The Association Between Handgrip Strength and Diabetes on Activities of Daily Living Disability in Older Mexican Americans

Abstract

Objective: The aim of this study is to determine the independent and joint effects of muscle weakness and diabetes on incident activities of daily living (ADL) disability in older Mexican Americans. Method: A subsample of 2,270 Mexican Americans aged at least 65 years at baseline were followed for 19 years. Handgrip strength was normalized to body weight (normalized grip strength [NGS]). Weakness was defined as NGS ≤0.46 in males and ≤0.30 in females. Diabetes and ADL disability were self-reported. Results: Compared with participants that were not weak and did not have diabetes, those that had diabetes only, were weak only, and were both weak and had diabetes experienced a 1.94 (95% confidence interval [CI] = [1.89, 1.98]), 1.17 (CI = [1.16, 1.19]), and 2.12 (CI = [2.08, 2.16]) higher rate for ADL disability, respectively. Discussion: Muscle weakness and diabetes were independently and jointly associated with higher rates for ADL disability in older Mexican Americans.

Keywords

aging geriatrics health muscle strength muscle weakness

Introduction

Life expectancy in both men and women has increased domestically and globally (World Health Organization, 2012), and yet, there has been a 71.8% median increase in diabetes-related mortality in the United States, and diabetes remains a leading cause of death worldwide (Guariguata et al., 2014; Murray et al., 2013). The number of years persons with diabetes are living with this disease and diabetes prevalence has also risen in older adults (Hung, Ross, Boockvar, & Siu, 2011; Murray et al., 2013). The expanding prevalence of older adults with chronic diseases such as diabetes often results in a variety of health-related complications. For example, older adults with diabetes have functional impairments associated with a diminished health status, thereby increasing their rate for incident activities of daily living (ADL) disability (Bruce, Davis, & Davis, 2005; Sinclair, Conroy, & Bayer, 2008). Moreover, other diabetes-related complications, such as neuropathy, are associated with reduced muscle strength and a higher risk for ADL disability in older adults (Almurdhi et al., 2016; Wong et al., 2013).

The age-related changes in body composition that occur from increased adipose tissue and reduced muscle mass also leads to a variety of functional limitations and disabilities in older adults, including ADL disability (Germain, Batsis, Vasquez, & McQuoid, 2016; Zamboni, Mazzali, Fantin, Rossi, & Di Francesco, 2008). The strong predictive ability of muscle weakness on ADL disability in various older adult populations has been demonstrated in both cross-sectional and longitudinal investigations (Vermeulen, Neyens, van Rossum, Spreeuwenberg, & de Witte, 2011). Many of the negative health outcomes associated with muscle weakness are of particular concern for older adults of Mexican descent, as they have lower skeletal muscle mass and greater total fat mass than older non-Hispanic White and non-Hispanic Black adults (Aleman Mateo et al., 2009). Muscle weakness has also been shown to be an independent predictor of ADL disability in older Mexican Americans (Al Snih, Markides, Ottenbacher, & Raji, 2004).

The prevalence of diabetes remains alarmingly high among Mexican Americans relative to other ethnicities in the United States (Spanakis & Golden, 2013). Furthermore, the risk of obesity, diabetes, and disability is greater in Hispanic and Mexican American older adults compared with other older adult populations (Gregg et al., 2014; Markides et al., 1999; Ogden, Carroll, Kit, & Flegal, 2014). This is concerning because the Mexican American population is estimated to increase in the United States by almost 115% between the years 2014 and 2060 (Colby & Ortman, 2015). Despite the known links between muscle weakness, diabetes, and ADL disability, the independent and joint contributions of weakness and diabetes on predicting ADL disability in older Mexican Americans remain unclear. Therefore, the purpose of this study was to determine the independent and joint associations of muscle weakness and diabetes on incident ADL disability in older Mexican Americans.

