Original Article
Combined impact of COVID-19 and renal failure on taste perception in a sample of the Egyptian population
2024 Volume 66 Issue 4 Pages 241-246
Details
2024 Volume 66 Issue 4 Pages 241-246
Purpose: The present study aims to investigate the prevalence and severity of taste impairment among post-coronavirus disease 2019 (COVID-19) hemodialysis patients in a sample of the Egyptian population.
Methods: This study was conducted on 272 post-COVID-19 subjects, of whom 136 were hemodialysis patients and 136 were healthy controls. History taking, clinical examination, and assessment of altered taste score, tongue coating index, salivary flow rate, and salivary pH were performed.
Results: The present study revealed a high prevalence of impaired taste function in post-COVID-19 hemodialysis patients with 72.06% affected in varying degrees; mild (25%), moderate (3.68%), severe (30.15%), and overwhelming taste impairment (13.24%). However, only 12.5% of the control group reported just a mild degree of taste impairment.
Conclusion: The current study has shown the high prevalence and severity of taste impairment in post-COVID-19 end-stage renal disease (ESRD) patients on hemodialysis (72.06%), which indicates the combined deteriorating effect of both COVID-19 and renal failure on taste function emphasizing the importance of prompt identification and management of COVID-19 associated taste impairment to improve the quality of life in hemodialysis patients.
Coronavirus disease 2019 (COVID-19) causes a wide variety of oral symptoms including, hyposalivation, aphthous‐like ulcers, petechiae, smell dysfunction, and taste impairment [1]. Taste perception depends on the stimulation of taste receptors distributed in the oral cavity perceiving sour, sweet, salty, and bitter tastes [2]. Normal taste perception is crucial to enjoy eating thus alteration in taste function may lead to food aversion, changes in food choices, and consumption patterns, causing weight gain or weight loss, and further malnourishment issues [3].
Diabetes, cardiovascular disease, old age, obesity, chronic obstructive pulmonary disease, and end-stage renal disease (ESRD) are among the high-risk factors for COVID-19 complications [4,5]. ESRD affects around 11-13% of the global populace [6]. The prevalence of COVID-19 in patients with ESRD is 20% more than in the general population and there is a great difference between COVID-19 infection in ESRD patients and the general population in terms of clinical outcomes, severity, and mortality rate [7].
Progression of ESRD often requires treatment by hemodialysis, which is the most common type of ESRD therapy. COVID-19 poses a special challenge to patients undergoing hemodialysis. However, the consequences of COVID-19 infection in patients on hemodialysis remain poorly investigated [8]. Patients undergoing hemodialysis are subjected to restricted food intake to improve acid-base balance, serum electrolytes, and blood pressure, thus increasing the effectiveness of hemodialysis. Nevertheless, poor adherence to beneficial prescribed diets has been reported in 25-86% of ESRD patients on hemodialysis [9]. This can predispose hemodialysis patients to a greater risk of malnourishment and therefore, worse patient outcomes, quality of life, and survival rates [10].
A possible justification for this poor dietary adherence is impaired taste function, which affects 43.8% of ESRD patients on hemodialysis [11]. Impaired taste acuity, metallic taste, and reduced detection of bitter or salty taste are among the reported taste disturbances [10,12]. Salt is necessary for preserving homeostasis. Nonetheless, excess salt intake is correlated with several harmful effects including stroke, cardiovascular disorders, and hypertension [13]. Excess salt consumption accelerates kidney disease progression in chronic kidney disease (CKD) and ESRD patients as they are sensitive to salt [14]. Thus, dietary salt limitation is advised to avoid deteriorating renal functions in those patients [15]. Nevertheless, adherence to limitation of salt consumption is not commonly attained despite. This might be attributed to the decreased tastiness of low-salt diets caused by defective taste function leading to an increase in dietary salt intake [12].
