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Background: Hypoglycaemia is a common and potentially avoidable adverse event in people with type 2 diabetes ( T2D). It can reduce quality of life, increase healthcare costs, and reduce treatment success. We investigated self‑man‑ agement issues associated with hypoglycaemia and self‑identified causes of hypoglycaemia in these patients. Methods: In this mixed methods study qualitative semi‑structured interviews were performed, which informed a subsequent quantitative survey in T2D patients. All interviews were audio recorded, transcribed verbatim and coded independently by two coders using directed content analysis, guided by the Theoretical Domains Framework. Descriptive statistics were used to quantify the self‑management issues and causes of hypoglycaemia collected in the survey for the respondents that had experienced at least one hypoglycaemic event in the past. Results: Sixteen participants were interviewed, aged 59–84 years. Participants perceived difficulties in managing deviations from routine, and they sometimes lacked procedural knowledge to adjust medication, nutrition or physical activity to manage their glucose levels. Grief and loss of support due to the loss of a partner interfered with self‑man‑ agement and lead to hypoglycaemic events. Work ethic lead some participant to overexerting themselves, which in turn lead to hypoglycaemic events. The participants had difficulties preventing hypoglycaemic events, because they did not know the cause, suffered from impaired hypoglycaemia awareness and/or did not want to regularly measure their blood glucose. When they did recognise a cause, they identified issues with nutrition, physical activity, stress or medication. In total, 40% of respondents reported regular stress as an issue, 24% reported that they regularly overes‑ timated their physical abilities, and 22% indicated they did not always know how to adjust their medication. Around 16% of patients could not always remember whether they took their medication, and 42% always took their medica‑ tion at regular times. Among the 83 respondents with at least one hypoglycaemic event, common causes for hypo‑ glycaemia mentioned were related to physical activity (67%), low food intake (52%), deviations from routine (35%) and emotional burden (28%). Accidental overuse of medication was reported by 10%. *Correspondence: firstname.lastname@example.org Department of Clinical Pharmacy and Pharmacology, University Medical Centre Groningen, University of Groningen, Groningen, Netherlands Full list of author information is available at the end of the article © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Crutzen et al. BMC Fam Pract (2021) 22:114 Page 2 of 13 Conclusion: People with T2D experience various issues with self‑managing their glucose levels. This study underlines the importance of daily routine and being able to adjust medication in relation to more physical activity or less food intake as well as the ability to reduce and manage stress to prevent hypoglycaemic events. Keywords: Type 2 diabetes, Hypoglycaemia, Self‑management, Patient perspective, Mixed methods Introduction the negative impact on their physical and psychosocial Hypoglycaemia is a common and potentially avoidable wellbeing . This often requires lifestyle changes, adverse event of treatment with insulin or medication monitoring of the disease and adequate medication which stimulates secretion of insulin in people with type taking behaviour. For people with T2D these require- 2 diabetes (T2D). Hypoglycaemia can reduce quality of ments change over the course of their disease . life, increase healthcare costs, and reduce treatment suc- When diagnosed with T2D, self-management and cess of glucose lowering medication [1–3]. Severe cases self-management support is mostly focussed on life- of hypoglycaemia can lead to hospitalization, brain dys- style changes, such as increasing physical activity and function and increased mortality [4–7]. The reported improving diet . As the disease progresses and rates of hypoglycaemia in people with T2D vary widely, medication is added, self-monitoring of blood glucose depending on the study population, study design and and adjusting medication accordingly may become severity of the hypoglycaemia studied . In a four week necessary. prospective global study in people with T2D, 47% of par- Many studies investigated the risk factors for hypo- ticipants using insulin reported at least one event and 9% glycaemia from a clinical perspective, but in-depth reported at least one severe event . In a Dutch study information on the self-management issues and behav- in people with T2D, 41% of participants using insulin ioural factors that contribute to hypoglycaemia from reported at least one event and 4% reported at least one the patient perspective is lacking [12–16]. Our first aim severe event in the past year . However studies with was therefore to explore self-management issues asso- continues glucose measurement indicate that hypogly- ciated with hypoglycaemia and subsequently quantify caemia is frequently unrecognized and more common these issues in a larger population. Among patients who than previously believed . have experienced at least one hypoglycaemic event, we The causes of hypoglycaemia are multifactorial and aimed to explore and quantify the factors these patients include the intrinsic risks of specific medication and identify as the causes of the hypoglycaemia. comorbidities. Behavioural factors of medication use, physical activity and nutrition also influence the occur - rence of hypoglycaemic events [12–16]. Few studies have Subjects, materials and methods looked at possible causes for hypoglycaemia from the Design perspective of patients. In those studies, participants We used a mixed methods study design, combining reported that they experienced hypoglycaemic events in-depth semi-structured interviews and a cross- due