Associations Between Vision,Hearing,and Olfactory Impairment With Handgrip Strength

Abstract

Objectives: We aimed to assess the cross-sectional associations between sensory impairments (vision, hearing, and/or olfactory loss) and handgrip strength. Method: In the Blue Mountains Eye Study, 947 participants aged 65+ years had handgrip strength measured using a dynamometer. Visual impairment was defined as visual acuity <20/40 (better eye), and hearing impairment as average pure-tone air conduction threshold >25 dBHL (500-4,000 Hz). Olfaction was measured using the San Diego Odor Identification Test. Results: Marginally significant associations between sensory impairment and handgrip strength were observed after multivariable adjustment. For example, women with two or three sensory impairments had lower adjusted mean handgrip strength (17.47 ± 0.5 kg) versus women who had no sensory loss (18.59 ± 0.3 kg; p = .06) or only one sensory impairment (18.58 ± 0.3 kg; p = .05), respectively. No significant associations were observed in men. Discussion: Women who had multiple sensory impairments had reduced muscle strength as indicated by ~1.1 kg lower mean handgrip strength.

Keywords

Blue Mountains Eye Study handgrip strength sensory impairment

Introduction

Epidemiological studies have shown that the age-related decline in physical performance and increasing functional disability are associated with adverse outcomes in older adults, such as poorer quality of life and increased mortality (Clemons, Rankin, & McBee, 2006; Gama et al., 2000; Gopinath, Kifley, Liew, & Mitchell, 2017; Stessman, Rottenberg, Fischer, Hammerman-Rozenberg, & Jacobs, 2017). Handgrip strength is an estimate of isometric strength in the upper extremity and also correlates with strength in other muscle groups, hence, it has often been used as an estimate of “overall strength” (Lauretani et al., 2003; Wu et al., 2012).

The prevalence of age-related sensory impairments also becomes more common as people get older (Attebo, Mitchell, & Smith, 1996; Gopinath et al., 2009 Karpa et al., 2010; Schneider et al., 2012). There have been several studies showing that older adults with sensory loss have increased functional disability or reduced ability to perform activities of daily living (ADL; Gopinath, Anstey, Kifley, & Mitchell, 2012; Gopinath et al 2012 Schneider et al., 2011). For instance, in the Blue Mountains Eye Study (BMES), we showed that olfactory impairment was associated with a 98% increased likelihood of experiencing ADL disability in adults aged 60+ years (Gopinath et al., 2012). The BMES also showed that participants with moderate-to-severe hearing loss compared with those who were not hearing impaired, had a 2.9-fold increased likelihood of reporting difficulty in ADL (Gopinath et al., 2012c). Keller, Morton, Thomas, and Potter (1999) showed that older patients with both hearing and vision impairment had mean ADL (p < .05) scores significantly lower than those with no impairments. In the longitudinal study on aging involving 5,151 people aged 70+ years, concurrent vision and hearing loss (dual sensory loss) increased the risk of difficulty with ADL tasks compared with those with no hearing loss or any sensory loss, but did not significantly increase risk over and above the vision impairment group (Brennan, Horowitz, & Su, 2005). This suggests most of the functional disability associated with dual sensory loss could be attributable to impaired vision rather than hearing (Schneider et al., 2011).

Less is known about the specific relationship between sensory impairments, muscle weakness, and low muscle mass (as indicated by handgrip strength) in older adults. Decline in sensory function may be an early sign of associated age-related changes in muscle strength, before muscle mass decline is even apparent. Hence, sensory function may serve as a marker of healthy physical aging (Fischer et al., 2016). Further research into this area is important given that reduced handgrip strength is subsequently associated with a negative profile of health parameters (Stessman et al., 2017). Therefore, in the BMES cohort of adults aged 65+ years, we aimed to assess the independent cross-sectional associations between having vision, hearing, or olfactory loss and mean handgrip strength. Furthermore, the link between the presence of multiple sensory impairments and handgrip strength was investigated.

