Abstract

Objectives: Diabetes knowledge among kidney transplant recipients with posttransplant diabetes has not been exhaustively assessed. Here, we evaluated the effects of structured diabetes education on development of diabetic micro- and macroangiopathies in kidney transplant patients with posttransplant diabetes.
Materials and Methods: This prospective randomized controlled study categorized 210 renal transplant patients with posttransplant diabetes mellitus into 2:1 groups according to type of diabetes education. Group 1 (n = 140) received structured education, and group 2 (n = 70) received conventional education. Patient data were collected through patient identification and metabolic control parameter forms.
Results: Most patients in groups 1 and 2, respectively, were Kuwaiti (60.7% vs 58.6%), men (57.9% vs 68.6%), and had high school-level education (43.6% vs 48.6%). Chronic glomerulonephritis was the original disease in 36.4% versus 35.4% of patients. Most patients (72.8% vs 78.6% in group 1 vs 2) received pretransplant hemodialysis. At study start, the rate of patients with diabetic neuropathy was comparable between groups (32.4% vs 27.9%). Moreover, after completion of 24 months of education, neurological evaluation by electromyograph and nerve conduction studies did not show any significant differences between the groups (P > .05). Similarly, the number of patients with fundus imaging showing retinopathy was comparable between groups at start and end of study (P > .05). Although macroangiopathic events were higher in group 1, this finding was not significant (P > .05). However, although the percentage of patients with nephropathy was comparable in both groups at start of study, the percentage decreased significantly in group 1 at 24 months after completion of education compared with group 2 and baseline value (P = .016).
Conclusions: Structured diabetes education was associated with reduced diabetic nephropathy but had no significant effects on other micro- or macroangiopathies. However, we recommend education for all kidney transplant recipients with diabetes.

Key words : Macroangiopathy, Microangiopathy, Renal transplant

Introduction

Diabetes is a chronic irreversible disease that directly affects individuals of all ages and their relatives. It brings a heavy economic burden, affects self-care activities, and shortens life expectancy due to chronic complications.^1,2

The incidence of diabetes ranges from 3% to 6%, and the number of patients with diabetes will be more than 300 million by 2025. The number of people with diabetes rose from 108 million in 1980 to 422 million in 2014. Approximately 20% of people who are 65 years of age or older have diabetes. Diabetes incidence is expected to increase by 165% in the next 50 years.^3,4 It is estimated that there are 17 million people with diabetes in the United States and that approximately 14.5 million of this population have type 2 diabetes. Diabetes prevalence increases with age, with 9% prevalence around age 20 years and more than 20% prevalence at age of 70 years and over.⁵

Diabetes is a chronic disease that requires lifelong self-care behavior.¹ Successful treatment of chronic diseases is closely associated with the education of both patients and their relatives.⁶ Patient education is one of the most important responsibilities of nurses. In the management of diabetes, helping patients improve their health and quality of life is considered an essential aspect of diabetes self-care education.⁷

The aim of self-care, a universal concept for maintaining and improving health, is to enable the individual to take all responsibilities regarding their health.⁸ Self-care constitutes 98% of diabetes care. To control their disease, diabetic patients need to adopt self-care activities, such as maintaining an appropriate diet, performing regular exercises, practicing control of blood glucose, appropriately using oral antidiabetics, having awareness of the effects and possible side effects of insulin treatment, avoiding alcohol use and smoking, preventing complications of diabetes, and having compliance with life-long medication use.⁹ With adoption of a healthy way of life, diabetes can be prevented or delayed, resulting in 44% to 58% risk reduction.¹⁰ In a meta-analysis on diabetes, education on exercise was reported to decrease glycated hemoglobin (HbA1c) levels of patients with type 2 diabetes.¹¹

According to the World Health Organization, education is the keystone of diabetes treatment and has a vital role in integrating diabetes with society. In patients with diabetes, education has resulted in increased knowledge and experience to enable patients with diabetes to feel better, protected patients from possible side effects by better disease control, reduced treatment costs, minimized treatment errors, and provided patients with skills to use new technology.¹² Blood glucose monitoring is key for diabetes management, and self-monitoring of blood glucose by patients can change diabetes care significantly.¹

Patient education, whereby patients with diabetes are informed about their disease and their awareness is raised, is of vital importance.¹³ In studies of patients with type 2 diabetes mellitus, disease-oriented education for patients provided positive effects on their self-care activities. Other studies demonstrated decreased lipid levels and arterial blood pressure values in patients with type 2 diabetes who were given education by diabetes nurse educators and monitored for approximately 3 months to 1 year.^14-16 Furthermore, in several studies that included patients with diabetes, a decrease was detected in HbA1c values of patients. However, body mass index either decreased or changed.^17,18