to delayed or skipped meals, alcohol use, dieting and sectional survey. The interviews were intended to inconsistent eating patterns [12, 13, 15, 16]. Also, incor- provide in-depth information from the patient per- rect timing or dosing of insulin, stress or exercising more spective. In addition, the results were used for the or more vigorously than planned were reported as pos- development of a survey to quantif y self-management sible causes of hypoglycaemia [12, 13, 15, 16]. These stud - issues and causes of hypoglycaemia. The Theoretical ies, however, mostly used questionnaires with predefined Domains Framework (TDF) was used as a framework answers, which limits the possible range of causes that to structure the topics of the interviews and identify can be identified. One study used a qualitative design, domains potentially related to changes in behaviour where patients were not restricted in their reporting, but [23, 24]. The TDF consists of the following domains: this study focussed only on the impact of fasting on self- knowledge, skills, social/professional identity, beliefs management of glucose levels . about capabilities, beliefs about consequences, moti- Self-management can be challenging for people with vation and goals, memory attention and decision pro- T2D. Social support from family members and other cesses, environmental context and resources, social personal networks as well as support from health care influences, emotion, behavioural regulation and providers can improve self-management of T2D [18, nature of the behaviours . The interviews were 19]. For chronic diseases, self-management is the abil- analysed using directed content analysis based on the ity of people to manage their disease in order to reduce TDF [23, 24]. C rutzen et al. BMC Fam Pract (2021) 22:114 Page 3 of 13 Interviews diabetes herself. This resulted in some minor changes in Subjects and setting the wording and the order of the questions. Recruitment for the interviews was done through eight Furthermore, participants completed a short question- general practices in the Northern part of the Nether- naire about their socio-demographic background and lands by purposive sampling, where nurse practitioners their lifestyle. Health literacy was assessed with the Set identified and approached potential study participants. of Brief Screening Questions in Dutch (SBSQ-D) [26, 27]. The Northern part of the Netherlands is characterized The medication that participants used was documented by relatively small cities, more rural areas and fewer by the interviewer. This medication list was confirmed minorities compared to other regions of the Nether- with the patients’ medical records by the nurse practi- lands. Most inhabitants are Caucasian. Diabetes care is tioners for all but two of the participants. organized in a similar way in all regions in the Neth- erlands. T2D patients were included when they used a sulfonylurea and/or insulin, experienced at least one Data analyses hypoglycaemic event in the past year and were able to Descriptive statistics were used for the patients’ char- speak Dutch. They were excluded when they had an acteristics. All interviews were audio recorded and estimated life expectancy of less than six months or transcribed verbatim using f4transkript, version 6.2.3. when the nurse practitioner and/or general practitioner Transcripts were not returned to the participants. Field thought they should not be approached for an inter- notes were used to enrich the transcripts with non-verbal view study, because of a recently experienced serious communication of participants and contextual informa- life event. Participants were approached by their nurse tion. The interviews were coded using Atlas.ti, version practitioner to participate in the study. They were then 5.2.18. A coding frame was developed prior to the analy- invited by TB by phone and received a letter with infor- sis of the interviews by TB and SC. It included the twelve mation on the purpose of the study. Written informed domains of the TDF, thematic codes about the broader consent was obtained and participants received a gift categories related to possible causes of hypoglycaemia card as compensation (€20). Recruitment continued and attribute codes to address important factual ele- until saturation was achieved, which was defined as ments of the statements. New attribute codes were added the point where no new information emerged from the in an iterative process to the coding frame. Both TB and interviews . Data saturation was discussed between SC coded all interviews, and any discrepancies between TB and SC. The interviews were conducted at the par - them were discussed until consensus was reached. ticipants’ homes between January and March of 2019. Directed content analysis was used to analyse the data Partners were allowed to be present during the inter- focussing on (1) self-identified causes and (2) self-man - view to provide more information about, for example, agement issues: medication use and experiences with severe hypogly- caemia. Field notes were taken during the interviews. 1. All quotes coded as “cause of hypoglycaemia” were The interviews were conducted by TB and SC. TB has extracted. This code was assigned to passages where a BSc in pharmacy and is a female pharmacy master participants talked about a possible cause of a hypo- student and SC is a male PhD candidate with an MSc glycaemic event or where the participants mentioned in pharmacy who performed scientific interviews prior that he/she did not know the cause of the event. to this study. TB received instructions on how to con- These extractions were used to identify and catego - duct interviews and she performed a practice interview rise the self-identified cause of hypoglycaemia. Those under the supervision of SC. The interviewers had no categories were then cross-linked with “cause of prior relationship with the patients. hypoglycaemia” for tabulation in the results. 