Method

Study Population

The BMES is a population-based study of common eye diseases and other health outcomes in a population living west of Sydney, Australia. Study methods and procedures have been described elsewhere (Attebo et al., 1996). Baseline examinations of 3,654 residents aged >49 years were conducted during 1992 to 1994 (BMES-1, 82.4% participation rate). Surviving baseline participants were invited to attend examinations after 5 years (1997-1999, BMES-2), 10 years (2002-2004, BMES-3), and 15 years (2007-2009, BMES-4) at which 2,334 (75.1% of survivors), 1,952 participants (75.6% of survivors), and 1,149 (55.4% of survivors) were reexamined, respectively. Handgrip strength was only measured at BMES-4 and of the 1,149 examined, 947 had handgrip strength data collected and included in the current cross-sectional analysis (Gopinath et al., 2017).

Assessment of Handgrip Strength

Handgrip strength was measured with a Jamar hand dynamometer (Sammons Preston Inc., Bolingbrook, IL). Participants were asked to stand up and hold the dynamometer in the dominant hand with the arm parallel with the body without squeezing the arm against the body. Three trials followed and the average score was used, that is, mean handgrip strength of the three trials (Gopinath et al., 2017).

Assessment of Sensory Impairment

Pure-tone audiometry was performed by audiologists in sound-treated booths, using TDH-39 earphones and Madsen OB822 audiometers (Madsen Electronics, Denmark). Bilateral hearing impairment was determined as the pure-tone average of audiometric hearing thresholds at 500; 1,000; 2,000; and 4,000 Hz (PTA_0.5-4kHz) in the better ear, defining any hearing loss as PTA_0.5-4kHz > 25 dB HL; mild hearing loss as PTA_0.5-4kHz > 25-40 dB HL; and moderate-to-severe hearing loss as PTA_0.5-4kHz >40 dB HL.

Monocular distance logMAR (logarithm of the minimum angle of resolution) visual acuity was measured with forced-choice procedures using a retroilluminated chart with automatic calibration to 85 cd/m² (Vectorvision CSV-100TM; Vectorvision Inc, Dayton, Ohio) according to the Early Treatment Diabetic Retinopathy Study protocol (Attebo et al., 1996). This was conducted with habitual correction (presenting visual acuity, with current eyeglasses, if worn) and after subjective refraction (best-corrected visual acuity). For each eye, visual acuity was recorded as the number of letters read correctly from 0 to 70. For the present study, any visual impairment was defined as best-corrected visual acuity of the better eye less than 39 letters (<20/40).

Participants were tested individually with the San Diego Odor Identification Test (SDOIT; Morgan, Nordin, & Murphy, 1995), an eight-item odor identification test. Odorants were presented to participants in random order, in an opaque container covered with gauze. An interstimulus pause of 45 s was used to prevent adaptation (Ekman, Berglund, Berglund, & Lindvall, 1967). A picture board illustrating the odorants as well as distracters was used for participants to identify each odorant. Scores were calculated from the number of odorants identified correctly. We defined any olfactory impairment as less than six correct responses out of a total of eight possible responses.

Assessment of Covariates

A face-to-face interview with trained interviewers was also conducted, and comprehensive data including information about medical history, demographic factors (age, sex), and socioeconomic characteristics were obtained from all participants. Participants reported who they lived with (alone or with, for example, partner, child, friend). Walking difficulty or use of a cane, walker, or wheelchair was observed by a trained examiner and categorized as “walking disability.”

Statistical Analysis

SAS statistical software (SAS Institute, Cary, NC, USA) Version 9.4 was used for analyses including t tests, χ² tests, and linear regression. Mean handgrip strength (SE) was the study outcome and assessed as a continuous variable; and sensory loss was the study factor. Linear regression models were constructed to assess cross-sectional associations between sensory loss and mean handgrip strength in kilograms. These models were first adjusted for age and sex, and subsequently adjusted for covariates known to be associated with handgrip strength (living status, walking disability, and hospital admissions; Gopinath et al., 2017). Although there was no statistically significant interaction between sex and sensory impairment on mean handgrip strength (p > .05); we still chose to stratify the analyses by sex as we have previously shown in the BMES that handgrip strength is substantially different among men and women, and that the predictors of mean handgrip strength are also different for men and women (Gopinath et al., 2017).

