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 Table of Contents  
ORIGINAL RESEARCH
Year : 2022  |  Volume : 14  |  Issue : 6  |  Page : 603-611

Assessment of serum and gingival crevicular fluid level of fibroblast growth factor 23 in patients having diseased periodontium with and without end-stage renal disease: A cross-sectional analytical study


1 Department of Oral Medicine and Periodontology, Faculty of Dentistry, The British University in Egypt (BUE), El Sherouk City, Egypt
2 Department of Oral Medicine and Periodontology, Faculty of Dentistry, The British University in Egypt (BUE), El Sherouk City, Egypt; Department of Oral Medicine and Periodontology, Faculty of Dentistry, Cairo University, Giza, Egypt

Date of Submission04-Aug-2022
Date of Acceptance15-Oct-2022
Date of Web Publication30-Dec-2022

Correspondence Address:
Dr. Asmaa Abou-Bakr Ras
Department of Oral Medicine and Periodontology, Faculty of Dentistry, The British University in Egypt (BUE), Shorouk City, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jioh.jioh_175_22

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  Abstract 

Aim: The aim of this study was to compare serum and gingival crevicular fluid (GCF) levels of fibroblast growth factor 23 (FGF23) in healthy patients with periodontitis versus gingivitis in end-stage renal disease (ESRD) patients undergoing hemodialysis and periodontitis in patients with ESRD undergoing hemodialysis. Materials and Methods: The study design was a cross-sectional analytical study that included a total of 45 patients with periodontal disease that were divided into three groups with 15 in each group. Group I (n = 15) was systemically healthy having periodontitis, group II (n = 15) had ESRD and gingivitis, and group III (n = 15) had ESRD and periodontitis. The clinical parameters for gingivitis and periodontitis, level of FGF in serum, and GCF were all evaluated in the three groups and the results were compared. Results: FGF23 levels in GCF and serum were statistically significantly higher in group III: ESRD with periodontitis (534 ± 92.7) and (448.2 ± 274.5), respectively, followed by group II: ESRD with gingivitis (150 ± 33.4) and (242.1 ± 31.1), respectively, while were significantly lower in group I: healthy patients with periodontitis (53.7 ± 8.1) and (52.9 ± 6.3), respectively, with a significant difference between the three groups with P < 0.001. Conclusion: Periodontitis patients on hemodialysis showed higher clinical scores (plaque index, bleeding on probing %, pocket depth, and clinical attachment loss) as compared with their counterparts with free medical conditions. The adverse effect of both periodontal and renal disease on clinical presentation and inflammatory markers were strongly evident by the high serum and GCF FGF23 levels with ESRD having the strongest impact.

Keywords: Egypt, Failure, FGF23, Gingivitis, Hemodialysis, Periodontitis, Renal


How to cite this article:
Ghalwash DM, Ras AA, Khalil E, Ahmed E. Assessment of serum and gingival crevicular fluid level of fibroblast growth factor 23 in patients having diseased periodontium with and without end-stage renal disease: A cross-sectional analytical study. J Int Oral Health 2022;14:603-11

How to cite this URL:
Ghalwash DM, Ras AA, Khalil E, Ahmed E. Assessment of serum and gingival crevicular fluid level of fibroblast growth factor 23 in patients having diseased periodontium with and without end-stage renal disease: A cross-sectional analytical study. J Int Oral Health [serial online] 2022 [cited 2023 Feb 1];14:603-11. Available from: https://www.jioh.org/text.asp?2022/14/6/603/366432




  Introduction Top


Chronic renal failure (CRF) is an advanced disease characterized by a gradual damage of nephrons and impairment of renal function.[1],[2]

CRF has usually an irreversible and progressive nature, which leads to end-stage renal disease (ESRD).[3] The prevalence of ESRD is still increasing in most countries.[4],[5] There is no recent information on the prevalence of ESRD in Egypt; however, the prevalence rate of ESRD in the Assiut governorate in upper Egypt was estimated to be 366 people per million (PMP).[6] The appraised annual incidence of ESRD in Egypt is approximately 74 per million and the total prevalence of patients on dialysis is 264 per million. Moreover, the prevalence of dialysis patients in Egypt is still increasing.[7]

