MATERIALS & METHODS

This study was conducted in compliance with guidelines on human experimentation and approved by the Institutional Review Board of Faculty of Medicine, Chulalongkorn University (IRB no. 211/57). The study was conducted at King Chulalongkorn Memorial Hospital, Chulalongkorn University from 2015 to 2018. All the participants had a Thai Mental State Examination [20] (TMSE) score of at least 23 and provided informed consent. PD was diagnosed according to the United Kingdom Parkinson’s Disease Society Brain Bank (UKPDSBB) criteria [21]. Participants were excluded from the study if they had atypical parkinsonism, allergic rhinitis, upper respiratory tract infection, chronic sinusitis, chronic alcoholism, postoperative status, a history of severe traumatic brain injury or base of skull injury, a history of malignancy, chronic kidney disease, or hypothyroidism or a history of chemotherapy.

Participants were asked about their perception of their sense of smell and taste. If they had abnormal perception, then they were further asked to identify whether the perception was decreased, absent or altered and whether the abnormalities were present only sometimes or all the time. Participants were asked to provide detailed information on food and taste preferences and appetite using a 25-item questionnaire. Participants’ weight and height were measured, and smell identification and gustatory tests were performed in both patients and controls.

Smell identification test

Patients and controls were tested with SS-16. We previously validated the SS-16 test kit in our patients with PD (unpublished data by T Kitjawijit and P Jagota, 2015). Only 14 odors were identified by more than 50% of the healthy controls and thus were considered culturally suitable. The cutoff score for olfactory dysfunction in patients with PD was identified as 9. For this study, we used only those 14 significantly relevant odors to test all the participants (turpentine and clove were not used), henceforth the test was designated the modified SS-16 (mSS-16).

Gustatory (taste) identification test

The filter paper disc method [22] (FPD) was modified by using cotton swabs to transfer the tastants instead of filter paper discs. In the FPD method, the filter paper discs are transferred to the tongue using forceps, where the examiner must ensure that the filter paper discs have been dropped onto the tongue and not moved elsewhere. Patients with PD experience rigidity and might have difficulty opening their mouths for a long time. Cotton swabs with the same bud size as filter paper discs (0.5 cm diameter) were used to ensure that an adequate amount of tastants transferred to overcome this problem.

Solutions were prepared to test sweet, salty, sour, bitter, and umami tastes. A sucrose solution was used for sweet, sodium chloride for salty, tartaric acid for sour, quinine for bitter, and monosodium glutamate (MSG) for umami tastes. The concentrations of the solutions for sweet, sour, salty and bitter were prepared at 5 levels based on the FPD method [22]. For umami taste, 6 concentrations of MSG solutions were prepared using the method developed by Satoh-Kuriwada et al. [23] (Table 1).

Participants had to refrain from smoking 1–2 hours before the test and refrain from eating, drinking, and chewing gum at least 30 minutes prior. They were tested by first applying the solution of a randomly selected taste with the lowest concentration (level 1), except for bitter, which was tested last to avoid unpleasantness. A cotton swab was dipped into the solution and then applied for 3 seconds onto the anterior (near the tip) part of the tongue. Then, the cotton swab was removed, and subjects were asked to swallow their saliva once to disperse the taste substance. Subsequently, the participants responded whether they had felt any taste and the name of the taste. If the taste was not identified, the next concentration of the same taste solution was tested using a new cotton swab until the taste was correctly identified or until the highest concentration of that taste solution was reached (level 5 for sweet, salty, sour, bitter and level 6 for umami). The concentration level at which the taste was identified was defined as the taste RT. If the taste was not identified, it was simply defined as “cannot be identified.” Then, the participants rinsed their mouth with water several times until no previous taste remained to avoid interference between tastes. The process was then repeated for other tastes in random order ending with bitter taste, as mentioned above. The same process was performed for both patients and controls. The total time for testing all the tastes in a participant was approximately 15 minutes.

Statistical analysis

The chi-square test and Fisher’s exact test were used for categorical data, the Mann–Whitney U test was used for ordinal data, and the independent t test was used for continuous data to test for significant differences between groups. Spearman’s rank correlation, point biserial correlation and Pearson’s correlation coefficients were calculated to study the correlations between variables. A p-value < 0.05 was considered statistically significant, except where a significant p-value was derived from the Benjamini-Hochberg procedure to adjust for multiple comparisons.

RESULTS

One hundred five patients with PD and a total of 101 age- and sex-matched controls were included. Some of the controls did not answer some parts of the questionnaires; therefore, the number of controls is different for different parts. Demographic data are provided in Table 2. Weight and height were not different between patients with PD and controls, but the BMI was significantly higher in controls (PD = 22.62, controls = 23.86, p = 0.028), as well as smoking and drinking history (p = 0.009 and p = 0.006, respectively). The median Hoehn and Yahr (H&Y) stage was 2.5 (range 1–4). The prevalence of diabetes mellitus (DM) in patients and controls was 14.29% and 11.88% (p = 0.761), and hypertension (HT) was 25.71% and 37.62% (p = 0.091), respectively.

