Author: admin

Introduction

Chronic kidney disease (CKD) is a common communicable disease affecting over 850 million people worldwide.¹ It is a major cause of morbidity and mortality, and its prevalence is increasing globally.² The cost of kidney replacement therapy is very high, posing a big threat to economic status in every country, especially in low- and middle-income countries. The expenditure on kidney replacement therapy (KRT) accounts for 0.91 to 7.1% of national healthcare budget.³ However, most developing countries do not have public funding support for the cost of KRT.⁴ Patients with CKD usually have shorter longevity and lower quality of life than controlled population.⁵ Thus, providing effective means for early recognition and treatment to delay kidney disease progression is of prime importance. Besides specific pharmacologic intervention, lifestyle modification is an indispensable part for delaying kidney disease progression.⁶ These include control of body weight, exercise, avoidance of tobacco and analgesic use, and control of dietary protein and salt intake. However, in real world practice, the patient’s compliance with this recommendation is still far from perfect. Among patients with diabetes, there were only 53.5% of cases who were able to achieve satisfactory body mass index (BMI).⁷ Only 25% to 50% of CKD patients could comply with dietary intake recommendation.⁸

Herbal, alternative, and supplementary therapies are commonly used by CKD patients, despite potential risks and limited evidence of efficacy.⁹ This is particularly true among Asian patients due to a common belief that natural products are healing remedies which should be harmless to the body.^10–12 Use of herbal medicines was as high as 42.65% of Thai patients with CKD.^13,14 Since detailed compositions of many medical herbs are unknown or not clearly identified, continuing consumption of herbal medicines poses a continuing risk factor of CKD progression.^15,16

Non-steroidal anti-inflammatory drugs (NSAIDs) are widely recognized as a risk factor for CKD progression.¹⁷ Despite this adverse effect, use of NSAID or other analgesics for pain relief is not uncommon among CKD patients. About 27% of CKD patients in a Canadian population-based study received at least one NSAID prescription.¹⁸ In Thailand, NSAIDs or analgesic use was found in 39% of CKD patients living in the rural area.¹⁹

A randomized controlled trial (RCT), the ESCORT-1 study, was conducted to evaluate the effectiveness of an integrated care approach for CKD patients at the community level.²⁰ In that study, patients with stage 3 or 4 CKD residing in a rural district of Kamphaengphet Province, approximately 400 kilometers north of Bangkok, Thailand, received multidisciplinary care at the district hospital and home visits conducted by community nurses from sub-district health offices in collaboration with village health volunteers. It was observed that patients assigned to the intervention group exhibited a reduced rate of kidney disease progression compared to those in the control group, who received conventional care. Furthermore, the intervention group consistently adhered to a low-salt, low-protein diet regimen throughout the study period. It could be inferred that such comprehensive care would empower patients in the intervention group to make more significant lifestyle modifications.

The ESCORT-2 Study was subsequently expanded to include five district hospitals. The care program was modified to be less strict and more aligned with the realities of community-level care in Thailand. Nevertheless, core care activities were maintained.²¹ Interventions included training healthcare personnel in CKD management, employing multidisciplinary care teams, conducting scheduled patient education during hospital visits, and implementing regular home visits with protocol checklists by sub-district community nurses and village health volunteers. After a 3-year observation period, the ESCORT-2 Study demonstrated a significantly lower rate of kidney disease progression among its participants when compared to the control group of the preceding ESCORT-1 Study.²¹ Given that adverse lifestyle factors can accelerate the progression of CKD, it is important to determine if an integrated care approach can improve these unhealthy behaviors. Thereafter, in planning the ESCORT-2 Study, we determined to prospectively and systematically monitor a set of unhealthy behaviors as well as clinical and biochemical parameters throughout the course of the study period. This study is a follow-up part of the ESCORT-2 study, which has already been published, but will focus on the change in unhealthy behaviors along the course of that study.

Materials and Methods

This article presents a post-hoc analysis of the ESCORT-2 Study data to examine the effect of an integrated care model on modifying unhealthy behaviors associated with CKD progression. The protocol of ESCORT-2 Study was approved by the Ethics Committee of Institutional Review Board, Ministry of Public Health, Thailand, and registered with www.clinicaltrials.in.th (TCTR-20160614001). It was conducted in accordance with the ethical principles of the Declaration of Helsinki. All study participants provided informed consent before the initiation of the study. It was a 3-year prospective cohort study.²¹ Those who were 18–70 years old and had estimated glomerular filtration rate(eGFR) of 15–59 mL/ min/ 1.73 m² body surface area (BSA) was enrolled. eGFR was calculated by using the 2009 CKD-EPI formula. Details of the exclusion criteria and methods of study have been described elsewhere.²¹ In brief, the integrated care program consisted of a hospital-based multidisciplinary care team (HMDT) at each district hospital, and a home-based community care network team (CCNT) at each sub-district health office. HMDT is comprised of 1–2 general practitioners, a CKD nurse practitioner, 1–2 pharmacists, a nutritionist, and a physical therapist. During patients’ hospital visit every 3 months, enrolled cases were interviewed about their current unhealthy behaviors. HMDT provides group education and clinical care to patients. The education included basic knowledge on and self-care for CKD; avoidance of high-salt and high-protein diet; avoidance of use of alcohol, tobacco, herbal medicines, and over-the-counter analgesics or NSAIDs; and advice on regular exercise. The cases were interviewed on their history of the use of herbal medicines, analgesics, or NSAIDs. The CCNT, comprised of a community nurse working at each sub-district health center, and village health volunteers (VHVs) who were responsible for caring for the cases residing in that village, conducted the interviews. CCNT gave advice during home visit every 6 months to the cases on how to conduct healthy behavior to delay CKD progression. CNNT also assessed exercise practicing at home, and consumption of salty or high-protein foods. Antihypertensive agents such as angiotensin-converting enzyme inhibitors (ACEI) and angiotensin receptor blockers (ARB) available at the public primary healthcare level were enalapril and losartan, respectively. Antihyperglycemic agents available for use were sulfonylurea, metformin, and insulin.

The body mass index was defined as actual weight in kg standardized to a square meter of body height. It was measured at baseline and every 12 months thereafter. An herb was defined as any medicinal product with ingredients made from one or more kinds of plants. Herbal or analgesic/NSAIDs use was defined, on a yes/no basis, as a history of using any herb or analgesic/NSAIDs once during each 3-month period. The term “NSAIDs use” was used exclusively only when a specific drug can be identified as an NSAID. In Thailand, the use of NSAIDs is often linked to the use of pre-packaged, over-the-counter painkiller drugs.²² Therefore, when collecting patient history, a broad term like “analgesic use” was applied to capture all potential NSAID exposure.

CCNT conducted home visits every 6 months, during which each patient was interviewed about their exercise frequency and salty food consumption in the past week. Exercise could be in the form of either cardiovascular, strengthening or stretching type. Due to the difficulty in distinguishing between authentic exercise and daily agricultural work, lack of exercise at home was defined as having one or fewer authentic exercise sessions in the past week.