2. All quotes coded with domains from the TDF were cross-linked with the code “cause of hypoglycae- Interview guide mia” to identify self-management issues. Addition- A semi-structured interview guide was developed based ally, to identify self-management issues that were not on the domains of the TDF and known causes and directly linked to a cause of hypoglycaemia, all quotes self-management issues of hypoglycaemia (Additional coded with the TDF and without the “cause of hypo- file 1). To avoid researcher bias, open ended questions glycaemia” code were extracted and inspected for were used with additional probing questions. The inter - possible self-management issues related to hypogly- view guide was discussed among the research team and caemia. Quotes were selected for the manuscript in improved accordingly. The interview guide was piloted order to illustrate certain issues and to provide addi- with a female patient representative, having type 1 tional context for the reader. Crutzen et al. BMC Fam Pract (2021) 22:114 Page 4 of 13 Survey online version of the questionnaire was created with Subjects and setting Qualtrics Software (Qualtrics, Provo, UT). Participants were recruited through five community pharmacies across the Netherlands. The recruitment Data analysis was done sequentially in order to facilitate age strati- Descriptive statistics were used to analyse the patient fication. Potential participants were stratified based on characteristics, the self-management issues, and the age: 24% of patients < 60 years, 32% 60–70 years, 28% self-identified causes among respondents who had expe - 70–80 years , and 16% > = 80 years in order to have a rienced at least on hypoglycaemic event. Related self- representative sample of Dutch primary care patients identified causes were first combined (see Additional with type 2 diabetes. Any differences in the age-distri- file 2). Stacked bar charts were used to visualize the self- bution of returned questionnaires were corrected by management issues, categorized by having experienced a altering the number of invitations per age-strata in fol- hypoglycaemic event in the past. Complete case analyses lowing community pharmacies. The community phar- were used for each item with less than 5% missing data. macist together with one of the researchers identified Descriptive statistics for all respondents, including those potential participants using the pharmacy informa- that had not experienced hypoglycaemic events, are sum- tion system. Inclusion criteria were: age of 40 years or marized in Additional file 3. older, use of a sulfonylurea and/or insulin, and able to read and write in Dutch. For the primary data analyses, Compliance with ethical standards patients were selected who had experienced at least A waiver was obtained by the Medical Ethics Review one hypoglycaemic event in the past. Invitations were Board of the University Medical Center (METc UMCG) sent using an email with a link to the online question- as they concluded that the study did not require approval naire (Qualtrics XM). In case no email address was because the study was not considered to be clinical available a paper version was sent by mail. Informed research with human participants as meant in the Medi- consent was collected from all participants. For par- cal Research Involving Human Subjects Act. ticipation, patients received a gift card of €10. Results All of the sixteen people who were invited to participate Questionnaire were willing to be interviewed. Data saturation occurred Themes from the interview study were translated to items after sixteen interviews. The duration of the interviews for the questionnaire by SC and TB. These themes were ranged from 20 to 120 min. The age of the participants related to the self-management of medication, nutrition ranged from 59 to 84 years, ten of the participants were and physical activity and to the domains of the TDF. For female, and thirteen were diagnosed with T2D more than five of the TDF domains, items about self-management ten years ago, eight experienced a hypoglycaemic event were developed in which respondents could indicate how within one week prior to the interview (Table 1). For the often they experienced these self-management issues survey, 208 of the 820 (25%) invited T2D patients com- on a five-point Likert scale. For the knowledge domain, pleted the questionnaire, 83 of which (40%) had expe- respondents were asked to indicate whether they knew rienced at least one hypoglycaemic event in the past how to adjust their medication in various situations in (Table 2). In the main analyses we report the results from which adjustments might be necessary. Additionally, the 83 respondents that had a hypoglycaemic event. On patients were asked whether or not they had experienced average, the respondents were 66 years old, 53% were a hypoglycaemic event. Respondents who had at least one female, and 76% were diagnosed with T2D more than ten hypoglycaemic event in the past were then asked about years ago. The other respondents, who had never experi - self-identified causes. They were allowed to select one or enced a hypoglycaemic event, more often had a diabetes more causes from a list of 18 options, that were based on duration less than 10 years, had less diabetes related com- the results from the interviews and literature [12–16]. All plications and used insulin less often compared to those questionnaire items were discussed with PD and KT until with hypoglycaemic events (Additional file 3, Table 1). consensus was reached about the content and phrasing. The questionnaire was piloted with four participants of Self‑management issues the interview study. Based on the results of this pilot, a Below we report the results of both the interviews and number of items were simplified and the phrasing of a the survey categorized by the domains of the TDF that number of items were improved. A translated version of were identified in the