Taste disorder including salty taste dysfunction commonly occurs in CKD and ESRD patients [16]. Accumulation of uremic toxins, fluid imbalances, ion imbalances, metabolic disorders, and zinc deficiency are some postulated factors associated with taste dysfunction in CKD and ESRD patients [10,17,18].
Additionally, chemosensory functions and taste dynamics in CKD and ESRD patients could also be affected by changes in salivary composition, where levels of several chemosensory active stimuli present in blood and saliva such as potassium, sodium, calcium, and urea are altered [19,20]. This may be enhanced by particular taste genetics making them more sensitive to the increased levels of urea in saliva often encountered in ESRD patients [2]. Moreover, salivary levels correlated with serum levels of these chemosensory active stimuli, and taste function were reported to improve following hemodialysis sessions [21].
Defective taste function has been identified as a prominent sign of COVID-19 infection. It affects the ability of CKD patients on hemodialysis to enjoy food leading to malnutrition and also has an enormous impact on outcomes, quality of life, and mortality rate [22]. Taste alterations are a common but often under-recognized complaint known to affect people with ESRD [23]. Yet, insignificant attention is paid to the identification of defective taste function and its predicting risk factors among renal disease patients especially those on hemodialysis [3]. Accordingly, this study aims to explore the prevalence and severity of taste impairment among post-COVID-19 hemodialysis patients in a sample of the Egyptian population.
Based on research published regarding the incidence of taste alterations and associated symptoms in ESRD patients in Lafayette USA [24], by fixing alpha at 0.05 and beta at 0.2, the expected odds ratio was 0.1. The minimal sample size is 136 hemodialysis patients and 136 healthy controls.
Study design and patient selectionThe present study is a single-centered cross-sectional observational study. Renal patients were selected from the hemodialysis center in Benha University Hospital, Benha Governorate, Egypt, over a period of 6 months. Healthy individuals were selected from the outpatient clinic of the Oral Medicine department at The British University in Egypt. Renal function tests were performed on control patients to ensure they did not have renal problems.
Inclusion criteriaFor both genders with an age range above 18 years, cases must be clinically diagnosed as having end-stage renal disease (for the test group), patients were on renal hemodialysis (for the test group), and a history of COVID-19 infection of moderate severity within the last 6 months for both groups.
Exclusion criteriaIndividuals with known taste dysfunction from childhood, kidney transplantation, patients who refused to participate in the study, those with a previous history of smoking, or current smokers were excluded.
The research protocol was reviewed by The British University in Egypt Research Ethics Committee with approval number (23-066). The research protocol was fully explained to the study subjects, and they signed an informed consent form.
Participants who met the eligibility criteria as in (Fig. 1) were subjected to the following procedures:
Personal history, demographic data (age and gender), medical history, history of duration of renal hemodialysis, hemoglobin level, and biochemical parameters (serum urea, creatinine levels) were obtained from the most recent blood analysis. Subjective clinical symptoms such as changes in the sense of taste and dry mouth are recorded through the use of patient questionnaires, and uremic breath is recorded at 10 cm from the patient’s mouth.
Tongue coating indexThe tongue coating index (TCI) [25] was used to evaluate tongue-coating status as follows. Score 0: tongue coating not visible, score 1: tongue coating thin, papillae of tongue visible, score 2: tongue coating very thick, papillae of tongue not visible.
Clinical examinationClinical examination was done using 2 plain mouth mirrors, explorer under artificial light with the patients according to inclusion criteria. Oral mucosa was examined carefully for any abnormalities. Proper oral hygiene improvement by scaling cleaning and giving oral hygiene instructions was done for all cases and controls. Patients were instructed to refrain from eating or smoking cigarettes for an hour before testing.
Salivary flow rateSalivary samples were collected on the day of dialysis between 8:00 and 11:00 AM to reduce the effects of the diurnal variation on the composition of saliva. Sample collection is carried out before meals or at least 2 h afterward. Saliva was collected using the spitting method [26]. Patients were asked to sit in an upright position with their heads slightly bent forward. They were given graduated plastic cups and asked to collect saliva in their mouths for about 5 min and spit into the cups. The collection was timed, so that flow rate (mL/5 min) could be measured and evaluated as <3.5 mL- very low, 3.5-5.0 mL-low, >5.0 mL-normal [27].