Consumption of high salt intake was obtained by using a standard food interview form (SFIF). It was designed by Department of Health Service Support, Ministry of Public Health, Thailand [Appendix 1] and had routinely been used by community nurses during their field works. In that form, 10 types of commonly consumed salty foods or food condiments were listed. During the home visit by CCNT, each patient was interviewed to figure out the frequency of salty food items consumed in a week preceding the home visit. The amount of daily protein intake (DPI) was assessed with a short protein food recall questionnaire (S-PFRQ) developed by a renal dietitian for this study [Appendix 2]. It was counted as the number of tablespoons of high-protein food items consumed during the preceding week and was expressed as a daily average. We have previously reported that DPI estimated from S-PFRQ correlated well with the protein-equivalent of total nitrogen appearance, which was calculated from 24-hour urinary urea-nitrogen excretion.²³

Outcomes

Continuous variables are presented as mean ± SD, while categorical data are presented as percentages. CKD was stratified into stages 3A, 3B, and 4 based on eGFR values. Usage of herbs and analgesic or NSAIDs obtained during each hospital visit were pooled together over a 12-month interval. If a patient reported such usage once or more at 12-month period, it would be scored as “having unhealthy behavior”. Prevalences of overweight were assessed at baseline and annually thereafter. Participants with BMI of 23 kg/m² or higher were labeled as being overweight. Lack of regular exercise, salt, and protein intake were assessed at baseline and during home visits every six months. Participants were labeled as having unhealthy behaviors if they reported any of these behaviors during any home visit in a given year. Participants whose unhealthy behaviors were observed in over 50% of recorded instances were classified as having persistent unhealthy behaviors. The cumulative prevalence of unhealthy behaviors was determined for each participant at baseline and annually. Each identified unhealthy behavior was assigned a value of 1 point. The impact of this cumulative unhealthy behavior score on the progression of CKD was analyzed. Although changes in blood pressure and proteinuria could affect the rate of progression of kidney disease, the results of these changes had already been reported in the previous study²² and will not be presented herein. Comparison between baseline and annual prevalence of each unhealthy behavior was made with McNemar’s chi-square test, The influence of the persistent unhealthy behavior on CKD progression was examined by comparing eGFR decline rates between the persistent and non-persistent groups using an independent t-test. Statistical analyses were using the SPSS program software version 23. Statistical analysis was regarded as significant when the p-value was < 0.05.

Results

Out of 1211 cases with CKD stages 3–4, aged 18–70 years-old who were screened for enrollment in the ESCORT-2 Study, fifty-two cases declined the study, 297 cases were excluded, leaving 914 cases for enrollment.²² The mean age was 62 + 6 years, and 67% were female (Table 1). About 80% of the case received primary education (up to grade 6 from the grade 1–12 scale). Hypertension, hyperlipidemia and diabetes were found in 92%, 68% and 53%, respectively. About 60% of the cases had overweight, defined as BMI equal to or more than 23.0 Kg/m² which is the cut-off limit of overweight for Asian population.²⁴ At enrollment, the histories of herbal medicine usage, analgesic usage and smoking were 23%, 35% and 36%, respectively.

The cases were stratified at baseline by stages of CKD and types of unhealthy behavior (Table 2), there was no significant difference among the CKD stages with respect to the proportion of cases with usage of herbal medicine or analgesic, moderate to high salt intake, and high protein intake. However, the prevalence of NSAID use, being overweight, and lack of exercise were significantly less observed in cases with stage 4 CKD than those in the earlier stages of CKD (P =0.001, P = 0.006, and P = 0.006, respectively).

Table 2 The Prevalence of Unhealthy Behaviors Among Study Participants Stratified by Stage of CKD at Baseline, No. of Cases (%)

Table 3 illustrated trends of change of unhealthy behaviors along the course of the study. Usage of herbal medicine declined from 23.3% of cases at baseline to 13.4% at the 1st year of follow-up (difference = −9.77, 95% CI [−13 to −6.5]), to 7% at the 2nd year of follow-up (−15, 95% CI [−18 to −12]), and to 5% at the 3rd year of follow-up (−17, 95% CI [−21 to −14]), P < 0.0001 for all comparisons.

Table 3 Percentage of Unhealthy Behaviors at Baseline and From the First year to Third year of Follow up

The prevalence of analgesic or NSAID usage decreased remarkably from 34.9% and 4.3%, respectively, at baseline to 18.6% and 2.6%, respectively, at the 1st year (P < 0.0001 and P < 0.036, respectively), to 16.0% and 2.0%, respectively, at the 2nd year (P < 0.0001 and P < 0.005, respectively), and to 7.8% and 1.3%, respectively, at the 3rd year (P < 0.0001 for both).

The percentage of overweight participants exceeded 60% throughout the study period and did not decrease with integrated care management (Table 3). Using the standard food interview form (SFIF), the baseline prevalence of moderate to high salt intake was 22.1%, which significantly decreased to 18% at the one-year follow-up (P=0.0021). Further reductions were observed at the two-year (12.9%) and three-year (14.1%) follow-ups (P<0.0001). In contrast, the prevalence of high protein intake, as estimated by the S-PFRQ, did not change significantly during the study.

The potential for unhealthy behaviors to exacerbate the progression of CKD has been suggested.²⁵ This study aimed to determine if the sustained accumulation of unhealthy behaviors over time correlated with a greater rate of decline in eGFR. We conducted a comparative analysis of eGFR decline between participants exhibiting persistent unhealthy behaviors and those without [Table 4]. However, the results did not reveal any statistically significant differences in eGFR decline between the two groups for any of the unhealthy behaviors investigated.

Table 4 Relationship Between Persistent Unhealthy Behaviors and Rate of eGFR Decline

Nevertheless, we observed a progressive decline in the percentage of participants with unhealthy behavior counts of 3 or more, from 26% at baseline to 17%, 14.8%, and 14.4% at years 1, 2, and 3, respectively, during the follow-up period (Figure 1). Furthermore, participants with unhealthy behavior counts of 3 or more at baseline exhibited a significantly faster rate of eGFR decline compared to those with fewer than 3 unhealthy behaviors (−2.04 vs −1.02 mL/min per 1.73 m² per year; mean difference 0.98 [95% confidence interval (CI) 0.48–1.48], P < 0.001) (Figure 2).

Figure 1 Trend of cumulative unhealthy behavior scores. UH count less than 3; UH count equal or more than 3. Abbreviation: UH, Unhealthy behavior.

Figure 2 Comparison of extrapolation lines represent eGFR decline rate between participants with UH count less than 3 and UH count equal or more than 3. UH count less than 3; UH count equal or more than 3. Abbreviations: UH, Unhealthy behavior; eGFR, estimated Glomerular filtration rate.

Discussion

Previous literature has shown that several unhealthy behaviors can negatively impact the progression of CKD, particularly during its early stages.²⁵ Clinical practice guidelines for CKD management emphasize the crucial role of lifestyle modifications as a fundamental component of treatment.⁶ However, these changes can be difficult for patients to comply with due to various factors including low health literacy, inadequate education programs, and lack of motivation. Therefore, effective CKD management strategies should prioritize patient support and education to facilitate the adoption of healthier behaviors.

The previous ESCORT-1 and ESCORT-2 studies utilized an integrated care approach that combined lifestyle modification into the clinical management of CKD patients.^21,22 This concerted approach involved a HMDT during hospital consultations and a CCNT during home visits. Each team member had a specific set of activities to provide for the patient during each visit. The activities were rotated throughout the year to maintain patient engagement with the advice. The core educational content, however, remained focused on basic CKD knowledge and lifestyle modifications to slow disease progression. The integrated care model incorporated several behavioral change techniques. Regular interviews and home visits provided opportunities for feedback and monitoring. Group education sessions offered instruction on healthy behaviors. Live demonstrations illustrate these behaviors, while home visits facilitated social support.²⁶ In the end, there was a reduced rate of CKD progression among participants in the intervention group who received integrated care. Nevertheless, the extent to which this model effectively modified unhealthy behaviors, and the precise nature of these changes requires further investigation.

