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J Korean Acad Fundam Nurs > Volume 30(2); 2023 > Article
Kim: Factors Affecting Hyperphosphatemia in Patients with Chronic Renal Failure Undergoing Hemodialysis

Abstract

Purpose

The purpose of this study was to investigate the status of hyperphosphatemia in patients with chronic renal failure (CRF) and to examine the effects of dialysis-related characteristics, nutritional status, self-care, stress, and social support on hyperphosphatemia.

Methods

This descriptive research study was designed to identify factors influencing the development of hyperphosphatemia in patients diagnosed with CRF. A convenience sample of 150 patients receiving hemodialysis was selected. Data were collected directly by the researchers from January to March 2022.

Results

The regression model showed statistically significant results (x2=137.24, p<.001). Regression analysis demonstrated that body mass index (BMI) and blood urea nitrogen (BUN) were predictive factors. The risk of hyperphosphatemia was 3.09 times (95% CI, 1.15~8.25) higher for a BMI ≥25 kg/m2 than for a BMI 18.5-22.9 kg/m2. The risk of hyperphosphatemia increased by 1.04 times (95% CI, 1.01~1.07) as the BUN levels increased.

Conclusion

BMI and BUN were identified as major predictive factors for hyperphosphatemia, which confirms the importance of nutritional intake in dialysis patients. To prevent hyperphosphatemia in hemodialysis patients, regular monitoring for dietary and nutritional status and nutrition education based on the results of monitoring should be carried out. Interdisciplinary strategies are also needed to prevent hyperphosphatemia.

INTRODUCTION

Chronic renal failure (CRF) is a condition characterized by deterioration of renal function to less than 10~15% of normal levels [1]. Renal replacement therapy, such as dialysis or kidney transplantation, is required to maintain normal renal function. Hemodialysis is used by approximately 70% of patients with CRF, and the number is increasing every year [1].
Hemodialysis patients with CRF have low glomerular filtration rates, and hyperphosphatemia develops due to difficulty reducing the phosphate load, despite receiving hemodialysis 2~3 times a week [2]. Hyperphosphatemia can cause renal osteodystrophy, cardiovascular calcification, and secondary hyperparathyroidism [35]. In patients with CRF, the risk of secondary complications were found to increase if the serum phosphorus level was ≥5.0 mg/dL or the serum calcium level was ≥10.0 mg/dL [35]. Accordingly, the Kidney Disease: Improving Global Outcomes recommends maintaining the serum phosphorus level at 3.5~5.5 mg/dL and the serum calcium level at 8.4~9.4 mg/dL [6].
In patients with CRF, hyperphosphatemia occurs when phosphorus intake from food cannot be excreted due to impaired renal function and accumulates in the blood. Intake of food high in phosphorus can result in an excess concentration of phosphorus, which is a metabolite of protein. Hyperphosphatemia increases the mortality rate of CRF patients due to cardiovascular disease that results from the calcification of blood vessels and causes other major health problems such as secondary hyperparathyroidism and renal bone disease [35].
Hyperphosphatemia in hemodialysis patients has been associated with nutrition indicators including albumin, total protein, blood urea nitrogen (BUN), creatine (Cr), total iron binding capacity (TIBC), and ferritin [710]. Also other factors including interdialytic weight change, self-care, dialysis-related stress, social support, cognitive function, and diet [710].
Specifically, a better subjective nutritional status and greater weight gain between dialysis treatments were found to be related to higher protein intake [7,8]. It has been reported that the risk of hyperphosphatemia increases when protein intake is high because of the high phosphorus content in protein-rich foods [10]. In addition, higher levels of albumin, total protein, BUN, Cr, and TIBC, which are indicators of the level of protein in the body, were associated with a higher risk of hyperphosphatemia [7,8,10].
Hyperphosphatemia in hemodialysis patients is closely related to dialysis stress and social support [11,12]. It has been reported that dialysis-related stress worsens the disease prognosis, impedes the treatment process, and in-duces diet failure, thereby resulting in the development of hyperphosphatemia [12]. In addition, low social support from family and others results in poor levels of dialysis-related self-care practices, thereby increasing the risk of hyperphosphatemia [13].
Previous studies on the nutritional status of hemodialysis patients have analyzed significant relationships between nutritional status, self-care behavior, hemodialysis-related stress, social support. The studies have shown that individuals with poor nutritional status exhibit lower levels of self-care behavior [14], while individuals with good nutritional status experience lower levels of hemodialysis-related stress [12]. Moreover, better social support is associated with good nutritional status [15], and these findings confirm that the nutritional status of hemodialysis patients is closely related to dialysis-related stress, social support, and self-care behavior. Although previous studies have identified factors that contribute to the development of hyperphosphatemia in hemodialysis patients, there is limited research that systematically and compre-hensively analyzes variables such as nutritional and dialysis-related blood parameters, subjective nutritional status, dialysis-related stress, social support, and self-care behav-iors. Furthermore, in the field of nursing, there is a significant shortage of research systematically analyzing the influencing factors of hyperphosphatemia in Korean hemodialysis patients. There is a need for repeated studies to analyze these factors in order to develop a hyperphosphatemia prevention program that reflects the characteristics of Korean hemodialysis patients. Consequently, this study replicated the previous research [7] to systematically analyze the influencing factors of hyperphosphatemia and establish a foundation for the development of an educational program that takes into account the characteristics of Korean hemodialysis patients.
This study aims to identify the factors affecting the development of hyperphosphatemia, including nutrition status, hematologic indices, self-care practices, stress, and social support, which have all been reported to be factors influencing the development of hyperphosphatemia.

