Taste perception and food preferences in patients with diabetic foot ulcers before and after hyperbaric oxygen therapy

In this study, prior to hyperbaric therapy, a number of negative differences in the perception of the five basic tastes were demonstrated by type II diabetes with diabetic foot ulcers when compared to the controls. These concerned the recognition threshold for basic tastes and the intensity of taste sensation of suprathreshold concentrations. Differences were also noted in the hedonic response of the suprathreshold concentrations of some basic tastes as well as in food preferences. The use of hyperbaric therapy increased chemosensory sensitivity to some extent, and diminished the pleasure derived from eating chocolate and crisps.

An increase in the recognition threshold for saltiness in people with diabetic foot ulcers, and differences for the hedonic response to 0.18% NaCl were found. In diabetics, the lack of reaction to this taste was predominant and no one indicated that the taste of this solution was unpleasant, while for more than 25% of healthy people, the salty taste of 0.18% NaCl was assessed negatively. These results may explain why people with diabetic foot ulcers derive greater pleasure from eating salty snacks such as salty sticks (e.g., salty breadsticks, pretzels) or crackers. This can translate into greater/more frequent consumption of this type of snack and other salty products. Excessive salt intake is harmful, and its effects depend on individual sensitivity to sodium chloride [17]. According to WHO recommendations [18], adults are advised to consume <2 g of sodium per day (5 g salt per day) to reduce hypertension and the risk of cardiovascular disease, stroke and coronary heart disease. The altered sense of saltiness in people with diabetic foot ulcers observed in this paper, corresponds with the results of Gondvikar et al. [19]. These studies included patients with type 2 diabetes with controlled and uncontrolled glycaemia. In both groups, a lower recognition threshold for the salty taste was detected.

In this study, people with type 2 diabetes showed an increase in the recognition threshold for sweet taste, but this did not translate into differences in the hedonic response to the suprathreshold concentrations of sucrose. According to Yu et al. [20], the recognition threshold for sweet taste in people with type 2 diabetes was higher than in healthy people, which is consistent with the results contained in this study. In addition, Yu et al. observed that people with type 2 diabetes preferred lower concentrations of sucrose than healthy people. Moreover, healthy people had a clear negative correlation between the recognition threshold and preferences for sweet solutions, which was not found in people with type 2 diabetes. The research methodology of Yu et al. differs from the methodology presented in this paper, so differences may arise regarding sweet taste preferences in people with diabetes in these two studies. Studies by Gondvikar et al. [19] in patients with type 2 diabetes confirm the occurrence of taste disturbances. Wasalathanthri et al. [21] also tested sweet taste sensitivity in pre-diabetics and diabetics. The sweet taste recognition threshold in pre-diabetic and diabetic people did not differ significantly from healthy people, but increasing the recognition threshold for sweet taste and decreasing the intensity of suprathreshold ratings indicate a sweet taste dysfunction. The effectiveness of chemosensory function of sweet taste is extremely important. In people with glucose intolerance/diabetes, a sweet taste dysfunction increased the incidence of vascular complications and other complications such as ischaemic heart disease, diabetic nephropathy and diabetic retinopathy [5].

In this study, patients with diabetic foot ulcers have an increased recognition threshold for umami taste. In addition, the assessment of three suprathreshold concentrations of monosodium glutamate showed a lower intensity of their taste sensation, and the hedonic response to a 0.3% solution of monosodium glutamate was more positive. No results confirming or challenging the results of this study were found in available literature.

Some light can be shed on this subject by results, in knockout mouse models. TRPM5−/− mice show a reduction in glucose-induced insulin secretion and a significantly reduced response to umami taste as well as sweet taste and bitter taste. Perhaps in patients with type 2 diabetes, umami, sweet and bitter taste dysfunctions are associated with decreased TRPM5 expression [22].

In people with diabetic foot ulcers, the recognition threshold for sour taste increases. In addition, they perceived 0.02% citric acid solution as less intense and 0.10% as less unpleasant. All these differences may contribute to the fact that people with diabetes like sour products more than healthy people. Sensitivity to sour taste in people with type 2 diabetes was studied by Gondvikar et al. [19]. They showed that the recognition threshold for sour taste in people with diabetes was higher than in the control.