Salivary pHSalivary pH was assessed immediately after salivary collection using the narrow-range pH strip system (universal indicator paper). The saliva was pipetted onto a pH test strip for 10 s and its color change reflected the pH of saliva ranging from (1-14).
Taste alterationAll subjects were requested to rate the acuteness of any taste change they suffered in the previous week on the 5-point Likert scale as per the integrated patient outcome scale (iPOS)-renal, from none (1), mild (2), moderate (3), severe (4) to overwhelming (5). In addition, subjects were requested to explain the taste dysfunction they suffered using free text [24].
Statistical analysisCategorical data were presented as percentage and frequency values and were analyzed using the chi-square test. Numerical data were represented as mean and standard deviation values. Shapiro-Wilk’s test was used to test for normality. Age data were normally distributed and were analyzed using an independent t-test. Other numerical data were non-parametric and were analyzed using the Mann-Whitney U test. Correlations were analyzed using Spearman’s rank-order correlation coefficient. The significance level was set at P < 0.05 within all tests. Statistical analysis was performed with R statistical analysis software version 4.3.2 for Windows (R Core Team, R Foundation for Statistical Computing, Vienna, Austria).
Results showed that there was no significant difference between the test and control groups concerning gender distribution (P = 0.138). In addition, they showed a substantial difference between both groups regarding, altered taste score and tongue coating score, with the ESRD group having significantly higher values than the control group (P < 0.001). Finally, they showed a significantly higher percentage of ESRD group cases being affected by xerostomia, oral ulceration, and altered taste (P < 0.05) as in (Table 1).
| Parameter | ESRD | Control | Test statistic | P-value | |
|---|---|---|---|---|---|
| Gender (n [%]) | male | 87 (63.97%) | 75 (55.15%) | 2.20 | 0.138 |
| female | 49 (36.03%) | 61 (44.85%) | |||
| Age (years) (mean ± SD) | 52.75±18.25 | 49.39±19.49 | 1.47 | 0.143 | |
| Xerostomia (n [%]) | no | 42 (30.88%) | 107 (78.68%) | 62.71 | <0.001* |
| yes | 94 (69.12%) | 29 (21.32%) | |||
| Oral ulceration (n [%]) | no | 115 (84.56%) | 130 (95.59%) | 9.25 | 0.002* |
| yes | 21 (15.44%) | 6 (4.41%) | |||
| Altered taste (n [%]) | none | 38 (27.94%) | 119 (87.50%) | 111.46 | <0.001* |
| mild | 34 (25.00%) | 17 (12.50%) | |||
| moderate | 5 (3.68%) | 0 (0.00%) | |||
| severe | 41 (30.15%) | 0 (0.00%) | |||
| overwhelming | 18 (13.24%) | 0 (0.00%) | |||
| Altered taste (n [%]) | none | 38 (27.94%) | 119 (87.50%) | 98.84 | <0.001* |
| affected | 98 (72.06%) | 17 (12.50%) | |||
| Altered taste score (mean ± SD) | 2.76±1.47 | 0.12±0.33 | 18173.00 | <0.001* | |
| Tongue coating score (mean ± SD) | 1.27±0.76 | 0.61±0.72 | 13347.00 | <0.001* | |
*Significant (P < 0.05)
Associations with altered taste score
Except for pallor occurrence, all associations were statistically significant (P < 0.05) as in (Table 2).