ESRD is a state where renal replacement therapy is needed, either by dialysis or renal transplant. If the glomerular filtration rate is approximately 5%–10% and there is a high level of uremia, then this situation requires renal dialysis.[3],[8]

Hemodialysis patients are more liable to infections because of impaired immunity, general debilitation, and the chronic inflammation. In addition, the local inflammatory reactions in the oral cavity, may progress more severely owing to the main ailment and infectious diseases.[9]

The unbalanced spread of oral pathogens disturbs oral health and leads to several dental and mucosal infectious diseases, which can perseverate in a chronic condition affecting in the status of the entire body.[10] There is a strong suggestion that chronic kidney diseases (CKDs) are affected by periodontal health.[11],[12]

Periodontitis is a chronic, progressive inflammatory disease. It ultimately results in the deterioration of the tooth-supporting structures and loss of teeth if untreated.[13] Prevalence of periodontitis is high in patients with early- and end-stage renal disease. The accelerated periodontal tissue damage, gingival recession, and tooth and bone loss is attributed not only to poor oral hygiene and inflammation but also to high urea concentration, and renal osteodystrophy.[14],[15],[16]

Fibroblast growth factor 23 (FGF23) is an endocrine hormone that controls phosphorus metabolism. FGF23 levels progressively increase as kidney function declines, ultimately reaching the highest concentrations in patients with CKD in comparison to any other systemic disease.[17]

Bearing in mind the strong link of FGF23 with inflammation, we anticipated an association linking FGF23 to both periodontal disease and renal disease.[18] Therefore, the aim of this study was to compare serum and gingival crevicular fluid (GCF) levels of FGF23 in healthy patients with periodontitis versus gingivitis in patients with ESRD undergoing hemodialysis and periodontitis in patients with ESRD undergoing hemodialysis.


  Materials and Methods Top


Ethics approval

Approval was obtained from the Research Ethics Committee, Faculty of Dentistry, the British University in Egypt with approval No. 21-012. Patients signed an informed consent after understanding the purpose of the research. Salivary and blood samples will not be used for any other purposes and individual patient’s results will be kept confidential. Individual patient’s personal data and results have been kept confidential by filing system with passwords to protect them being preached. Patient’s names were not shown in the analyzed data; instead, they were encoded by a coding system known by the main investigator only.

Study design

This was a cross-sectional analytical study design.

Sample size calculation

According to a previous study by Ghalwash et al.,[18] serum FGF level was 52.85 ± 6.34 RU/mL in patients with periodontal disease. Isakova et al. (2011) stated that the median value of FGF23 was 145 and that this value is 3 folds higher than that of a population with low prevalence of CKD[19]. A large effect size of approximately 1.79 is expected. A total sample size of 45 (15 in each group) will be sufficient to detect an effect size of approximately 1.79, with a power (1-β error) of 0.95 (95%) using a two-sided hypothesis test, with a significance level (α error) 0.05 for data. G power program version 3.1.9.2 was used for sample size calculation.

Selection and description of participants

45 patients with periodontal disease were recruited and then divided into three groups with 15 in each group. Group I (n = 15) were systemically healthy having periodontitis, group II (n = 15) were had ESRD and gingivitis, group III (n = 15) were had ESRD and periodontitis. Patients with ESRD were recruited from the hemodialysis center at Benha University Hospital. Subjects with periodontal diseases were recruited from the Periodontology Clinic at the Faculty of Dentistry, British University in Egypt.

Group I: Systemically healthy and periodontitis

Inclusion criteria

Individuals over 30 years of age with a minimum of 20 natural teeth.

Stage II periodontitis diagnosed as having 3–4 mm interdental clinical attachment level (CAL), coronal radiographic bone loss 15–33% that is mostly horizontal, no tooth loss because of periodontitis, and pocket depth (PD) ≤ 5 mm.[19]

Exclusion criteria

Systemic diseases such as, cancer, human immune-deficiency virus, uncontrolled diabetes, or any other diseases that may affect the level of biomarkers and the periodontal tissues. Exposure radiation, steroids, or drug allergies. Smoking and lactating females.

Group II: End-stage renal disease and gingivitis

Inclusion criteria

Both genders with age ranging from 30 years to 60 years.