interviews. There was overlap the questionnaire can be found in Additional file 2. The in the interview quotes for the domain “beliefs about C rutzen et al. BMC Fam Pract (2021) 22:114 Page 5 of 13 Table 1 Interview participants’ characteristics (N = 16) domains were combined. No self-management issues were identified in the domains “behavioural regulation” Sex and “skills". Female 10 Male 6 Nature of behaviour Age group (years) In the interviews, daily routine was mentioned often as < 60 2 an important behavioural factor for self-management 60–70 6 and the prevention of hypoglycaemic events. Most par- 70–80 4 ticipants had a strict daily routine and emphasized the ≥ 80 4 importance of this for their self-management. A few Level of education participants reported that they had difficulties adher - Primary school 2 ing to the strict routine that was needed to control their Secondary school 7 glucose levels. Some participants struggled with events Vocational education 4 that disrupted their routine which led to hypoglycaemic Higher education 3 events (Table 3, [A]). Disruptions affected medication Level of health literacy taking, physical activity, food intake and/or their men- Low 2 tal state. For other participants, the rigidness of the daily Medium 0 routine was sometimes problematic (Table 3, [B]). In High 14 the survey, 42% of the respondents reported they always Use of alcohol took their medication at the same time, 27% always ate Yes 11 at the same time and 15% always got out of bed at the No 5 same time (Fig. 1A). Smoking Yes 1 Knowledge No 15 Lacking specific knowledge to self-manage glucose lev - Diabetes duration (years) els was another important theme identified in the inter - < 1 0 views. Participants had a good basic understanding of the 1–5 3 relationship between their glucose levels and their medi- 5–10 0 cation, nutrition and physical activity. This basic under - > 10 13 standing, however, was not always sufficient to anticipate Last hypoglycaemic event or prevent hypoglycaemic events. Participants some- < 1 week ago 8 times lacked procedural knowledge on how to address 1–2 weeks ago 1 deviations from their routine, especially when medica- 2–4 weeks ago 1 tion adjustments might be necessary (Table 3, [C]). Some > 1 month ago 6 did not know how to adjust their insulin or they did not Glucose lowering medication adjust it at all. Sometimes participants struggled to deter- Insulin 4 mine the right insulin dose, which led to injecting more Insulin + metformin 7 insulin than needed. To treat the resulting low blood glu- Insulin + sulfonylurea 1 cose levels they overate, which caused their blood glucose Insulin + GLP‑1 1 levels to rise again above the desirable threshold. This Insulin + sulfonylurea + metformin 1 resulted in a vicious circle that they did not know how Sulfonylurea 1 to break. Some participants reported that they experi- Sulfonylurea + metformin 1 enced hypoglycaemia symptoms at relatively high glucose Glucose monitoring levels, which they managed –incorrectly- by consuming Daily 9 foods or drinks high in sugar. One participant reported Weekly 3 that she was supposed to inject more insulin when the Rarely 3 glucose level was low (Table 3, [D]). This problem of hav - Never 1 ing inadequate knowledge was aggravated by the fact that she was not comfortable to ask her nurse practitioner questions, because she was afraid to appear stupid. capabilities” with “beliefs about consequences”, and In the survey, the majority (94%) of respondents indi- for the domain “social/professional role and identity” cated that they had enough knowledge to use their glu- with “social influences”. Therefore, the results for these cose lowering medication. Many indicated that adjusting Crutzen et al. BMC Fam Pract (2021) 22:114 Page 6 of 13 Table 2 Survey respondents’ characteristics Table 2 (continued) Respondents Respondents Number of respondents 83 Antihypertensive use 63 (76%) Age (years), mean (SD) 66 (11) Glucose meter at home 78 (94%) < 60 years, n (%) 20 (24%) Severe hypoglycaemia 15 (18%) 60–69 years, n (%) 27 (33%) Nocturnal hypoglycaemia 31 (37%) Frequency hypoglycaemia 70–79 years, n (%) 23 (28%) Daily 1 (1%) ≥ 80 years, n (%) 12 (14%) Weekly 4 (5%) Missing, n (%) 1 (1%) Monthly 21 (25%) Female, n (%) 53 (42%) Yearly or less 57 (69%) Diabetes duration, n (%) 0–5 years 9 (11%) 6–10 years 11 (13%) ≥ 10 years 63 (76%) medication was not necessary when they ate or exercised Missing 0 (0%) more or less than usual (Table 4). Furthermore, 22% indi- Diabetes related complication(s) 49 (59%) cated they did not always know how to adjust their medi- Body weight, n (%) cation for at least one specific situation. This included Underweight 0 (0%) 16% indicating that they did not adjust their medication Healthy Weight 18 (22%) in one or more of these situations because they did not Overweight 29 (35%) know how, and 6% indicating that did adjust their medi- Obese 34 (41%) cation although they did not know how. These specific Missing 2 (2%) situations included changes in physical activity, food Alcohol use, n (%) 49 (59%) intake or being ill (Table 4). Smoking, n (%) 7 (8%) Physical activity > 30 min/day, n (%) Emotion 0 days 5 (6%) In the interviews, stress and cognitive overload were 1–3 days 28 (34%) mentioned as issues interfering with managing glucose 4–6 days 28 (34%) levels. Some participants reported that stress caused their 7 days 22 (27%) glucose to rise, while others identified stress as a cause of Missing 0 (0%) their hypoglycaemic events. Cognitive challenging tasks, Working, n (%) 39 (47%) for example, administrative work on a computer, or grief Working irregular hours, n (%) 13 (16%) could lead to hypoglycaemia. Sometimes this was due to Marital status/household situation (%) forgetting to eat. One participant attributing some of her Married/living together 55 (66%) hypoglycaemic events to grief noted that she had to deal Living independent 27 (32%) with grief more often due