Patients were more likely to perceive themselves as having abnormal smell and taste sensations than controls (p < 0.001 and p = 0.008, respectively) (Table 3). Most patients identified themselves as having decreased olfaction and gustation, with abnormalities present all the time in approximately 45% of the patients. Patients significantly preferred sweet (p = 0.001), salty (p = 0.004), and umami (p = 0.029) tastes compared to controls. The prevalence of dry mouth in both groups was not different (p = 0.461).

Of the 25 items on the food and appetite questionnaire (Table 4), 3 items were significantly different between patients and controls after adjusting for multiple comparisons using the Benjamini-Hochberg procedure with a false discovery rate of 0.2. Patients felt that they had lost appetite (p = 0.001). Food taste was more important to the patients than controls (p = 0.001), and they had to add sugar or other sweet ingredients to their food more frequently than the controls (p = 0.012).

The mean mSS-16 score (14 items) was 10.7 for controls and 6.4 for patients with PD (p < 0.001) (cutoff score for normal is 9) (Table 3). The gustatory RT test revealed that patients identified the correct tastes at a significantly higher concentration level for all tastes (Figure 1). The mode (highest frequency) of recognition for each taste in patients was level 3 for sweet, 2 for salty, 3 for sour, 3 and 4 for bitter and 6 for umami. In controls, it was level 2 for sweet, 2 for salty, 3 for sour, 2 for bitter and 4 for umami.

Spearman’s correlation tests showed no correlation between the BMI and mSS-16 score in either patients or controls, or between the BMI and H&Y stage, and H&Y stage and mSS-16 in patients. In patients with PD, BMI exhibited a small but significant (p = 0.037, ρ = 0.204) correlation with the salty taste RT, and small correlations were observed between the H&Y stage with bitter (p = 0.030), and umami (p = 0.021) taste RTs (ρ = 0.212 and ρ = 0.258, respectively), indicating that a poorer salty taste sensation was associated with an increased BMI and poorer bitter and umami taste sensations were associated with more severe disease stages. In the control group, the bitter taste RT exhibited a small but significant inverse correlation with the mSS-16 score (p = 0.026, ρ = -0.258). Thus, a poorer bitter taste sensation was associated with a poorer olfactory score in controls.

Spearman’s correlation analysis was conducted to study whether the five taste RTs had any correlations. All the tastes correlated positively with each other in both patients and controls, with moderate to large effect sizes (Table 5), except for umami and sweet RTs in patients with PD (p = 0.486), and umami and sweet (p = 0.059), umami and bitter (p = 0.055) and umami and sour (p = 0.369) RTs in controls.

Regarding Pearson’s correlation coefficients between the 25 items on the food and appetite questionnaire (Table 4) and the five taste thresholds, the salt RT was negatively and mildly correlated with question 14 in patients with PD (p = 0.041, r = -0.20). The umami taste RT was also negatively and mildly correlated with question 14 (p = 0.019, r = -0.263) in the patients. Based on these results, higher salt and umami RTs, i.e., poorer salt and umami taste sensations, tend to be associated with a poorer ability of patients with PD to discriminate between different tastes of food. Umami was additionally mildly and negatively correlated with questions 15, 16 and 17 in patients (p = 0.026, r = -0.248; p = 0.012, r = -0.281; p = 0.026, r = -0.249, respectively). Therefore, a poorer umami taste sensation in patients with PD tends to be associated with a lower ability to discriminate the taste of food (e.g., sweet, salty, bitter, and sour), what dish it is and how spicy the food is. The sour taste RT was mildly correlated with question 5 in controls (p = 0.029, r = 0.253) and mildly and negatively correlated with question 20 in patients with PD (p = 0.029, r = -0.214). Based on this finding, a poorer sour taste sensation tends to be associated with weight loss in controls, and patients with PD are less likely to lose their appetite because of depression. The bitter taste RT was mildly correlated with question 6 in patients with PD (p = 0.029, r = 0.213). Thus, a poorer bitter taste sensation tends to be associated with the addition of extra seasoning to food by patients with PD. The sweet RT was not correlated with any of the questions in either patients or controls.

The point biserial correlation analysis was conducted for the 25-item questionnaire and BMI and mSS-16. In patients with PD, BMI was negatively correlated with questions 5 and 19 (p = 0.029, r_pb = -0.24 and p = 0.021, r_pb = -0.25, respectively). BMI was positively correlated with question 25 (p = 0.027, r_pb = 0.24). These results indicate that weight loss and financial difficulties tend to be associated with lower BMI values in patients with PD. Liking to eat what the patient or the patient’s family cooks rather than ready-to-eat food tends to be associated with higher BMI values. mSS-16 scores for both the patients and the controls and BMI of the controls were not correlated with any of the questions.