Gingivitis diagnosed as those with no loss of clinical attachment (due to periodontal disease), PD ≤ 3 mm, and the scores of bleeding on probing (BOP) in the whole mouth was more than 10%.[19]

Patients were clinically diagnosed of having ESRD (stage 5) and undergoing hemodialysis. Patients were on hemodialysis for a duration of 3 months.[20] The patients with ESRD were recruited from dialysis center in Benha Governorate, Egypt (Benha Hospital).

Group III: End-stage renal disease and stage II periodontitis

Inclusion criteria

Both genders with age ranging from 30 years to 60 years.

Stage II periodontitis. Patients were diagnosed clinically of having stage 5 ESRD and undergoing hemodialysis. Patients were on hemodialysis for a duration of 3 months.[20]

Exclusion criteria

Patient with a history of a kidney transplant, or any serious disease as malignancy.

Patients who had received periodontal therapy in the past 6 months.

Patients who currently smoke or smoked in the past 6 months.

Vulnerable groups such as pregnant females, prisoners, mentally and physically handicapped individuals,

Patients with early stages of kidney diseases that didn’t require hemodialysis.

Patients that refused to participate in the study.

Periodontal examination

Patients who met the eligibility criteria were assessed clinically for the following clinical parameters using the university of Michigan’s O probe with William’s markings periodontal probe (Nordent Manufacturing, Illinois). The clinical parameters were recorded in the online colored Periodontal chart by the Periodontology Department, University of Bern 2010 (http://www.periodontalchart-online.com/uk). The clinical parameters were recorded as follows:

Plaque %

The percentage of plaque at total sites was automatically measured by the online colored Periodontal chart by the Periodontology Department, University of Bern 2010 (http://www.periodontalchart-online.com/uk).

BOP%

The percentage of BOP sites was automatically measured by the online colored Periodontal chart by the Periodontology Department, University of Bern 2010 (http://www.periodontalchart-online.com/uk).

PD[

21]


To measure PD the probe was introduced parallel to the vertical axis of the tooth to the deepest point of the pocket, recording the distance between the gingival margin and the base of the pocket manually to the closest millimeter marking. Six readings were recorded for each tooth.

Two parameters were recorded concerning PD

Mean PD

The PD was measured for each patient (total PD/number of surfaces).

Mean deepest PD

The deepest pocket measured for each patient was recorded and the mean of deepest pocket was calculated for each group.

Clinical attachment level[

22]


CAL was recorded manually and was measured as the distance between the fixed reference points, that is, base of the pocket to the cemento-enamel junction and for six sites at each tooth.

Two parameters were recorded concerning CAL:

Mean CAL

CAL was measured for each patient (total CAL at all sites/number of surfaces).

Mean highest CAL site

The highest clinical attachment loss measured for each patient was recorded and the mean of the highest CAL was calculated for each group.

Gingival crevicular fluid sample collection

Samples from groups II and III were collected in the morning before the dialysis session and before taking the anticoagulant. Group I samples were collected 2–3 hours after breakfast.[23]

The sample sites were isolated with cotton rolls and gently air-dried. For each individual, the most affected site of the deepest PD was chosen for sampling. GCF samples were attained from disto-buccal or mesio-buccal sites in teeth with the most severe attachment loss. Paper strips were lightly placed for 30 seconds into the pocket till a minimum of resistance was sensed. Any blood containing sample was discarded and sampling was repeated 2 days after. Paper strips of each participant were placed in a single (coded) Eppendorf container, and stored quickly at -80C till assessed.

Fibroblast growth factor 23 detection

All serum samples were drawn before dialysis procedure for groups II and III, and then all the collected samples including group I were stored in a central depository at –80°C until they were dispatched to the laboratory for analysis.

FGF23was detected via a human FGF23 ELISA kit. Using the sandwich ELISA technique for accurate quantitative detection of human FGF 23 in serum and GCF. The plate was coated with FGF 23 antibody. FGF 23 present in the sample was added and binds to antibodies coated on the wells. And then biotinylated Human FGF23 Antibody was added and binds to FGF23 in our samples. Then Streptavidin-HRP was added and bonded to the Biotinylated FGF23 antibody. After incubation unbound Streptavidin-HRP was washed away during step. Substrate solution was added and color developed in proportion to the amount of Human FGF23. The reaction was terminated by addition of acidic stop solution and absorbance that was measured at 450 nm.

