Predictors of Taste Dysfunction and Its Severity Among Patients With Chronic Kidney Disease

Abstract

Background:

Patients with chronic kidney disease (CKD) often complain of taste dysfunction. The prevalent taste dysfunction among patients with CKD predisposes them to malnutrition, poor quality of life, and worsen disease prognoses. To appropriately treat the taste dysfunction in this group of patients, it’s imperative that factors that predict taste dysfunction and its severity are identified for prompt treatment.

Aim:

To identify factors associated with taste dysfunction and its severity among patients with CKD.

Materials and Methods:

This was a hospital-based case–control study of adult patients with CKD at the University College Hospital, Ibadan, Nigeria. The control group was made up of age- and gender-matched healthy volunteers with no clinical and laboratory evidence of CKD. Relevant clinical and social data obtained include demographics, symptoms, and signs of taste dysfunction and its risk factors. The 4 basic taste modalities namely sweet, sour, bitter, and salt taste senses of the participants were tested with validated “taste strips.” Factors that predict taste dysfunction were identified among the spectrum of the disease.

Results:

There were 100 patients with CKD and 100 healthy controls, age ranges between 19 and 86 years (mean ± standard deviation [SD] = 46.3 ± 13.9 years) and 20 and 85 years (mean ± SD = 43.4 ± 14.9 years), respectively. There was no statistically significant difference between cases and control gender distribution (P = .57). Hypogeusia was found in 27.0% of patients with CKD, while total taste function score of all the control was within normal range. Increasing duration of CKD was identified as a predictor of taste dysfunction among patients with CKD (odds ratio: 4.889, P = .038). The stages of CKD had no statistically significant relationship with the severity of taste dysfunction (P = .629).

Conclusion:

The prevalence of taste dysfunction among patients with CKD was high and this showed significant correlation with increasing duration of CKD; in contrast, the severity of CKD is not significant in the development of taste dysfunction.

Keywords

taste dysfunction chronic kidney disease taste strip predictors

Introduction

The oral cavity is the first part of the alimentary tract and houses the teeth, tongue, and openings of major and minor salivary glands that help in mastication, taste, swallowing, and digestion of some classes of food. Taste is the chemical stimulation of taste receptor cells in the oral cavity perceived as the primary tastes of sweet, sour, salty, bitter, and umami.¹ Appreciation of taste is one of the factors that gives satisfaction derived from eating and when it is defective may lead to aversion for food. Impairment of taste can be devastating to a patient since it does not only affect the ability to enjoy food products but also alter food choices and patterns of consumption, thereby resulting in weight loss or weight gain, and other forms of malnutrition.² Defective taste function among patients with chronic kidney disease (CKD) was implicated as the cause of malnutrition among them.³

Previous studies^4
-6 reported that patients with CKD have high prevalence of taste dysfunction through several mechanisms postulated that include dry mouth, tongue coating, mucosal inflammation, or oral ulceration. The features are common findings in patients with CKD⁷ and might have contributed to taste disorder in them. Uremia was also suggested to cause taste dysfunction due to its effect on the taste bud preventing its regeneration and also its effect on the nerves of taste. Other mechanisms underlying taste dysfunction that have been reported include medication usage, changes in salivary composition, differences in dietary intake, and nutritional status, including zinc deficiency.^2,4,5,6,8

The impact of taste dysfunction is enormous on the patient’s outcomes, survival, and the overall reduced quality of life. However, little attention is often paid to taste dysfunction and its risk factors during routine patient evaluations. The benefits of taste assessment, prompt identification of taste dysfunction, and treatment of the risk factors during routine clinical encounters cannot be overemphasized. These benefits include adequate nutrition, retarding progression of kidney disease, improved survival, and quality of life.

