Abstract
Background
Severe hypoglycemia is a serious adverse drug event associated with hypoglycemia-prone medications; older patients with diabetes are particularly at high risk. Economic food insecurity (food insecurity due to financial limitations) is a known risk factor for hypoglycemia; however, less is known about physical food insecurity (due to difficulty cooking or shopping for food), which may increase with age, and its association with hypoglycemia.
Objective
Study associations between food insecurity and severe hypoglycemia.
Design
Survey based cross-sectional study.
Participants
Survey responses were collected in 2019 from 1,164 older (≥ 65 years) patients with type 2 diabetes treated with insulin or sulfonylureas.
Main Measures
Risk ratios (RR) for economic and physical food insecurity associated with self-reported severe hypoglycemia (low blood glucose requiring assistance) adjusted for age, financial strain, HbA1c, Charlson comorbidity score and frailty. Self-reported reasons for hypoglycemia endorsed by respondents.
Key Results
Food insecurity was reported by 12.3% of the respondents; of whom 38.4% reported economic food insecurity only, 21.1% physical food insecurity only and 40.5% both. Economic food insecurity and physical food insecurity were strongly associated with severe hypoglycemia (RR = 4.3; p = 0.02 and RR = 4.4; p = 0.002, respectively). Missed meals (“skipped meals, not eating enough or waiting too long to eat”) was the dominant reason (77.5%) given for hypoglycemia.
Conclusions
Hypoglycemia prevention efforts among older patients with diabetes using hypoglycemia-prone medications should address food insecurity. Standard food insecurity questions, which are used to identify economic food insecurity, will fail to identify patients who have physical food insecurity only.
Supplementary Information
The online version contains supplementary material available at 10.1007/s11606-024-08801-y.
INTRODUCTION
Food insecurity occurs when people don't have enough to eat and don't know where their next meal will come from; in the United States, food insecurity affects over 44 million people.1 Rates of “economic food insecurity”, defined as a lack of consistent access to enough food due to financial limitations (e.g., food running out before having enough money to buy more)2 have almost doubled in the past 20 years among older adults.3,4 Economic food insecurity is typically identified using a standard set of questions (USDA Household Food Security Survey Module (HFSSM))2 which can miss patients with physical food insecurity or other, non-financial reasons.5 An NHANES study found that a quarter of older (≥ 60 years) adults in the U.S, experienced physical food insecurity (difficulty shopping for food and preparing meals) despite living in an economically food secure household.6
Several observational studies and the ACCORD Trial have documented that missed meals or other food-related behaviors (e.g., neglecting to consume sufficient carbohydrates after taking a rapid-acting insulin or sulfonylurea) are the most common antecedents of hypoglycemia.7–9 More recent studies have shown economic food insecurity to be a strong risk factor for hypoglycemia in low-income, safety-net populations.10,11 Hypoglycemia is the most common and serious adverse drug event associated with glucose-lowering medications, particularly insulin and sulfonylureas; it surpassed hyperglycemia as a cause of hospital admissions among older diabetes patients12–14 and has become a critical public health and drug safety concern.15–17 Severe hypoglycemia is defined as an event necessitating assistance from another person to actively administer carbohydrates, glucagon, or other resuscitative actions.18 We estimated that ~ 95% of severe hypoglycemic events are handled outside of the healthcare system and not captured in the electronic medical record;19 thus self-report provides a more complete capture of severe hypoglycemia. Among patients with diabetes, severe hypoglycemia has been associated with a tripling of the risk of mortality,20–23 as well as substantial increases in cognitive decline,24–28 stroke,29 falls,30,31 fall-related fractures,32 motor vehicle accidents,33 and cardiovascular events;34–36 as well as poorer quality of life37,38 and emotional challenges.39 Hypoglycemia risk and the clinical consequences of hypoglycemia increase steeply with age.14,40 Hypoglycemia among older patients with diabetes is now a National Committee for Quality Assurance (NCQA) quality measure (Healthcare Effectiveness Data and Information Set (HEDIS)) and targeting hypoglycemia prevention interventions to high-risk, older patients is a national public health objective.41 At risk patients should be screened for economic food insecurity which is a known risk factor for hypoglycemia. However, it is unknown whether physical food insecurity is also a risk factor for hypoglycemia.
We used patient-reported data from the Diabetes and Aging Study42 to examine economic and physical food insecurity and their associations with severe hypoglycemia in older patients with type 2 diabetes taking insulin or sulfonylureas.