DISCUSSION

Our study showed a significantly lower BMI in patients than in controls, consistent with previous studies [24,25], although their BMI was within the normal category. As reported in the literature, patients have impaired olfactory function. The present study showed that patients also have impaired gustatory function for all tastes, including umami, compared to controls. Previous studies have tested sweet, salty, sour, and bitter tastes [9-17]. They did not test umami taste. This study, to our knowledge, is the largest study testing taste sensation in patients with PD and is the only study that has tested umami taste sensation in patients with PD. Hypogeusia for all tastes was present, where patients identified all the tastes at higher concentration levels than the controls. One patient could not identify sweet taste, 2 could not identify salty taste, and 9 could not identify umami taste. All patients could identify sour and bitter tastes. Hence, the level of taste loss in patients may be unequal for different tastes. Cecchini et al. [26] showed that sour and salty taste identification was worse in patients with PD presenting a mild cognitive impairment and executive dysfunction. Another study in Asia by Kim et al. [15] found that female patients with PD had taste impairment, as identified by lower filter paper taste strip test (TST) scores, which tested sweet, sour, salty and bitter tastes (not umami). However, the impairment was attributable to a lower Mini-Mental State Examination (MMSE) score [15]. Therefore, differential taste loss might be the result of differential anatomical dysfunction. Regardless, all the patients in this study could still taste some of the tastants, although at higher concentrations.

The loss of various tastes is correlated significantly and positively with each other. Hence, the loss of one taste will be associated with the loss of another taste, although they may be at different levels, as mentioned above. The exception for this is the umami taste. The umami taste threshold was not correlated with the sweet RT in patients or with the sweet, bitter or sour thresholds in controls. Moreover, more umami nonidentifiers were observed than any other taste. The level of the umami RT was also the highest (level 6 in patients and 4 in controls). It may explain the lack of a correlation. Previous studies have also reported a higher RT for umami than for other tastes in the elderly [27].

Thai people consume more MSG per day than Japanese people (3.6 g/day vs. 1.2–1.7 g/day) [27]. Regular consumption of a larger amount of a tastant may increase its RT [28]. For the umami non-identifiers (as with other tastes) in this study, we do not know whether they have a RT that is higher than the maximum level in this study or whether they are ageusic for the taste. A study with a higher concentration of tastants may provide insights into this issue.

Patients significantly perceived their abnormal olfaction and gustation. However, although the number of patients who perceived that their olfactory and gustatory functions were impaired was significantly higher than that of the controls, the majority of the patients still perceived them to be normal. This finding confirms previous reports that subjective taste and smell impairment identification is low [29,30].

Based on the responses to the questionnaire, patients had to add sugar or other sweet ingredients to their food. Overall, the food and appetite questionnaire showed that dysgeusia in patients is associated with a poorer appetite, poorer ability to discriminate the taste of food and its spiciness, and a poorer ability to identify the dish. These limitations may have resulted in patients adding extra seasoning to their food. Losing weight and having financial difficulties were associated with a lower BMI, while eating home-cooked food was associated with a higher BMI in patients. On the other hand, the mSS-16 score was not associated with any of the questions. Their ageusia may have been attributed to their loss of appetite and rendered the taste of food more important to them. Hence, education on home-cooked, nutritious food with appropriate seasoning may be provided to patients and their caregivers to improve the patients’ appetite and nutrition and reduce their financial burden.

In the present study, BMI did not correlate with olfactory function (mSS-16 score) in either patients or controls. It showed a small correlation with salty taste. The severity of the disease, as represented by H&Y staging, showed a small correlation with bitter and umami tastes but not with BMI and mSS-16 scores. Interestingly, in the controls, bitter taste exhibited a small inverse correlation with mSS-16 scores. Therefore, the poorer the olfactory function, the less participants can identify bitter taste. Correlation results vary from study to study. In contrast to this study, Roos et al. [11] found a small correlation between olfactory function and BMI but not gustatory function and BMI. Shah et al. [13] did not observe effects of age, disease severity or duration on gustation in patients with PD. In contrast, De Rosa et al. [10] identified a correlation between gustation and disease severity and stage. Kim et al. [15] found no significant correlations between the TST score and age, H&Y stage, disease duration, MMSE score, MoCA score, or smell test score, even when their data were analyzed separately according to sex.