A standard curve was constructed by plotting the average optical density for each standard on the vertical (Y)-axis against the concentration on the horizontal (X)-axis and draw a best fit curve through the points on the graph. These calculations were performed with computer-based curve-fitting software and the best fit line can be determined by regression analysis.

Statistical analysis

Data were fed to the computer and analyzed using the IBM SPSS software package, version 20.0. (Armonk, New York: IBM Corp). Categorical data were represented as numbers and percentages. Chi-square test was applied to investigate the association between the categorical variables. For continuous data, they were tested for normality by the Shapiro–Wilk test. Quantitative data were expressed as range (minimum and maximum), mean, standard deviation and median analysis of variance (ANOVA) was used for comparing the three studied groups for normally distributed quantitative variables and followed by post hoc test (Tukey) for pairwise comparison. On the contrary, Kruskal–Wallis test was used to compare different groups for not normally distributed quantitative variables and followed by post hoc test (Dunn’s for multiple comparisons test) for pairwise comparison. Significance of the obtained results was judged at the 5% level.


  Results Top


A flow diagram was conducted as shown in [Figure 1].
Figure 1: Flow diagram for all participants

Click here to view


Our study was conducted on a total of 45 subjects divided into three groups; group I: healthy with stage II periodontitis included 15 patients (5 males and 10 females) with mean age (46.7 ± 8.7), group II: Gingivitis patients with ESRD on hemodialysis included 15 patients (11 males and 4 females) with mean age (33.3 ± 4.9), group III: stage II periodontitis patients with ESRD on hemodialysis included 15 patients (7 males and 8 females) with mean age (52.9 ± 8.1).

Regarding descriptive data, group II patients were significantly younger in age compared with the other two groups, with no difference between the three studied groups regarding sex distribution.

[Table 1] presents the comparison between the three studied groups regarding clinical parameters (plaque index [PI], BOP%, PD, and CAL).
Table 1: Comparison between the studied groups according to clinical parameters

Click here to view


PI was statistically significantly the lowest in group I followed by group I, while PI was statistically significantly higher in group III compared with both other groups.

All groups showed high score of BOP%; however, group III showed statistically significant higher BOP% than do group II. While group I showed insignificant difference compared with both other groups.

Regarding PD and CAL, they were statistically significantly higher in group III compared with group II.

[Figure 2] shows a comparison in serum and GCF level of the studied groups. GCF level of FGF23 was statistically significantly higher in group III: renal patients with periodontitis (534 ± 92.7) followed by group II: renal patients with gingivitis (150 ± 33.4), and significantly lower in group I: healthy patients with periodontitis (53.7 ± 8.1) with significant difference between the three groups with P < 0.001.
Figure 2: Comparison between the three studied groups according to GCF and serum FGF23

Click here to view


The same result was found for serum FGF23 level, where it was statistically significantly higher in renal patients with periodontitis (448.2 ± 274.5) followed by renal patients with gingivitis (242.1 ± 31.1) and significantly lower in healthy patients with periodontitis (52.9 ± 6.3) with significant difference between the three groups with P < 0.001.


  Discussion Top


Periodontal disease is linked to some systemic diseases, such as atherosclerosis, diabetes, stroke, coronary heart disease and kidney disease.[24],[25],[26] Recently, several epidemiological and clinical data showed a strong correlation between Periodontitis and CKD. An increased frequency of some oral bacteria that are closely related with periodontal disease as Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola was reported in patients with CKD.[27]

The direct or indirect effects of inflammatory mediators from infected or inflamed periodontal tissues and circulating bacteria on the body contribute to systemic inflammation in general,[28] and to the progression of CKD in particular.[29] Periodontal pathogens cause the release of cytokines by immune cells, thereby causing renal damage. Interleukin-6 (IL-6) further upsurges renal inflammation by attracting more neutrophils into the kidneys aggravating renal damage.[30] IL-8 is generally associated with neutrophil accumulation at sites of acute and chronic inflammation and is also involved in renal damage and.[31],[32] Tumor necrosis factor-α (TNF-α) is involved in the progression of renal failure through its pro-inflammatory and cytotoxic effects.[32],[33]