| Parameter | Taste score | Test statistic | P-value | |||||
|---|---|---|---|---|---|---|---|---|
| 1 | 2 | 3 | 4 | 5 | ||||
| Xerostomia (n [%]) |
no | 110 (70.06%) |
21 (41.18%) |
1 (20.00%) |
13 (31.71%) |
4 (22.22%) |
37.57 | <0.001* |
| yes | 47 (29.94%) |
30 (58.82%) |
4 (80.00%) |
28 (68.29%) |
14 (77.78%) |
|||
| Uremic breath (n [%]) |
no | 38 (100.00%) |
34 (100.00%) |
5 (100.00%) |
2 (4.88%) |
1 (5.56%) |
124.25 | <0.001* |
| yes | 0 (0.00%) |
0 (0.00%) |
0 (0.00%) |
39 (95.12%) |
17 (94.44%) |
|||
| Pallor (n [%]) |
no | 13 (34.21%) |
14 (41.18%) |
1 (20.00%) |
7 (17.07%) |
2 (11.11%) |
8.90 | 0.064 |
| yes | 25 (65.79%) |
20 (58.82%) |
4 (80.00%) |
34 (82.93%) |
16 (88.89%) |
|||
| Dialysis duration (n [%]) |
<13 m | 38 (100.00%) |
28 (82.35%) |
2 (40.00%) |
0 (0.00%) |
0 (0.00%) |
111.44 | <0.001* |
| ≥13 m | 0 (0.00%) |
6 (17.65%) |
3 (60.00%) |
41 (100.00%) |
18 (100.00%) |
|||
| Oral ulceration (n [%]) |
no | 157 (100.00%) |
45 (88.24%) |
5 (100.00%) |
32 (78.05%) |
6 (33.33%) |
88.49 | <0.001* |
| yes | 0 (0.00%) |
6 (11.76%) |
0 (0.00%) |
9 (21.95%) |
12 (66.67%) |
|||
*Significant (P < 0.05)
Correlations with altered taste score
There was a strong positive correlation between altered taste severity and tongue coating score which was statistically significant (P < 0.001). Other correlations were not statistically significant (P > 0.05) as in (Table 3, Fig. 2).
| Parameter | Correlation coefficient (95% CI) | Test statistic | P-value |
|---|---|---|---|
| Tongue coating score | 0.905 (0.869:0.931) | 39805.43 | <0.001* |
| Salivary pH | 0.103 (-0.067:0.267) | 376072.90 | 0.233 |
| Salivary flow rate | -0.042 (-0.209:0.127) | 436974.84 | 0.624 |
| Blood urea | -0.133 (-0.294:0.037) | 474790.53 | 0.124 |
| Serum creatinine | -0.062 (-0.228:0.107) | 445262.65 | 0.472 |
| Hemoglobin | -0.136 (-0.297:0.034) | 476048.49 | 0.116 |
*Significant (P < 0.05)
Cases with xerostomia had significantly lower salivary flow rates, significantly higher tongue coating scores, and significantly higher incidences of ulceration in comparison to free cases (P < 0.001) as shown in (Table 4).