METHODS

1. Study Design

This is a descriptive research study designed to identify factors influencing the development of hyperphosphatemia in patients diagnosed with CRF and regularly receiving hemodialysis

2. Study Participants

The participants of this study were patients from two cities in South Korea who had been diagnosed with CRF by an internal medicine specialist and were receiving regular hemodialysis 2~3 times a week in the artificial kidney centers of three university hospitals. The required number of participants was calculated to be 135 using the G*Power 3.1.9.2 program, with an odds ratio of 4.86 based on a previous study [7], a significance level of .05, and a power of 0.90 in logistic regression analysis. In consideration of the dropout rate, questionnaires were distributed to 155 participants. After excluding questionnaires with one or more unanswered questions per tool, data from 150 questionnaires were analyzed.

3. Data Collection

As a descriptive research study, this study was conducted using surveys and medical records. Data were collected directly by the researchers from January 2022 to March 2022. The purpose and goals of the study were explained to the hospitals’ artificial kidney center staff, and the research was conducted with the approval of the institutions. Data collection was conducted while patients were in the waiting room, either before receiving dialysis or after dialysis was finished. The survey papers were distributed and collected directly by the researcher, and the collection rate was 100.0%. Electronic medical record (EMR) were reviewed and recorded directly by the researcher.

4. Measures

1) General characteristics and hemodialysis characteristics

The general characteristics and hemodialysis characteristics were set from the that were found to affect hyperphosphatemia in the preceding studies [7,9]: age, gender, marital status, Job, religion, BMI (<18.5 kg/m2: under-weight, 18.5~22.9 kg/m2: normal, 23~24.9 kg/m2: over-weight, ≥25 kg/m2: obese) [16], weekly hemodialysis frequency, hemodialysis period, hemodialysis hours, hemodialysis adequency, dietary education, taking phorsphorus binders, and self meal preperation.

2) Subjective nutritional status

Subjective nutritional status was assessed using the Mini Nutritional Assessment Short-Form developed by Rubenstein, Harker, Salva, Guigoz, and Velas [17] and translated into Korean, which was provided free of charge by the Nestle Nutrition Institute [18]. The tool consists of six items: appetite change, weight loss, mobility, acute and psychiatric disorders, and BMI. The total possible score was 14 points, with a score of 7 or lower considered “ malnutrition,” 8~11 “ borderline malnutrition,” and 12 or higher “ normal.”

3) Weight gain between hemodialysis

Interdialytic weight gain was calculated by subtracting the weight measured immediately after the last dialysis from the weight measured just before the current dialysis. The dialysis record from the patient's EMR was used to obtain the interdialytic weight gain recorded in the first week of each month. The average of three collected values was considered as the patient's weight gain between dialysis sessions. Based on previous studies [7], the weight gain between hemodialysis was analyzed by classifying it based on 2 kg. Weight was measured using a wheelchair scale (CI-2001B, CAS, Yangju, Korea).