to her increasing age. Another Missing 1 (1%) participant lost his wife recently causing stress and grief, Education, n (%) which resulted in poorer self-care and self-management, No/primary education 13 (16%) in turn leading to multiple hypoglycaemic events. In the Pre‑ vocational education 24 (29%) survey, 40% of the respondents had to deal with stress at Vocational education 15 (18%) least regularly, 22% had to deal with sadness or grief at Pre‑ college/pre‑university 11 (13%) least regularly, and 19% experienced cognitive overload at College/university 18 (22%) least regularly (Fig. 1B). Missing 2 (2%) Number of medications Memory, attention and decision processes 1–5 medication(s) 32 (39%) In the interviews, issues with memory or attention 6–10 medications 38 (46%) were mostly stated in relation to medication taking or > 10 medications 11 (13%) forgotten meals. Some participants mentioned acci- Missing 2 (2%) dentally administering more units or a double dose of Insulin use 54 (65%) insulin. When asked about accidentally using too much Sulfonylurea use 47 (57%) medication, participants often said it was possible that Statin use 55 (66%) this happened, but they were not sure. One participant C rutzen et al. BMC Fam Pract (2021) 22:114 Page 7 of 13 Table 3 Quotes of participants in the interviews translated from Dutch to illustrate the self‑management issues categorized by TDF domain Quotes TDF [A] “No, I do not have them very often [low blood sugar]. No, but then with my husband [he broke his hip due to a fall] Nature of behaviour ( …) But I just had to get used to it, to the new routine, until it was over.” (female, 70–80 years old) [B] “I should have prepared the warm meal earlier, but I am used to eating lunch at 12 o’clock. And I have the food ready Nature of behaviour at 12 o’clock, and I could not make that.” (female, 70–80 years old) [C] “I do not really know this very well yet ( …) It is not that easy for me to skip one tablet or to take one tablet extra the Knowledge/ Nature of behaviour next day. That is my problem, because I don’t have a sufficiently regular daily schedule. I’m trying to change that.” (Female 60–70 years old) [D] “So when it is low they say: ‘you need to inject more’, ok, how much more?” [Interviewer: “If it is low you need to Knowledge inject more insulin?”] “Yes, so that it will go up again, as it were. [Interviewer: “Insulin lowers your sugar.”] “Yes, exactly. So I think, I will do it my way. I get a small bottle of soda or two biscuits with jelly and then it’s all fine again.” (Female ≥ 80 years old) [E] “Yes, I have had days, that I think like, ( …) I want to finish my work, my assignment, but then a colleague said like: Social influences and social/pro ‑ ‘leave it for a while, we will take it over and you just sit down for a while.” (Female < 60 years old) fessional role and identity [F] “I went to the gym for a while, ( …) and there I sometimes overestimated myself a little, and then I would get a hypo, Beliefs about capabilities because I would use a treadmill more than I could handle with my bad legs.” [G] “So, I injected 4 [units] ( …) But, sometimes, it is too much and then I think that I should inject only 3 units. ( …) But Motivation and goals then again my glucose gets close to 10 and I really want my glucose to be as low as possible.” (Female 70–80 years old) [H] “I love mashed potato stews; I allow myself this once in a while. I think I should be able to do that, otherwise life is not Motivation and goals pleasant anymore.” (Female 60–70 years old) TDF Theoretical Domains Framework said he had once forgotten to lower the units of insulin Being an active person or doing a good job was impor- after instructions from his nurse practitioner to do so. tant, which led to exerting themselves too much (Table 3, Another participant said he accidentally had increased [E]). In the survey, 86% of the respondents reported to his long acting insulin instead of his short acting insu- manage their own medication. For those with a partner, lin, when adjusting the dose because of a high glucose 69% of the partners at least regularly noticed hypoglycae- level. Impaired hypoglycaemia awareness was often mic events and 52% at least regularly helped when they mentioned in relation to severe events. Some of the par- had a hypoglycaemic event (Fig. 1D). ticipants who reported that they usually felt the warning symptoms still experienced some events with no warn- Beliefs about capabilities and consequences ing signs. In the survey 16% of respondents indicated In the interviews, participants mentioned issues with that they could not always remember whether they had their ability to deal with variations in physical activity or already taken their medication and 12% said they had stress. Some participants overestimated what they could experienced difficulties in remembering dosing changes do and underestimated the impact of an activity on their to their medication. In the survey 43% reported that they glucose levels (Table 3, [F]). Adapting to their diminish always experienced impaired hypoglycaemia awareness, ing physical ability was something they struggled with. whereas 7.5% never experienced impaired hypoglycae - One participant mentioned she felt unable to prevent the mia awareness (Fig. 1C). stress that led to her hypoglycaemic events. In the survey, 24% of the respondents at least regularly overestimated what they were able to handle physically (Fig. 1E). Social influences and social/professional role and identity In the interview, several participants mentioned that their partners played an important role in the manage- ment of the diabetes. This could be up to the extent that Motivation and goals the partner fully managed their medication. Often part- In the interviews, some participants did not see hypo- ners helped the participant when they had a hypoglycae- glycaemia as a major issue in comparison with other mic event, bringing them food or drinks. One