Transplant recipients are at elevated risk for developing prediabetes and overt diabetes mellitus due to a number of factors, including immunosuppressive therapies. Posttransplant diabetes mellitus (PTDM) has emerged as an increasingly important determinant of outcomes and survival in transplant recipients.¹⁹ Nampoory and colleagues²⁰ reported poor patient survival in patients with pretransplant diabetes mellitus due to coronary artery disease and infections. In contrast, overall long-term graft survival was equally good in transplant recipients with pretransplant diabetes mellitus versus those without diabetes.

Solid-organ transplant is now the standard of care for patients with end-stage organ failure, and primary care physicians are frequently involved in the follow-up care of transplant recipients. Posttransplant diabetes mellitus has emerged as an increasingly important determinant of outcomes and survival in transplant recipients. Patient education and self-management are crucial for ensuring successful outcomes posttransplant.²¹

In addition to type 1 and type 2 diabetes, PTDM is now a well-recognized consequence of organ transplantation, especially after solid-organ and bone marrow and hematopoietic stem cell transplant. Rates of PTDM can vary over different posttransplant intervals, with PTDM at 12 months or longer after kidney transplant ranging from 20% to 50%.²²

Adverse clinical outcomes of PTDM among renal transplant patients include loss of the renal allograft, infections, cardiovascular events, and mortality.²³ The hyperfiltration that accompanies diabetes, and even prediabetes, is believed to negatively affect allograft survival.²⁴ Patients with PTDM may also develop microvascular complications more rapidly than patients with nontransplant-related diabetes.²⁵

With diabetes education having a crucial effect on posttransplant morbidity and mortality, we aimed to evaluate the effects of structured diabetes education in a group of transplant recipients with PTDM with regard to their self-care activities and the development of diabetic microangiopathies.

Materials and Methods

Our study group included kidney transplant recipients with PTDM who were followed up at the Hamed AL-Essa Organ Transplant Center of Kuwait (OTC) and who met the eligibility criteria. Our prospective randomized controlled study enrolled 210 study patients. Inclusion criteria were as follows: (1) time since transplant of >6 months, (2) outpatient status, (3) no history of psychiatric illness, (4) written consent to participate in the research, and (5) age >21 years. Patients younger than 21 years and those who were mentally challenged were excluded. For randomization, patients were first divided into male and female groups and then all patients in each subgroup were arranged alphabetically using Excel and given a specific number. Patients in group 1 (n = 140) were selected according to the serial number given (starting from 1, 2, 5, 6, 8, 9); group 1 patients received individual structured diabetes education. Patients in group 2 (n = 70) were selected from the next serial number (starting from 3, 7, 10); group 2 patients received a conventional education program. Patient files were marked with stickers according to the corresponding group to facilitate the collection of data.

Ethical principles of the research
Written permission was received from the institutions where the research was carried out. Information on the aim and scope of the research was submitted to Ethical Committees of both the Ministry of Health and the Dasman Diabetes Institute (DDI; file number 2009-034-f), and written informed consent was obtained before participation from study patients. This trial was registered as https://clinicaltrials.gov/ct2/show/NCT04030013.

Patient identification form
The patient identification form included information on identifying characteristics such as age, sex, and education status and disease-related information such as duration of the disease and the management of diabetes.

Metabolic control parameter form
The metabolic control parameter form included metabolic control variables of patients, such as HbA1c, lipid levels, and results of renal and liver function tests. Metabolic control parameters were measured at the OTC outpatient clinic and were sent with each patient to the DDI within 1 week of patient evaluation for starting an educational program.

Diabetes self-care scale
An Arabic-translated 24-item questionnaire on diabetes self-care based on that developed in English by Lee and Fisher²⁶ was used. The diabetes self-care scale (DSCS) was used to measure the self-care of patients with diabetes; the questionnaire was applied to patients before and after the education program.

The questionnaire for our study was created under the supervision of the medical and nursing staff of DDI and OTC with experience in nursing research and medical and surgical nursing. Questions were tested to evaluate clarity, relevance to the studied problem, and adequacy in electing responses to cover the variables under study. Juried responses were incorporated into the list of questions, and a final interview schedule was developed. A pilot study was conducted to obtain preliminary ideas about the developed tool. The interview schedule was tested on 10 volunteer kidney transplant patients who were more than 6 months posttransplant and who were selected by convenience sampling.