4) Nutrition-related biochemical parameters

To assess nutrition-related biochemical parameters, the average of three consecutive monthly test results, as recorded in the patient's EMR, was used in the analysis. The investigated nutrition-related hematological indices were albumin (3.2~4.8 g/dL), total protein (6.7~8.3 g/dL), TIBC (220~460 ㎍/dL), and ferritin (male 22~322 ng/dL, female 10~291 ng/dL). The criteria presented by the Korean Society for Laboratory Medicine [19] were used to determine the reference range for each index. The Nutrition-related biochemical parameters were measured prior to hemodialysis

5) Biochemical parameters related to renal function

For the assessment of renal function-related biochemical parameters, the average of three consecutive monthly test results recorded in the dialysis record of the EMR was used. Calcium (Ca; 8.4~9.4 mg/dL), phosphorus (P; 3.5~5.5 mg/dL), BUN (9~23 mg/dL), and Cr (0.1~0.3 mg/dL) data were collected. The reference range for each index was determined using the criteria presented by the Korean Society of Laboratory Medicine [19]. The renal function related biochemical parameters were measured prior to hemodialysis.

6) Hemodialysis-related self-care

To assess the self-care of hemodialysis patients, the hemodialysis-related self-care practice tool developed by Cho and Choi [20] was used. It is a 35-item tool composed of subdomains of self-care including diet, blood vessel management, blood pressure and weight management, appropriate exercise and rest, medication, body care, and social activities. A 5-point Likert scale was used for the assessment, and higher scores indicated higher levels of self-care practice. The reliability of the tool in our previous [20] study was shown by a Cronbach's ⍺ of .88, and in our study, Cronbach's ⍺ of .91. The Cronbach's ⍺ of the subdomains are as follows: Diet .83, blood vessel management .82, blood pressure and weight management .83, appropriate exercise and rest .85, medication .81, body care .76, and social activities .86.

7) Hemodialysis-related stress

Hemodialysis-related stress was assessed using a tool developed by Baldree, Murphy and Powers [21], which consists of 27 items related to physical, social, and emotional stress. The tool was scored using a 5-point Likert scale, and higher scores indicated greater hemodialysis- related stress. The reliability of the tool in our previous [21] study was shown by a Cronbach's ⍺ of .82, and in our study, Cronbach's ⍺ of .90. The Cronbach's ⍺ of the subdomains are as follows: Physical stress .89, social stress .76, and emotional stress .71.

8) Social support

Social support was assessed using a tool developed by Kim [22] for hemodialysis patients after obtaining approval to use it. The tool assessed family support and medical staff support, and a 5-point Likert scale was used for scoring. A high score indicated higher degrees of support. The reliability of the tool in our previous [22] study was shown by a Cronbach's ⍺ of .82, and in our study, Cronbach's ⍺ of .89. The Cronbach's ⍺ of the subdomains are as follows: Family support .92 and medical staff support .88.

5. Ethical Considerations

The Daejeon University Institutional Review Board (IRB) (IRB No. 1040647-2021112-HR-010-02) approved this study. The experimental protocol was approved by the Institutional Review Board of the Daejeon University Medical Center (IRB) (IRB No. 1040647-2021112-HR-010-02). All methods were performed in accordance with the relevant guidelines and regulations. All participants of the study were informed about the study, and they gave written informed consent to be included in the study. The anonym-ity of all participants was warranted as personal identi-fiers weren’ t traced during data collection and analysis. The manuscript does not include identifying information/images of a study participant.

6. Data Analysis

The collected data were analyzed using SPSS version 24.0 (IBM Corp., Armonk, NY, USA). The general and hemodialysis-related characteristics of the participants, including hyperphosphatemia, nutritional status, biochemical parameters were analyzed with descriptive statistics. Variables were analyzed using means and standard deviations. Differences in general characteristics, hemodialysis- related characteristics and research variables according to the presence or absence of hyperphosphatemia patients were analyzed by the x2 test and independent t-test. Factors affecting the development of hyperphosphatemia were analyzed using binary logistic regression analysis.

