually, little distinction pared to the respective contents of the GLUT2 transporters, which are is made between the content mandarins and . expressed more strongly this case. of different varieties of apple, even This relieves some of the strain on though initial results show that GLUT5 transporters, which are the there are indeed differences between Method transporters that are primarily res- the varieties [8, 9]. Mandarins and ponsible for fructose absorption [3]. bananas are better tolerated alter- For each variety of apple, five Therefore, tolerance of sucrose, as natives to apples due to their more samples from various shopping well as foods that have at least a bal­ favorable fructose/glucose ratios outlets were investigated. The anced fructose/glucose ratio (≤ 1) is [3]. same procedure was followed for far better than tolerance of fructose mandarins and bananas. Each of the alone [3]. This glucose-induced fruc- measurements was done as a double Objectives tose transport is particularly useful determination. during the abstinence phase. In order to better evaluate whether The fruit was first peeled and- ho Apples are the most popular fruit in consumption of apples is feasible in mogenized. In order to perform the Germany [6]. However, they have a the case of fructose intolerance if measurements, in each case, 1 g

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strate fructose, but their pathome- chanisms are completely different. glucose fructose In the case of HFI, apples and other foods containing fructose must be ATP ATP strictly banned from the diet, where- HK HK as in the case of FM, fructose intake ADP ADP only needs to be restricted and re- moved from the diet in a more mod­ PGI G-6-P F-6-P erate fashion. Since the literature only provides NAD insufficient data on fructose and G-6P-DH glucose content of various varieties of apple, these measurements were NADH carried out using the three most commonly consumed varieties of gluconate-6-phosphate apple in Germany in the years 2014 and 2015 [19]. Fig. 1: Diagram of reaction for the enzymatic determination The measurements show that the of glucose and fructose [18] different varieties of apple differ in ADP = adenosine diphosphate; ATP = adenosine triphosphate; F-6-P = fructose-6-phosphate; G-6-P = glucose-6-phosphate; their fructose and glucose content. G-6P-DH = glucose-6-phosphate-dehydrogenase; In every variety, there was more HK = hexokinase; NAD(H) = nicotinamide adenine dinucleotide fructose than glucose. The values also differ significantly from those published in the literature. This of the homogenized material was • Figure 1 shows the reaction for trend is confirmed by a research pro- suspended in demineralized water. the enzymatic determination of glu- ject in the field of ecotrophology that After Carrez clarification for elimi- cose and fructose. was conducted at Münster Univer- nation of turbidity, 10 mL 0.1 M sity of applied sciences (FH Münster) NaOH solution was added, and the and found the sugar content values solution was then topped up to Results for other apple varieties that are 100 mL and centrifuged for 20 min­ shown in • Table 2 [20]. More exact utes at 4 000 rpm. The measurements show that fruc- verification would require further The sugar in the supernatant was tose and glucose content differs measurements. By way of compa- then determined. The Enzytec™ depending on the variety of apple. rison, the concentration of the two fluid glucose/fructose test kit from • Fig­ure 2 shows the mean values monosaccharides present in bananas Thermo-Scientific was used for this. with information on the standard and mandarins was measured and Fructose and glucose were first phos- deviation of the glucose and fruc- presented. phorylated by the enzyme hexo­ tose determination, as well as the The fructose content of apples and kinase. In the next step, glucose- fructose/glucose ratio (F/G-R) of fruit in general depends on exo- 6-phosphate was oxidized by the fruit varieties that were investi- genous factors [21]. In order to NAD+ to gluconate-6-phosphate gated (red and green boxes). Across obtain representative data despite after catalysis by the enzyme glu- all apple varieties, fructose content this, the samples were taken from cose-6-phosphate-dehydrogenase. is significantly higher than - glu different shopping outlets and mea- The amount of NADH is equivalent cose content. Unlike in the case of sured using double determination. to the original glucose amount and mandarins (F/G-R slightly > 1) and The relatively high variation in the can be determined photometrically bananas (F/G-R always < 1), the five individual measurements is at- at 340 nm (measurement 1). After ratio is significantly greater than tributable to natural fluctuations. that, fructose-6-phosphate is con- one. The measured values differ sig­ Larger sample sizes would be useful verted by phosphoglucose nificantly from the values reported in order to unambiguously prove to glucose-6-phosphate, which is for apples in general in the litera- the variety-specific differences and further transformed by the glucose- ture. to obtain the most stable values 6-phosphate-dehydrogenase that possible. is already present (measurement 2) Despite the variations in fructose [18]. Fructose content can be calcu- Discussion content, due to the extremely high lated from the difference between fructose values, the varieties that measurement 1 and measurement FM and HFI are related in the sense were investigated should not be 2. that they both involve the sub­ recommended in the case of FM in

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Fig. 2: Fructose and glucose content of various apple varieties and of bananas and mandarins, along with the values for the concentration of each type of sugar in apples in general according to the literature The boxes indicate the fructose/glucose ratio (F/G-R): green box = F/G-R ≤ 1: tends to be tolerated by patients with fructose malab- sorption; red box = F/G-R ≥ 1: tends not to be tolerated by patients with fructose malabsorption (n = 5)

apple variety glucose content fructose content fructose/glucose on the tolerability of the apple. in g per 100 g of in g per 100 g of ratio In addition, methods that may im- fruit fruit prove fructose absorption include 1.1a 2.3a 2.1 spreading out fructose intake by Boskop 1.4a 3.1a 2.2 consuming several small portions throughout the day, and above all, Pink Lady 1.4a 4.8a 3.4 combining fructose consumption 2.0a 5.2a 2.6 with main meals or having it as a b b Royal 2.3 6.9 3.0 dessert [17]. Furthermore, simulta- 3.3b 7.7 b 2.3 neous consumption of and pro- Tab. 2: The fructose and glucose content and fructose/glucose ratio of different tein-rich meals leads to better tolera- varieties of apple1 bility of fructose due to the increased a [20], b [9] intestinal transit time [3]. Adding glucose to fructose-rich the abstinence phase or the testing According to the research results, meals as a therapeutic measure phase. However, it is not necessa- the Elstar variety has a relatively to improve fructose absorption is rily essential to abstain from the low fructose content. This is com- com­ing under increasing criticism. consumption of apples completely. parable to the Granny Smith vari- The results of the study show that By choosing the variety with the ety, which has an average fructose glucose does indeed demonstrably lowest possible fructose content and content of 2.33 g/100 g fruit [20]. increase fructose absorption, but it simultaneously consuming glucose- • Table 2 shows the fructose and could not be demonstrated that it rich foods, it is possible to balance glucose contents and fructose/glu- improved gastrointestinal symp­ out the unfavorable F/G-R. In ad- cose ratios of some apple varieties toms [22]. Since the assertions of dition, it would be interesting to found in the literature. Significant investigate older varieties of apple variations can be found here too, in order to determine whether they showing that the variety of apple 1 The values taken from the literature have may have lower fructose content. selected can have a significant effect been rounded to one decimal place.

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