METHODS
During 2019, the Diabetes and Aging Study surveyed a cohort of older patients with type 2 diabetes who were community-dwelling members of Kaiser Permanente Northern California (KPNC) without a diagnosis of cognitive impairment using age-stratified (65–74, 75–84, 85–100 years of age), random sampling (N = 6,000, 50.5% female).42 The goal of the survey was to capture patient-reported outcome data not routinely available in the electronic health record. A written survey was mailed to each participant in their preferred language (English, Spanish or Chinese) with an option to complete the survey by telephone interview or online in their preferred language. Of the 2,246 survey respondents (40.7% response rate), we excluded those not treated with insulin or sulfonylureas (n = 1,036), no longer KPNC members at the time of the survey (n = 6), and not having type 2 diabetes (n = 40); the remaining 1,164 were the basis for these analyses. In Supplemental Table 1, we detail age-specific, baseline characteristics of the survey cohort and the sampling frame of older adults with diabetes; variables included: demographics, limited English proficiency,43 Neighborhood Deprivation Index,44, 45 smoking, sedentary behavior (no physical activity),46 continuous medication gaps based on pharmacy dispensing,47 self-monitoring of blood glucose, underweight, HbA1c, chronic kidney disease, Charlson co-morbidity score,48 use of glucose-lowering medications, outpatient, ED and inpatient utilization.
We studied: i) self-reported economic and physical food insecurity and their associations with self-reported severe hypoglycemia; and ii) reasons endorsed by patients for their low blood sugar. Economic food insecurity was defined by responses of “often” or “sometimes” to the standard USDA food insecurity question:49 “In the past 12 months, how often did the food you bought just not last and you didn't have money to get more?”. Physical food insecurity was defined by responses of “often” or “sometimes” to the following question developed specifically for our survey: “In the past 12 months, how often did you not have enough food to eat because of difficulty cooking or shopping for food?”. Survey respondents were also asked to endorse reasons for low blood sugar from a proffered list (all that apply): skipped a meal, did not eat enough or waited too long to eat; did more physical activity than usual; was sick or had an infection; made a mistake with my insulin (wrong type, dose or timing of insulin); took too many diabetes pills by mistake; changed my dose of insulin or other diabetes medication; drank too much alcohol; started a new diabetes medication (pills or shots); other.
The primary outcome was self-reported severe hypoglycemia based on the question: “In the past 12 months, have you had low blood sugar that resulted in passing out or needing help from someone else? (For example, you were unable to treat yourself, were unconscious or were given glucagon or intravenous glucose)”, originally developed and validated as part of the Diabetes Care Profile.50–52
Relative risks (RR) were estimated from log binomial regression models of severe hypoglycemia with robust error variance. The models were adjusted for several variables that could confound the relationship between food insecurity and severe hypoglycemia including age, frailty (based on Segal’s Frailty Index ≥ 0.2)53, HbA1c, Charlson comorbidity score and general financial strain.54 Financial strain was based on the survey item: “During the past 12 months, how often did it happen that you did not have enough money to buy food, clothes or other things you needed?”; because responses were highly skewed, they were dichotomized as never versus ever.
To evaluate the face validity of our survey items, the rates of physical and economic food insecurity were compared among respondents who reported financial stress (insufficient funds to pay for basic needs) and those who were financially secure.
All statistics were weighted to account for the complex sampling design using the inverse of the sampling fractions in the age-stratified sampling design and survey non-response using inverse probability censoring weighting. This study was approved by the Kaiser Permanente Northern California (KPNC) Institutional Review Board.
RESULTS
The survey cohort was demographically similar to the sampling frame (i.e., cohort from which we derived our sample), but respondents were less likely to be female or minority, to have limited English proficiency or to live in a deprived neighborhood (supplemental Table 1). Compared to the sampling frame, respondents were less likely to smoke or be poorly adherent to cardiometabolic medications and more likely to be sedentary and to self-monitor their blood sugar. Compared to the sampling frame, respondents had similar mean HbA1c, proportions in good glycemic control (HbA1c < 7%) but smaller proportion in poor glycemic control (HbA1c > 9%); there was a greater proportion with chronic kidney disease; and similar proportions were underweight (BMI < 18 kg/m2). Respondents had higher levels of health care utilization (outpatient visits, emergency department visits or inpatient stays) in the 2 years prior to baseline.