RESULTS

1. General Characteristics and Hemodialysis Characteristics

Sixty-seven (44.7%) of the total 150 participants had hyperphosphatemia (serum phosphorus ≥5.5 mg/dL) and 83 (55.3%) were normal. The average serum phosphorus was 5.77 mg/dL, and the average age was 55.37 years. Among the participants, 111 (74.0%) took phosphate binders (Table 1).
Table 1.
General Characteristics and Hemodialysis-related Characteristics of Participants (N=150)
Variables Characteristics Categories Total M± SD
n (%)
General characteristics Hyperphosphatemia (mg/dL) Yes 67 (44.7) 5.77±5.06
No 83 (55.3)
Age (year) <50 51 (34.0) 55.37±13.79
50~59 41 (27.3)
≥60 58 (38.7)
Gender Male 91 (60.7)
Female 59 (39.3)
Marriage Married 94 (62.7)
unmarried 56 (37.3)
Job Yes 56 (37.3)
No 94 (62.7)
Religion Yes 66 (44.0)
No 84 (56.0)
BMI (kg/m2) <18.5 16 (10.7) 22.75±3.90
18.5~22.9 75 (50.0)
23~24.9 27 (18.0)
≥25 32 (21.3)
Hemodialysis characteristics Frequency of dialysis per week 2 11 (7.3)
3 139 (92.7)
Dialysis hours per session (hour) 1~2 12 (8.0)
3~4 138 (92.0)
Hemodialysis adequacy <1.2 52 (34.6)
≥1.2 98 (65.4)
Duration of hemodialysis (year) <4 54 (36.0)
4~7 42 (28.0)
≥8 54 (36.0)
Dietary education for dialysis Yes 54 (36.0)
No 96 (64.0)
Taking phosphorus binders Yes 111 (74.0)
No 39 (26.0)
Meal preparation (self) Yes 84 (56.0)
No 66 (44.0)

BMI=body mass index; SD=standard deviation.

2. Differences in General and Hemodialysis Charac-tieristics according to the Presence or Absence of Hyperphosphatemia

The general characteristics that showed significant differences according to the presence or absence of hyperphosphatemia were age (x2=14.12, p=.001) and BMI (x2= 9.61, p=.022). In the hyperphosphatemia group, age under 50 years (40.3%) and a BMI of 18.5~22.9 kg/m2 (38.8%) were the most common age and BMI categories, while in the normal group, age over 60 years (51.8%) and a BMI of 18.5~22.9 kg/m2 (59.0%) predominated (Table 2).
Table 2.
Comparison of General Characteristics and Hemodialysis-related Characteristics between the Normal and Hyperphosphatemia Groups (N=150)
Variables Characteristics Categories Normal (n=83) Hyperphosphatemia (n=67) x2 p
n (%) n (%)
General characteristics Age (year) <50 24 (28.9) 27 (40.3) 14.12 .001
50~59 16 (19.3) 25 (37.3)
≥60 43 (51.8) 15 (22.4)
Gender Male 46 (55.4) 45 (67.2) 2.14 .179
Female 37 (44.6) 22 (32.8)
Marriage Married 52 (62.7) 42 (62.7) 0.00 .996
Unmarried 31 (37.3) 25 (37.3)
Job Yes 24 (28.9) 32 (47.8) 5.62 .057
No 59 (71.1) 35 (52.2)
Religion Yes 41 (49.4) 25 (37.3) 2.19 .186
No 42 (50.6) 42 (62.7)
BMI (kg/m2) <18.5 10 (12.0) 6 (9.0) 9.61 .022
18.5~22.9 49 (59.0) 26 (38.8)
23~24.9 13 (15.7) 14 (20.9)
≥25 11 (13.3) 21 (31.3)
Hemodialysis characteristics Frequency of dialysis per week 2 6 (7.3) 5 (7.5) 0.07 .789
3 77 (92.7) 62 (92.5)
Duration of dialysis (year) <4 25 (30.1) 29 (43.3) 2.85 .240
4~7 26 (31.3) 16 (23.9)
≥8 32 (38.6) 22 (32.8)
Dialysis hours per session (hour) 1~2 6 (7.3) 6 (9.0) 0.02 .874
3~4 77 (92.7) 61 (91.0)
Hemodialysis adequacy <1.2 15 (18.1) 13 (19.4) 0.85 .355
≥1.2 68 (81.9) 54 (80.6)
Dietary education for dialysis Yes 27 (32.5) 27 (40.3) 0.97 .324
No 56 (67.5) 40 (59.7)
Taking phosphorus binders Yes 56 (67.5) 55 (82.1) 4.11 .060
No 27 (32.5) 12 (17.9)
Meal preparation (self) Yes 42 (50.6) 42 (62.7) 2.77 .189
No 41 (49.4) 25 (37.3)

BMI=body mass index.

There were no significant differences between the two groups in gender, marriage, job, religion, frequency of dialysis per week, dialysis hours, hemodialysis adequency, duration of dialysis, dietary education for dialysis, taking phosphorous binders and Meal preparation (Table 2).