Method

Data Source and Participants

An analysis of data was conducted from the Hispanic Established Population for the Epidemiological Study of the Elderly (HEPESE), an ongoing longitudinal study of Mexican Americans aged at least 65 years living in Arizona, California, Colorado, New Mexico, and Texas. The primary goal of the HEPESE is to estimate the prevalence of important physical and mental health conditions and functional impairments in older Mexican Americans, and to compare these estimates with those of other older adult populations. An area probability sampling procedure was used to ensure representativeness of older Mexican Americans in the Southwest region of the United States. Sample weights were used in all analyses to account for the sampling method and to compensate for the differential probability selection that was applied during data collection. As a result of weighting the dataset, HEPESE participants represent approximately 500,000 Mexican Americans aged at least 65 years that reside in the Southwest region of the United States. At baseline (Wave 1; 1993-1994), 3,050 older Mexican Americans (2,873 in person and 177 by proxy) participated in interviews (conducted in English or Spanish languages) and limited medical assessments with a participant response rate of 83.0%, which is comparable with other epidemiological studies of the elderly (Cornoni-Huntley et al., 1990). Participants were followed for 19 years after baseline measures and follow-ups were conducted in Wave 2 (1995-1996; n = 2,438), Wave 3 (1998-1999; n = 1,980), Wave 4 (2000-2001; n = 1,682), Wave 5 (2004-2005; n = 1,167), Wave 6 (2006-2007; n = 921), Wave 7 (2010-2011; n = 659), and Wave 8 (2012-2013; n = 452). Newly enrolled participants from Wave 5 (n = 902), Wave 6 (n = 621), Wave 7 (n = 419), and Wave 8 (n = 292) that did not take part in baseline measures were excluded. Participants provided informed consent to participate in the study and HEPESE protocols were approved by the University of Texas Medical Branch Institutional Review Board.

Measures

A hand-held dynamometer (Jamar Hydraulic Dynamometer model #5030J1; J. A. Preston Corporation, New York, NY) was used to assess handgrip strength; the test protocol is described in detail elsewhere (Alfaro-Acha et al., 2006; Al Snih et al., 2004). Measuring handgrip strength with a hand-held dynamometer has been shown to be reliable and valid in older adults (Al Snih et al., 2004; Legrand et al., 2013). Handgrip strength was normalized to body weight (normalized grip strength [NGS]; grip strength [kg] / body weight [kg]). Male participants were considered weak if their NGS was ≤0.46; whereas, female participants were considered weak if their NGS was ≤0.30. NGS cut points were specific to the age and ethnicity of the participants in the present investigation (Peterson, McGrath, et al., 2016). Participants who self-reported that a doctor had ever diagnosed them with diabetes were classified as having diabetes.

The primary outcome variable was incident ADL disability, which was determined with a modified version of the Katz ADL questionnaire. ADL parameters questioned participants about their ability to walk across a small room, bathe, groom, dress, eat, transfer from a bed to a chair, and use a toilet, as previously described (Al Snih et al., 2004). Continence was removed from the Katz ADL scale because incontinence may be present in persons that display no ADL disability; however, grooming and ability to walk across a small room were added (Branch, Katz, Kniepmann, & Papsidero, 1984; Katz, Ford, Moskowitz, Jackson, & Jaffe, 1963). The short-term test–retest reliability (95%-98%) and internal reliability (α = .90) were both high (Al Snih et al., 2004; Smith et al., 1990). Interviewers asked each participant if they could complete the ADLs without help, if they needed help performing the activity, or if they were unable to perform the activity. Participant responses were dichotomized into having an ADL disability (needed help, or were unable to perform one or more ADLs) or not having an ADL disability (able to complete all ADLs without help). To determine the contribution of baseline muscle weakness and diabetes on incident ADL disability, participants with an ADL disability at baseline were excluded.