Results

Table 1 shows the characteristics of study participants included in cross-sectional analysis. Participants with sensory loss compared with those without any sensory loss were more likely to be older, male, and have a walking disability (Table 1). There were 376 (54.0%), 100 (10.7%), and 329 (35.5%) with hearing, vision, or olfactory loss, respectively. Although mean handgrip strength was lower in participants with hearing, vision, or olfactory impairment, it did not reach statistical significance after multivariate adjustment (Table 2).

Table 1.

Baseline Characteristics of Study Participants.

Characteristics	Any sensory loss (n = 578)	No sensory loss (n = 369)	p value
Age, years (SD)	78.2 (6.7)	73.6 (5.6)	<.0001
Male sex	262 (45.3)	137 (38.6)	.04
Lives alone	206 (36.1)	122 (34.5)	.62
Admission to hospital in the last 12 months	122 (21.5)	70 (19.8)	.53
Walking disability	120 (21.3)	31 (8.9)	<.0001

Note. Data are presented as mean (SD) and n (%).

Table 2.

Cross-Sectional Linear Associations Between Sensory Loss and Handgrip Strength.

Sensory impairment	Adjusted mean handgrip strength (SE) in kg^a
Sensory impairment	All (n = 947)	Women (n = 544)	Men (n = 403)
Hearing impairment
None, n = 320	24.78 (0.35)	18.73 (0.34)	32.82 (0.67)
Any hearing loss, n = 376	24.63 (0.32)	17.99 (0.33)	33.40 (0.58)
p value	.76	.14	.53
Best corrected visual impairment
None, n = 837	24.58 (0.20)	18.43 (0.21)	32.87 (0.37)
Any vision loss, n = 100	23.79 (0.62)	17.57 (0.57)	31.61 (1.30)
p value	.23	.16	.35
Olfactory impairment
None, n = 598	25.66 (0.25)	18.39 (0.24)	33.11 (0.48)
Any olfactory loss, n = 329	24.23 (0.34)	18.23 (0.37)	32.48 (0.59)
p value	.31	.72	.42
Overall sensory impairment
None, n = 369	24.46 (0.32)	18.59 (0.31)	32.44 (0.62)
One sensory impairment, n = 369	24.84 (0.31)	18.57 (0.31)*	33.32 (0.56)
Two/three sensory impairment, n = 209	23.89 (0.44)	17.47 (0.47)**	32.21 (0.76)

Adjusted for age, living alone, admission to hospitals, and walking disability. Sex was included in the model when assessing associations in the overall cohort and not when analyzing men and women separately.

p = .06 compared to no sensory impairment. **p = .05 compared to no sensory impairment.

After adjusting for age, women who had two or three sensory impairments (hearing, vision, and olfactory loss) compared with women who did not have any sensory loss had significantly lower mean handgrip strength, 17.45 (0.4) kg and 18.60 (0.3) kg, respectively (p = .04). Also, women who had two or three sensory impairments versus one sensory impairment had significantly lower mean handgrip strength, 17.45 (0.4) kg and 18.60 (0.3) kg, respectively (p = .03). After multivariate adjustment, these associations became only marginally significant. That is, women who had two or three versus no sensory impairments had lower mean handgrip strength, 17.47 (0.47) kg versus 18.59 (0.31) kg (multivariable-adjusted p = .06; Table 2). Similarly, women with two or three versus one sensory impairments had lower mean handgrip strength, 17.47 (0.47) kg versus 18.57 (0.31) kg (multivariable-adjusted p = .05; Table 2). No significant associations were observed with multiple sensory impairments and handgrip strength among men or in the overall cohort (Table 2).