Meanwhile, the severity of taste dysfunction among healthy population has been shown to be worse among males.^9
-11 Liu et al⁹ observed that the prevalence of taste dysfunction doesn’t increase with aging in contrast to the reports by Landis et al¹⁰ and Doty et al.¹¹ Racial or ethnic variation has been associated with taste disorders and it strongly suggests genetic predisposition to taste disorder.^9,12 These findings have not been confirmed or refuted among patients with CKD, who often have taste disorder. Middleton and Allman-Farinelli⁶ found an inverse correlation between age and sweet taste but found no correlation between severity of CKD and taste threshold.

The factors that been putatively considered to be associated with development of taste disorders among patients with CKD include age, gender, oral cavity/oropharyngeal lesion, stages of CKD, nutritional status (body mass index [BMI]), hemoglobin concentration (packed cell volume [PCV]), treatment modalities, and duration of illness. Prompt identification and treatment of risk factors predicting taste dysfunction and its severity among patients with CKD will provide more insight into the pathophysiology of taste disorder in them, in addition to providing preventable and treatable options for taste dysfunction in CKD. This study therefore aim to determine the predictors of taste disorder and its severity among patients with CKD.

Methods

Study Population

The method has been fully described in our previous publication on assessment of olfactory dysfunction, and only a summary is provided in the article.¹³ This was a hospital-based case–control study conducted at the Medical Outpatient clinic; medical wards; and ear, nose and throat clinic of the University College Hospital, Ibadan. Consenting adult patients (≥18 years) with clinical and laboratory diagnosis of CKD defined as estimated glomerular filtration rate (eGFR) < 60 mL/min/1.73 m² with or without albuminuria, while the controls were healthy volunteers who were age- and gender-matched individuals with no clinical or laboratory evidence of CKD. Excluded from the study were individuals with known taste dysfunction from childhood, those with diabetes mellitus, known thyroid hormone disorder, known dysfunction of smell, those having chronic suppurative otitis media, previous history of smoking, or current smoker.

Informed Consent

Written informed consent was obtained from all participants after the study and its purpose have been fully explained to them.

Ethical Approval

Ethical approval was sought and obtained from the Joint ethics committee of the University of Ibadan/University College Hospital with the approval number UI/EC/18/0536.

Study Procedure

Interviewer’s assisted questionnaire was administered on all participants to obtain relevant data including participants’ sociodemographic data, duration of ailment, medical history, symptomatology of CKD, symptoms of taste dysfunction and its severity, primary causes of CKD, treatment modalities for CKD, and duration of CKD. Blood samples were collected to determine serum creatinine which was used to calculate the eGFR of each participant, using the CKD-EPI equation. Height and weight of the participants were measured and BMI was calculated. The oral examination findings of the participants were also documented, and the taste function was assessed with taste strips (Burghart) which have been previously validated and used for the assessment of taste function among Nigerian population.¹⁴

The strips contained 4 basic taste (sweet, sour, salty, bitter) each in 4 different concentrations, impregnated at 1 end with 0.05, 0.1, 0.2, or 0.4 g/mL of sucrose (sweet taste); 0.05, 0.09, 0.165, or 0.3 g/mL of citric acid (sour taste); 0.016, 0.04, 0.1, or 0.25 g/mL of sodium chloride (salty taste); or 0.0004, 0.0009, 0.0024, or 0.006 g/mL of quinine hydrochloride (bitter taste) in increasing order. Plain strips with no tastants impregnated in them were also used to determine the possibility of phantogeusia or patients confabulating.¹⁵ The strips were placed in the center of the anterior two-third of the extended tongue at about 1.5 cm from the tip of the tongue and participants were then asked to close their mouth for whole mouth testing in a total of 18 trials. Before each administration of a strip, the mouth was rinsed with water. The tastes were presented in order of increasing concentrations, starting with the lowest concentration until patient could appreciate the taste or fails to appreciate it in the strips with highest concentration for each of the taste modalities and they were scored appropriately; no score was allotted to the blank strips.