Height and body weight were collected in each participant’s home and were rounded to the nearest 0.1 cm and 0.1 kg, respectively. Participants stood next to a tape measure against a wall to determine height and a Metro 9800 scale (Metro Scale & Systems Inc., Fort Myers, FL) was used to determine body weight. Body mass index (BMI) was calculated as body weight in kilograms divided by height in meter squared. Participants with a BMI of ≥30.0 kg/m² were considered obese (Ogden et al., 2014). Self-reported sociodemographic factors at baseline that were included in analyses were sex, marital status, highest grade of education completed, stroke diagnosis, and personal yearly income.

Statistical Analysis

All statistical analyses were performed with SAS 9.4 software (SAS Institute; Cary, NC) and an alpha level of .05 was used for all analyses. To complete a 2 × 2 factorial design, participants were stratified into four separate groups on the basis of their baseline handgrip strength and diabetes categorization: 0 = weakness with no diabetes (reference group), 1 = diabetes only, 2 = weakness only, and 3 = both weakness and diabetes.

A Kaplan–Meier estimator (proc lifetest) was used to determine the median age for incident ADL disability using each group as the strata and to produce respective survival curves. A Cox proportional hazard regression model (proc phreg) was used to examine the independent and joint association between muscle weakness and diabetes on incident ADL disability, using age as the entry variable, and after controlling for sex (male, female), marital status (married, not married), highest grade of education completed, obesity status (obese, not obese), stroke diagnosis (had a stroke, have not had a stroke), and personal yearly income. To avoid multicollinearity with NGS, neither BMI nor body weight was not included in the model as a continuous variable. Data were left-truncated because participants entered the study at different ages and had to be at least 65 years of age to be included in the HEPESE. To account for this, time was defined as the number of years since age 65. Right censoring occurred if participants did not have ADL disability at the end of follow-up, were lost to follow-up, or died. More information regarding the details and interpretation of a Cox model has been published elsewhere (Spruance, Reid, Grace, & Samore, 2004).

A sensitivity analysis was conducted to account for potentially influential observations. First, outliers in the outcome variable were identified using deviance residuals. As previously recommended, observations with residuals >2.5 were considered influential and were removed (Fitrianto & Jiin, 2013). The model was then rerun without the outliers to determine how estimates changed. If any hazard ratio within the 2 × 2 factorial design changed by more than 10% (a priori threshold), the outliers were considered influential and the results of the sensitively analysis would be presented (Ryan et al., 2015).

Multiple imputation (proc mi) was performed as an additional sensitivity analysis to understand the impact of missingness, by imputing missing data from a distribution of plausible values. Our imputation model was imputed 5 times using participants from the baseline wave (Wave 1). The imputation model for handgrip strength included age, height, body weight, sex, diabetes diagnosis, highest grade of education completed, marital status, obesity status, stroke diagnosis, personal yearly income, interview language, self-reported rating of health, arthritis diagnosis, total number of ADL problems at baseline, and time to ADL disability. These variables were included because they were each factors that may have contributed to missing handgrip strength data. Each of the five datasets were analyzed using the same Cox regression model as the primary analysis. We then combined the results using Rubin’s rules (proc mianalyze)(Rubin, 1976). A Markov Chain Monte Carlo method was used to compute continuous variables that had an arbitrary missing pattern; whereas, a fully conditional specification method using discriminant function methods with 100 burn-in interactions was used for imputed personal yearly income and health status. After imputing handgrip strength, it was normalized to body weight to obtain NGS and then classify participants as weak and not weak. We removed participants with baseline ADL disability before running the Cox model. The results of the multiple imputation procedure are presented as an appendix because we did not plan to impute a priori.

Results

There were 3,050 participants at baseline. Of these, 421 participants had an ADL disability at baseline and were excluded from the subsequent analyses. Another 251 participants were excluded for missing handgrip strength, 25 for missing highest grade of education completed, 70 for missing personal yearly income, and 13 for missing stroke data. After the exclusions, 2,270 participants were included and their baseline descriptive characteristics are presented in Table 1.

Table 1.

Baseline Descriptive Characteristics of the Participants.