In addition, IL-1 is implicated in the pathogenesis of periodontitis and renal disease.[34] In patients with CKD, plasma concentrations of TNF-α and IL-6 seemed to be more accurate markers of oral inflammation.[35] There was also a positive correlation between clinical parameters and IL-8 and TNF-α levels in GCF of patients with CKD on hemodialysis, and their GCF levels were significantly higher than those in the healthy patients.[32],[36]

Moreover, the levels of several acute phase proteins in GCF, such as C-reactive protein, PTX, haptoglobin, and fibrin, are affected by the local inflammation in periodontitis. This increase in their concentration endorses the production of proteolytic enzymes in the whole body, resulting in increase in endothelial cell permeability, renal endothelial damage, glomerular filtration dysfunction, and ultimately aggravating renal disease, which is considered to be a significant link between systemic inflammation and periodontitis.

FGF23 is a bone derived hormone that is a powerful regulator of bone mineral metabolism and augmented FGF23 release causes hypophosphatemia, reduced levels of vitamin D and PTH in inflammatory systemic diseases in which FGF23 is reported to be markedly enhanced.[37]

Moreover, the circulating levels of FGF23 in patients with CKD is positively correlated IL-6, TNF-α, CRP, fibrinogen, and the severity of inflammation in these patients[32],[38] Furthermore, FGF23 directly stimulates hepatic secretion of pro-inflammatory cytokines, indicating a strong association between FGF23 and chronic inflammation.[39]

FGF23 is also reported to be produced by pro-inflammatory macrophages and specifically upregulated by interferon gamma (IFN-γ) and lipopolysaccharide, indicating that FGF23 may augment the innate immune reaction to tissue injury.[39]

This study was conducted on a total of 45 patients to compare the clinical parameters and both serum and GCF level of FGF23 in in healthy patients with periodontitis versus gingivitis and periodontitis in patients with ESRD undergoing hemodialysis.

Some prior studies investigated the role of FGF23 in renal disease but to the best of our knowledge no previous study explored its relation with periodontitis and renal disease.

In our study, plaque score was found to be significantly higher in periodontitis patients on hemodialysis compared with systemically healthy periodontitis patients. This goes in line with Al Wahadni and Al Omari[40] in their study to examine the levels of periodontal disease in individuals on renal dialysis in a Jordanian population. They concluded that patients on hemodialysis might neglect their oral hygiene due to the long time they spend in the dialysis center. They further found an enhanced rate of calculus accumulation in these patients, which was accredited to raised levels of salivary urea. Our results are in agreement with the study conducted by Davidovich et al.[41] who found that the plaque scores were higher in dialysis and predialysis group than systemically healthy group. Gupta et al.[42] also found that the mean PI of dialysis patients significantly higher than controls.

Similarly, Abou-Bakr et al.[43] reported high plaque score among periodontitis patients on hemodialysis in an Egyptian population sample. Their explanation was that these patients likely might be depressed due to their severe systemic ailment and poor social level. Thus, they ignore oral health care and display poor compliance to dental treatments.

Group III (periodontitis patients on hemodialysis) showed statistically significant higher BOP % than do group II (gingivitis patients on hemodialysis). While group I showed insignificant difference compared with both other groups. It goes without saying that high plaque score is usually associated with higher inflammatory response and hence higher bleeding tendency.

This was in accordance with Bots et al.[44] who found that in addition to high plaque score in patients on hemodialysis specially patients with periodontitis compared with those with gingivitis, some medications of the patients with CKD, such as anticoagulant therapy could lead to increased BOP.

Sedý et al.,[45] stated that poor oral hygiene due to plaque accumulation and decreased salivary flow rate that is evident in patients with CRF is most probably related to sustained inflammation of periodontal tissues in patients with CKD and hence increased bleeding tendency.

Regarding PD and CAL, they were statistically significantly higher in group III compared with group I and group II. This reflects the increased severity of periodontitis in patients on hemodialysis compared with those with healthy medical condition.

This was in accordance with Gupta et al.,[42] whose results showed that the periodontal condition of hemodialysis patients was significantly higher in mean scores of OHI-S, PI, and clinical attachment loss than systemically healthy subjects. This can be attributed to the cumulative effect of poor oral hygiene over the years leading to increased periodontal attachment loss in these patients.