Discussion

Our findings provide novel evidence of a potential link between the presence of multiple sensory impairments (vision, hearing, and olfactory impairment) and modest reduction in muscle strength as indicated by lower mean handgrip strength. Specifically, women who had two to three sensory impairments had ~1.1 kg lower mean handgrip strength compared with those who had one or no sensory loss. This association was not evident in men. Moreover, there was no observed association between having a single sensory loss and mean handgrip strength. These findings suggest that women with a single sensory impairment may be able to better compensate than women who have lost two or three major sensory inputs.

The observation that the presence of two or three sensory impairments rather than a single sensory impairment was associated with lower mean handgrip strength in the BMES, is in agreement with previous reports suggesting that the presence of more than one sensory impairment increases morbidity relative to single sensory impairment (Crews & Campbell, 2004; Fischer et al., 2016; Schneider et al., 2011). The report by Reuben, Mui, Damesyn, Moore, and Greendale (1999) showed that there is likely to be a synergistic relationship between vision and hearing loss with respect to functional activity. That is, the association between sensory impairment with muscle strength or muscle function (as assessed by handgrip strength) is likely to involve more than just one sensory system in older adults. Nevertheless, we cannot disregard the possibility of chance findings; hence, our observations require further validation and confirmation by other studies.

There are several pathways by which sensory impairments could be associated with reduced handgrip strength or overall muscle function. For instance, it could be explained by the common-cause theory where one or more factors contribute to the development of both sensory impairments and reduced muscle strength (Fischer et al., 2016). One such factor or influence may be a generalized aging effect (Fischer et al., 2016). Sensory decline may be an early sign of concomitant age-related changes in muscle strength, before decline in muscle mass is even apparent. Thus, sensory health may serve as a marker of healthy physical aging. Vascular disease might be another plausible common cause. There is evidence that vascular disease risk factors (e.g., diabetes and body weight) are predictors of handgrip strength (Moy, Darus, & Hairi, 2015). Cardiovascular-related risk factors and conditions were also found to be associated with impaired hearing, vision, and olfaction (Bergman, Nilsson-Ehle, & Sjostrand, 2004; Karpa et al., 2010). Therefore, vascular changes may be associated with both sensory and muscle strength decline. It is likely, however, that sensory impairments and muscle weakness share more than age and vascular disease as common causes. Sensory loss and handgrip strength could be a surrogate for poorer overall health, and it is highly unlikely that an adequate set of covariates accounting for all aspects of poor health can be measured and included in modeling (Fischer et al., 2016).

The sex-specific associations between sensory loss and handgrip strength observed in this study are difficult to explain given its observational nature. It is known that handgrip strength is substantially different among men and women, and that the predictors of handgrip strength are also different for men and women (Gopinath et al., 2017; Lino et al., 2016; Moy et al., 2015). For instance, Moy et al. (2015) found that occupation was a predictor of handgrip strength in men, but not women, and the opposite was observed for body weight, that is, it is a predictor of handgrip strength in women, but not men. These differences between men and women could underpin the varying associations observed with sensory impairment in the BMES, and thus, warrants further exploration.

As sensory problems are common experiences within older adults, they are often overlooked or dismissed (Crews & Campbell, 2004), and our findings underscore the public health importance of identifying persons with these treatable conditions early on. Brief questions such as “Have you ever worn glasses or contact lenses?” plus an affirmative answer to “Do you have trouble seeing even with corrective lenses?” can identify older persons at risk of subsequent functional visual impairment (Reuben et al., 1999). For hearing impairment, a positive response to a question such as “Do you feel you have a hearing loss?” can effectively identify hearing loss in older adults (Gopinath et al 2012). Those who have measured combined sensory impairment appear to be at particular risk of muscle weakness or dynapenia. It is unclear whether early correction of these impairments can prevent long-term functional decline in muscle strength, although several studies have demonstrated that sensory aids or surgical corrections can improve the quality of life, social relations, and functional status of those with hearing and vision impairment (Fong et al., 2013; Gopinath et al., 2012; Reuben et al., 1999; Schneider et al., 2010).