In this study, an increase in the recognition threshold for bitter taste and a decrease in the intensity of sensation for 0.002% quinine hydrochloride was demonstrated in patients with diabetic foot ulcers. In the publication of Gondvikar et al. [19] it was not shown that the recognition threshold for bitter taste in diabetic people differed from healthy people. However, the dysfunction of bitter taste perception at the front and back of the tongue and on the soft palate was revealed by a different test method—the spatial taste test.

Furthermore, research using electrogustometry has shown reduced taste sensitivity in patients with type 2 diabetes in correlation with the duration of the disease [6].

Aside from diabetic foot ulcers treatment, the HBOT partly fulfilled the authors’ expectations by improving the sense of taste and changing food preferences. Although the effects of hyperbaric therapy made no difference to the perception of salty, sweet and bitter taste, there was an improvement in umami and sour taste sensitivity and beneficial changes in food preferences.

After HBOT in patients with diabetic foot ulcers, the recognition threshold for umami taste decreased and the intensity of taste sensation for suprathreshold concentrations (0.1% and 1.0%) of monosodium glutamate increased. Changes in perception of umami taste correlate with the lower pleasure derived from eating crisps. These unhealthy snacks are usually spiced with monosodium glutamate and/or disodium 5-ribonucleotide which give food its umami flavour. Increasing the umami taste sensitivity could make the taste of crisps too intense and reduce the pleasure derived from eating them. However, given the many factors that might affect food preferences and the numerous hyperbaric therapy effects on the human body, this is only one of many possible hypotheses which could account for changes in the pleasure derived from eating crisps. The diabetic patients post HBOT declared less pleasure from eating chocolate products, but there was no change in sweet taste sensitivity. Nevertheless, the recognition threshold for the sour taste increased while the pleasure from eating sour products did not change. This confirms the multifactorial causes of changes in food preferences.

In people with diabetic foot ulcers, HBOT produces a number of positive effects on the body including a decrease in HbA1c levels and leucocyte counts [23]. In addition, studies on diabetic rats showed a decrease in blood glucose, and triglyceride levels as a result of HBOT [24, 25]. Studies in adult insulin-dependent diabetes mellitus patients [26] found a reduction of total cholesterol, triglycerides and low-density lipoprotein. In addition, there was an increase in expression of insulin-like growth factor binding protein 1 and a decrease in insulin level. HBOT causes beneficial metabolic changes, such as an increase in the oxidative capacity of the skeletal muscle and a slowing down of the age-related decrease in oxidative capacity of the skeletal muscle, known as a hypothetical mechanism of counteracting insulin resistance [24]. Increased serum levels of IL-10, IL-6, IFN-γ, IL-4 and adiponectin have been shown in patients with diabetic foot ulcers treated with hyperbaric oxygen [27]. In healthy rats during HBOT an increase in the expression of leptin and visfatin genes, as well as IL-1β and IL-10 were also demonstrated [28]. Taste sensitivity and food preferences are dependent on hormonal activity and metabolic changes in the body [2], so, perhaps the changes resulting from HBOT, described above, are the basis for improving taste sensitivity and reducing the pleasure of eating unhealthy snacks in patients with diabetic foot ulcers.

Due to the lack of publications (to the best of the authors’ knowledge) on the effect of HBOT on taste sensitivity, oral mucosa and salivation in patients with type 2 diabetes, this issue was analysed based on the results of tests on irradiated people and animals. Gerlach et al. [29] have shown that in patients receiving radiation therapy for head and neck cancer, the use of HBOT reduced swallowing difficulties, decreased mouth dryness, improved taste sensitivity and increased saliva volume. Studies about the effect of HBOT on irradiated oral mucosa showed that 6 months after treatment microvessel density and the cross-sectional area of blood vessels increased in the sub-epithelial area and deeper connective tissue [30]. Spiegelberg et al. [31] confirmed the positive effect of HBOT on damaged tissues in irradiated mice. Despite the fact that the oral mucosa in patients after radiation therapy and in patients with diabetic foot ulcers certainly shows a different degree and type of dysfunction, perhaps the mechanisms supporting its regeneration after HBOT, described in people after radiation therapy, partially explain the improvement in the perception of taste sensations in diabetics. The assumption that HBOT improves the condition of the oral mucosa in people with diabetes also indirectly confirms the effects obtained in the diabetic foot ulcers itself in which fibrosis and angiogenesis can occur [27]. In addition, studies using diabetic mice have shown not only angiogenesis but also an increase in stem cells proliferation [32].