Participants who were enrolled in the ESCORT-2 Study were living in rural communities of a province in northern Thailand. They could be representative of typical Thai rural population. This communication addresses seven unhealthy behaviors known to contribute to CKD progression. These behaviors fall into three categories: 1. Medication use-related unhealthy behaviors (usage of analgesics or NSAIDs, and herbal medicine); 2. Unhealthy dietary behaviors (consumption of food items containing moderate to high salt content, and high protein content); and 3. Lifestyle-related behaviors (lack of exercise, and obesity). The baseline prevalence rates of these unhealthy behaviors were largely consistent with those reported in previous studies.²⁵ However, it is noteworthy that the prevalence of being overweight and the use of analgesics or NSAIDs were notably high, reaching 60% and 40%, respectively. In our study, the prevalence of NSAIDs use alone appeared to be lower than what has been reported for the general population in previous studies.²⁷ This is because the inclusion of both analgesic and NSAIDs terminology was utilized to ensure a comprehensive capture of all possible exposures to NSAIDs. In Thai rural areas, people often get NSAIDs from pre-packaged analgesic drugs sold in local pharmacies or grocery stores. If we combine the prevalence of analgesic and NSAIDs use described herein, the overall prevalence becomes higher than what has been previously reported for the general Thai population but is comparable to a previous report of 39% among CKD patients in a rural area of another part of Thailand.¹⁹ This could be attributed to the fact that the population enrolled in this study consisted primarily of agricultural workers engaged in physically demanding jobs. Moreover, the widespread availability of over-the-counter pain-relieving packages containing multiple analgesics and NSAIDs in village-level stores could have facilitated easy access to potentially harmful medications for CKD patients.

The prevalences of these unhealthy behaviors at baseline were analyzed separately for each stage of CKD. A lower prevalence of overweight, NSAID utilization, and physical inactivity was observed among patients with CKD stage 4 when compared to stages 3A and 3B. It is plausible that individuals in this advanced stage of the disease had a heightened understanding of their condition’s seriousness, leading to improved compliance with recommended healthy behaviors.

The present study provides compelling evidence of a substantial decrease in several critical unhealthy behaviors throughout the study duration. Although the improvement of unhealthy behaviors demonstrated variability across different categories, the findings of our study indicate a marked and consistent decrease in medication-usage related unhealthy behaviors. Medication use-related unhealthy behaviors are frequently more amenable to change than other categories of unhealthy behaviors. This is due to factors such as the ability to deliver explicit instructions to the patient and the ease of implementing, monitoring and support systems.

The reduction in dietary-related unhealthy behaviors, while significant and consistent, was less pronounced than the reduction in medication use-related unhealthy behaviors. These results indicate that the integrated care model, while promising, may not be sufficient to ensure consistent adherence to dietary recommendations. The difficulty of implementing dietary interventions in CKD populations is widely acknowledged.²⁸ The formulation of effective strategies to enhance dietary counseling is a complex endeavor, influenced by numerous variables.²⁹ While the integrated care model addresses key factors like group education, live demonstrations, and regular monitoring, incorporating supplementary techniques such as personalized educational sessions, motivational interviewing, and access to affordable healthy food options could significantly enhance the effectiveness of dietary counseling.²⁹

Yet, there was no significant improvement in lifestyle-related behaviors, specifically exercise and weight control. Regular exercise levels improved initially, but a notable decline occurred in the last year of follow-up. This pattern aligns with the expected response to lifestyle modification programs, characterized by an initial period of improvement, followed by a plateau and a subsequent decline. Weight control is a complex process influenced by numerous factors, including dietary intake, physical activity, sleep patterns, stress management, and smoking cessation. Consequently, weight control is often the most challenging lifestyle modification for CKD patients, which is consistent with our findings.

Over a 36-month observation period, we aimed to determine if improvements in unhealthy behaviors were associated with a reduced rate of eGFR decline. Unfortunately, we found that individual improvements in specific unhealthy behaviors did not significantly affect the rate of eGFR decline. This lack of impact may be due to the complex and multifaceted mechanisms that contribute to GFR decline in kidney disease. However, we did observe that individuals with a baseline cumulative score of 3 or more unhealthy behaviors experienced a faster rate of eGFR decline compared to those with a score below 3.

To our knowledge, this is the first longitudinal, prospective observational cohort study of patients with CKD in a primary healthcare setting. This article demonstrates that a structured, integrated care program effectively reduces unhealthy behaviors. The program’s success in slowing the progression of CKD is attributed to a combination of lifestyle modifications and the close control of key clinical and biochemical parameters, as previously shown in our original ESCOR2 study.²² The model is likely to be implemented at a nationwide level. Furthermore, since such program utilized in this study is not a costly or technically advanced intervention, it could be generalized to the other rural communities as well.

The findings of this study must be interpreted with certain limitations. Firstly, the majority of unhealthy behaviors examined in this study were obtained via self-report, a methodology recognized for its potential limitations in terms of accuracy and reliability. Additionally, most of the enrolled patients had only a primary education level, which could introduce qualitative error, especially in their ability to accurately recall information.

Secondly, the questionnaires employed for assessment of dietary intake behavior were designed to be both user-friendly for primary health care personnel and suitable for integration into routine clinical practice. Therefore, the list may not be complete. Several food items were omitted from the questionnaire list. Furthermore, some unhealthy behaviors, such as alcohol consumption and illicit drug use, were not included in our study. Accurately measuring these behaviors in Thailand presents significant challenges, and our intervention was not designed to effectively address them.

Thirdly, information collected by healthcare providers may be biased due to the Hawthorne effect. This occurs when participants who are aware of being observed alter their behavior, often by providing overly positive responses. Finally, it is important to note that we did not collect data on direct outcomes associated with each unhealthy behavior. For example, we did not assess the prevalence of acute kidney injury (AKI) in patients with a history of NSAID use or the correlation between muscle mass and regular exercise.

While this study provides valuable insights, further research is needed to explore the optimal strategies for promoting sustained behavioral change and to elucidate the precise mechanisms by which these changes impact CKD progression. Future studies should consider incorporating more rigorous assessment methods, such as objective measures of dietary intake and physical activity, to enhance the accuracy of data collection. Additionally, exploring the impact of targeted interventions for specific unhealthy behaviors, such as personalized dietary counseling and tailored exercise programs, may yield more significant results.

Conclusion

This study demonstrates the feasibility and effectiveness of an integrated care model in addressing multiple unhealthy behaviors among CKD patients in a primary care setting. The intervention led to significant reductions in medication-related and dietary-related unhealthy behaviors, particularly in the early stages of the study. However, maintaining long-term adherence to lifestyle modifications, especially weight control and physical activity, remains a challenge.

Data Sharing Statement

The data supporting the findings of this study are available from the corresponding author (Teerawat Thanachayanont, [email protected]) upon reasonable request.

Acknowledgments

Preliminary data analysis from this study was presented as a poster at the 25th World Congress of Nephrology in 2019. https://www.kireports.org/article/S2468-0249(19)30449-8/fulltext.

Funding

This study received funding from Bhumirajanagarindra Kidney Institute Hospital, which was not involved in the study’s design, data analysis, or reporting.

Disclosure

The authors declare no conflicts of interest in this work.