Each of the 2 sequences of 18 taste strips (4 concentrations of each taste quality plus 2 blanks) were applied in a pseudorandomized order. While closing the mouth over the taste strip and with or without tongue movement within the closed mouth patients were asked to identify the taste from a list of 5 descriptors, that is, sweet, sour, salty, bitter, and no taste (multiple forced choice). Gustatory function was obtained by the number of correctly identified taste added up to a “taste score,”^10,15 lowest concentration was 4 points, the highest concentration was 1 point, while failure to appreciate strips with highest concentration was 0. Therefore, minimum score of 0 and maximum of 16 could be obtained and the whole testing procedure for the 4 tastants required about 30 minutes.

Definition of terms

The GFR was graded as stage 1 CKD ≥ 90, stage 2 CKD 60 to 89, stage 3 CKD 30 to 59, stage 4 CKD 15 to 29, and stage 5 CKD (end-stage chronic kidney disease) <15.¹⁶ Body mass index was calculated using this equation for BMI, BMI = weight (kg)/height (m)², which applies equally to men and women. Body mass index was categorized¹⁷ as underweight = <18.5, normal = 18.5 to 24.9, overweight = 25.0 to 29.9, and obesity = 30.0 to >40. While taste was graded as taste score normal values defined as “Taste Strip” scores above the 10th percentile of a group of healthy population.¹⁵ Normogeusia was total taste score ≥9, hypogeusia was <9, while ageusia was 0. Normogeusia for salt, sour,and sweet was taste score >/= 2 while for bitter it was assigned a taste score of 1. Hypogeusia was defined as taste score of 1 or falseidentification taste modalities (salt, sour, and sweet but only false while for bitter only false identification was used to define it. Ageusia was 0 for all taste modalities.¹⁵

Statistical Analysis

Data obtained were entered and analyzed using statistical package (IBM-SPSS statistic, version 22). Demographic variables were represented using tables, while qualitative sociodemographic characteristics of patients with CKD and healthy controls were compared using chi-square tests.

Association between eGFR (stages of CKD) and severity of taste dysfunction was determined using f tests. Factors associated with taste dysfunction were determined using analysis of variance for categorical variables or correlation for continuous variables, binary logistic regression was used to determine predictor variables. Level of statistical significance was set at P value of <.05.

Results

There were 100 patients with CKD and 100 age- and gender-matched healthy controls. The age ranged between 19 and 86 and 20 and 85 years, respectively, while the mean age (standard deviation) were 46.3 (13.9) and 43.4 (14.9) years, respectively (Table 1). There were 56 males and 44 females among the cases, while the control had 52 males and 48 females. There was no statistically significant difference between cases and control gender distribution (P = .57). The mean BMI of cases, 23.4 ± 4.7 kg/m², was significantly lower than that of the controls, 25.1 ± 4.5 kg/m² (P = .009; Table 1).

Table 1.

Sociodemographic and Clinical Characteristics of Participants.

Continuous variables	Case Mean (SD)	Control Mean (SD)	t test	P value
Age (years)	46.3 (13.9)	43.4 (14.9)	1.414	.159
Age range (years)	19-86	20-85
Mean eGFR (mL/min/1.73 m²)	23.7	122.8	20.848	.001
Body mass index (kg/m²)	23.4 (4.7)	25.1 (4.5)	−2.649	.009
Demographic data for categorical data			χ² test	P value
Sex	N (%)	N (%)	0.322	.570
Male (n = 108)	56 (56.0)	52 (52.0)
Female (n = 92)	44 (44.0)	48 (48.0)

Abbreviations: eGFR, estimated glomerular filtration rate; SD, standard deviation.

The cases consisted of 4 (4%) stage 1 CKD, 8 (8%) stage 2 CKD, 19 (19%) stage 3 CKD, 22 (22%) stage 4 CKD, and 47 (47%) stage 5, while all the control had eGFR ≥ 90 (normal) as shown in Figure 1.

Figure 1.

Distribution of cases and control based on eGFR. eGFR indicates estimated glomerular filtration rate.

Taste dysfunction was found in 27 (27.0%) cases, all were hypogeusia (total taste score <9, >0; Figure 2), while the prevalence of taste dysfunction among the control was 0.0%, all had total taste score > 9 (normogeusia).