3. Differences in Nutritional Status according to the Presence or Absence of Hyperphosphatemia

An analysis of the nutritional status of hemodialysis patients according to the presence or absence of Hyperphosphatemia is shown in Table 3. There was a significant difference between the two groups according to weight gain between hemodialysis (x2=7.14, p=.010) and TIBC (x2=4.61, p=.039). The number of patients with ≥2 kg weight gain between dialysis treatments was 59 (88.1%) in the hyperphosphatemia group and 58 patients (69.9%) in the normal group, showing a greater degree of weight gain between hemodialysis in the hyperphosphatemia group. There were more patients with a normal TIBC (220~460 μ g/dL) in the hyperphosphatemia group (50 patients, 74.6%) than in the normal group (48 patients, 57.8%).
Table 3.
Comparison of Nutritional Status Characteristics between the Normal and Hyperphosphatemia Groups (N=150)
Characteristics Categories Total (n=150) Normal (n=83) Hyperphos -phatemia (n=67) x2 p
n (%) n (%) n (%)
Subjective nutritional status Malnutrition 13 (8.7) 10 (12.0) 3 (4.5) 3.26 .196
Borderline malnutrition 62 (41.3) 36 (43.4) 26 (38.8)
Normal 75 (50.0) 37 (44.6) 38 (56.7)
Weight gain between hemodialysis (kg) <2 33 (22.0) 25 (30.1) 8 (11.9) 7.14 .010
≥2 117 (78.0) 58 (69.9) 59 (88.1)
Albumin (g/dL) Low (<3.2) 11 (7.3) 5 (6.1) 6 (8.9) 3.36 .112
Normal (3.2~4.8) 139 (92.7) 78 (93.9) 61 (91.1)
Total protein (g/dL) Low (<6.7) 39 (26.0) 26 (31.3) 13 (19.4) 2.73 .134
Normal (6.7~8.3) 111 (74.0) 57 (68.7) 54 (80.6)
TIBC (μ g/dL) Low (<220) 52 (34.7) 35 (42.2) 17 (25.4) 4.61 .039
Normal (220~460) 98 (65.3) 48 (57.8) 50 (74.6)
Ferritin (ng/dL) Normal (Male 22~322) 78 (85.7) 39 (84.8) 39 (86.7) 0.06 .797
High (Male>322) 13 (14.3) 7 (15.2) 6 (13.3)
Normal (Female 10~291) 37 (62.7) 24 (64.9) 13 (59.1) 0.19 .782
High (Female>291) 22 (37.3) 13 (35.1) 9 (40.9)

TIBC=total iron binding capacity.

There were no significant differences between the two groups in subjective nutritional status, albumin, total protein, and ferritin (Table 3).

4. Differences in Renal Function-related Biochemical Parameters according to the Presence or Absence of Hyperphosphatemia

Table 4 presents the results of the analysis of differences in renal function-related biochemical parameters according to the presence or absence of hyperphosphatemia. The results of the analysis indicate significant differences in BUN (t=-3.73, p=.001) and Cr (t=-2.87, p=.005) between the two groups (Table 4). The average BUN was significantly higher in the hyperphosphatemia group than in the normal group (62.35 mg/dL vs. 59.94 mg/dL). The average Cr value was significantly higher in the Hyperphosphatemia group than in the normal group (12.16 mg/dL vs. 10.72 mg/dL). There was no significant difference in Ca values between the two groups (Table 4).
Table 4.
Comparison of Biochemical Parameters, Self-care, Stress, and Social Support between the Normal and Hyperphosphatemia Groups (N=150)
Characteristics Total (n=150) Normal (n=83) Hyperphos -phatemia (n=67) t p
M± SD M± SD M± SD
Ca (mg/dL) (normal: 8.4~9.4) 9.27±0.82 9.30±0.89 9.10±0.71 1.49 .137
BUN (mg/dL) (normal: 9~23) 63.25±14.01 59.94±14.82 62.35±11.81 -3.73 .001
Creatinine (mg/dL) (normal: 0.1~0.3) 11.36±3.13 10.72±3.14 12.16±2.94 -2.87 .005
Self-care
    Total 117.01±18.65 117.00±18.75 116.32±18.65 0.40 .688
    Diet 18.58±4.14 19.06±4.08 17.98±4.17 1.58 .115
    Vessel management 23.47±4.28 23.09±4.27 23.94±4.28 -1.20 .232
    Exercise and rest 12.61±3.42 12.81±3.52 12.35±3.31 0.81 .415
    Taking medication 7.83±1.54 7.96±1.45 7.80±1.65 0.62 .535
    BP and weight management 8.53±2.74 8.75±2.81 8.25±2.64 1.12 .263
    Social activities 6.10±2.37 6.06±2.44 6.14±2.30 -0.22 .820
    Body care and activities 39.82±7.18 39.80±6.87 39.83±7.60 0.89 .607
Stress 82.37±18.90 78.95±17.13 84.91±19.84 -0.02 .981
Social support
    Total 68.41±13.31 66.08±13.96 71.29±11.94 -0.24 .017
    Family support 36.72±9.69 34.59±10.45 39.35±7.98 -3.07 .002
    Medical staff support 31.69±5.58 31.49±4.98 31.94±6.28 -0.48 .628

