Introduction

The World Health Organisation (WHO) advocates to move towards a more positive model of healthy ageing, emphasising an individual’s intrinsic capacity over a disease-focussed approach [1]. Intrinsic capacity encompasses five different domains: locomotion, sensory, cognition, psychological and vitality [2, 3]. Vitality capacity has been suggested as an important domain, since underlying physiological changes can influence other domains of intrinsic capacity [4]. Recently, a new international consensus definition of vitality capacity for healthy longevity was published defining vitality capacity as a “physiological state (due to normal or accelerated biological ageing processes) resulting from the interaction between multiple physiological systems, reflected in (the level of) energy and metabolism, neuromuscular function, and immune and stress response functions of the body” [5]. Along this new conceptual definition, potential biomarkers for vitality capacity were identified. The next step is now to develop an operational definition for vitality capacity by identifying those biomarkers for which the best scientific evidence is available. In this umbrella review, we focus on the biomarkers for the neuromuscular attributes of vitality capacity.

Neuromuscular function refers to the interaction of the nervous system and the muscular system that results in isolated muscle contraction. This requires interaction between motor neurons, release of neurotransmitters and activation of muscle fibres [6]. Dysfunction of neuromuscular function might influence other domains of intrinsic capacity [4]. The international expert panel that generated the consensus definition of vitality capacity proposed handgrip strength, knee extensor strength and respiratory muscle strength as excellent candidate biomarkers for neuromuscular function; however, no specific instruments were recommended by the international panel to measure these biomarkers [5]. It has been shown that reduced handgrip strength is strongly related to negative health outcomes such as mortality and disability [7]. Besides, knee extensor strength in older adults is related to other healthy ageing indicators such as functional ability, quality of life [8] and falls [9]. As a result of the age-related decline in muscle strength in the whole body, the respiratory muscle function also decreases [10] which can result in breathlessness that negatively affects daily activities in older adults [11].

The present umbrella review aims to provide an overview of the available instruments and their measurement properties to assess handgrip strength, knee extensor strength and respiratory muscle strength as biomarkers for neuromuscular function in older adults.

Methodology

Study protocol and registration

The umbrella review protocol was registered in the international prospective register of systematic reviews (PROSPERO, registration number: 375906). Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed [12].

Literature search

The databases PubMed, Web of Science and Embase were systematically screened using two different search strings: one for grip strength combined with knee extensor strength (last search 14th February 2023), and another for respiratory muscle strength (last search 6th March 2023). For this review, the following PICO question was used: ‘What are the available screening or assessment tools and their psychometric properties (I) for measuring handgrip strength, knee extensor strength and respiratory muscle strength, as a biomarker of vitality capacity (O) in persons without specific diseases (P)?’. There were no restrictions on the publication date. The full search strategy is presented in Appendix A and included the following keywords: (risk assessment OR screening OR measurement) AND systematic review. For grip strength and knee extensor strength those were combined with: AND (hand strength OR muscle strength dynamometer OR knee extensor strength). For respiratory muscle strength the keywords were combined with: AND (respiratory function tests OR spirometry).

The results were screened independently by two reviewers based on the title and abstract. As a second step, the full text was screened. The reviewers were blind to each other’s decisions. Disagreement between the two reviewers was resolved by discussion and if needed, a third reviewer was consulted. An overview of the selection process can be found in Fig. 1.

Fig. 1
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The study selection process

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Selection criteria

Studies on assessment tools for neuromuscular function were eligible when they met the following criteria: the studies had to describe instruments for the assessment of handgrip strength, knee extensor strength or respiratory muscle strength, studies had to be systematic reviews or meta-analyses and the participants had to be 18 years or older. Studies that explicitly stated that the sample included participants with (chronic) diseases were excluded; however, studies describing participants at increased risk for disease were not excluded. The studies had to be written in English.