Figure 2.

Distribution of taste function among the cases (total taste score, ie, the sum of the scores of each of the 4 taste modalities; >9 = normogeusia, <9, >0 = hypogeusia, 0 = ageusia).

There was no significant relationship between age and taste function score among patients with CKD as shown in Table 2 (P = .122). However, significant relationship between age and taste function score was found among the control as shown in Table 3 (P =.0001). The association between age and taste function score among the control was further analyzed using post hoc test, this confirmed that the age-group ≥55 years was responsible for the significant taste score reduction among the control as shown in Table 4.

Table 2.

Age and Taste Function Scores Among Patients With CKD.^a

Age group	Number of patients	Score of taste function		f test	P value
Age group	Number of patients	Mean ± SD	Range	f test	P value
18-34	19	11.2 ± 3.4	2.0-15.0
35-54	56	9.4 ± 3.4	2.0-15.0	2.154	.122
≥55	25	9.5 ± 2.6	4.0-14.0
Total	100	9.8 ± 3.3	2.0-15

Abbreviations: CKD, chronic kidney disease; SD, standard deviation.

^a N = 100.

Table 3.

Age and Taste Function Scores Among Control.^a

Age group	Number of patients	Score of taste function		f test	P value
Age group	Number of patients	Mean ± SD	Range	f test	P value
18-34	31	14.0 ± 1.5	11.0-16.0
35-54	50	13.6 ± 1.3	11.0-16.0	11.532	.0001
≥55	19	12.1 ± 1.4	10.0-16.0
Total	100	13.4 ± 1.5	10.0-16.0

Abbreviation: SD, standard deviation.

^a N = 100.

Table 4.

Dependent Variable: Post Hoc Multiple Comparison of Total Taste Score.

Test statistic	(I) Age group_taste	(J) Age group	Mean difference (I − J)	P value
Tukey HSD	15-34	35-54	0.47226	.309
	15-34	≥55	1.92699	.000
	35-54	15-34	−0.47226	.309
	35-54	≥55	1.45474	.001
	≥55	15-34	−1.92699	.000
	≥55	35-54	−1.45474	.001
Bonferroni	15-34	35-54	0.47226	.433
	15-34	≥55	1.92699	.000
	35-54	15-34	−0.47226	.433
	35-54	≥55	1.45474	.001
	≥55	15-34	−1.92699	.000
	≥55	35-54	−1.45474	.001

Gender of both the patients with CKD and the controls had no significant relationship with taste dysfunction among them (t = 0.751, P = .388; t = 0.304, P = .762, respectively). Oral cavity and oropharyngeal lesions were seen only in 2 patients, 1 has whitish tongue coating lesion, the other has multiple ulcers in the oral cavity. These are too small for any analysis.

Stages of CKD have no significant association with taste dysfunction among patients with CKD. The relationship between stages of CKD and severity of taste dysfunction was analyzed in 2 different forms using 2 staging system of CKD. The first was the conventional eGFR staging system which has 5 stages of the CKD, that is, stages 1 to 5, while the second categorized patients with CKD based on urine albumin creatinine ratio (ACR) into 3 categories, that is, categories 1 to 3. The severity of CKD in both methods has not been proven to have any statistically significant relationship with severity of taste dysfunction, eGFR (f = 2.247, P = .070) and ACR (f = 0.228, P = .652).

The duration of CKD shows significant association with taste dysfunction among the patients with CKD, considering the duration in less than 1 month, 2 to 6 months, 7 months to 1 year, 1 year up to 2 years, and greater than 2 years as shown in Table 6 (f = 3.015, P = .022). The duration of CKD >24 months was significant as a predictor of taste dysfunction among patients with CKD (odds ratio [OR]: 4.889, P = .038) as shown in Table 5.

Table 5.

Duration of CKD and Taste Function Score Among Patients With CKD.