Food insecurity was reported by 12.3% of the respondents. Among those with food insecurity, 38.4% reported only economic food insecurity, 21.1% reported only physical food insecurity, and 40.5% reported both types of food insecurity. Economic and physical food insecurity were most prevalent among participants reporting financial strain (50.0% and 30.1%, respectively), but was also reported by financially secure respondents (1.2% and 2.8%, respectively).
Among the 1,164 survey respondents with type 2 diabetes treated with insulin or sulfonylureas (mean (SD) age: 74.5 (6.5) years), 62 (5.4%) reported a severe hypoglycemic event in the last 12 months (Table 1).
Table 1.
Sample Characteristics of Older Patients on Insulin or Sulfonylureas Stratified by Food Insecurity (n = 1,164)*
| All (N = 1164) N (weighted percent†) |
Food insecurity (N = 107) N (weighted percent†) |
No food insecurity (N = 1026) N (weighted percent†) |
p-value | |
|---|---|---|---|---|
| Age, mean (SD), years | 74.5 (6.5) | 73.7 (6.5) | 74.7 (6.5) | 0.11 |
| Ages 65–74 | 365 (60.4) | 39 (66.8) | 326 (60.8) | 0.42 |
| Ages 75–84 | 459 (32.0) | 42 (26.7) | 402 (31.9) | |
| Ages 85–100 | 340 (7.6) | 26 (6.6) | 298 (7.3) | |
| Female | 516 (44.7) | 53 (41.7) | 442 (43.9) | 0.73 |
| Race and Ethnicity | 0.001 | |||
| African American | 98 (9.1) | 17 (14.6) | 75 (7.8) | |
| Asian | 212 (21.6) | 34 (30.3) | 175 (20.6) | |
| Latino | 137 (14.2) | 15 (17.5) | 115 (13.4) | |
| Multiethnic/Other | 66 (5.8) | 7 (11.9) | 54 (4.9) | |
| White | 651 (49.3) | 34 (25.7) | 607 (53.3) | |
| Financial strain | 167 (19.2) | 68 (77.1) | 93 (10.4) | < 0.0001 |
| HbA1c (mean, SD) | 7.71 (1.47) | 8.13 (1.6) | 7.60 (1.4) | < 0.0001 |
| Multi-comorbid burden‡ | 769 (56.2) | 74 (59.7) | 674 (56.1) | 0.0009 |
| Frailty§ | 449 (18.5) | 41 (18.6) | 394 (18.6) | 1.00 |
| Hypoglycemia-prone medications dispensed | 0.41 | |||
| Insulin only | 342 (28.4) | 32 (29.5) | 303 (28.1) | |
| Sulfonylurea only | 595 (51.9) | 52 (45.5) | 526 (53.1) | |
| Insulin and sulfonylurea | 227 (19.8) | 23 (25.0) | 197 (18.7) | |
| Economic food insecurity (due to financial limitations) | 75 (9.9) | 75 (78.8) | 0 | NA |
| Physical food insecurity (due to difficulty cooking or shopping for food) | 72 (7.6) | 72 (61.5) | 0 | NA |
| Self-reported severe hypoglycemia episode in the past 12 months | 62 (5.4) | 11 (15.3) | 48 (4.1) | 0.0002 |
Among respondents who self-reported hypoglycemia symptoms, the most common reason (78%) endorsed for their hypoglycemia was “skipped a meal, did not eat enough or waited too long to eat” (Table 2).
Table 2.
Self-Reported Reasons* for Hypoglycemia among 468 Older Patients on Insulin or Sulfonylureas
| Self-reported reason | N | Weighted percentage† |
|---|---|---|
| Skipped a meal, did not eat enough or waited too long to eat | 365 | 77.5% |
| Did more physical activity than usual | 157 | 34.2% |
| Was sick or had an infection | 47 | 10.3% |
| Changed my dose of insulin or other diabetes medication | 28 | 7.2% |
| Made a mistake with my insulin (wrong type, dose or timing of insulin) | 31 | 5.3% |
| Other | 12 | 2.2% |
| Started a new diabetes medication (pills or shots) | 12 | 1.9% |
| Drank too much alcohol | 6 | 1.4% |
| Took too many diabetes pills by mistake | 3 | 0.8% |
| Don’t know | 35 | 7.9% |
*Question: “If you have ever had low blood sugar, was it because of any of the following reasons (check all that apply)?”