	Group 0 (n = 660)	Group 1 (n = 149)	Group 2 (n = 1,015)	Group 3 (n = 446)
Male (%)	32.7	32.2	49.9	47.0
Age (years)	71.5 ± 5.4	71.7 ± 5.2	73.7 ± 6.3	71.9 ± 5.8
Height (cm)	158.9 ± 10.4	158.3 ± 9.8	161.4 ± 10.2	161.5 ± 10.3
Body weight (kg)	65.2 ± 11.6	65.6 ± 11.2	74.6 ± 13.5	77.6 ± 14.5
Body mass index (kg/m²)	25.9 ± 4.4	26.0 ± 3.8	28.7 ± 5.1	29.8 ± 5.6
Obese (%)	17.1	14.0	35.7	65.4
Absolute grip strength (kg)	27.8 ± 8.3	28.1 ± 8.8	20.8 ± 8.3	20.2 ± 8.7
Normalized grip strength	0.43 ± 0.10	0.42 ± 0.09	0.28 ± 0.10	0.26 ± 0.10
Married (%)	56.3	53.6	56.4	65.4
Had a stroke (%)	1.9	5.3	4.1	5.6
Highest grade of education completed	5.1 ± 4.0	5.3 ± 4.4	4.7 ± 3.7	4.8 ± 3.7
Personal yearly income (%)
US$0-US$4,999	41.2	38.9	34.1	33.6
US$5,000-US$9,999	41.2	42.9	51.5	52.4
US$10,000-US$14,999	11.5	12.7	9.1	9.1
US$15,000-US$19,999	3.6	2.6	3.3	2.9
US$20,000-US$29,999	1.8	1.3	0.9	1.3
US$30,000-US$39,999	0.1	0.0	0.3	0.2
US$40,000-US$49,999	0.0	0.0	0.1	0.2
≥US$50,000	0.4	1.3	0.3	0.0

Note. Results are presented as mean ± standard deviation or percentage as indicated. Group 0 = not weak and does not have diabetes; Group 1 = not weak and has diabetes; Group 2 = weak and does not have diabetes; Group 3 = weak and has diabetes.

The Kaplan–Meier estimator revealed the median age to ADL disability for participants that were not weak and did not have diabetes, those that had diabetes only, were weak only, and were both weak and had diabetes was 88.0 (95% confidence interval [CI] = [87.0, 89.0]), 85.0 (CI = [83.0, 87.0]), 87.0 (CI = [87.0, 88.0]), and 84.0 years (CI = [83.0, 86.0]), respectively. Figure 1 provides the Kaplan–Meier curves for time to incident ADL disability across group strata.

Figure 1.

Kaplan–Meier curves for incident activities of daily living disability.

Table 2 shows the covariate-adjusted Cox regression model that was used to determine the independent and joint association between muscle weakness and diabetes on ADL disability. Table 3 presents the results of the sensitivity analysis for the Cox regression model after removing 140 outliers. The sensitivity analysis revealed a 12.1% change in the hazard ratio for participants that had diabetes only, indicating that outlier observations had an influential effect on the results of the Cox model, thereby suggesting the results that underwent the sensitivity analysis should be presented. Accordingly, relative to participants that were not weak and did not have diabetes, those that had diabetes only, were weak only, and were both weak and had diabetes had a 1.94 (CI = [1.89, 1.98]), 1.17 (CI = [1.16, 1.19]), and 2.12 (CI = [2.08, 2.16]) higher rate for incident ADL disability, respectively.

Table 2.

Results of the Cox Proportional Hazard Regression Model for Incident Activities of Daily Living Disability.

	Hazard ratio^a	95% CI
Group 1^b	1.73	[1.69, 1.77]
Group 2^b	1.25	[1.23, 1.27]
Group 3^b	2.10	[2.07, 2.14]
Sex (reference: female)	0.89	[0.88, 0.90]
Married (reference: not married)	0.93	[0.92, 0.94]
Highest grade completed	0.99	[0.98, 0.99]
Obese (reference: not obese)	1.14	[1.12, 1.15]
Stroke (reference: no stroke)	1.37	[1.34, 1.41]
Personal yearly income	0.84	[0.84, 0.85]

Note. CI = confidence interval; Group 1 = not weak and has diabetes; Group 2 = weak and does not have diabetes; Group 3 = weak and has diabetes.