For translation into English, 2 independent bilingual speakers and experts in diabetes treatment performed the forward translation. The results were reviewed and matched by the developmental team. Ultimately, the back-translated and original questionnaires were matched, and the English version was finalized.

The questionnaire created for our study comprised 44 questions on general data, anthropometric data, medical history, diet (5 questions), exercise (2 questions), self-blood sugar monitoring (4 questions), foot care (5 questions), and smoking (4 questions). In addition, the questionnaire delivered educational items for self-care activities, transplant care lifestyle, logbook use, sharps disposal, hypo- and hyperglycemic episodes, sick day management, fasting on Ramadan, pregnancy and diabetes, information about HBA1c, and diabetes-related complications (15 questions). Educational items and questions also included adherence to medications (immunosuppressive agents, cardiovascular, antidiabetic medications, food supplement and multivitamins) and information on malignancy prevention (regular breast examination and avoiding sun exposure) (9 questions).

Scoring of the questionnaire was calculated as sums of item scores and then transformed to a scale ranging from 0 to 10 (raw score/theoretical maximum score × 100). For example, for the subscale “glucose management,” a raw score of 12 leads to a transformed score of 12/15 × 100 = 80.

Data collection method
In the pretest phase of the research, patients were given a patient identification form, metabolic control parameter form, and the DSCS questionnaire. The forms were completed within 15 to 25 minutes by the patients in the presence of the researcher. Telephone numbers and addresses of patients were taken for proper communication if needed.

Patient education
Patients in the one-to-one structured education group (group 1) received education sessions individually in closed education clinics at the DDI. The first session lasted for 60 minutes, and then subsequent sessions lasted for 30 minutes. The content of education was repeated entirely or partly by the researcher according to individual patient needs. Mixed education techniques, such as description, question, and answer techniques, were used as an education method, and feedback was stimulated to enable patients to independently understand their self-care management. Refresher education sessions were then delivered every 3 months until the end of the study.

For patients in group 2, each patient received a conventional (nonstructured) education program at their home hospital (OTC).

A patient education brochure (developed by DDI) covered 2 main sections: general information on diabetes (definition, pathophysiology, and symptoms of diabetes) and diabetes management (including general care principles such as HbA1c, ketones/protein in the urine, healthy diet, regular exercise, regular use of oral antidiabetic drugs, regular insulin application, early problems in diabetes, possible long-term problems, foot care, individual self-monitoring of blood glucose and self-care in diabetes, skin care, oral and dental health, diabetes and travel, diabetes and smoking, diabetes and alcohol, diabetes and sex). Both groups received patient education brochures as procedural educational material in order to strengthen patient-specific education, skills, and oral information.

Regarding patients of group 1, the first education session was given once the patient was referred from the home hospital (OTC), and then subsequent sessions were given on an appointment basis. Patients received appointments for the next education session based on a patient-suitable date. Six interviews were conducted with each patient. The first interview was followed by a 3-month education program (with 2 weeks between each session).

In the phase after completion of education sessions, patients had to complete the DSCS again. Metabolic control parameters, such as HbA1c, lipids, blood pressure, body mass index, and waist circumference, were again measured and recorded. All parameters were assessed and collected every 6 months until the end of the study.

Diabetic microangiopathies (neuropathy, retinopathy, and nephropathy) were assessed before and 1 year after the educational program by electromyography/nerve conduction velocity; fundus evaluation was performed at the Ibn Sina Hospital (Sabah area, Kuwait) and regular urine analysis/graft biopsy (whenever indicated) was performed at the OTC.

Statistical analyses
For statistical analysis, we used the SPSS package (version 25.0). To analyze the identifying and disease-related characteristics of patients, matched t tests were used to compare the means and standard deviations of numerical variables of the 2 groups and to test whether there were differences in score averages before and after education sessions. Categorical data were compared using the chi-square test. P < .05 was considered significant.

Results

The 2 study groups were comparable regarding their demographic data (Table 1). Male patients predominated among both groups without significant difference (P = .13) between the groups, with mean age around 44 years in both groups (P = .62). Most patients were Kuwaiti (60.7% in group 1 vs 58.6% in group 2), with level of education of secondary school and above (65.7% vs 71.5%, respectively; P = .23). Hypertensive kidney disease and chronic glomerulonephritis represented the most commonly reported original kidney disease (46.4% vs 41.5%, respectively; P = .72).

Most patients received hemodialysis before transplant (72.8% vs 78.6% in group 1 vs group 2) without significant difference between the 2 groups (P = .61). The 2 groups had comparable pretransplant comorbidities, especially hypertension, ischemic heart disease, treated tuberculosis, and anemia (P > .05).