†Weights account for both the age-stratified random sampling design as well as survey non-response
Food insecurity overall (i.e., food insecurity due to either economic or physical food insecurity) was strongly associated with severe hypoglycemia (RR = 4.1 (95% CI, 1.7–9.9); p = 0.002) after adjusting for age, frailty, HbA1c, Charlson comorbidity score and financial strain (Table 3). Economic food insecurity and physical food insecurity were each independently strongly associated with severe hypoglycemia (RR = 4.3 (95% CI, 1.3–14.0); p = 0.02 and RR = 4.4 (95% CI, 1.8–10.8); p = 0.002, respectively). There was an even stronger association with severe hypoglycemia when economic and physical food insecurity were both present relative to being food secure or having only one type of food insecurity (RR = 5.4 (95% CI, 1.5–19.2); p = 0.009).
Table 3.
Bivariate and Multivariate Associations of Food Insecurity and Severe Hypoglycemia: Weighted* Frequencies and Relative Risks (95% CI) from Weighted Log-Binomial Regression Analyses
| Variable Name | Level | Total participants No. (%) | Self-reported severe hypoglycemia, Weighted Row % | Unadjusted (bivariate) Relative Risk (95% CI; p-value) | Adjusted† Relative Risk (95% CI; p-value) |
|---|---|---|---|---|---|
| Any food insecurity | No | 993 (90.9) | 4.1 | REF | REF |
| Yes | 100 (9.2) | 15.3 | 3.76 (1.82–7.76; p = 0.0003) | 4.12 (1.71–9.92; p = 0.002) | |
| Economic food insecurity (due to financial limitations) | No | 1006 (93.3) | 4.3 | REF | |
| Yes | 72 (6.7) | 16.4 | 3.80 (1.74–8.32; p = 0.0008) | 4.31 (1.33–14.02; p = 0.02) | |
| Physical food insecurity (due to difficulty cooking or shopping for food) | No | 1020 (94) | 4.1 | REF | |
| Yes | 65 (6) | 18.6 | 4.52 (2.07–9.88; p = 0.0002) | 4.36 (1.76–10.78; p = 0.002) | |
| Both economic and physical food insecurity‡ | No | 1064 (96.4) | 4.4 | REF | |
| Yes | 40 (3.6) | 22.6 | 5.18 (2.16–12.4; p = 0.0002) | 5.44 (1.54–19.23; p = 0.009) |
*In 1,122 patients who responded to question about severe hypoglycemia. Weights account for both the age-stratified random sampling design as well as survey non-response
†Adjusted for age, frailty, HbA1c, Charlson comorbidity score and financial strain
‡The reference group includes patients who have no or only one type of food insecurity (i.e., either economic or physical) but not both
DISCUSSION
In this survey study of older patients with type 2 diabetes on insulin or sulfonylureas, food insecurity was common (~ 12%) and strongly associated with the risk of severe hypoglycemia. In prior research conducted among low-income safety-net populations, economic food insecurity was associated with a greater risk of severe hypoglycemia among patients with type 2 diabetes.10,56 This study extends previous findings by demonstrating that physical food insecurity is associated with a more than fourfold higher risk of severe hypoglycemia among older patients with type 2 diabetes. Difficulty cooking or shopping for food represent underrecognized and potentially modifiable risk factors for severe hypoglycemia.
Economic food insecurity is common among older patients and affects one in seven Americans overall (with higher rates among lower income individuals).57 Economic food insecurity has been linked to greatly increased risk of hypoglycemia-related emergency department visits.10 Those findings were further validated as patients experiencing severe hypoglycemia were more likely to attribute hypoglycemia episodes to their inability to afford food.56 Individuals with household incomes below the national median, often exhaust their food budgets by the end of the month; this monthly cycle of financial strain may explain higher rates of hypoglycemia-related emergency department visits and hospitalizations at the end of the month.58 Moreover, financial strain could also impact physical food security (e.g., lack of transportation to get groceries). Physical food insecurity has received much less attention compared to economic food insecurity. We found that the economic and physical food insecurity should both be evaluated as they often do not occur together. Moreover, each type of food insecurity is associated with severe hypoglycemia, and each likely requires a different type of intervention.