References

1. Jager KJ, Kovesdy C, Langham R, Rosenberg M, Jha V, Zoccali C. A single number for advocacy and communication-worldwide more than 850 million individuals have kidney diseases. Nephrol Dial Transplant. 2019;34:1803–1805. doi:10.1093/ndt/gfz174

2. Kovesdy C. Epidemiology of chronic kidney disease: an update 2022. Kidney Int Suppl. 2022;12(1):7–11. doi:10.1016/j.kisu.2021.11.003

3. Ismail H, Abdul Manaf MR, Abdul Gafor AH, Mohamad Zaher ZM, Nur Ibrahim AI. International comparisons of economic burden of end-stage renal disease to the national healthcare systems. IIUM Med J Malays. 2019;18(3):188–196.

4. Yeung E, Bello AK, Levin A, et al. Current status of health systems financing and oversight for end-stage kidney disease care: a cross-sectional global survey. BMJ open. 2021;11(7):1–10. doi:10.1136/bmjopen-2020-047245

5. Nagassawa H, Sugita I, Tachi T, et al. The relationship between dialysis patients’ quality of life and caregivers’ quality of life. Front Pharmacol. 2018;9:1–10. doi:10.3389/fphar.2018.00770

6. Kidney Disease Improving Global Outcomes. KDIGO 2024 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int. 2024;105(4S):S117–S314. doi:10.1016/j.kint.2023.10.018

7. Kittiskulman P, Sripaiboonkij T, Katavetin P, et al. The magnitude of obesity and metabolic syndrome among diabetic chronic kidney disease population: a nationwide study. PLoS One. 2018;13(5):1–14.

8. Ricardo AC, Anderson CA, Yang W, et al. Healthy lifestyle and risk of kidney disease progression, atherosclerotic events, and death in CKD: findings from the Chronic Renal Insufficiency Cohort (CRIC) study. Am J Kidney Disease. 2015;65:412–424. doi:10.1053/j.ajkd.2014.09.016

9. Osman NA, Hassanein SM, Leil MM, NasrAllah MM. Complementary and Alternative medicine use among patients with chronic kidney disease and kidney transplant recipients. J Ren Nutr. 2015;25(6):466–471. doi:10.1053/j.jrn.2015.04.009

10. Tsai MY, Huang YC, Cheng BC, Chin CY, Hsu YT, Lee WC. Prevalence and Varieties of complementary and alternative medicine usage among individuals with pre-dialysis chronic kidney disease in Taiwan: an investigative cross-sectional analysis. BMC Complentary Med Ther. 2024;24:1–11.

11. Tangkiatkumjai M, Boardman H, Praditpornsilpa K, Walker DM. Prevalence of herbal and dietary supplement usage in Thai outpatients with chronic kidney disease: a cross-sectional survey. BMC Complementary Alternative Med. 2013;13:1–9. doi:10.1186/1472-6882-13-153

12. Mohammadi S, Asghari G, Emami-Naini A, Mansourian M, Badri S. Herbal supplement use and herb–drug interactions among patients with kidney disease. J Res Pharm Pract. 2020;9(2):61–67. doi:10.4103/jrpp.JRPP_20_30

13. Ingsathit A, Thakkinstian A, Chaiprasert A. Prevalence and risk factors of chronic kidney disease in the Thai adult population: Thai SEEK study. Nephrol Dial Transplant. 2010;25:1567–1575. doi:10.1093/ndt/gfp669

14. Tangkiatkumjai M, Boardman H, Praditpornsilpa K, Walker DM. Reasons why Thai patients with chronic kidney disease use or do not use herbal and dietary supplements. BMC Complementary Alternative Med. 2014;14:473. doi:10.1186/1472-6882-14-473

15. Yang B, Xie Y, Guo M, Rosner MH, Yang H, Ronco C. Nephrotoxicity and Chinese herbal medicine. Clin J Am Soc Nephrol. 2018;12:1605–1611. doi:10.2215/CJN.11571017

16. Kilis-Pstrusinska K, Wiela-Hojenska A. Nephrotoxicity of herbal products in Europe-a review of an underestimated problem. Int J Mol Sci. 2021;22:4132. doi:10.3390/ijms22084132

17. Nderitu P, Doos L, Jones PW, Davies SJ, Kadam UT. Non-steroidal anti-inflammatory drugs and chronic kidney disease progression: a systematic review. Fam Pract. 2013;30(3):247–255. doi:10.1093/fampra/cms086

18. Armstrong MJ, Zhang K, Ye F, Klarenbach SW, Pannu NI. Population-based analysis of nonsteroidal anti-inflammatory drug prescription in subjects with chronic kidney disease. Can J Kidney Health Dis. 2023;10:1–10. doi:10.1177/20543581221149621

19. Cha’on U, Tippayawat P, Sae-ung N, et al. High prevalence of chronic kidney disease and its related risk factors in rural areas of Northeast Thailand. Sci Rep. 2022;12:1–11.

20. Jiamjariyapon T, Ingsathit A, Pongpirul K, et al. Effectiveness of integrated care on delaying progression of stage 3–4 chronic kidney disease in rural communities of Thailand (ESCORT study): a cluster randomized controlled trial. BMC Nephrol. 2017;18:83. doi:10.1186/s12882-016-0414-4

21. Thanachayanont T, Chanpitakkul M, Hengtrakulvenit J, et al. Effectiveness of integrated care on delaying chronic kidney disease progression in rural communities of Thailand (ESCORT-2) trials. Nephrology. 2021;26:333–340. doi:10.1111/nep.13849

22. Sunpuwan M, Punpuing S, Jaruruengpaisan W, Kinsman J, Wertheim H. What is in the drug packet?: access and use of non-prescribed poly-pharmaceutical packs (Yaa Chud) in the community in Thailand. BMC Public Health. 2019;19(1):971. doi:10.1186/s12889-019-7300-5

23. Thanachayanont T, Chanpitakkul M, Saetie A, Lekagul S, Tungsanga K. Correlation of the dietary protein intake between those estimated from a short protein food-recall questionnaire and from 24-hour urinary urea-nitrogen excretion in stages 3–4 chronic kidney disease patients. Intl J Nephrol. 2023;2023:1–8. doi:10.1155/2023/9713045

24. WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157–163. doi:10.1016/S0140-6736(03)15268-3

25. Schrauben SJ, Apple BJ, Chang AR. Modifiable lifestyle behaviors and CKD progression: a narrative review. Kidney 360. 2022;3:752–778. doi:10.34067/KID.0003122021

26. Evangelidis N, Craig J, Bauman A, Manera K, Saglimbened V, Tong A. Lifestyle behaviour change for preventing the progression of chronic kidney disease: a systematic review. BMJ Open. 2019;9:1–15. doi:10.1136/bmjopen-2019-031625

27. Phueanpinit P, Pongwecharak J, Krsk J, Jarernsiripornkul N. Evaluation of community pharmacists’ roles in screening and communication of risks about non-steroidal anti-inflammatory drugs in Thailand. Prim Health Care Rev Dev. 2018;19:598–604. doi:10.1017/S1463423618000142

28. Lambert K, Mansfield K, Mullan J. How do patients and carers make sense of renal dietary advice. A qualitative exploration. J Ren Care. 2018;44:238–250. doi:10.1111/jorc.12260

29. Pereira RA, Alvarenga MS, Avesani CM, Cuppari L. Strategies designed to increase the motivation for and adherence to dietary recommendations in patients with chronic kidney disease. Nephrol Dial Transplant. 2021;36:2173–2181. doi:10.1093/ndt/gfaa177

He added, “In some people, due to less levels of the lactase enzyme in the small intestine, it becomes difficult for the body to digest the sugar (known as, lactose) present in milk and dairy products, this inability is known as lactose intolerance.”