Duration of treatment (months)	Number of patients	Score of taste function		f test	P value
Duration of treatment (months)	Number of patients	Mean ± SD	Range	f test	P value
≤1	25	12.0 ± 3.2	3.0-15.0
2-6	33	9.5 ± 2.9	2.0-14.0	3.015	.022
7-12	10	10.3 ± 2.9	4.0-14.0
13-24	12	8.5 ± 4.4	2.0-15.0
>24	20	9.5 ± 4.0	2.0-15.0
Total	100	9.8 ± 3.3	2.0-15.0

Abbreviations: CKD, chronic kidney disease; SD, standard deviation.

Table 6.

Predictors of Taste Dysfunction in CKD.

Variables	Categories	df	OR	95% CI	P value
Age (years)	18-34	Reference
	35-54	1	3.400	0.703-16.4	.128
	>55	1	4.781	0.893-25.6	.068
BMI	Normal	Reference
	Underweight	1	0.588	0.131-2.638	.488
	Overweight	1	1.333	0.237-7.510	.744
	Obesity	1	0.857	0.124-5.944	.876
Gender	Gender	1	1.842	0.732-4.634	.194
PCV	Normal reference
	Mild	1	2.000	0.409-9.785	.392
	Moderate	1	2.769	0.877-8.746	.083
	Severe	1	1.273	0.403-4.021	.0681
Stage of CKD	Stage 1 (> or =90)	Reference
	Stage 2 (60-89)	1	0.646	0.062-6.719	.714
	Stage 3 (30-59)	1	0.277	0.031-2.450	.248
	Stage 4 (15-29)	1	0.517	0.147-1.816	.303
	Stage 5 (<15)	1	0.570	0.178-1.828	.344
Duration of CKD	≤1	Reference
	2-6	1	0.205	0.659-11.480	.165
	7-12	1	1.833	0.257-13-063	.545
	13-24	1	5.238	0.991-27.686	.051
	>24	1	4.889	1.089-21.950	.038

Abbreviations: BMI, body mass index; CKD, chronic kidney disease; OR, odds ratio; PCV, packed cell volume.

Significant value for is set at 0.05.

Body mass index has no significant relationship with taste dysfunction among patients with CKD, this has been shown with statistical analysis (f = 0.883, P = .453; Table 5). There was no statistically significant difference in the mean value of PCV of patients with CKD with normogeusia and those with hypogeusia (P = .264). The mean PCV of the 2 groups was 28.0 ± 7.4 and 26.2 ± 7.2, respectively. Treatment modalities including observation, medication, dialysis, and renal transplantation show no relationship with taste dysfunction in patients with CKD. (f = 0.243, P = .866).

Discussion

This study has revealed high prevalence of taste dysfunction among patients with CKD and insignificant modality dysfunctions among the control group. The duration of CKD was identified as an important factor that predicts taste dysfunction in patients with CKD while age predicted taste dysfunction among the controls.

In this study, there was no statistically significant association between advancing age and taste disorder among patients with CKD, although the proportion of taste dysfunction among older participants was higher than those in the younger age-group. Generally, it is believed that aging affects taste perception and this has been shown to be true in this study among healthy population similar to previous studies.^10,18,19 Although the taste scores of the controls were within normal range (normogeusia), there was still significant reduction in taste scores among them with aging. However, some studies did not report any association between increasing age and taste dysfunction.⁹

The larger proportion of cases with taste dysfunction was males, although males have slightly larger population than females in this study. However, the difference was not statistically significant. Females have been adjudged to have better taste perception and this has been reported in previous studies.^10,15 Liu et al⁹ and Bhattacharyya and Kepnes¹⁹ could not prove that females have better taste perception. These can be compared to the finding in this study where gender of both the patients with CKD and the control has no significant influence on their taste perception.

Oral cavity and oropharyngeal lesions were not observed to be associated with taste dysfunction in this study, in addition, oral cavity or oropharyngeal lesion was not prevalence among patients with CKD in this study and obviously cannot be considered a predictor of taste dysfunction. Previous studies⁷ also reported lesions in oral cavity and oropharynx to be predictive of severity of CKD but not a predictor of taste dysfunction among patients with CKD.