BP=blood pressure; BUN=blood urea nitrogen; Ca=calcium; M=mean; SD=standard deviation.

5. Hemodialysis-related Self-care, Stress, and Social Support according to the Presence or Absence of Hyperphosphatemia

Table 4 presents the results of the analysis of hemodialysis-related self-care, stress, and social support according to the presence or absence of hyperphosphatemia. The results of the analysis showed no significant difference between the two groups in the overall scores and sub-Factors of self-care (Table 4). There was also no significant difference in hemodialysis-related stress between the two groups. Regarding social support, family support was significantly higher in the hyperphosphatemia group than the normal group (t=-3.07, p=.002) (Table 4).

6. Factors related to Hyperphosphatemia in Hemodialysis Patients

Binary logistic regression was used to analyze the Factors affecting the development of hyperphosphatemia in hemodialysis patients. Age, BMI, weight gain between hemodialysis, TIBC, BUN, Cr, and family support, which all showed statistically significant differences between the hyperphosphatemia and normal groups, were used as independent variables in the analysis. As a result, the regression model was found to be significant (x2=137.24, p<.001). The Cox and Snell coefficient of determination (R2=.59), which represented the explanatory power of the model, showed an explanatory power of 59.1%; and the Nagelkerke coefficient of determination (R2=.80) showed an explanatory power of 80.2%.
Regression analysis among the general characteristics found that BMI was a predictive factor. The risk of hyperphosphatemia was 3.09 times (95% CI, 1.15~8.25) higher for a BMI ≥25 kg/m2 than for a BMI 18.5~ 22.9 kg/m2. The risk of hyperphosphatemia increased by 1.04 times (95% CI, 1.01~1.07) as the BUN levels increased (Table 5).
Table 5.
Factors Affecting Hyperphosphatemia
Characteristics Categories B SE OR (95% CI) p
Age (year) (ref.<50) 50~59 0.49 0.83 1.64 (0.32~8.41) .551
≥60 -1.26 0.79 028 (0.59~1.33) .110
BMI (kg/m2) (ref. 18.5~22.9) <18.5 0.02 0.62 1.02 (0.03~3.43) .967
23~24.9 0.73 0.52 2.07 (0.74~5.75) .162
≥25 1.13 0.50 3.09 (1.15~8.25) .025
Weight gain between hemodialysis (kg) (ref.<2) ≥2 1.10 0.87 3.02 (0.69~13.26) .141
TIBC (μ g/dL) (ref.<220) 220~460 -0.24 0.68 0.78 (0.24~2.99) .718
BUN (mg/dL) 0.04 0.02 1.04 (1.01~1.07) .019
Creatinine (mg/dL) -0.36 0.15 0.69 (0.51~0.93) .116
Social support (family) 0.05 0.41 1.05 (0.97~1.14) .175

BMI=body mass index; BUN=blood urea nitrogen; CI=confidence interval; OR=odds ratio; ref.=reference; SE=standard error; TIBC=total iron binding capacity.