Hazard ratios all p < .0001.

Reference group: Group 0 = not weak and does not have diabetes.

Table 3.

Sensitivity Analysis of the Cox Proportional Hazard Regression Model for Incident Activities of Daily Living Disability.

	Hazard ratio^a	95% CI
Group 1^b	1.94	[1.89, 1.98]
Group 2^b	1.17	[1.16, 1.19]
Group 3^b	2.12	[2.08, 2.16]
Sex (reference: female)	0.93	[0.92, 0.94]
Married (reference: not married)	0.95	[0.94, 0.96]
Highest grade completed	0.99	[0.99, 0.99]
Obese (reference: not obese)	1.22	[1.21, 1.24]
Stroke (reference: no stroke)	1.30	[1.26, 1.33]
Personal yearly income	0.85	[0.84, 0.85]

Note. CI = confidence interval; Group 1 = not weak and has diabetes; Group 2 = weak and does not have diabetes; Group 3 = weak and has diabetes.

Hazard ratios all p < .0001.

Reference group: Group 0 = not weak and does not have diabetes; there were 140 influential outliers.

The results of the multiple imputation procedure to determine the independent and joint association between muscle weakness and diabetes on ADL disability are presented in the appendix Participants that were weak only, those that had diabetes only, and those that were both weak and had diabetes had a 1.52 (CI = [1.39, 1.67]), 1.21 (CI = [1.15, 1.28]), and 1.90 (CI = [1.83, 1.98]) higher rate of incident ADL disability relative to those that were not weak and did not have diabetes, respectively.

Discussion

The principle findings from this investigation demonstrated that the combination of muscle weakness and diabetes was robustly associated with incident ADL disability in older Mexican Americans. Specifically, those that were weak and had diabetes at baseline had the highest rate for ADL disability, as compared with those that had diabetes only or were weak only. Moreover, the rate for incident ADL disability was higher for participants that had diabetes only at baseline versus participants that were weak only, when comparing each group with participants that were not weak and did not have diabetes. These findings demonstrate that muscle weakness and diabetes, both independently and jointly, are associated with an increased rate for incident ADL disability in older Mexican Americans.

The results of this investigation are compatible with previous studies that demonstrated those who were weak only had a higher rate for ADL disability compared with persons that were not weak (Bohannon, 2008; Vermeulen et al., 2011). Another longitudinal investigation of older Mexican Americans demonstrated weakness was associated with ADL disability, whereby participants in the lowest grip strength quartile had the highest risk of incident ADL disability compared with those in the strongest grip strength quartile (Al Snih et al., 2004). Recent cross-sectional and longitudinal studies have also shown muscle weakness is associated with diabetes (McGrath, Vincent, Al Snih, Markides, & Peterson, 2017; Peterson, McGrath, et al., 2016; Peterson, Zhang, Choksi, Markides, & Al Snih, 2016), which in turn may impact disability status in older adults.

Persons with diabetes often experience higher levels of muscle weakness from intramuscular fat accumulation or neuropathy compared with persons without diabetes (Almurdhi et al., 2016), thereby putting older adults with diabetes at increased odds for ADL disability (Kalyani, Saudek, Brancati, & Selvin, 2010). Our results suggest the independent effects of diabetes were associated with a higher rate for ADL disability in older Mexican American compared with persons that were not weak and did not have diabetes. Similar results were seen in a 7-year prospective cohort study of older Mexican Americans, where the presence of diabetes was associated with an increased rate for disability in the lower extremities, including ADL disability (Al Snih et al., 2005). Given the independent associations of muscle weakness and diabetes, the co-occurrence of these conditions may exacerbate the rate for incident ADL disability in this population.