participant health-related issues. Mild events were often not con- explained that his partner noticed his hypoglycaemic sidered very burdensome. Other participants, however, events before he did. Not long after his partner passed feared the consequences of hypoglycaemic events. One away, he had experienced a severe hypoglycaemia, in part participant stated that she found it hard to navigate due to the loss of support from his partner. The work eth - between too low and too high glucose levels, because she ics of some participants led to self-management issues. did not want hypoglycaemic events, but she also did not Crutzen et al. BMC Fam Pract (2021) 22:114 Page 8 of 13 Fig. 1 Potential self‑management issues related to hypoglycaemia categorized per domain of the Theoretical Domains Framework for survey respondents with a hypoglycaemic event in the past want her glucose to rise too much (Table 3, [G]). Some self-management. One of the participants who used a sul- participants did not want to measure glucose too often, fonylurea, for which blood glucose meters and test strips mainly due to the physical discomfort. For many par- are not reimbursed in the Netherlands, mentioned that ticipants, it was important that the diabetes did not take he sometimes used the glucose meter of his wife. Another over their life, which was mostly expressed in relation participant stated that she was reluctant to use test strips to being active and dietary choices (Table 3, [H]). In the because she felt they were too expensive. In the survey, survey, 18% of the respondents had experienced a severe 94.0% of the respondents had a glucose meter at home. hypoglycaemia. Most experienced hypoglycaemic events either monthly or yearly (Table 2). Self‑identified causes of hypoglycaemia In the interviews, participants expressed that they Environmental context and resources were not always able to identify a direct cause of their In the interviews, lack of resources to use blood glucose hypoglycaemic events. All but one of the participants meters and test strips were mentioned as a problem for attributed at least some events to factors related to C rutzen et al. BMC Fam Pract (2021) 22:114 Page 9 of 13 Table 4 Survey results of questions about knowledge on how to adjust medication in various situations which require adjustment of medication Yes I know Yes, but I do not No, I do not No, I am not allowed No that how to do know how to do know how to do to do so by my HCP is not that that that necessary I adjust my medication when I exercise more than usual 25.0 2.5 5.0 5.0 62.5 (n = 80), (%) I adjust my medication when I exercise less than usual 21.3 1.3 5.0 5.0 67.5 (n = 80), (%) I adjust my medication when I eat more than 34.2 1.2 4.9 9.8 50.0 usual(n = 82), (%) I adjust my medication when I eat less than usual 30.5 0.0 4.9 8.5 56.1 (n = 82), (%) I adjust my medication based on measured glucose 35.9 5.1 3.9 18.0 37.2 levels (n = 78), (%) I adjust my medication when I am ill (n = 79), (%) 24.1 0.0 12.7 3.8 59.5 I adjust my medication when I am on a diet (n = 35), (%) 40.0 0.0 14.3 11.4 34.3 HCP Health care provider In one or more of the situation described in the table, 22% did not know how to adjust their medication, 16% did not know how to adjust their medication in one or more of these situations and 6% did adjust their medication although they did not know how medication, nutrition, physical activity, and/or emo- a cause by 28%, accidental overuse of medication was tional burden (Table 5). reported by 10% and lack of knowledge on how to adjust In the survey, the most common self-identified causes medication by 7% of the respondents. were too much physical activity (67%), not enough food intake (52%), deviations from routines (35%) (Fig. 2). Discussion Sadness, stress or cognitive overload were reported as Summary Many patients with T2D acknowledged self-manage- ment issues contributing to hypoglycaemia. Particularly, Table 5 Interview results: List of self‑identified causes issues within the TDF domains nature of behaviour, of hypoglycaemia categorised by theme and number of knowledge, emotions and capabilities appeared rel- participants mentioning the particular theme evant for adequate self-management and prevention of Medication (6 participants) hypoglycaemic events. Although most patients seemed Accidentally overdosing medication to have a basic knowledge about their medication and Forgetting adjustment made to the medication regimen the factors that may lead to hypoglycaemia, they some- Adjusting the wrong type of insulin times lacked procedural knowledge for specific situa - Fluctuating glucose levels tions or the ability to deal with deviations from routines Physical activity (9 participants) or handling negative emotions such as stress and grief. Household chores The inability to correctly estimate the impact of physical Sports activity was an issue for a quarter of the respondents. Physical leisure activities The most common self-identified causes of hypoglycae - Sexual activity mia were issues with handling physical activity, insuf- Nutrition (10 participants) ficient food intake, deviations from routine, and stress Skipped, delayed, forgotten meals and in relatively few cases also accidental overuse of Low appetite/premature satiation medication. Some of the hypoglycaemic events were Meals low on carbohydrates considered difficult to prevent, because the patients could not identify a cause or suffered from impaired Fatty meals hypoglycaemia awareness. Alcohol consumption Low‑ carb diet Stress/emotion (4 participants) Comparison with previous research Stress From our study, it becomes clear that the TDF domain Cognitive overload nature of behaviour is crucial for the prevention of Grief Crutzen et al. BMC Fam Pract (2021) 22:114 Page 10 of 13 Fig. 2 Percentage of participants reporting specific causes for their hypoglycaemia among 83 participants who had at least one hypoglycaemic event in the past. 1 ‑ Physical