| Parameter | Xerostomia | Test statistic | P-value | ||
|---|---|---|---|---|---|
| no | yes | ||||
| Uremic breath (n [%]) | no | 25 (59.52%) | 55 (58.51%) | 0.01 | 0.912 |
| yes | 17 (40.48%) | 39 (41.49%) | |||
| Pallor (n [%]) | no | 32 (76.19%) | 67 (71.28%) | 0.35 | 0.552 |
| yes | 10 (23.81%) | 27 (28.72%) | |||
| Dialysis duration (n [%]) | <13 m | 21 (50.00%) | 47 (50.00%) | 0.00 | 1 |
| ≥13 m | 21 (50.00%) | 47 (50.00%) | |||
| Oral ulceration (n [%]) | no | 140 (93.96%) | 105 (85.37%) | 5.57 | 0.018* |
| yes | 9 (6.04%) | 18 (14.63%) | |||
| Salivary pH (mean ± SD) | 7.05±0.85 | 6.96±0.77 | 2074.00 | 0.615 | |
| Blood urea (mean ± SD) | 145.57±40.50 | 137.52±32.40 | 2191.50 | 0.307 | |
| Salivary flow rate (mean ± SD) | 2.16±1.03 | 1.37±1.16 | 2868.00 | <0.001* | |
| Hemoglobin (mean ± SD) | 8.89±1.72 | 8.97±1.67 | 2061.50 | 0.680 | |
| Serum creatinine (mean ± SD) | 6.08±1.70 | 5.52±1.41 | 2332.50 | 0.092 | |
| Tongue coating score (mean ± SD) | 0.68±0.79 | 1.25±0.73 | 12676.50 | <0.001* | |
*Significant (P < 0.05)
Defective taste function may be one of the factors predisposing hemodialysis patients to poor nutritional status [28]. Taste dysfunction is one of the most frequent manifestations of COVID-19 infection [1]. It could also be caused by metabolic disturbances, dry mouth, medications, reduced number of taste buds, and change in salivary composition, mucosal inflammation, tongue coating, or oral ulceration. These factors are frequently found in CKD patients [29]. It can also be caused by low levels of zinc and high levels of urea in CKD patients as uremia prevents the regeneration of taste buds and adversely affects the nerves involved in taste perception. [12,30].
Prompt diagnosis of taste impairment and the underlying risk factors during the evaluation of CKD and ESRD is of great importance as this enhances the nutritional status, hinders the progression of renal disease, and improves the survival rate, and quality of life for those patients [3]. Pre-existing comorbidities such as ESRD have been described to ally with the presence and severity of COVID-19 manifestations. Moreover, pre-existing comorbidities could relate to COVID-19 because the immune and metabolic systems are already compromised owing to these comorbidities [4].
CKD has become a major public health burden in Egypt, as it has increased in recent years by 36% which is comparable to the global increase of CKD burden, and it represents the fifth leading cause of death in Egypt in the last two decades Approximately 54,000 patients (0.65 patients per 1,000 people) are undergoing dialysis [31]. Few studies have addressed the oral complications in post-COVID-19 patients with ESRD on regular hemodialysis and to the best of the authors’ knowledge, the current investigation is the first to assess the prevalence and severity of taste impairment among post-COVID-19 patients on hemodialysis in a sample of Egyptian population.
Results of the present study revealed a high prevalence of impaired taste function in post-COVID-19 ESRD patients undergoing hemodialysis as 72.06% were affected in varying degrees; mild (25%), moderate (3.68%), severe (30.15%), and overwhelming taste impairment (13.24%). However, only 12.5% of the control group reported just a mild degree of taste impairment. Additionally, ESRD patients had significantly higher altered taste scores than the control group. The reported prevalence of altered taste in this study is definitely higher than that reported in previous research conducted on CKD patients, as one study stated that taste dysfunction affected 38% of CKD patients [24], 43.8% prevalence was reported in other studies conducted in hemodialysis [11], and a prevalence of 56% was recounted in stage 4-5 CKD [2]. This higher prevalence and severity of altered taste is obviously caused by the exposure of patients in the present investigation to COVID-19 infection during the last 6 months, further predisposing renal patients to taste impairment.
Furthermore, a significantly higher percentage of hemodialysis patients were affected by xerostomia, oral ulceration, and tongue coating score values than the control group. No significant difference was found in gender distribution, and age of the cases in both groups. The presence of altered taste was significantly associated with xerostomia, oral ulcerations, and tongue coating score (P < 0.001).
Xerostomia was reported by 69.12% of hemodialysis patients, which is significantly higher than the control group (21.32%). This agrees with other studies of dialysis patients [32,33]. Increased xerostomia in hemodialysis patients may be caused by hyposalivation due to COVID-19 infection, in addition to limited water intake, medications, salivary gland changes, and mouth breathing caused by impaired lung perfusion [34,35].
