GRAPHICAL ABSTRACT

INTRODUCTION

The occurrence of hypoglycemia in outpatients with type 2 diabetes mellitus (DM) is often considered just the tip of the iceberg. Previous studies have indicated that many cases of hypoglycemia go undetected and unrecorded within the healthcare system. Furthermore, it is estimated that between 30% and over 90% of type 2 DM outpatients experience this condition, with incidents occurring at least once every 4 weeks [1–3]. Several reports have also shown that more than 60% of affected individuals had hypoglycemic events within the past year, with 15% experiencing severe episodes [4,5].

Previous studies have indicated that the high prevalence of hypoglycemia among type 2 DM outpatients is associated with the treatment process [6–8]. According to the guidelines for managing type 2 DM therapy in Indonesia, sodium/glucose cotransporter 2 inhibitors and glucagon-like peptide-1 receptor agonists are often recommended as first-line options for outpatients with atherosclerotic cardiovascular disease, heart failure, and renal dysfunction [9,10]. However, in practice, insulin and sulfonylureas are primarily used due to cost constraints and treatment limitations outlined in the national formulary under the National Health Insurance (JKN) in Indonesia [11]. Several reports have identified these 2 classes of drugs as strong predictors of hypoglycemia [12,13]. Additionally, a lack of knowledge about the disease and medications has been reported to significantly influence patient behavior [14,15]. In addition, outpatients with poor treatment adherence are typically at a higher risk of experiencing hypoglycemia [16]. A 2021 study in Ethiopia demonstrated that low knowledge and negative attitudes toward treatment led to inappropriate insulin use among participants with type 2 DM [17]. This inappropriate use of insulin also increased the risk of hypoglycemia, which in turn led to various complications due to insufficient knowledge about self-management. A previous study revealed that only 65.7% of outpatients had knowledge of the appropriate actions to take when experiencing symptoms of hypoglycemia [2].

Healthcare providers are recognized as playing a crucial role in addressing hypoglycemia, as supported by multiple studies [18–20]. However, outpatients frequently receive inadequate education from these providers during their treatment. Moreover, outpatients with type 2 DM typically receive less attention than inpatients within hospital settings. Additionally, factors such as poor adherence to treatment, insufficient education, and limitations in healthcare providers’ ability to monitor treatment processes can together heighten the risk of hypoglycemia [21,22].

An effective strategy for addressing hypoglycemia includes the implementation of diabetes self-management education/support (DSME/S) [23,24]. These programs are recommended by the American Diabetes Association due to their ability to improve knowledge, abilities, and skills in managing diabetes independently. Additionally, their implementation typically involves interprofessional collaboration among healthcare providers, including doctors, nurses, diabetes educators, dietitians, and pharmacists [25–27]. Such collaborative efforts can significantly improve therapy outcomes, outpatient care, and safety [19,28,29]. To prevent adverse drug reactions in cases of hypoglycemia, healthcare providers must monitor the safe use of medications. This involves conducting initial assessments of hypoglycemia risk in type 2 DM outpatients using a patient behavior assessment instrument.

Based on previous research, there is no existing assessment tool in Indonesia for evaluating behavior related to hypoglycemia risk among type 2 DM outpatients. This study adapted, modified, and expanded the Diabetes Self-Management Questionnaire-Revised (DSMQ-R) [30] to suit the specific characteristics of the Indonesian type 2 DM outpatient population. Additionally, the DSMQ-R can serve as a useful tool for pharmacists and other healthcare providers to facilitate communication with professionals involved in DSME/S. This underscores the importance of developing an assessment instrument to gauge behavior toward hypoglycemia risk among outpatients.

METHODS

This study was conducted in 3 stages. Stage I involved assessing face and content validity through expert panel activities. Stage II was dedicated to evaluating construct validity and conducting reliability tests. Stage III focused on establishing criterion validity.