activity (work/exercise); 2 ‑ Not enough food consumed (forgotten/skipped/too small portion/late meal); 3 ‑ Deviations from routine; 4 ‑ Emotional burden (stress/grief/cognitive overload); 5 ‑ Impaired hypoglycaemia awareness; 6 ‑ No carbohydrates/ sugar available to treat low blood glucose; 7 ‑ Highly fluctuating glucose levels/poorly controlled glucose; 8 ‑ Accidental medication overuse (e.g. injecting insulin twice or injecting more units); 9 ‑ Hard to prevent when at work; 10 ‑ Fat food; 11 ‑ Lack of knowledge on how to adjust medication; 12 ‑ Prescribed a too high dosage of sulfonylureas or insulin hypoglycaemic events. People with T2D need to man- time, changes in a person’s life may lead to new self- age their lifestyle and medication use to keep their management issues. Some have to do with permanent glucose levels adequately controlled and prevent hypo- changes in medication regimen or diet, which require glycaemic events. Routine behaviour plays an impor- adjustments that are sometimes forgotten. Others are tant role in adequate self-management. People with related to loss of support or changes in physical abili- T2D particularly have difficulties with medication ties or appetite due to aging. self-management when they change their daily routine Diabetes-related knowledge, beliefs and skills are . Our study showed that both short-term deviations considered important for self-management of people from routine behaviour as well as long-term changes with T2D [21, 30]. Our study indicates that patients in daily life could lead to problems. In acute situations, have basic knowledge about the relationship between patients experienced issues with medication self-man- nutrition, physical activity and medication with glu- agement, such as difficulties interpreting glucose lev - cose levels. They acknowledged that changes in any of els and adjusting medication when needed. Providing these factors could cause hypoglycaemic events, and instructions how to adjust insulin can reduce the fre- they believed to have enough knowledge to use their quency of hypoglycaemia in T2D patients . Over diabetes medication. However, some of them seem C rutzen et al. BMC Fam Pract (2021) 22:114 Page 11 of 13 to lack the ability to translate general knowledge into importance of support from partners for the manage- adequate actions to prevent hypoglycaemic events from ment and prevention of hypoglycaemic events. In the happening. This is in line with findings from a recent majority of the patients who have a partner, this part- study among T2D patients with low health literacy, ner often recognizes and helps dealing with hypogly- where most participants first expressed that they had caemic events. When a T2D patient loses his or her an adequate level of medication self-management but partner the combination of stress, grief and loss of sup- additional questions showed that this was often insuf- port put these patients at more risk of hypoglycaemic ficient . events. Negative emotions such as stress, grief and cogni- Finally, in line with previous studies, we found that tive overload can influence self-management. Stress is patients were not always able to identify the cause of a factor that may have mixed effects on glucose levels. their hypoglycaemic events [12, 13]. This leads to the Stress can increase glucose levels but stress can also perception that they cannot prevent these events. This hinder self-management in diabetes patients [31, 32]. is especially problematic since the majority suffers from Our study confirms that many patients with T2D expe - impaired hypoglycaemia awareness. rience stress regularly, which may be difficult to man - age by T2D patients . Previous research showed Strengths and limitations that the impact of stress on self-management could be This study is unique in investigating self-identified causes particularly problematic in diabetes patients with low of hypoglycaemia and underlying self-management issues self-efficacy . among people with T2D using a mixed methods design. Belief about capabilities can play an important role in The design allowed us to investigate in a qualitative study how older people deal with physical activity. Especially the behavioural related factors preceding hypoglycaemia inactive older people tend to overestimate what they can from the perspective of patients and subsequently quan- handle physically, increasing the risk of hypoglycaemia tify these factors in a larger population. By using the TDF . Physical activity not only increases energy expendi- in both the development of our topic list and the coding ture but can also result in a prolonged increase in insulin of the interviews, we were able to get a comprehensive sensitivity. To prevent hypoglycaemia after exercising less picture of self-management issues related to the domains insulin or additional carbohydrate intake is needed . that can influence behaviour and obstruct behavioural Injecting less insulin is especially important to counter change . Some limitations of this study need to be the increase in insulin sensitivity but few survey respond- taken into account when interpreting the results. Recruit- ents knew how to adjust medication when they exercised ment for the interviews was done in the Northern part more than usual. of the Netherlands. Although health care for people with Some specific issues with medication were identi - T2D is organized similarly across the Netherlands, there fied, such as not remembering whether medication was are regional differences in the general population which already taken or not taking medication at regular times. may influence how patients experience and cope with Problems with memory and attention can lead to acci- their disease in general and with hypoglycaemia specifi - dental overdosing of medication. In turn this can lead to cally. Due to the limited recruitment area and due to the a severe hypoglycaemic event but in line with other stud- exclusion