The strengths of this study include a representative cohort of a reasonable sample size; and the use of standardized and validated audiometric, vision, and olfactory testing. There are limitations that also require discussion. First, the data analyzed were cross-sectional and as such, this study does not allow for causality considerations. Hence, other large studies of prospective nature are needed to determine the temporal associations between sensory impairment and handgrip strength. We also did not use a standardized procedure for assessing handgrip strength. Finally, we cannot exclude the possibility of residual confounding from unaccounted factors, which might have influenced the observed associations (Gopinath et al., 2017).

In summary, this cross-sectional study is the first to show a modest association between combinations of vision, hearing, and olfactory loss with mean handgrip strength. The association was more marked in women compared with men. A better understanding of how multiple sensory impairments prospectively influences muscle weakness and overall physical strength of older adults is warranted, in order to develop effective interventions to delay the onset of disability and preserve independence and quality of life in older age.

Footnotes

Author Contributions

B.G. and P.M. conceived, designed, and performed the experiments. B.G., G.B., G.L., and P.M. analyzed and interpreted the data. P.M. and G.B. contributed reagents, materials, and analysis tools or data. Finally, B.G. wrote the paper.

Ethical Approval

The University of Sydney and the Western Sydney Area Human Ethics Committees approved the study, and written informed consent was obtained from all participants.

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: The Blue Mountains Eye Study was supported by the Australian National Health and Medical Research Council (Grants 974159, 991407, 211069, 262120).

ORCID iD

Bamini Gopinath

References

Attebo

Mitchell

Smith

(1996). Visual acuity and the causes of visual loss in Australia: The Blue Mountains Eye Study. Ophthalmology, 103, 357-364.

Bergman

Nilsson-Ehle

Sjostrand

(2004). Ocular changes, risk markers for eye disorders and effects of cataract surgery in elderly people: A study of an urban Swedish population followed from 70 to 97 years of age. Acta Ophthalmologica Scandinavica, 82, 166-174.

Brennan

Horowitz

Y. P.

(2005). Dual sensory loss and its impact on everyday competence. The Gerontologist, 45, 337-346.

Clemons

T. E.

Rankin

M. W.

McBee

W. L.

(2006). Cognitive impairment in the Age-Related Eye Disease Study: AREDS report no. 16. Archives of Ophthalmology, 124, 537-543.

Crews

J. E.

Campbell

V. A.

(2004). Vision impairment and hearing loss among community-dwelling older Americans: Implications for health and functioning. American Journal of Public Health, 94, 823-829.

Ekman

Berglund

Lindvall

(1967). Perceived intensity of odor as a function of time of adaptation. Scandinavian Journal of Psychology, 8, 177-186.

Fischer

M. E.

Cruickshank

J. K.

Schubert

C. R.

Pinto

A. A.

Carlsson

C. M.

Klein

B. E.

. . . Tweed

T. S.

(2016). Age-related sensory impairments and risk of cognitive impairment. Journal of the American Geriatrics Society, 64, 1981-1987.

Fong

C. S.

Mitchell

Rochtchina

Teber

E. T.

Hong

Wang

J. J.

(2013). Correction of visual impairment by cataract surgery and improved survival in older persons: The Blue Mountains Eye Study Cohort. Ophthalmology, 120, 1720-1727.

Gama

E. V.

Damian

J. E.

Perez

D. M.

Lopez

M. R.

Lopez

P. M.

Gavira Iglesias

F. J.

(2000). Association of individual activities of daily living with self-rated health in older people. Age and Ageing, 29, 267-270.

10.

Gopinath

Anstey

K. J.

Kifley

Mitchell

(2012). Olfactory impairment is associated with functional disability and reduced independence among older adults. Maturitas, 72, 50-55.

11.

Gopinath

Hickson

Schneider

McMahon

C. M.

Burlutsky

Leeder

S. R.

Mitchell

(2012a). Hearing-impaired adults are at increased risk of experiencing emotional distress and social engagement restrictions five years later. Age and Ageing, 41, 618-623.