Stage I (Face and Content Validity)

The development of the instrument began with activities conducted by an expert panel, which included five healthcare practitioners from both hospital and primary care settings. This panel comprised internal medicine specialists (endocrinologists), nurses, hospital pharmacists, primary healthcare pharmacists, and dietitians. During these sessions, the author documented a summary of the discussions. Additionally, a moderator with expertise in both academia and diabetes clinic practice provided guidance throughout the process. The topics addressed by the experts encompassed various behaviors of type 2 DM outpatients, including dietary habits, physical activity, blood glucose monitoring, medication adherence, and collaboration with healthcare providers. These topics aligned with the domains outlined in the DSMQ-R [30]. The questionnaire utilized in this study was specifically chosen and modified to reflect the cultural and characteristic nuances of the type 2 DM outpatient population in-Indonesia. The DSMQ-R, a self-assessment tool featuring closed-ended questions, aids pharmacists and other healthcare providers in evaluating patient behavior during treatment. The discussions held by the expert panel culminated in the creation of a draft set of questions for the behavior assessment instrument.

Stage II (Construct Validity and Reliability Testing)

In Stage II of the study, the validity and reliability of the instrument were assessed using a cross-sectional method with 60 respondents. The assessment was divided into 3 subtests, each involving 20 respondents. The inclusion criteria were as follows: patients with type 2 DM, aged 18 years or older, currently receiving outpatient therapy, and willing to participate by signing informed consent. However, patients with gestational diabetes were excluded from the study. The purpose of this stage was to determine whether the questionnaire items were interrelated and aligned with the theoretical framework. The data processing and analysis for the validity and reliability tests were performed using SPSS version 25 (IBM Corp., Armonk, NY, USA).

Construct validity testing

The draft instrument created in stage I was distributed to 20 respondents who met the previously listed inclusion and exclusion criteria. In this test, if the results were not valid, the language was corrected and the test is repeated until all items were validated. This process was conducted 3 times, with each test involving 20 respondents, to ensure that all question items were valid.

The validity of each item in the instrument was assessed using the Pearson product-moment correlation between the item scores and the total scores. The instrument was deemed valid if the correlation value (Pearson correlation) was positive and the p-value (2-tailed) was less than 0.05 or the r-table value exceeded 0.433.

Reliability testing

The reliability test in stage II utilized a 1-shot method, involving the administration of the questionnaire to different respondents on a single occasion. The results were then compared with those of other questions or analyzed based on the correlation between responses. The data collected were processed using SPSS version 25.

Cronbach’s α was utilized for the reliability test, with α values ranging from 0 to 1. A value of zero indicated that the instrument was unreliable, whereas a value of 1 indicated complete reliability. A reliability coefficient (α) of 0.60 or higher was considered acceptable.

Stage III (Criterion Validity)

Stage III involved testing the instrument to assess the relationship between behavior and the risk of hypoglycemia. The study design for this stage was cross-sectional, employing consecutive sampling to select participants. A total of 237 individuals were involved, meeting the same inclusion and exclusion criteria as the stage II research sample. These criteria included patients with type 2 DM, aged 18 years and older, who were undergoing outpatient treatment and had voluntarily agreed to participate in the study. The exclusion criteria applied to patients with gestational DM.

Outpatients who met the inclusion and exclusion criteria were asked to complete a behavior assessment instrument. Those who agreed to participate signed an informed consent form. The responses were scored, calculated, and then interpreted by the pharmacist. Based on these results, the respondents were categorized into 2 groups: poor (at risk) and good (not at risk of hypoglycemia). Subsequently, these outpatients were queried about any hypoglycemic events they had experienced in the past 2 months. The relationship between behavior and the occurrence of hypoglycemia was statistically analyzed using bivariate (chi-square) and multivariate (logistic regression) methods.

As a moderating variable that can influence behavior and the incidence of hypoglycemia, respondents’ knowledge and beliefs were measured in this study. To assess these factors, we utilized the Knowledge Diabetes Questionnaire-24 and the Diabetes Health Beliefs Measurement Questionnaire. Both questionnaires were tested for validity and reliability with a sample of 20 respondents. Based on the scores from the questionnaire responses, respondents were categorized into two groups: those with good and poor knowledge, and those with good and poor beliefs. The impact of knowledge and belief variables on the incidence of hypoglycemia was analyzed using both bivariate and multivariate tests.

Ethics Statement

This phase of the study was carried out at a general hospital in Jakarta from April 2023 to September 2023. The research received approval from the Fatmawati Hospital Ethics Committee, approval No. PP.08.02/D.XXI.18/11/2023.