Similarly, Sedý et al.,[45] found that most of patients on hemodialysis usually suffer from several medical conditions such as Diabetes Mellitus, hypertension and hyperparathyroidism, this usually leads to a frail immune response which could explain the augmented incidence and severity of periodontitis in patients with CKD. In addition to the immune vulnerability that accompanies hemodialysis, greater plaque and dental calculus accumulation, high salivary pH levels, and salivary urea concentration have been suggested to be linked to the increased severity of periodontal diseases.[46],[47]

Our results were not in line with the study by Rahman et al.[48] where no significant difference was perceived between hemodialysis group and corresponding healthy controls. Comparable results were also observed in a study by Marakoglu et al.[49] who claimed that host factors, such as gene polymorphism, systemic diseases, or drugs can modify the host response to periodontal infection or altering the susceptibility to infection by periodontal pathogens.

GCF level of FGF23 was statistically significantly higher in group III: renal patients with periodontitis followed by group II: renal patients with gingivitis, and significantly lower in group I: healthy patients with periodontitis with significant difference between the three groups. The same result was found for serum FGF23 level, where it was statistically significantly higher in renal patients with periodontitis followed by renal patients with gingivitis and significantly lower in healthy patients with periodontitis with significant difference between the three groups. This is in accordance with previous studies that reported markedly enhanced FGF23 level in inflammatory conditions.[37]

To the best of our knowledge, this is the first study to assess the level of FGF23 level in periodontal conditions associated with renal diseases, so comparison with other studies isn’t possible.

Our observation is that both serum and GCF level of FGF23 were significantly higher in hemodialysis patients with periodontitis, patients with gingivitis on hemodialysis also showed a significantly higher level both in GCF and serum compared with those healthy patients with periodontitis. This shed light on the pronounced role of renal condition on local and systemic inflammation rather than the role of the periodontal inflammatory condition.

Currently, FGF23 has been shown to directly modulate the host defense to bacterial infections. It also impairs the recruitment and activation of neutrophils. In addition, while FGF23 levels decrease leukocyte functions, inflammatory conditions may also-in a reverse fashion-contribute to raised FGF23 plasma levels. Suggestive of the existence of a “feed-forward” loop whereby in systemic inflammation and local inflammatory conditions as periodontal disease, so the effects of inflammation and FGF23 intensify each other, leading to poorer outcomes.[50],[51] This explains the significant rise in both GCF and serum levels in periodontitis patients with renal disease on hemodialysis.

According to previous research periodontal treatment reduces the risk of renal failure, suggesting that closer cooperation between dentists and physicians may facilitate the management of patients with CKD.[52] Patients with severe CKD commonly neglect their oral hygiene, even when they have periodontitis. Even though scientific data confirm an increased prevalence of periodontitis in patients with CKD, self-awareness of periodontitis in those patients is poor.[53]

Conclusion

Periodontitis patients on hemodialysis showed higher clinical scores (PI, BOP%, PD, and CAL) as compared with their counterparts with free medical condition. The adverse effect of both periodontal and renal disease on clinical presentation and inflammatory markers were strongly evident by the high-serum and GCF FGF23 level with renal disease having the strongest impact.

Acknowledgement

We would like to acknowledge the contributions of the nephrologists in hemodialysis centers for helping us throughout the study.

Financial support and sponsorship

This research was self-funded.

Conflicts of interest

There are no conflicts of interest.

Author contributions

DMG: Conceptualization, supervision, writing original draft, and writing-review and editing. AA-B: Resources, writing original draft, data collection, data interpretation, and methodology. EK: Investigation and visualization. EA: Supervision, visualization, and writing-review & editing.

Ethical policy and institutional review board statement

Approval was obtained from the Research Ethics Committee, Faculty of Dentistry, the British University in Egypt with approval No. 21-012. The study was conducted in accordance with the Declaration of Helsinki on Ethical Principles for Medical Research Involving Human Subjects. Salivary and blood samples will not be used for any other purposes and individual patient’s results will be kept confidential.

Patient declaration of consent

Not applicable.

Data availability statement

The data that support the findings of this study are available from private hemodialysis centers in Egypt and restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the corresponding author upon reasonable request.



 
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