DISCUSSION

This study was conducted to identify the factors affecting the development of hyperphosphatemia in hemodialysis patients and to provide basic data that could be used to develop intervention programs for the prevention of hyperphosphatemia.
The average serum phosphorus was 5.77 mg/dL, which was higher than the reference range of 3.5~5.5 mg/dL. In the management of hyperphosphatemia, regular dialysis, dietary management, and timely medication are essential [6]. Our results indicate that nearly half of all hemodialysis patients in this study have hyperphosphatemia despite undergoing periodic hemodialysis. Additionally, 44.7% of the participants showed hyperphosphatemia, even though 74.0% of the participants were taking phosphorus binders. In particular, 82.1% of the participants with Hyperphosphatemia continued to have hyperphosphatemia even though they were taking phosphorus binders for treatment. Through these results, it can be inferred that hemodialysis patients may not be efficiently taking phosphorus binders to prevent hyperphosphatemia. These results can be analyzed in relation to the findings reported in previous studies [23], which indicated that the level of medication adherence among hemodialysis patients was low. However, in this study, there is a limitation in identifying the relationship between the use of phosphorus binders and the occurrence of hyperphosphatemia, as no analysis has been conducted on the types and timing of phosphorus binders currently being taken. In a previous study [24], which analyzed the effect of reducing blood phosphorus levels according to the type of phosphorus binders widely used for the treatment of hyperphosphatemia, no difference was observed based on the type of phosphorus binders, but differences were reported according to the duration of administration. Accordingly, a follow-up study is proposed to analyze the relationship between the occurrence of hyperphosphatemia in hemodialysis patients, medication adherence, and the duration of taking phosphorus binders.
These results suggest that hemodialysis patients need more intensive intervention programs for the prevention of hyperphosphatemia. A dietary education program ap-plied to CRF patients undergoing hemodialysis has been shown to be effective in reducing serum levels of phosphorus. Dietary phosphorus restriction is an important component of the management of hyperphosphatemia in CRF. A previous study [24] applying dietary education intervention for preventing hyperphosphatemia in patients with CRF showed that regular food diary writing and dietary education based on it, with monitoring of dietary intake and phosphate binder adherence, were effective in reducing serum phosphorus levels. In To lower serum phosphorus levels in chronic kidney disease patients, a multidimensional and intervention strategy is necessary, including continuous monitoring of dietary intake and phosphate binder usage, as well as implementing appropriate dietary education to ensure optimal phosphorus intake. Therefore, a team of various professionals, such as nutritionists, physicians, nurses, therapists, and exercise specialists, should work together to establish an effective intervention plan.
Among the general characteristics of hemodialysis patients, BMI was found to be a significant factor affecting the development of hyperphosphatemia. Patients with a BMI ≥25 kg/m2 were approximately 3.09 times more likely to develop hyperphosphatemia than those with a BMI 18.5~22.9 kg/m2. These results are consistent with those reported in previous study [25] where BMI was positively correlated with the risk of hyperphosphatemia. In patients with CRF, serum phosphorus can be removed through regular hemodialysis, but hemodialysis alone cannot effectively remove the phosphorus intake from food [26]. Diet is a vital component in the health management of hemodialysis patients, and secondary health problems such as obesity may occur without proper dietary management. Obesity is a factor that leads to CRF and aggravates its symptoms. It has been reported that 20~25% of patients with CRF are obese [27]. High BMI has been associated with a high risk of proteinuria, a low glomerular filtration rate, and a high serum phosphate level [7,25,28]. Furthermore, obesity is a factor in the high mortality rate of patients with CRF due to exacerbation of arteriosclerosis, hypertension, and diabetes [28]. Therefore, it is necessary to develop and apply dietary education and obesity management programs for CRF patients undergoing hemodialysis. In particular, It has been reported that ongoing dietary education and counseling for CRF patients was effective in controlling adequate protein and phosphorus intake and reducing serum phosphorus [29]. However, the results of our study indicate that more than 60.0% of the participants had no received any dietary education within the last year. These results indicate that CRF patients are mainly provided dietary education at the beginning of the hemodialysis, and then they are not provided any regular dietary education thereafter. An investigation should be conducted regularly in the hemodialysis patients for monitoring their dietary and nutritional status as the disease progresses. The individual dietary education should be provided based on each patient's clinical symptoms, hematological indices, and nutritional status. Also dietary phosphorus intake may differ depending on the dietary culture of each country, assessment of dietary phosphorus intake and nutrition education should be based on the patients’ nutritional status and dietary culture. The limitation of our study is that we did not sufficiently assess the characteristics of the participants' diet. Therefore, we suggest a follow-up study to identify the factors that can influence hyperphosphatemia in the patients by using a systematic dietary survey and measuring their dietary phosphorus intake.