RESULTS

Study Population

The expert panel included healthcare practitioners such as internists, nurses, pharmacists, and dietitians, each with experience ranging from 5 years to over 10 years. The validity and reliability testing of the instrument involved 60 respondents, divided into three subtests. The distribution of male and female respondents was nearly equal; half of them were aged between 56 years and 65 years. Most were participants in the JKN and had completed high school education.

Based on the inclusion and exclusion criteria, 237 type 2 DM outpatients participated in the stage III study. Of the type 2 DM patients, 71.8% were aged ≥56 years, 59.5% were females, 65.4% had a body mass index (BMI) ≥23.0 kg/m² and 67.9% had been diagnosed with DM for more than 5 years. Regarding lifestyle, the majority of these outpatients did not smoke (88.6%), abstained from alcohol (96.2%), and engaged in active physical activity (54.9%). Most patients had controlled hemoglobin A1c levels (64.4%) and presented with comorbidities (81.9%). However, not all patients had complete medical records for glomerular filtration rate values and blood lipid levels (total cholesterol, low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, and triglycerides). This was due to the fact that these tests were only conducted on patients with a history of impaired kidney function or dyslipidemia, those with uncontrolled blood lipid levels, or patients who had undergone changes in their dyslipidemia therapy. The study population details are included in Supplemental Material 1.

Qualitative Analysis of the Expert Panel

Based on the expert panel, an assessment of behavior regarding hypoglycemia risk among type 2 DM outpatients was conducted using an instrument consisting of 9 question domains. These domains included blood glucose monitoring, diet, physical activity, medication use, hypoglycemia management, assistance from healthcare providers, self-care, family support, and insulin use. The discussions among the experts led to the addition of a new domain, family support, which is not present in the DSMQ-R.

At this stage, the DSMQ-R contained 9 questions unrelated to hypoglycemia that were also not addressed in the expert panel discussion. These questions fell into the domains of diet (5 questions excluded), physical activity (3 questions excluded), and assistance from healthcare providers (1 question excluded). These excluded questions primarily aimed to assess the patient’s blood glucose control. Meanwhile, the expert panel contributed an additional 11 questions covering dietary habits, physical activity, medication use, hypoglycemia management, assistance from healthcare providers, and family support. Consequently, the instrument comprised a total of 29 questions. The outcomes of the expert discussion are detailed in Table 1.

The draft behavior assessment instrument for type 2 DM at this stage consisted of 29 questions across 9 domains. A comparison of questions between the DSMQ-R [30] and behavior assessment instrument for type 2 DM is shown in Supplemental Material 2.

Construct Validity and Reliability Testing of the Instrument

The construct validity test of the behavior assessment instrument was conducted 3 times due to several questions being neither valid nor reliable. The first validity test included 20 type 2 DM outpatients. Questions were deemed invalid if the r-count was less than the r-table; for a sample size of 20, the r-table value was 0.433. Consequently, 12 questions were identified as invalid. These 12 invalid questions underwent language revisions in the instrument, followed by a second evaluation.

In validity test II, 20 type 2 DM outpatients participated. This test focused on the 12 previously identified invalid questions, revealing that only 2 of these questions were indeed invalid (r-count<0.433). Both questions belonged to the treatment domain. These invalid questions were then re-evaluated in validity test III, where they were found to be valid. The algorithm for the instrument development process is available in Supplemental Material 3.

A reliability test was conducted to assess the dependability of the developed instrument. The findings indicated that the behavior assessment instrument was reliable, with a Cronbach’s α of 0.891. The outcomes of the validity and reliability tests are detailed in Table 2.

The instrument, which was validated and found to be reliable, comprises 29 questions spanning 9 domains. These include monitoring blood glucose levels, diet, physical activity, medication use, hypoglycemia management, interactions with healthcare providers, self-care, family support, and insulin use, as shown in Supplemental Material 4.