Taste preference in humans has developed since childhood. The body usually prefers particular tastes to obtain the nutrients it needs–sweet for energy (carbohydrates), salty for minerals and umami (savory) tastes for proteins [31]. A bitter taste represents toxic food, and sour represents acids, and thus these foods are usually avoided [31]. Patients in this study preferred sweet, salty, and umami tastes more than the controls. Increased energy and nutritional requirements from motor symptoms and malnutrition may explain these preferences [24,32]. Patients added significantly more sweet ingredients to their food. The sweet preference in humans is evident beginning in the prenatal period [33]. Some studies have shown that, unlike other tastes’ RT, sweet RT does not significantly increase with aging [30,34,35]. Meyers et al. [36] reported an increased sweet preference, sweet consumption, and ice cream preference in patients with PD compared to controls. However, in another study by Sienkiewicz-Jarosz et al. [37], pleasantness ratings of sucrose solutions did not differ between patients and controls. However, this study involved only 20 patients.

Malnutrition is more prevalent in the later stages of PD [32]. As patients with a low BMI have a poorer survival prognosis [38], malnutrition prevention should be initiated early in the course of the disease to maintain a normal BMI. Knowledge of patients’ preferences for food taste and type can help relieve this issue. Flavor has sometimes been confused with taste. Olfaction, gustation, and mechanosensation of the tongue together send signals to the orbitofrontal cortex where the pleasantness or unpleasantness of food is perceived. This perception constitutes flavor. The smell or taste of the food along with the texture, sight, and anticipation of the food affect flavor. Therefore, studies aiming to improve nutrition or quality of life (QoL) related to food intake may need to consider factors other than olfaction and gustation.

This study has a few limitations. First, the validation of SS-16 in patients with PD by our group is unpublished (by T Kitjawijit and P Jagota, 2015). Second, although the BMI of patients was lower than that of the controls, patients with PD included in the present study had a normal BMI. Hence, the result may be different in malnourished or low BMI patients. As the study showed impaired gustation in this group with an almost high BMI, the impairment may be more pronounced in the lower BMI group. Further studies will be needed to validate this assumption. We did not study the effects of medications on tastes, which is another limitation of this study, although a previous study has shown that the taste test score was not associated with the levodopa equivalent dose [9]. Some small correlations between some tastes and the H&Y stage and BMI were observed in patients. As stated above, correlation studies remain controversial. More extensive studies are needed to investigate this issue further.

Conclusions

This study confirms olfactory and gustatory dysfunction for all tastes, including umami, in patients with PD. Most of the patients are unaware of them. They may unconsciously add extra seasoning or sweet ingredients to overcome taste dysfunction.

Patients have a preference for sweet, salty, and umami tastes. Increased sweet consumption is evidenced by adding extra sweet ingredients to their food. This information may be of use when providing counseling or adjusting patients’ diets to treat or prevent malnutrition. Adjustments in the diet must counterbalance increased risks of DM, HT, and other acquired disorders in patients. The addition of artificial sweeteners, food enhancers and seasonings, an understanding of food combination types according to ethnicity, or other strategies may need to be used to improve the “flavor” of food and QoL of patients.

Notes

Conflicts of Interest

The authors have no financial conflicts of interest.

Funding Statement

This study was funded by the Ratchadapiseksompotch Fund, Faculty of Medicine, Chulalongkorn University, grant number RA57/112, Chulalongkorn Academic Advancement Fund into Its 2nd Century Project of Chulalongkorn University (2300042200), and Centre of Excellence Grant of Chulalongkorn University (GCE6100930004-1).

Author Contributions

Conceptualization: Priya Jagota, Nattida Chotechuang, Chanchai Boonla, Roongroj Bhidayasiri. Formal analysis: Priya Jagota, Nattida Chotechuang. Funding acquisition: Roongroj Bhidayasiri. Investigation: Teeraparp Kitjawijit. Methodology: Priya Jagota, Nattida Chotechuang, Chanchai Boonla, Roongroj Bhidayasiri. Project administration: Priya Jagota, Nattida Chotechuang, Chanawat Anan, Teeraparp Kitjawijit. Resources: Priya Jagota, Nattida Chotechuang, Chanawat Anan, Teeraparp Kitjawijit. Supervision: Chanchai Boonla, Roongroj Bhidayasiri. Writing—original draft: Priya Jagota. Writing—review & editing: all authors.

Figure 1.

Results of the taste recognition threshold. Gustatory results showing a significantly higher taste recognition threshold (RT) in patients with Parkinson’s disease (PD) than in controls for all tastes, implying poorer gustation in PD. A: PD patients’ mode (highest frequency) for sweet RT is 3, while it is 2 for controls. B: PD patients’ mode for salty RT is 2 as in controls but > 50% of the patients have RT > 2. C: Mode for sour RT is 3 for both PD and controls, but more PD patients have RT of 4 and 5. D: Mode for umami RT is 6 in PD and 4 in controls. E: Modes for bitter RT are 3 and 4 in PD and 2 in controls.

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Figure & Data

References

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