Is lactose intolerance similar to milk allergy?

“Unlike milk allergy (an immune-mediated reaction), lactose intolerance is not life-threatening but can cause significant discomfort and affect dietary quality and variety,” the gastroenterologist explained.

Lactose intolerance symptoms:

The doctor noted the symptoms of lactose intolerance that usually start to appear within 30 minutes to 2 hours of consuming lactose. “These may include bloating, abdominal distension, loose stools or diarrhoea, excessive gas, abdominal cramps or pain, and occasionally nausea or vomiting. In children, it can present as recurrent abdominal pain, irritability, or refusal to drink milk.”

Nutritional alternatives to lactose:

1. Plant-based milks: For anyone avoiding cow’s milk, plant-based options like soy, oat, almond, and pea milk can be excellent choices. The key is to pick versions that are fortified with calcium and vitamin D, since these nutrients are vital for strong bones and healthy growth. Soy and pea milks are the most similar to cow’s milk in terms of nutrition, especially protein, making them good everyday replacements. Almond and oat milks are lighter, but still useful if included alongside other protein-rich foods. Also read | Are you lactose intolerant? Doctor says, it’s different from being allergic to dairy

2. Calcium sources: Calcium doesn’t have to come only from milk. Foods like tofu, ragi (finger millet), sesame seeds, almonds, and leafy greens all contribute to bone health. For children and adults alike, including these in daily meals helps build a balanced, nourishing diet. Traditional foods such as ragi porridge or millet rotis are naturally rich in calcium, while sesame paste (tahini) or a handful of almonds can make easy, healthy snacks.

3. Vitamin D: Even with good calcium intake, bones cannot stay strong without enough vitamin D. Sunlight is a natural source, but lifestyle, weather, or skin sensitivity often limit exposure. For this reason, many people, especially children, may need supplements after medical advice. Vitamin D also helps reduce the risk of bone weakness later in life, making it an important part of daily nutrition.

4. Protein sources: Milk is a natural protein source, but if it’s avoided, it’s important to make up for it with other foods. Soy milk and pea-protein drinks are excellent substitutes, as they provide good quality protein. For those who prefer almond or oat milk, pairing them with foods like pulses, lentils, chickpeas, or tofu ensures the diet remains well-balanced. Also read | Dietician explains if lactose-intolerant people are missing out on calcium; suggests 5 alternatives for dairy-free diet

Note to readers: This article is for informational purposes only and not a substitute for professional medical advice. Always seek the advice of your doctor with any questions about a medical condition.

Introduction

Vaccination is one of the key strategies for preventing pediatric diseases, which has contributed to a 24% global decrease in the death rate for children under five.¹ The primary aim of vaccination is to stimulate the immune system’s response against infection and stop the development of serious diseases in childhood by ensuring adequate immunization coverage.²

The World Health Organization (WHO) has advised against delays or disruptions in immunization services. Despite this recommendation and the efforts of the Ministry of Health to inform the population, it was discovered that 26% of parents in Saudi Arabia did not vaccinate their children on schedule following the national immunization guidelines under normal circumstances.³

The Saudi national immunization program began in 1979, initially focusing on diphtheria, tetanus, and pertussis (DTP) and later expanding to include other vaccines. Vaccination is mandatory for school entry, contributing to high coverage rates (98% for DTP and MMR in 2019).⁴ This school requirement can be an effective strategy for ensuring high immunization rates.⁵

The primary and most important individuals who make decisions about children’s health are their parents. They are the only ones who can drive and significantly promote the implementation of full immunization programs and higher compliance rates. They can experience “vaccine hesitancy”, which is the reluctance or postponement of receiving vaccinations, even in the presence of immunization services.⁶ There are several reasons for this, such as socioeconomic or religious beliefs, a lack of confidence in the healthcare system, worries about the safety of the vaccines, and their possible relation to the development of other diseases like autism.^7–9 It is believed that concerns regarding vaccinations are one of the primary reasons for their underutilization. A prior study carried out in Jeddah, Saudi Arabia, found a link between vaccine hesitancy and parents’ awareness.¹⁰

Due to the lack of awareness, many parents underestimate the danger of diseases while overestimating vaccine risks.⁸ A study conducted in Saudi Arabia by Alaamri et al found that 43% of participants expressed some concern about the safety of childhood vaccine doses, while another 43% were somewhat worried about the effectiveness of these doses in preventing diseases.¹¹

Even in cases with high vaccination coverage, assessing parental knowledge and attitude about vaccinations is greatly important, as they affect their children’s vaccination status. The presence of any parental misconceptions or uncertainties may represent a possible future obstacle to obtaining widespread vaccine adoption and adherence. Also, this can be considered as a part of proactive action by authorities, tailoring long-term interventions to improve the uptake, maintain the high vaccination coverage, and prevent outbreaks.¹² Many studies in Saudi Arabia explored knowledge, attitudes, and practices regarding childhood vaccination among parents, but showed a wide discrepancy in results between different regions. To the best of our knowledge, this is the first study in Tabuk City, Saudi Arabia, to determine parental knowledge and attitude about childhood vaccination as well as address their perceived barriers to vaccination.

Materials and Methods

Study Design and Setting

The study was cross-sectional and took place in Tabuk, Saudi Arabia, over three months, from the end of December 2024 to the end of March 2025.

Participants

Sample Size Calculation

It was calculated by the OpenEpi online calculator, version 3, based on a 95% confidence interval, 80% power, and a prior study by Alshammari et al (2021)⁷ in Riyadh, KSA, which indicated that 73.3% of the parents knew a lot about childhood vaccinations. The estimated sample size was 301 parents, and 10% was added for failure to respond; hence, there will be 330 parents in all.

Sampling Technique

In order to satisfy the participation requirements, a convenience sample was obtained from the parents who went to various primary healthcare facilities to vaccinate their children.

Inclusion and Exclusion Criteria

The eligible participants were the parents who attended several primary healthcare facilities to vaccinate their children and had at least one kid, were willing to give their informed consent to participate in the study, or could read, comprehend, and complete the study survey in Arabic. Those who do not live in the designated geographic area (Tabuk City) or who are not the children’s primary guardians (such as neighbors or family) will be excluded.

Research Tools

After receiving permission to use the valid questionnaire from a prior study of a similar nature,⁷ it was given to the participants. It had a Cronbach alpha greater than 0.7 for the knowledge and attitude scores. The first section of the questionnaire assessed the parents’ sociodemographic information, including their age, gender, place of residence, level of education, occupation, and number of children. It also collected data on the sources of their information about vaccinations, offering four options: from friends and family, social media, doctors, or attending a health session. Ten statements on a three-point Likert scale, with the choices being “I do not know”, “No”, and “Yes”, made up the second section, which assessed their understanding of childhood vaccinations. The code one was assigned to the right response and zero to the incorrect response. Then, the third segment was composed of 10 questions about the parents’ opinions on childhood immunizations using a five-point Likert scale ranging from strongly agree to disagree strongly. The median for knowledge and attitude total scores was used as the cutoff criterion to divide scores into inadequate knowledge or negative attitude (<50%) and adequate knowledge or positive attitude (≥50%). Lastly, yes/no questions about parents’ compliance with childhood vaccination and their perceived obstacles to vaccination were asked.