In addition, cases with xerostomia, uremic breath, and oral ulcerations were associated with a significantly higher altered taste score (P < 0.05). Uremic breath observed in hemodialysis patients results from the high urea concentration in the saliva of these patients, which will be converted into ammonia. This uremic fetor is a contributing factor to altered taste perception and might even cause an unpleasant taste [32], and this is in line with the results of this study.
Moreover, altered taste score was significantly associated with the duration of hemodialysis as most patients reporting severe and overwhelming taste alterations were those with longer duration of hemodialysis (more than 13 months), and lower taste scores were reported by patients with shorter hemodialysis duration (less than 13 months). This is in line with recent research reporting a significant association of the duration of CKD with taste dysfunction and that CKD duration of more than 2 years is considered a significant forecaster of taste impairment among those patients [3]. Moreover, another study reported that taste perception is more affected by the duration of CKD treatment than by the duration of CKD itself [36]. In the same context, a significant association of mucosal pallor, uremic breath, and unpleasant taste with hemodialysis duration was reported indicating the importance of oral health maintenance in this patient group [32].
In the current study, oral ulceration was noticed in 15.4% of hemodialysis patients which was significantly higher than in controls where oral ulcers affected only 4.4%. This higher prevalence of ulcers in ESRD was significantly associated with both the presence and the severity of altered taste function. These oral ulcers could be caused by the existing xerostomia, enzymatic degradation of urea in the oral cavity, and anemia which is very common in ESRD patients, possibly due to folic acid or erythropoietin deficiencies, inhibition of erythropoiesis, short life span of erythrocyte, increased hemolysis resulting from hemodialysis [37].
No significant correlation was found between the severity of altered taste and salivary pH, salivary flow rate, blood urea, serum creatinine, or hemoglobin. In the same way, a previous study did not find any correlation between creatinine, serum urea, and altered taste severity [38]. Whereas another study reported a correlation between the severity of altered taste and stages of CKD [39]. However, the present results revealed a strong positive statistically significant correlation between the severity of altered taste and tongue coating score. This was in accordance with recent research conducted to discover the effect of tongue coating on taste sensitivity in the elderly which reported a statistically significant correlation between tongue coating index and taste sensitivity level [40].
Among the limitations of this study, smell dysfunction was not specifically assessed. This is because the present study mainly focused on taste dysfunction, a prominent sign of COVID-19 infection, and one of the contributing factors for poor nutrition in hemodialysis patients with an enormous impact on the patient’s outcomes and quality of life. Additionally, a number of factors predisposing to altered taste are associated with hemodialysis such as uremic breath, oral ulcerations, and xerostomia which may be also caused by the hyposalivation effects of COVID-19 infection. Thus, the current study focused on the assessment of the prevalence and severity of taste dysfunction in this patient category.
CI: confidence interval; CKD: chronic kidney disease; COVID-19: coronavirus disease 2019; ESRD: end-stage renal disease; SD: standard deviation; TCI: tongue coating index
Approval was obtained from the Research Ethics Committee, Faculty of Dentistry, The British University in Egypt with approval number (23-066). The procedures were fully explained to the patients, and they signed an informed consent form to share their clinical data for scientific purposes. Individual patients’ data and results have been kept confidential by a filing system with passwords to protect them from being disclosed. Patient’s names were not shown in the analyzed data; instead, they were encoded by a coding system known by the main investigator only.
The authors have no conflicts of interest to declare.
This research is self-funded.
DG: conceptualization, investigation, visualization, writing - review and editing; AA: data curation, investigation, writing - original draft; EK: conceptualization, supervision
DG*: Dalia.Ghalwash@bue.edu.eg, https://orcid.org/0000-0003-2541-7243
AA: Asmaa.aboubakr91@gmail.com, https://orcid.org/ 0000-0001-5069-8257
EK: Eman.khalil@bue.edu.eg, NA
The authors acknowledge the contributions of the internal medicine staff in the hemodialysis center at Benha University Hospital for their assistance throughout the study.
All data generated or analyzed during this study are included in this published article.