The percentage of patients in group 1 who received grafts from living donors was significantly higher compared with that shown in group 2 (P = .015). However, most patients showed immediate graft function (77.1% vs 74.2% in group 1 vs group 2; P = .14). Most patients were maintained on calcineurin-based immunosuppression (either tacrolimus or cyclosporine) without significant differences between the 2 groups (P = .55).

As shown in Table 2, a low score of healthy food knowledge was significantly higher in group 1 (93.3% vs 76.5%; P = .004). At the end of the study, the percentage of patients with a high score of healthy food knowledge was significantly higher in group 1 (80.5% vs 10.1%; P < .001). Most patients in both groups showed a low score of exercise knowledge (92.8% vs 97%, respectively) without significant difference between the 2 groups (P = .16). However, at the end of the study, exercise knowledge was significantly higher in group 1 (32.2% vs 0%, respectively; P = .001). Similar achievements were observed with regard to improvement of knowledge of healthy foot care and blood sugar monitoring after completion of education (P < .001). This was translated into a significant improvement in logbook use at the end of the study (99.2% vs 1.7%, respectively; P < .001).

We found no significant difference between the 2 groups in knowledge on risk factors of PTDM either at the start or the end of the study, especially with regard to viral infection as hepatitis C or cytomegalovirus (P > .05). Knowledge concerning antidiabetic drugs before education (start of study) was comparable between the 2 groups (50.4% vs 39.1% in group 1 vs group 2; P = .12), with scores significantly improving in group 1 at the end of the study (97.5% vs 67.8%, respectively; P < .001). Reduction of HbA1C was significantly higher in group 1 at 24 months after completion of education (P = .002).

As shown in Table 3, nephropathy (represented by proteinuria) was comparable in the 2 groups at the start of the study (P = .45). However, at the end of the study, we found that the percentage of patients with proteinuria was significantly less than the baseline value and the value in group 2 (P = .016). On the other hand, diabetic retinopathy (as indicated by fundus imaging results) and neuropathy (as indicated by electromyography/nerve conduction results) were comparable in the 2 groups at the start and end of the study (P > .05).

Discussion

Early studies on the effects of diabetes education on glycemic control showed varying results; however, later meta-analyses on this subject confirmed a tendency toward improved glycemic control,²⁷ especially when the ability to measure HbA1c became widely available.

Muhlhauser and Berger²⁸ recommended that patients with diabetes should receive evidence-based information on their disease to assist them in making informed decisions regarding management of their diabetes. Various forms of structured diabetes education have shown significant positive effects on glycemic control compared with controls.^29-31 In a meta-analysis, Deakin and associates observed a significant reduction in HbA1c, fasting blood glucose, and body weight among patients who received structured education.³²

The impact of structured diabetes education on diabetic microangiopathies is unclear. Therefore, we aimed to evaluate the effects of structured diabetes education given to renal transplant recipients with PTDM on their self-care activities and the development of diabetic microangiopathy and macroangiopathy. In our study, we randomized 2 groups with equivalent demographics. Men in their early fifth decade of life predominated in both groups (P = .62), similar to that reported by Guad and associates³³ in which most patients were men in their late fourth decade of life.

Effective health education should be provided at the patients’ level of education and understanding of the illness,³⁴ as patients with limited literacy and lower knowledge about diabetes and self-management had poorer health outcomes.³⁵ The relatively high level of education among our patients who received structure diabetes education might explain the better response in our study.

In our study, the most commonly reported original kidney diseases were hypertension and chronic glomerulonephritis, which was similar to those reported by Guad and associates³³ who also reported these as the most commonly reported original kidney diseases. Most of our patients received hemodialysis before transplant. As reported by Guad and associates,³³ an increased duration of dialysis before transplant was associated with a lower risk of PTDM. Differences between the studies could be due to different ethnicities and genetic predisposition.

Zieli?ska and associates³⁶ reported that ischemic cardiomyopathy was more frequent in patients with new-onset diabetes mellitus posttransplant (P = .001). In our study, we found the 2 patient groups were comparable with regard to pretransplant comorbidities, especially hypertension and ischemic heart disease (P > .05). Therefore, this risk factor for PTDM was nullified in our study. Moreover, macroangiopathic events in both groups at the end of the study were comparable.