of non-Dutch speaking participants we may ies, patients in our study seldom acknowledged this as a have missed some causes of hypoglycaemia in the inter- cause [14, 16]. views. Due to the cross-sectional design of the survey no Intrinsic motivation is an important factor in engag- causal relationships can be established between hypogly- ing in self-management [35, 36]. Our interview study caemia and self-management issues. Furthermore, our showed that for some patients hypoglycaemic were rela- study relies on self-report, which is inherent to inter- tively mild and considered unimportant because other views and surveys. Participants mentioned that they did health-related issues inflicted a much higher burden on not always know what the cause was of their hypoglycae- them. This low priority could prevent people with T2D mic events. Because we relied on self-reporting we do not from taking the necessary steps to prevent hypoglycae- know whether these events were unpredictable or that an mic events.Most respondents in our survey did not expe- underlying lack of knowledge made it difficult for patient rience very frequent or severe events. to identify a cause. Furthermore, not all topics addressed Social influences and support can be important for in the interviews were translated to corresponding ques- self-management of chronic diseases like T2D . tions in the survey. For instance, where some patients Involving family members in self-management educa- expressed that their hypoglycaemic events were relatively tion has shown to have a positive effect on the man - mild and unimportant, we only quantified the frequency agement of T2D . Our study also illustrated the and severity of the hypoglycaemic events in the survey. Crutzen et al. BMC Fam Pract (2021) 22:114 Page 12 of 13 Acknowledgements Finally, there may be a risk of recall bias for the self-iden- The authors would like to express our gratitude to the Royal Dutch Pharma‑ tified causes because for some of the participants the last cists Association (KNMP) for providing funds to perform this study. hypoglycaemic event was relatively long ago. Authors’ contributions SC, PD and KT: research idea and study design. SC and TB: Data acquisition. SC, Implications for clinical practice TB,PD and KT: analysis and interpretation. PD and KT: supervision or mentor‑ Our findings underline the importance of offering per - ship. All authors contributed substantially to the intellectual content during manuscript drafting or revision. All authors approved the manuscript and this sonalized and easy to access support to address acute submission. problems as well as changing needs for self-manage- ment support . Our findings are also useful to revise Funding An unconditional grant was provided by the Royal Dutch Pharmacists Associa‑ self-management programs for people with T2D. An tion (KNMP), they had no role in the execution of this study or in the drafting important component of many self-management edu- of the article. cation programs is knowledge transfer . Providing Availability of data and materials knowledge is an important step but may be insufficient The datasets generated and analysed during the current study are not publicly to improve actual self-management . Our study sug- available as this would be in conflict with the informed consent given by the gests that patients need hands-on practice on how to participants, but are available from the corresponding author on reasonable request. balance their medication, nutrition and physical activity when there are deviations from daily routine. Also, pro- Declarations grams need to address how to deal with stress and how to improve self-efficacy related to managing stress, par - Ethics approval and consent to participate ticularly in those with a lack of social support. Finally, The Medical Ethics Review Board of the University Medical Center Gronin‑ gen provided a waiver for Research Involving Human Subjects Act ( WMO) tailored support is needed for the group of patients approval because it is not a clinical research with human participants as who suffer from hypoglycaemia in combination with meant in the Medical Research Involving Human Subjects Act. Approval was poorly controlled glucose levels. Relaxing haemoglobin therefore given to perform the study as a non‑ WMO study with all rules and regulation that apply to non‑ WMO research. For all participants in both the A1c (HbA1c) targets is not an option since they are in a interviews and the survey informed consent was collected. vicious circle of alternating high and low glucose levels. These patients need to be trained in self-management to Consent for publication Not applicable. prevent both hypoglycaemic and hyperglycaemic events. Competing interests The authors have no competing of interests to declare. Conclusion This study provides insights in the behavioural causes Author details of hypoglycaemia and the underlying self-management Department of Clinical Pharmacy and Pharmacology, University Medical Centre Groningen, University of Groningen, Groningen, Netherlands. Unit issues from the perspective of people with T2D. It under- of PharmacoTherapy, Epidemiology and Economics, Groningen Research lines the importance of daily routines, having the knowl- Institute of Pharmacy, University of Groningen, Groningen, The Netherlands. edge on how to adjust medication in relation to changes Received: 22 December 2020 Accepted: 17 May 2021 in physical activity, food intake or illness, and the ability to deal with stress to prevent hypoglycaemic events. Guidelines and regulations References All methods were carried out in accordance with relevant 1. Williams SA, Pollack MF, DiBonaventura M. 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BMC Family Practice – Springer Journals
Published: Jun 14, 2021
Keywords: Type 2 diabetes; Hypoglycaemia; Self-management; Patient perspective; Mixed methods
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