Ethics Approval and Consent to Participate

“All procedures carried out in studies involving human participants were following the 1964 Helsinki Declaration and its subsequent amendments or comparable ethical standards”. The University of Tabuk’s Local Research Ethics Committee (LREC) in Tabuk, Saudi Arabia, granted ethical approval for the study with reference number UT-486-265-2024. An anonymous questionnaire was used to collect data; each participant was asked for their informed consent on the first page of the questionnaire, which also included a description of the study’s goal and a confirmatory statement about the confidentiality of the data gathered.

Statistical Analysis

Statistical package for social sciences (SPSS) version 23.0 was used to analyze the data. The quantitative and qualitative variables were described using descriptive statistics by mean, standard deviation (SD), and percentages. The Chi-square test was used to examine the relationship between parents’ sociodemographic (the independent factors) and their knowledge and attitude scores (dependent variables). When cells with expected value less than 5, Fisher’s exact probability test was applied. To determine the factors associated with parents’ knowledge and attitudes on vaccinations, multiple binary logistic regression was conducted with the “enter” method, as a model selection technique. The relationship between attitude and total knowledge scores was examined using the Pearson correlation coefficient. A p-value of less than 0.05 was regarded as statistically significant.

Results

Three hundred and thirty parents were included in this study. Their age ranged from 20 to 60 years old, with 79.7% of them being between 30 and less than 50 years old. 80.3% were mothers, and 94.5% lived in Tabuk City. Regarding the educational level, the majority (73.9%) were at the university level. 42.4% of the studied parents had more than three children. 89.4% of them worked in occupations not related to the health sector. Most of them (71.2%) received information about childhood vaccination from family and friends, while others learned from doctors or attended health sessions or social media (14.2%, 9.7%, or 4.8%, respectively) [Table 1].

Of the 330 parents who participated in the study, 218 (66.1%) had adequate knowledge about children’s vaccination when their scores were categorized using the median [Table 1].

When compared to parents with inadequate information, the parents with acceptable knowledge were between the ages of 30 and 40 (56.9% versus 45.5%; P<0.05). On the other hand, fewer parents in the 20–30 age range had sufficient knowledge (11.0% versus 23.2%; P<0.05). Additionally, all illiterate parents had an inadequate level of knowledge, and 80.3% of those with adequate knowledge had a university education compared to 61.6% of those with inadequate knowledge. Compared to parents who did not work in the health sector, those who did had better adequate knowledge (13.3% versus 5.4%; P<0.05). In contrast to parents who had inadequate knowledge, the parents who knew enough about childhood vaccinations were more likely to get information from doctors and health sessions (17.9% and 11.9% versus 7.1% and 5.4%, respectively) than from friends and family (64.2% versus 84.8%, P<0.05) [Table 1].

By classifying the parents’ attitude scores using the median, the study revealed that 183 (55.5%) of the 330 parents had a positive attitude [Table 2].

Table 2 The Relationship Between Attitude Score Categories and Sociodemographic Characteristics of the Studied Parents in Tabuk, Saudi Arabia, 2024–2025

Parents who had a positive attitude were more likely to be between the ages of 30 and 40 than parents who had a negative attitude (60.1% versus 44.2%; P<0.05), and fewer were older than 50 (3.8% versus 6.8%; P<0.05). While 82.0% of parents with a positive attitude had a university degree, 63.9% of parents with a negative attitude had this degree (P<0.05). Parents who worked in the medical field showed more positive attitudes than those who had negative attitudes (15.8% compared to 4.1%; P<0.05), as did parents who learned about children’s vaccinations from medical professionals and health sessions (20.2% and 16.4% versus 6.8% and 1.4%, respectively). On the other hand, more people with negative attitudes got their knowledge from friends and family than those with positive attitudes (86.4% versus 59.0%, P<0.05) [Table 2].

In terms of binary logistic regression, those between the ages of 30 and <40 and 40 and <50 had considerably higher adequate knowledge, with 2.6 (OR with 95% CI: 2.6 with 1.3–5, P<0.05) and 2.3 (OR with 95% CI: 2.3 with 1.1–4.7, P<0.05) years, respectively. University-educated parents were twice as knowledgeable (OR with 95% CI: 2.1 with 1.6–2.8, P<0.05), and those who worked in the medical field were 2.7 times more knowledgeable (OR with 95% CI: 2.7 with 1.1–6.7, P<0.05). However, those between the ages of 30 and under 40 (OR with 95% CI: 2.3 with 1.2–4.4, P<0.05) and those with a university education (OR with 95% CI: 1.7 with 1.3–2.3, P<0.05) exhibited a statistically significant positive attitude and were about twice as positive as others. The positive attitude of those working in the medical field was four times higher than that of those in other occupations (OR with 95% CI: 4.4 with 1.7–10.9, P<0.05). Additionally, parents who received information about vaccinations from doctors were 15 times more likely to have a positive attitude (OR with 95% CI: 15 with 2.6–85, P<0.05) and from health sessions approximately four times (OR with 95% CI: 3.7 with 1.1–12.3, P<0.05) [Table 3].

Table 3 Multiple Binary Logistic Regression to Detect Associated Factors of Good Knowledge and Attitude Scores Among the Studied Parents in Tabuk, Saudi Arabia, 2024–2025

In this research, the higher the level of knowledge score among the studied parents, the greater their attitude score (r = 0.603, P < 0.05) [Table 4].

Table 4 The Correlation Between Knowledge and Attitude Scores of the Studied Parents in Tabuk, Saudi Arabia, 2024–2025

The percentage of participants who complied with the immunization schedule was 62.9% [Figure 1a]. Their perceived obstacles to immunization were the child’s illness (32.8%), a family member’s sickness (36.7%), being occupied on the day of vaccination (31.4%), fear regarding the side effects of the vaccine (21.9%), or being unaware of the next dose (6.8%) [Figure 1b].

Figure 1 The compliance with childhood vaccination and the perceived barriers to vaccination among the studied parents in Tabuk, Saudi Arabia, 2024–2025.

Discussion

As a cost-effective intervention for promoting children’s health, vaccination has been recognized as one of the most significant public health accomplishments, lowering morbidity and mortality from related vaccine-preventable diseases.¹³ Increasing the vaccine coverage rate and parents’ adherence to the vaccination schedule depends heavily on parental awareness and attitude toward childhood vaccinations, which will be reflected in the long-term incidence and prevalence of major childhood infectious diseases.¹² The purpose of this study was to ascertain the knowledge and attitudes of parents in Tabuk, Saudi Arabia, about childhood vaccinations as well as address their perceived barriers to vaccination.

The current study’s findings indicate that 66% of participants knew adequately about vaccinations for their children. The results are greater than those of research in Indonesia,¹⁴ where only roughly half of the participants had adequate knowledge, but they are nearly consistent with similar studies carried out in Malaysia,¹⁵ Cyprus,¹⁶ Rwanda,¹⁷ and Saudi Arabia.^7,10,11,18 Even though we would prefer to find higher levels of parental knowledge, the reported medium-degree level of knowledge is more important and preferable than being unaware of the health advantages of vaccinations in preventing infectious diseases in children, which is linked to low vaccination coverage rates.¹⁹ Also, the study’s findings are an important reflection of the policies and practices that Saudi Arabia’s Ministry of Health has put in place concerning the country’s immunization program in recent years.