The calcineurin inhibitors (CNIs) cyclosporine and tacrolimus have diabetogenic properties that worsen by the concomitant use of high-dose glucocorticoids. These drugs can induce glucose intolerance by different mechanisms, including a decrease in insulin secretion,³⁷ an increase in insulin resistance,³⁸ and toxicity on β-cells.³⁹ Most patients in our 2 groups showed immediate graft function (77.1% and 74.2%, P = .14) and had comparable CNI-based immunosuppression (either tacrolimus or cyclosporine; P = .55). In addition, we found no significant differences between patient groups regarding knowledge on other risk factors of PTDM either at the start or at the end of the study, especially with regard to viral infections such as hepatitis C or cytomegalovirus (P > .05).

Structured education should be delivered by expert and trained educators during specific and periodic sessions. Nutritional education can significantly improve diabetes knowledge, although not satisfactorily, but has had limited effects on attitudes toward diabetes.⁴⁰ Structured, individual diabetes education was more effective than conventional, group education in improving glycemia in adults with long-duration diabetes.⁴¹

In our study, there were significant improvements in the percentage of patients with a high score of healthy food knowledge who received structured education by the same well-trained diabetes educator (80.5% vs 10.1%; P < .001), with exercise knowledge scores also significantly better (P = .001). We also found that the number of patients with HbA1C reduction at 24 months of the study was significantly higher in the structured education group (P = .002). This observation was similar to that reported in a meta-analysis that showed that effects on HbA1c were not significant when physicians delivered the intervention but had greater effects when delivered by nurses and dietitians (-0.71% and -0.88%, respectively).⁴² We also found that patients who received structured diabetes education had improved knowledge on healthy foot care and blood sugar monitoring (P < .001) versus those who received conventional education. This was translated into a significant improvement in logbook use at the end of the study (P < .001). As shown previously, improving diabetes self-management and education can effectively improve blood glucose control.⁴³

Knowledge, frequency, and accuracy of self-monitoring blood glucose, dietary habits, and glycemic control have been positively affected after short-term follow-up.⁴⁴ After 10 sessions of a diabetes management education program, Miller and colleagues⁴⁵ found that older individuals with type 2 diabetes showed significant improvements in diabetes knowledge (P < .0001), disease management skills (P < .01), and decision-making abilities (P < .0001). However, Nathan and colleagues,⁴⁶ in their large meta-analysis, showed that the effects of diabetes education were not sustained beyond 4 months. In another study, Padgett and colleagues⁴⁷ found that dietary education had the largest effect on glucose control and the lowest effect on relaxation techniques. In an Italian study from Trento and associates,⁴⁸ 815 non-insulin-treated patients with type 2 diabetes were randomized into intervention and control groups. The intervention group received seven 1-hour educational sessions over 2 years, which were repeated. At study end of 4 years, the intervention group had lower HbA1c (7.3 ± 0.9% vs 8.8 ± 1.2%) with an adjusted mean difference of -1.49 (confidence interval, -1.63 to -1.34; P < .001) and also had improvements in psychological and metabolic parameters.

Other observations in our study were the significantly improved knowledge on antidiabetic drugs in patients who received structured education at the end of the study (97.5% vs 67.8% respectively; P < .001). We also observed that nephropathy (represented by proteinuria), although comparable between groups at the start of the study, was significantly reduced in patients who received structured education compared with the baseline value and level shown in patients who received conventional education (P = .016). This observation was similar to that shown by Li and associates⁴⁹ who evaluated the benefits and harms of education programs for people with diabetic kidney disease. They found that educational programs appeared to have beneficial effects on improving patients’ self-efficacy and resulted in some changes in beliefs with regard to diabetes and microalbuminuria. However, our study was the first to confirm the benefits of structured education on nephropathy among renal transplant recipients with PTDM.

Although our patient groups had comparable diabetic retinopathy findings (as indicated by fundus imaging) and neuropathy findings (as indicated by electromyography/nerve conduction study) before and after education, there are some risk factors for diabetic retinopathy, as reported by Li and associates,⁵⁰ which include significantly longer duration of diabetes, insulin therapy, higher HbA1c level, male sex, and lower level of education. In our cohort, these risk factors were comparable in the 2 groups. These complications may need longer follow-up to show any differences.

In our study, structured diabetes education was conducted by a single diabetes educator, with conventional education provided by different sources. In a meta-analysis, Steinsbekk and colleagues51 concluded that, based on current evidence, interventions delivered by a single educator, delivered in less than 10 months, with more than 12 hours and between 6 and 10 sessions, have the best results.

Conclusions

We found that structured diabetes education was associated with reduced diabetic nephropathy but did not have significant effects on other micro- or macroangiopathies. However, we recommend that structured education be delivered to kidney transplant recipients with PTDM.

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