The BUN was identified as a factor influencing the development of hyperphosphatemia in hemodialysis patients. This result is consistent with a previous study on the factors affecting hyperphosphatemia [7]. A positive correlation was also observed between BUN and serum phosphorus in an additional study [10]. BUN is an indicator that can be used to evaluate kidney function and the level of protein intake from food. If a hemodialysis patient has excess protein intake, nitrogenous waste products are overproduced and BUN increases [7,28]. Physiological indicators such as BUN are used as objective indicators to determine whether the hemodialysis patients’ are implementing self-care behavior continuously and effectively [14]. In a previous study, when self-care behavior scores were high, BUN and hyperphosphatemia were reported to be low [8]. Further, it was found that the improvement of self-care behavior in the hemodialysis patients also im-proved their physiological indicators. However, in this study, the self-care compliance of the participants was 117 out of 175 points, which was similar to the 122 points reported in previous study [8] that were measured using the same tool. However, this score indicates a performance level that is not particularly high or in the intermediate range. Although being on periodic hemodialysis, 44.7% had hyperphosphatemia, and 78.0% had a weight gain of 2.0 kg or more between dialysis. These results suggest that hemodialysis patients need more intensive management and it is necessary to develop and apply a systematic educational program to improve self-care. A previous study found that multidisciplinary CRF intervention was positively correlated with high self-care behavior scores, which further reduced the risk of rapid decline of the renal function [30]. Therefore, we suggest a follow-up study to verify the effects of regular and multidisciplinary education on the self-care behaviors and the hematological indicators, and in preventing hyperphosphatemia.
This study was conducted to accumulate evidence for the development of a prevention program in the absence of previous research on hyperphosphatemia. Based on previous research [7], various measurement variables were selected as factors related to hyperphosphatemia. These include general characteristics and hemodialysis Characteristics, subjective nutritional status, nutritional biochemical parameters, renal function-related biochemical parameters, hemodialysis-related stress, self-care, and social support. However, this study aimed to further analyze the effects of nutritional factors and the use of phosphate binders. Therefore, it included characteristics such as marital status, self-meal preparation, and the use of phosphate binders, which can affect nutritional status. In contrast to previous research [7], this study analyzed the association between hyperphosphatemia and BMI levels based on the criteria of the Korean Society for the Study of Obesity and the WHO, and excluded biochemical parameters containing P and Ca*P. In the previous study [7], subjective nutritional status, weight gain on hemodialysis, and BUN were analyzed as the main influencing factors. However, in this study, BMI and BUN were identified as the main influencing factors. This difference is analyzed to be due to the difference in BMI level categorization. Obesity is not only a major influencing factor in hyperphosphatemia [25,27], but also has a significant correlation with the occurrence of complications [28]. This study has identified obesity as a major influencing factor to hyperphosphatemia. The significance of this study lies in providing evidence that future prevention programs for hyperphosphatemia should include measures to prevent obesity.
The limitation of this study is that it may be difficult to generalize the results since the study was conducted among a convenience sample of hemodialysis patients from three university hospitals. There is a limitation in that the study on the participant' diet characteristics were not sufficiently conducted. Based on the results of this study, a follow-up study is warranted to investigate the development and ap-plication of intervention programs for the management of hyperphosphatemia. This study has the limitation of re-peating previous research to accumulate evidence on the factors influencing hyperphosphatemia in hemodialysis patients. For a comprehensive analysis of hyperphosphatemia development, it is recommended to conduct further research that includes a wider range of variables, in addition to those measured in this study. To systematically analyze the factors that influence the development of hyperphosphatemia in hemodialysis patients, repeated studies are necessary to analyze the correlations between dialysis-related stress and social support, self-care behavior, as well as the influence of hematological indices, nutritional characteristics, diet characteristics, dialysis-related char-acteristics, and underlying diseases that affect Hyperphosphatemia.

CONCLUSION

This study was conducted to analyze the factors affecting the development of hyperphosphatemia in hemodialysis patients. Results showed that high BMI and BUN levels were associated with a high risk of developing hyperphosphatemia. Therefore, to prevent and manage the development of hyperphosphatemia, it is necessary to regular monitoring for dietary and nutritional status as the disease progresses, individual dietary education should be provided based on each patient's clinical symptoms, hematological indices, and nutritional status. In addition, a multidimensional program for preventing hyperphosphatemia should be developed, which includes nutrition and dietary education, phosphate binder medication, and obesity prevention programs. And it is necessary to promote self-care behavior by providing accurate information about the disease and providing systematic education.

Notes

CONFLICTS OF INTEREST
The authors declared no conflict of interest.
AUTHORSHIP
Study conception and design acquisition - Kim J; Data collection - Kim J; Data analysis & Interpretation -Kim J; Drafting & Revision of the manuscript - Kim J.
DATA AVAILABILITY
The data that support the findings of this study are available from the corresponding author upon reasonable request.

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