The methodology of taste recognition testing in the world of science is varied. There is still no so-called gold standard. Each method has its advantages and disadvantages. For example, a difference between objective methods (recording of evoked potentials in encephalography (EEG) and magnetoencephalography (MEG) or modern fMRI imaging (functional magnetic resonance imaging)) and subjective methods, such as specific gustometry and electrogustometry exists [33]. Objective methods do not require the patient to answer questions, however, they do require complex devices and there may be difficulties in analysing the results. Subjective methods do not require complicated devices, however, they require the patient to understand the procedure and to cooperate. In the research of specific gustometry, different concentrations of solutions and different flavours are used, as well as different techniques for the application of flavours. Depending on the procedure used, the results may be inconsistent. In this study, the method described in the ISO 3972 procedures [16] was used. This was modified, based on previous research experience, by increasing the number of samples to also include people with lower taste sensitivity. In order to eliminate methodological differences and obtain reliable results, the same procedures were applied during the taste examination both in the control group and in the diabetic patients with a diabetic foot ulcer. The disturbances in the perception of taste between the control group and the diabetic patients with a diabetic foot ulcer, as shown in this research, are consistent with the picture presented in literature [19,20,21]. This, in turn, confirms the reliability of the obtained results and the procedure used in the taste examination.

The clinical significance of the results obtained in this research is difficult to determine. Formation of food preferences and eating behaviour is very complicated. Food preferences depend on numerous, interdependent factors, e.g., on the characteristics of the consumed product (colour, temperature, texture, serving aesthetics), the social context of the meal, as well as the psychological and biological characteristics of a consumer [34]. The chemosensory sensitivity improvement certainly affects the nutritional behaviour of diabetic patients, but the range of this effect cannot be determined based on the presented results. In order to assess the clinical significance of the observed changes in taste sensitivity and food preferences due to hyperbaric oxygen therapy, the patients’ diet should be fully monitored at least 1 week prior to treatment and for an extended period of time after treatment. It can only be assumed that, to some extent, the improvement in the metabolic status of diabetic patients described by other researchers [23, 26] is based on the mechanisms presented in this study.

In people with diabetes, healthy eating behaviours are important in preventing the development of complications. This study shows that patients with diabetic foot ulcers have a distorted perception of taste sensations and to some extent different food preferences. HBOT increases taste sensitivity and alters the patient’s food preferences to more beneficial ones. Unfortunately, we do not know to what extent the diet of patients with diabetes will change, which is the main limitation of this study. Further research is required to fully explain the effects of HBOT on nutrition. However, based on the positive effects described in this paper and in other studies, the more frequent use of HBOT as an adjunct therapy in complications of type 2 diabetes is worth considering.

This study involved patients with advanced diabetes. This meant having a diagnosis of diabetes at least 10 years ago and where some complications, including non-healing wounds, had already appeared. At the same time, it should be remembered that those patients with severe complications, where there was a problem with understanding the test procedure, collecting taste samples or marking answers, were not invited to participate in the study. Due to the particular character of the studied group, the obtained results can only refer to a relatively narrow group of people suffering from type II diabetes. The development of diabetes mellitus type II can be slowed down with appropriate treatment at the initial stage before complications occur and patients can maintain relatively good health for many years. On the other hand, diabetes which is not treated properly is associated with numerous and serious complications that may be a direct cause of death. Observation of the influence of hyperbaric oxygen therapy on the taste sensitivity and food preferences in people at different stages of the disease could indicate the target group in which such interactions bring the best results. The limitation of the study is the lack of glycated haemoglobin tests. This parameter, used in monitoring glycaemia and the effectiveness of diabetes treatment, could complement the clinical picture of patients participating in the study and serve as a reference point in the interpretation of the results.

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