It’s documented that children’s immunization status is significantly impacted by parents’ attitudes.²⁰ The results of this study showed that slightly more than half of the participants had a positive attitude. This acceptable attitude is thought to be a reflection of the level of adequate knowledge. This is consistent with other comparable investigations.^7,21,22

Parents’ attitudes toward vaccinating their children and their level of knowledge were found to be significantly positively correlated in this study. It demonstrates that the commitment to getting their children vaccinated increases with their level of knowledge. A research study in Malaysia reported a similar finding.¹⁵

The participating parents, who were middle-aged, had significantly adequate knowledge and positive attitudes toward vaccination. This is similar to a study conducted in Saudi Arabia,⁷ while contradictory to the study conducted in Malaysia,¹⁵ which found parents with younger age groups had higher knowledge and better attitudes. The difference between the studies’ results may be due to differences in the characteristics of the participants as well as the abundance of vaccination centers and easy and free access to vaccination services in Saudi Arabia.

It was proposed that mothers’ academic standing had a major impact on their decisions to vaccinate their children.¹⁵ As demonstrated by the current study, the majority of parents with higher levels of knowledge and attitude held a university degree. This is consistent with previous similar studies carried out in Rwanda,¹⁷ Saudi Arabia,¹⁸ and Malaysia,²¹ but it differs from another study conducted in Malaysia that discovered no significant association between parents’ educational backgrounds and the decision to vaccinate their children.²³ This might be because parents with higher education levels are more likely than parents with lower education levels to be health literate, to recognize, understand, and apply health-related information, and to recognize the importance of children’s vaccinations and appropriate medical procedures.²⁴

Parents who worked in occupations related to the healthcare sector had significantly higher levels of adequate knowledge and positive attitudes regarding vaccination compared to those who did not work in healthcare. This is comparable to an investigation conducted in Malaysia, in which the medical professionals’ opinions and attitudes toward vaccines were more favorable than non-healthcare professionals.²¹ The present finding is important, as healthcare workers are the key to the success of the healthcare system in improving population health in any community; if they have inaccurate knowledge about vaccinations, this can lead to vaccine hesitancy and a negative attitude toward vaccinations among the public.^25–27

Our findings reflect the assumption that parents’ knowledge and subsequent attitude and behavior are primarily based on the proficiency of medical professionals who recommend and advise the immunizations.²⁸ The majority of parents with higher levels of knowledge and attitudes significantly get their trusted information on vaccinations from their children’s doctors and health personnel and health sessions, emphasizing the healthcare providers’ ability to influence parental knowledge and choices and reassure them about the safety of vaccines. Our results are in line with those of several earlier investigations.^16,29,30 These highlight how important doctors are in providing up-to-date, evidence-based vaccine information and helping parents decide whether to vaccinate their children.

A prior study in Jordan found that mothers who got their immunization information from medical personnel knew more about vaccinations than mothers who got their information from other sources, such as websites, mass media, friends, and family. Other sources can provide inaccurate information, which will create a negative attitude and eventually result in the underutilization of vaccinations.³¹

More than half of the parents who took part in the study were complied to the vaccine schedule, which is consistent with other studies.^32,33 Nonetheless, the Ministry of Health’s contribution is clear in the fact that childhood vaccinations are accessible without requiring payment or transportation. There were still some instances of non-compliance brought on by a lack of awareness or a negative attitude, such as not knowing the timetable or being afraid of its negative effects. This is consistent with another study conducted in Saudi Arabia by Bin Alamir (2024), who discovered that the main obstacle to vaccination compliance was vaccine hesitancy.³⁴ The same findings were seen in other studies conducted in Iraq³² and India,³³ but there were other explanations, such as vaccination unavailability, travel difficulties, or budgetary constraints.

Strengths and Limitations

This study is, as far as we are aware, the first research that provides insightful information about parents’ awareness and attitude toward childhood vaccinations in Tabuk, Saudi Arabia, and their perceived vaccination barriers, which can guide future investigations and programs. However, some limitations were recognized; since this study was cross-sectional, it’s difficult to conclude the causal relationships between various underlying factors and parents’ knowledge or attitudes. Additionally, selection bias may cause the odds ratio (OR) to not accurately reflect the true prevalence ratio (PR). Multivariate analysis, which is used to control for confounding, was attempted to be used to overcome this and assist in minimizing these constraints by adjusting for potential confounders. Among the limitations of this study is that the results cannot be generalized to all Saudi Arabian parents because of the convenience sampling method and the fact that it was conducted in just one Saudi Arabian city.

Practical Implications

There are numerous significant implications of this study. Ministry of Health and policymakers should create a vaccination communication plan targeting parents who exhibit low knowledge attitude levels reflected in their practice regarding vaccine utilization, considering the factors that contribute to these situations, to maintain and increase the immunization rate. Open communication between physicians and parents will help to raise understanding about vaccine safety and the significance of immunization by eliminating vaccine myths and rumors, clearing up false information, and scientifically addressing vaccine safety concerns. Such approaches aim to build confidence in children’s vaccination. The Ministry of Health requires new, more advanced communication methods, such as social media and social marketing technologies, and an internet channel could be initiated to be used by nurses and other medical professionals to spread accurate information and emphasize the advantages of vaccination on the national level.

Conclusions

More than half of the parents in the study had favorable attitudes and sufficient knowledge about children’s vaccinations. These parents were middle-aged, university-educated, had occupations in the health sector, and primarily relied on doctors for information. The most common vaccine barriers among the parents surveyed were being busy on the day of the vaccination and a family member’s illness.

To ascertain the relationship between parental attitudes and knowledge and children’s immunization behavior, more studies are necessary. Additionally, it is recommended that further longitudinal studies be performed to prove the predictors of parents’ knowledge and attitudes regarding children’s vaccinations. Myths and false information about vaccines can be dispelled by collaboration between doctors, parents, public health experts, governments, and civil society. It is essential to promote awareness initiatives that highlight the importance, efficacy, and safety of childhood vaccinations.

Data Sharing Statement

Available from the corresponding author upon request.

Acknowledgments

We extend our gratitude to Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2025R90), Princess Nourah Abdulrahman University, Riyadh, Saudi Arabia. Also, a heartfelt thanks to the parents who took the time to offer their precious perspective.

Author Contributions

All authors made a significant contribution to the work reported, whether that is in the conception, study design, execution, acquisition of data, analysis and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.

Funding

This research was funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2025R90), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Disclosure

The authors declare no conflict of interest.

References

1. Vassiliki P, Ioanna K, Artemis V, et al. Determinants of vaccination coverage and adherence to the Greek national immunization program among infants aged 2-24 months at the beginning of the economic crisis (2009-2011). BMC Public Health. 2014;14:1192. doi:10.1186/1471-2458-14-1192

2. World Health Organization (WHO). Vaccines and immunization. Available from: https://www.who.int/health-topics/vaccines-and-immunization#tab=tab_1. Accessed February 22, 2025.