12.

Gopinath

Kifley

Liew

Mitchell

(2017). Handgrip strength and its association with functional independence, depressive symptoms and quality of life in older adults. Maturitas, 106, 92-94.

13.

Gopinath

Rochtchina

Wang

J. J.

Schneider

Leeder

S. R.

Mitchell

(2009). Prevalence of age-related hearing loss in older adults: Blue Mountains Study. Archives of Internal Medicine, 169, 415-416.

14.

Gopinath

Schneider

Hickson

McMahon

C. M.

Burlutsky

Leeder

S. R.

Mitchell

(2012b). Hearing handicap, rather than measured hearing impairment, predicts poorer quality of life over 10 years in older adults. Maturitas, 72, 146-151.

15.

Gopinath

Schneider

McMahon

C. M.

Teber

Leeder

S. R.

Mitchell

(2012c). Severity of age-related hearing loss is associated with impaired activities of daily living. Age and Ageing, 41, 195-200.

16.

Karpa

M. J.

Gopinath

Rochtchina

Jie

J. W.

Cumming

R. G.

Sue

C. M.

Mitchell

(2010). Prevalence and neurodegenerative or other associations with olfactory impairment in an older community. Journal of Aging and Health, 22, 154-168.

17.

Keller

B. K.

Morton

J. L.

Thomas

V. S.

Potter

J. F.

(1999). The effect of visual and hearing impairments on functional status. Journal of the American Geriatrics Society, 47, 1319-1325.

18.

Lauretani

Russo

C. R.

Bandinelli

Bartali

Cavazzini

Di Iorio

. . . Ferrucci

(2003). Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia. Journal of Applied Physiology, 95, 1851-1860.

19.

Lino

V. T.

Rodrigues

N. C.

O’Dwyer

Andrade

M. K.

Mattos

I. E.

Portela

M. C.

(2016). Handgrip strength and factors associated in poor elderly assisted at a primary care unit in Rio de Janeiro, Brazil. PLoS ONE, 11, e0166373.

20.

Morgan

C. D.

Nordin

Murphy

(1995). Odor identification as an early marker for Alzheimer’s disease: Impact of lexical functioning and detection sensitivity. Journal of Clinical and Experimental Neuropsychology, 17, 793-803.

21.

Moy

F. M.

Darus

Hairi

N. N.

(2015). Predictors of handgrip strength among adults of a rural community in Malaysia. Asia-Pacific Journal of Public Health, 27, 176-184.

22.

Reuben

D. B.

Mui

Damesyn

Moore

A. A.

Greendale

G. A.

(1999). The prognostic value of sensory impairment in older persons. Journal of the American Geriatrics Society, 47, 930-935.

23.

Schneider

J. M.

Gopinath

Karpa

M. J.

McMahon

C. M.

Rochtchina

Leeder

S. R.

Mitchell

(2010). Hearing loss impacts on the use of community and informal supports. Age and Ageing, 39, 458-464.

24.

Schneider

J. M.

Gopinath

McMahon

C. M.

Leeder

S. R.

Mitchell

Wang

J. J.

(2011). Dual sensory impairment in older age. Journal of Aging and Health, 23, 1309-1324.

25.

Schneider

J. M.

Gopinath

McMahon

C. M.

Teber

Leeder

S. R.

Wang

J. J.

Mitchell

(2012). Prevalence and 5-year incidence of dual sensory impairment in an older Australian population. Annals of Epidemiology, 22, 295-301.

26.

Stessman

Rottenberg

Fischer

Hammerman-Rozenberg

Jacobs

J. M

. (2017). Handgrip strength in old and very old adults: Mood, cognition, function, and mortality. Journal of the American Geriatrics Society, 65, 526-532

27.

Pang

Zhang

Jiang

Wang

. . . Tan

(2012). A cross-sectional analysis of age and sex patterns in grip strength, tooth loss, near vision and hearing levels in Chinese aged 50-74 years. Archives of Gerontology and Geriatrics, 54, e213-e220.