Previous systematic reviews have suggested that muscle weakness and diabetes are associated with ADL disability in older adult populations (Vermeulen et al., 2011; Wong et al., 2013), but the combined effects of both factors on predicting the rate for ADL disability remains unclear. A prospective cohort study of 8,762 men aged 20 to 80 years showed the age-adjusted mortality rates in participants that demonstrated high levels of muscle strength and cardiorespiratory fitness was 60% lower than participants that were weak and unfit (Ruiz et al., 2008). The results of our Cox proportional hazard regression models indicate that the incidence of ADL disability was highest in older Mexican Americans that were both weak and had diabetes at baseline, compared with those that were not weak and did not have diabetes at baseline. This suggests that the co-occurrence of muscle weakness and diabetes potentiates the rate for ADL disability in older Mexican Americans. Considering the independent and joint associations of muscle weakness and diabetes on ADL disability, older Mexican Americans may benefit from adopting healthy behaviors earlier in life to avoid or postpone the development of these factors later in life as outlined by the Diabetes Prevention Program (2008). Furthermore, older Mexican Americans that are weak and have diabetes may experience an improvement in ADL function by engaging in behavior change strategies that aim to improve strength (e.g., physical activity, particularly resistance exercise) and manage diabetes (Chou, Hwang, & Wu, 2012; Hamman et al., 2006; Tak, Kuiper, Chorus, & Hopman-Rock, 2013). Continued investigations of how chronic diseases and functional limitations can be prevented through behavior change are necessary to help shape the development of cost-effective prevention programs and health policy change.

Some limitations of the present investigation should be noted. Although our results highlight the effects of muscle weakness and diabetes on incident ADL disability in older Mexican Americans, these findings may lack generalizability to Mexican Americans residing outside the five states included in this investigation or other Hispanic American populations. The assessment of diabetes and ADL disability was self-reported, which may have led to misinterpretation and inconsistencies between reported diabetes and ADL disability. However, the present investigation has a number of strengths. Data used in this investigation were from a large cohort of older Mexican Americans, followed for 19 years, to determine the independent and joint associations of muscle weakness and diabetes on ADL disability. Mexican Americans are also a large subset of Hispanic Americans in the United States and their population is projected to grow substantially (Colby & Ortman, 2015).

The rate for incident ADL disability was highest in older Mexican Americans that were both weak and had diabetes, compared with those that were not weak and did not have diabetes. The independent effect of diabetes demonstrated a higher rate for incident ADL disability than the independent effect of muscle weakness, when compared with persons that were not weak and did not have diabetes. Future investigations should consider examining the effect of muscle strengthening and diabetes reducing strategies for lowering the rate of ADL disability in Mexican Americans.

Footnotes

Appendix

Table A1.

Using Multiple Imputation for the Cox Proportional Hazard Regression Model for Incident Activities of Daily Living Disability.

	Hazard ratio^a	95% CI
Group 1^b	1.52	[1.39, 1.67]
Group 2^b	1.21	[1.15, 1.28]
Group 3^b	1.90	[1.83, 1.98]
Sex (reference: female)	0.86	[0.84, 0.87]
Married (reference: not married)	0.94	[0.93, 0.96]
Highest grade completed	0.99	[0.98, 0.99]
Obese (reference: not obese)	1.18	[1.16, 1.19]
Stroke (reference: no stroke)	1.41	[1.36, 1.46]
Personal yearly income	0.85	[0.83, 0.88]

Note. CI = confidence interval; Group 1 = not weak and has diabetes; Group 2 = weak and does not have diabetes; Group 3 = weak and has diabetes.

Hazard ratios all p < .0001.

Reference group: Group 0 = not weak and does not have diabetes.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This investigation was funded by a grant from the National Institute on Aging (R01-AG010939, K.S.M. is the principal investigator). R.P.M. is supported by an Advanced Rehabilitation Research Training award (90AR5020-0200) from the National Institute of Disability and Rehabilitation Research Program in Community Living and Participation. M.D.P. is funded by the NIH (1K01-HD074706).

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