There was no established relationship between stages of CKD or severity of renal failure and taste dysfunction in this study. The stages of CKD were considered in 2 forms, firstly using the patients eGFR with 5 stages and secondly using the ACR with 3 groups.²⁰ Despite the varieties of CKD stages in this study, the severity of taste dysfunction in all the stages was the same (hypogeusia) and the prevalence among each stages almost directly proportion to their population sizes.

Only few studies have assessed the correlation between stages of CKD and severity of taste dysfunction in adults with CKD. Finding in this study can be compared to a study by Kim et al²¹ that reported no correlation between severity of salty taste dysfunction and stages of CKD. Also, Middleton and Allman-Farinelli⁶ found no correlation between serum urea and creatinine (CKD biochemical parameters) and taste threshold. However, Armstrong et al²² reported positive correlation between stages of CKD (eGFR) and severity of taste dysfunction, but it was found among children with CKD. Similar to findings in this study, Armstrong et al²² also reported incidence of taste dysfunction among children in early stages of CKD.

Body mass index is an indirect measure of nourishment among patients with CKD. Although there was significant difference between the BMI of patients with CKD and healthy controls, majority of the cases still had the normal BMI categories, so also were the cases with the taste dysfunction. The index study observed no association between BMI or nutritional status of patients with CKD and taste dysfunction among both patients with CKD and the control. This can be compared to report by Armstrong et al²² that observed no association between nutritional status (BMI) of children with CKD and taste dysfunction in them. This is in contrast to report from previous other studies^23,24 where taste dysfunction was associated with malnutrition, however the evaluation of nutritional status did not only involve BMI but also other methods including biochemical markers.

The packed cell volume is a measure of hemoglobin concentration of the patients with CKD, this study observed no association between taste dysfunction and PCV. However, the impact of abnormal taste function can affect the intake of the various hemopoietic factors such as iron, folic acid, vitamin C, and vitamin B complex, thus resulting in anemia which is a common finding among patients with CKD. Conversely, patients with severe anemia may have anorexia and altered taste.

Lifestyle modifications, medication, hemodialysis, and renal transplantation were the modalities of treatment for patients with CKD in this study, and they have shown no association with taste dysfunction. No single treatment modality has an association with taste dysfunction among patients with CKD. Unlike this study, Middleton and Allman-Farinelli⁶ reported taste affectation among hemodialysis patients especially the sweet and sour taste while Kusaba et al⁸ reported impaired salt taste among patients with CKD on diuretics. This may be due to uneven distribution of patients with CKD across the different treatment modalities or perhaps due to different method of taste assessment in the comparative studies.

Increasing duration of CKD was found to be a predictor of taste dysfunction among patients with CKD. Larger proportion of patients with CKD duration greater than 24 months had taste dysfunction compared to the proportion of patients with taste dysfunction in the shorter duration of CKD. Statistically, it was proven that duration of CKD greater than 24 months could predict taste dysfunction among patients with CKD by a factor of 5 (OR: 4.887). This can be compared to study by Pechalova et al,²⁵ where the taste dysfunction among patients with CKD was subjectively assessed and it was reported that the duration of CKD does not affect taste perception but the duration of CKD treatment does. Although, some of these studiesemployed subjective assessment of taste and this subjectivity made them unreliable.^9,26

The limitation of this study was the inability to recruit equal proportion of CKD stages because most of patients seen at the hospital were those in advanced stages of CKD. This study used patients with CKD as subjects similar to our earlier study¹³; however, some considerations in inclusion and exclusion criteria, as stated above, resulted in some differences in the subject population used for the 2 studies.

Conclusion

The prevalence of taste dysfunction among patients with CKD in this study was 27.0%. Increasing duration of CKD was identified as a predictor of taste dysfunction among patients with CKD while increasing age was found to predict taste dysfunction among the healthy controls. Incorporation of assessment of taste function and identification and treatments of its predictors in the routine clinical encounter will improve the quality of life and patients’ outcomes.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Akeem. O. Lasisi

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