Our results must be interpreted in the context of the observational, cross-sectional study design and, while suggestive, cannot be considered causal. Because both the exposures and outcomes were gathered simultaneously from survey data, these findings could be attributable to reverse causality. That said, reverse causality while theoretically possible, is unlikely as it would require severe hypoglycemia (which is a transient, short-term state) to cause subsequent food insecurity (which is typically episodic or longer-term circumstance). While we observed a robust association between economic or physical food insecurity and hypoglycemia (relative risks of 4.3 and 4.4, respectively), it's important to acknowledge that residual confounding might still influence these observations. Therefore, it is essential to cautiously interpret these results as exploratory in nature, despite our efforts to account for potential confounding factors. That said, food insecurity is associated with hypoglycemia and identifies a population at risk even though that relationship may not be entirely causal. Current national food insecurity surveys focus on economic food insecurity and there are no validated questions that evaluate physical food insecurity. Accordingly, the question regarding physical food insecurity was developed de novo and has not been psychometrically tested or externally validated. Psychometric research to develop the best performing instrument to identify physical food insecurity would be beneficial. Additional limitations include the 40.7% non-response rate, which may have impacted findings. While the prevalence of food insecurity in the U.S. has increased in 2022 compared with 201959 at the time of conduct of the survey, we assume that the relationship between food insecurity and hypoglycemia is unlikely to be affected by these changes. Even though missed meals was endorsed as a primary reason for hypoglycemia, objective data on missed meals was not available, and we can make no conclusions about their mediating role in the pathway from food insecurity to severe hypoglycemia. Reliance on self-reported hypoglycemia provides a more complete capture than EHR data given most severe hypoglycemic events are cared for outside of the medical system and are not recorded.19 We did not include patients with type 1 diabetes in this survey sample and thus cannot address whether the findings generalize to that group.
Current clinical standards for diabetes care fail to adequately address both economic and physical food insecurity in vulnerable populations.60–62 Food insecurity is an important structural and social determinant of health63 and healthcare providers should consider food insecurity screening and interventions to be critical components of diabetes care for vulnerable populations.64 Although clinicians may not be able to directly improve food security for their patients, clinicians can use information about food insecurity to tailor an insulin regimen that is safer for the patient (i.e., “social risk-informed care”), or they can target food insecurity through a referral to social services or to other community programs (i.e., “social risk-targeted care”).65 A randomized trial of medically-tailored meal delivery significantly reduced hypoglycemia in vulnerable patients with type 2 diabetes who had economic food insecurity.66 Understanding the causes of food insecurity should help inform the choice of intervention (e.g., referral to food pantry for economic food insecurity versus home health aide for physical food insecurity). Additional research is needed to study interventions to address physical and economic food insecurity in older patients with diabetes and evaluate whether those interventions reduce the risk of hypoglycemia.
CONCLUSIONS
This study found that food insecurity more than quadruples the risk of severe hypoglycemia among older patients with type 2 diabetes. These findings are important given rates of food insecurity among older adults more than tripled during the periods 1999–2003 to 2015–2019.3 This study disaggregated economic food insecurity and physical food insecurity and examined their separate associations with severe hypoglycemia. The physical and economic causes of food insecurity may require distinct solutions; failure to consider both causes can lead to underestimating the burden of food insecurity, overlook a segment of the population who need food assistance or interventions to prevent the clinical consequences of food insecurity or lead to inappropriate responses to different underlying problems. In research and practice, standard food insecurity questions are often limited to querying only about economic food insecurity which will fail to identify patients (1 in 5 older patients with diabetes in our study) who have physical food insecurity only.
Supplementary Information
Below is the link to the electronic supplementary material.
Abbreviations
- EHR
Electronic health record
- KPNC
Kaiser Permanente Northern California
- ED
Emergency department
Author Contributions
AJK, ESH, HHM, JYL, KJL, MMP, NL, RWG designed the survey. AJK and MMP researched the data. AJK, KJL, MMP, HHM wrote the first draft of the manuscript. All authors reviewed and edited the manuscript. All authors approved the final version of the manuscript.
AJK is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Funding
This research was supported by funding from grants from National Institute of Aging (R01-AG051683: Preferences, Management, and Outcomes in the Oldest Patients with Diabetes and R01-AG063391: Optimizing Medical Decision Making for Older Patients with Type 2 Diabetes) and National Institute of Diabetes and Digestive and Kidney Diseases (Centers for Diabetes Translational Research: P30 DK092924 (Karter and Seligman) and P30 DK092949 (Huang and Laiteerapong)). Funding from Centers for Medicare & Medicaid Services to develop and evaluate publicly reported quality measures and royalties from UpToDate (Lipska).
Declarations:
IRB Approval
Kaiser Permanente Northern California Institutional Review Board approved the study.
Conflicts of Interest:
The authors declare that they do not have a conflict of interest.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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