In the instrument, positive statements were assigned a value of 3 for “applies to me very much,” 2 for “applies to me to a considerable degree,” 1 for “applies to me to some degree,” and 0 for “does not apply to me.” Conversely, negative statements received the opposite values. The maximum score for non-insulin users was 75, calculated as 3 points multiplied by 25 questions. For insulin users, the maximum score increased to 87, derived from 3 points across 29 questions. This maximum value served as the divisor for calculating the total score obtained by respondents from their answers in the instrument. The resulting quotient was then multiplied by 10, which helped categorize patients into behavior groups on a scale ranging from 1 to 10.

Instrument Trial (Criterion Validity)

The assessment instrument for behavior, which was both valid and reliable, consisted of 29 questions. The results from this assessment could be utilized to determine the risk of hypoglycemia. This study explored the relationship between behavior and the risk of hypoglycemia. Stage III of the study included 237 type 2 DM outpatients. The findings indicated that 164 (69.2%) of these patients experienced hypoglycemia in the past two months.

Based on instrument scoring results, patients with a score greater than 5.8 were categorized as exhibiting good behavior, using the median value as a benchmark. Meanwhile, those with a score of 5.8 or lower were considered to have less satisfactory behavior. The distribution of hypoglycemia events and type 2 DM behavior is presented in Table 3.

The distribution of patient answers on the instrument (Supplemental Material 5) showed that the majority of patients did not regularly perform self-monitoring of blood glucose (SMBG) or document their results. Additionally, many patients did not adhere to the dietary guidelines recommended by healthcare professionals. In the realm of support from healthcare providers, it was evident that most patients do not follow the prescribed control schedule. Over 90% of patients reported not taking their medication as directed by their physician. Such behaviors may lead to hypoglycemia. The reasons behind these behaviors are explored further in the discussion section.

To test the instrument, other variables that might influence the incidence of hypoglycemia, such as patient characteristics and medication, were controlled. The bivariate test results indicated that 7 variables warranted further analysis through multivariate testing. These variables are sex, age, BMI, duration of DM, smoking, level of knowledge, and behavior. The results of the bivariate and multivariate tests are presented in Tables 4 and 5, respectively.

After conducting a multivariate analysis, it was determined that 5 factors significantly affected the incidence of hypoglycemia in outpatients with type 2 DM. These factors included age, BMI, duration of DM, level of knowledge, and behavior. Among these, age was the most significant predictor of hypoglycemia risk. Older patients faced a higher risk compared to their younger counterparts. Specifically, patients aged 56–65 years and those over 65 years were 3.54 times and 3.73 times more likely, respectively, to experience hypoglycemia than patients under 46 years. Additionally, BMI, duration of DM, level of knowledge, and behavior also played roles in influencing hypoglycemia incidence, even when adjusted for sex and smoking habits.

DISCUSSION

In the stage I study, all domains of the DSMQ-R were discussed by the expert panel, and an additional domain was identified: family support. This domain could influence the incidence of hypoglycemia in type 2 DM outpatients. The study noted that many type 2 DM patients who frequently experienced hypoglycemia are older individuals living alone or those who reside with family but attend hospital visits unaccompanied. Consequently, there is often no one to remind them to adhere to their diabetes treatment, including both pharmacological and non-pharmacological interventions.

The validity and reliability test of stage II study was carried out 3 times, because in the first and second tests several invalid questions were still found. Lack of understanding of the questions on the instrument is one of the factors that cause the question items to be invalid. Then, we modified the language of the question to make it simpler and easier for laypeople to understand.

The results of the stage III study indicate that several factors significantly influence hypoglycemia in type 2 DM patients, including age, BMI, duration of DM, and levels of knowledge and behavior. Research has consistently shown that older patients face a higher risk of hypoglycemia compared to younger ones, with risk increasing with age. This heightened risk is attributed to various factors such as physiological changes, the pharmacokinetics and pharmacodynamics of drugs in older bodies, diminished organ function, counter-regulatory failure, and reduced cognitive function. Specifically, a decline in counter-regulatory mechanisms (including glucagon, epinephrine, growth hormone, cortisol, and liver auto-regulatory factors) in older adults impairs the body’s ability to maintain normal blood sugar levels, leading to hypoglycemia [31]. Furthermore, diminished cognitive function in the elderly can exacerbate hypoglycemia [32]. When patients fail to recognize the signs and symptoms of hypoglycemia, they do not manage the condition effectively.