3. Al-Nafeesah AS, Aldamigh AS, Almansoor BA, Al-Wutayd O, AlE’ed AA. The impact of the COVID-19 pandemic on parents’ behavior toward scheduled pediatric vaccinations in Saudi Arabia. Infect Dev Ctries. 2021;15(8):1054–1058. doi:10.3855/jidc.13765

4. Alsubaie SS, Gosadi IM, Alsaadi BM, et al. Vaccine hesitancy among Saudi parents and its determinants. Result from the WHO SAGE working group on vaccine hesitancy survey tool. Saudi Med J. 2019;40(12):1242–1250. doi:10.15537/smj.2019.12.24653

5. Shaw J, Mader EM, Bennett BE, Vernyi-Kellogg OK, Yang YT, Morley CP. Immunization mandates, vaccination coverage, and exemption rates in the United States. Open Forum Infect Dis. 2018;5(6):ofy130. doi:10.1093/ofid/ofy130

6. Alamer F, Alamir A, AlJohani S, et al. Childhood vaccination hesitancy in Saudi Arabia: a time for action. J Infect Public Health. 2022;15(1):94–99. doi:10.1016/j.jiph.2021.11.009

7. Alshammari SZ, AlFayyad I, Altannir Y, Al-Tannir M. Parental awareness and attitude about childhood immunization in riyadh, saudi arabia: a cross-sectional study. Int J Environ Res Public Health. 2021;18(16):8455. doi:10.3390/ijerph18168455

8. Oldfield BJ, Stewart RW. Common misconceptions, advancements, and updates in pediatric vaccination administration. South Med J. 2016;109(1):38–41. doi:10.14423/SMJ.0000000000000399

9. Koslap-Petraco M. Vaccine hesitancy: not a new phenomenon, but a new threat. J Am Assoc Nurse Pract. 2019;31(11):624–626. doi:10.1097/JXX.0000000000000342

10. Alghamdi AA, Alghamdi HA. Knowledge, attitude, and practice of vaccination among parents in Jeddah City, Saudi Arabia. Cureus. 2023;15(7):e41721. doi:10.7759/cureus.41721

11. Alaamri O, Okmi EA, Suliman Y. Vaccine hesitancy in Saudi Arabia: a cross-sectional study. Trop Med Infect Dis. 2022;7(4):60. doi:10.3390/tropicalmed7040060

12. Santos CA, Costa RD, Silva JL, Santos MD, Gomes BL. Conhecimento, atitude e prática dos vacinadores sobre vacinação infantil em Teresina-PI, 2015 [Knowledge, attitude and practice on childhood immunization personnel in Teresina-PI, Brazil, 2015]. Epidemiol Serv Saude. 2017;26(1):133–140. doi:10.5123/S1679-49742017000100014

13. Bedford H, Elliman D. Concerns about immunisation. BMJ. 2000;320(7229):240–243. doi:10.1136/bmj.320.7229.240

14. Elbert B, Zainumi CM, Pujiastuti RAD, et al. Mothers’ knowledge, attitude, and behavior regarding child immunization, and the association with child immunization status in Medan City during the COVID-19 pandemic. IJID Reg. 2023;8:S22–6. doi:10.1016/j.ijregi.2023.03.014

15. Makhdzir N, Rashid A, Pien LS, Zaini NH. Mothers’ knowledge on immunization and the commitment to get their child immunized in a Suburban Region of Selangor, Malaysia. Int J Care Scholars. 2024;7:76–84. doi:10.31436/ijcs.v7i3.375

16. Kyprianidou M, Tzira E, Galanis P, Giannakou K. Knowledge of mothers regarding children’s vaccinations in Cyprus: a cross-sectional study. PLoS One. 2021;16(9):e0257590. doi:10.1371/journal.pone.0257590

17. Mbonigaba E, Yu F, Reñosa MDC, et al. Knowledge and trust of mothers regarding childhood vaccination in Rwanda. BMC Public Health. 2024;24(1):1067. doi:10.1186/s12889-024-18547-1

18. Almutairi WM, Alsharif F, Khamis F, et al. Assessment of mothers’ knowledge, attitudes, and practices regarding childhood vaccination during the first five years of life in Saudi Arabia. Nurs Rep. 2021;11(3):506–516. doi:10.3390/nursrep11030047

19. Balbir Singh HK, Badgujar VB, Yahaya RS, et al. Assessment of knowledge and attitude among postnatal mothers towards childhood vaccination in Malaysia. Hum Vaccin Immunother. 2019;15(11):2544–2551. doi:10.1080/21645515.2019.1612666

20. Dyda A, King C, Dey A, Leask J, Dunn AG. A systematic review of studies that measure parental vaccine attitudes and beliefs in childhood vaccination. BMC Public Health. 2020;20(1):1253. doi:10.1186/s12889-020-09327-8

21. Mukhtar AF, Abdul Kadir A, Mohd Noor N, Mohammad AH. Knowledge and attitude on childhood vaccination among healthcare workers in hospital Universiti Sains Malaysia. Vaccines. 2022;10(7):1017. doi:10.3390/vaccines10071017

22. Kumar P, Kavinprasad MA. study to assess the parent’s knowledge and attitudes on childhood immunization. Int J Commun Med Public Health. 2018;5:4845. doi:10.18203/2394-6040.ijcmph20184582

23. Ahmad NA, Jahis R, Kuay LK, Jamaluddin R, Aris T. Primary Immunization among children in Malaysia: reasons for incomplete vaccination. J Vaccines Vaccin. 2017;8:358. doi:10.4172/2157-7560.1000358

24. Csima M, Podráczky J, Keresztes V, Soós E, Fináncz J. The role of parental health literacy in establishing health-promoting habits in early childhood. Children. 2024;11(5):576. doi:10.3390/children11050576

25. Verger P, Fressard L, Collange F, et al. Vaccine hesitancy among general practitioners and its determinants during controversies: a national cross-sectional survey in France. EBioMedicine. 2015;2(8):891–897. doi:10.1016/j.ebiom.2015.06.018

26. Karafillakis E, Dinca I, Apfel F, et al. Vaccine hesitancy among healthcare workers in Europe: a qualitative study. Vaccine. 2016;34(41):5013–5020. doi:10.1016/j.vaccine.2016.08.029

27. Elizondo-Alzola U, Carrasco G, Pinós M, L PCA, Rius C, Diez E. Vaccine hesitancy among paediatric nurses: prevalence and associated factors. PLoS One. 2021;16(5):e0251735. doi:10.1371/journal.pone.0251735

28. Larson Williams A, Mitrovich R, Mwananyanda L, Gill C. Maternal vaccine knowledge in low- and middle-income countries-and why it matters. Hum Vaccin Immunother. 2019;15(2):283–286. doi:10.1080/21645515.2018.1526589

29. Gellin BG, Maibach EW, Marcuse EK. Do parents understand immunizations? A national telephone survey. Pediatrics. 2000;106:1097–1102. doi:10.1542/peds.106.5.1097

30. Šeškutė M, Tamulevičienė E, Levinienė G. Knowledge and attitudes of postpartum mothers towards immunization of their children in a Lithuanian tertiary teaching hospital. Medicina. 2018;54(1):2. doi:10.3390/medicina54010002

31. Masadeh MM, Alzoubi KH, Al-Azzam SI, Al-Agedi HS, Abu Rashid BE, Mukattash TL. Public awareness regarding children vaccination in Jordan. Hum Vaccin Immunother. 2014;10(6):1762–1766. doi:10.4161/hv.28608

32. Abdullah S, Mustafa I. Knowledge and attitude of mothers about children immunization and barriers to adherence the program, in Erbil City. Erbil J Nurs Midwifery. 2022;5(1):51–60. doi:10.15218/ejnm.2022.06

33. Jelly P, Jeenwal N, Kumari N, et al. Knowledge, attitude, compliance and barriers of immunization among Parents’ of under-five children. Int J Africa Nurs Sci. 2023;19:100608. doi:10.1016/j.ijans.2023.100608

34. Bin Alamir AA. Childhood vaccination hesitancy in Saudi Arabia: are we still facing a problem? Saudi Med J. 2024;45(6):551–559. doi:10.15537/smj.2024.45.6.2024011