The next factor influencing hypoglycemia was found to be BMI. Iatrogenic hypoglycemia occurs more frequently in type 2 DM patients with lower BMIs. This association is linked to malnutrition and the diminished capacity of patients with low BMI to mount counter-regulatory responses [33].

In this study, it was found that patients who had been diagnosed with DM for ≥5 years more frequently experienced hypoglycemia than those diagnosed with the condition for <5 years. It is well-established that the duration of DM correlates with both microvascular and macrovascular complications, as well as comorbidities. Among patients with type 2 DM, comorbidities that affect the incidence of hypoglycemia include cerebrovascular disease, malignancy, heart failure, obesity, decreased cognitive function, and chronic kidney disease [34,35]. Impaired kidney function in DM patients can lead to reduced clearance of antidiabetic medications, thereby increasing their concentration in the blood and causing hypoglycemia. Additionally, dyslipidemia is linked to reactive hypoglycemia, further contributing to the risk of hypoglycemia [36].

Patient knowledge about type 2 DM and their behavior are closely linked to hypoglycemia. There is an inverse relationship between a patient’s understanding of diabetes self-management and the incidence of hypoglycemia: the greater the patient’s knowledge, the lower the risk of hypoglycemia, and vice versa. Patients who are unaware of hypoglycemia tend to experience more frequent hypoglycemic events and are at a higher risk of progressing to severe hypoglycemia [37]. A lack of understanding about the disease and the medications used can affect how patients manage their treatment [38–40]. Furthermore, patients who exhibit poor medication management behaviors are at an increased risk of developing hypoglycemia [16].

Based on patient responses to the survey, it is evident that most patients do not perform SMBG. This may be due to the fact that not all patients own a gluometer; they typically check their blood glucose levels only during visits to a doctor or the nearest health service facility. Blood glucose testing is free for JKN participants, so they usually check their blood glucose only once a month while receiving their routine medication at the hospital.

Many patients fail to adhere to the dietary guidelines recommended by healthcare professionals. Nutritionists, as part of the diabetes education team at Fatmawati General Hospital, consistently remind patients to follow the 3J (schedule/jadwal, quantity/jumlah, and type/jenis) diet, which emphasizes the right type, amount, and schedule of food. However, not all patients maintain the discipline required to adhere to a diabetes diet. Environmental factors, such as family or work commitments, are believed to contribute to this issue.

It is also known that the majority of patients do not adhere to the prescribed control schedule. Several suspected factors include busy daily schedules, lack of companionship, and the considerable distance and fatigue associated with traveling to healthcare facilities. Additionally, over 90% of patients have reported not following their medication regimen as directed by their doctor. Having been diagnosed with DM for an extended period (over 5 years) and receiving ongoing education from the diabetes team at Fatmawati Hospital, patients often believe they understand their treatment well enough to adjust their therapy independently. However, such behavior can increase the risk of hypoglycemia if treatment adjustments are made without medical consultation.

The results of this study demonstrated that the instrument for assessing behavior could be effectively used to evaluate the risk of hypoglycemia in type 2 DM outpatients. Patients exhibiting poor behavior were found to be 2.36 times more likely to experience hypoglycemia compared to those demonstrating good behavior. In conclusion, the assessment instrument for evaluating the behavior of type 2 DM outpatients regarding hypoglycemia was both valid and reliable. This developed instrument can be used to prevent hypoglycemia in type 2 DM outpatients, with a cutoff score of ≤5.8 identifying patients at greater risk of hypoglycemia.

Supplemental Materials

Notes

Conflict of Interest

The authors have no conflicts of interest associated with the material presented in this paper.

Funding

None.

Author Contributions

Conceptualization: Sauriasari R. Data curation: Veryanti PR, Mokoagow MI. Formal analysis: Veryanti PR, Sartika RAD. Funding acquisition: None. Methodology: Sartika RAD, Elya B. Project administration: Veryanti PR, Mokoagow MI. Visualization: Veryanti PR. Writing – original draft: Veryanti PR. Writing – review & editing: Sauriasari R, Sartika RAD, Elya B, Mokoagow MI.

Acknowledgements

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