Data extraction

Two reviewers independently collected data from the selected studies, including the first author, publication year, number of participants, sex, residential status (e.g. community-dwelling), age and the assessment tools used. As a first step, we identified all assessment tools for handgrip strength, knee extensor strength or respiratory muscle strength that were found in the included systematic reviews. However, whilst some of these assessments were described as measures of muscle strength, this characterisation was not consistently applicable across all cases. Therefore, we selected only those instruments that directly measure handgrip strength, knee extensor strength or respiratory muscle strength (as biomarkers of neuromuscular function). Then the psychometric properties of the selected assessment tools and/or the relationship between neuromuscular function and longevity were extracted from the included reviews if this was available. As a last step, the selected assessment tools were discussed by two reviewers and assessed according to criteria for the potential biomarkers, proposed by the international expert panel [5]: (1) feasible to quantify biomarkers or proxy biomarkers, (2) feasible to measure or collect in low-resource setting, (3) useful and informative for monitoring, (4) distinct attribute, (5) acceptable cost and resource demand, (6) sufficient availability and no ethical concern, (7) implementable, and (8) robust psychometric properties. Regarding criterion 8, an extra step was needed in which we used the COSMIN checklist to assess the psychometric properties of the tools that were described [13]. We used the psychometric properties that were described in the included systematic reviews (no additional literature search was performed).

Quality assessment

The internal validity of the included reviews was assessed using the ‘measurement tool to assess the methodological quality of systematic reviews’ (AMSTAR) [14]. The ‘consensus-based standards for the selection of health status measurement instruments’ (COSMIN) was used to assess the psychometric properties, including validity (criterion, content, structural, predictive, cross-cultural), internal consistency, measurement invariance, reliability (test–retest) and hypothesis testing for construct validity [13]. The COSMIN guidelines were used to evaluate the measurement properties of the assessment tools in terms of adequate ( +), inadequate (−), indeterminate (?) or inconsistent ( ±) based on the study design and methodology. Two reviewers independently rated the AMSTAR and COSMIN. In case of disagreement, consensus was reached after discussion between the reviewers, and if needed, a third reviewer was consulted.

Results

The literature search resulted in 5,251 articles for the search on hand grip strength and knee extensor strength, and 2,304 articles for the search on respiratory muscle strength. Three hundred sixty-four articles were eligible based on title and abstract. Finally, 27 systematic reviews that were published between 2004 and 2022 were included in this umbrella review (see Fig. 1).

Quality assessment

The AMSTAR checklist indicated moderate to good methodological quality of the included reviews (see Table 1). No systematic reviews were excluded based on the quality assessment. Only three studies assessed the likelihood for publication bias [15,16,17].

Table 1 Risk of bias assessment
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Characteristics of included studies and instruments

For hand grip strength and knee extensor strength, we included 25 systematic reviews. Table 2 shows the study characteristics and identified assessment tools. The included studies reported on at least 4,704,240 participants, 11 studies did not report the number of participants [7, 9, 15, 20, 26, 30, 32, 34, 36, 38, 39]. Six articles included a ‘healthy’ population [15, 20, 32, 33, 37, 38], and three articles included a specific population: participants with a cognitive risk [19], participants with disability components based on the ICF [18] and one study included participants at risk for diabetes mellitus type 2 [29]. Ten studies included community-dwelling people [18, 20,21,22,23, 31, 36,37,38,39] and only one study included people living in assisted facilities [36]. Most studies included participants at middle-age (40 years or older) [7, 29, 31] or aged 60 years or older [9, 18, 20,21,22,23, 25, 26, 30, 34, 36, 37], though a few also included younger adults (18 years and older) [24, 27, 28]. Almost all studies included men and women, only three studies did not specify [9, 15, 36]. For respiratory muscle strength, we included two systematic reviews, shown in Table 3. One of the included studies reported 9,643 participants [40] and the other study did not report the number of participants [16]. Both of the articles included a ‘healthy’ population [16, 40]. Only one study reported the inclusion of both men and women of 18 years and older [40]. The other study did not report the age and gender of the participants [16].

Table 2 Summary of included studies for grip strength and knee extensor strength
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Table 3 Summary of included studies for respiratory muscle strength
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Instruments for assessing handgrip strength

Only handheld dynamometers were described for the assessment of handgrip strength. The assessment tools were often described in general and did not specify the type or test protocol. The most reported instruments were hydraulic dynamometers such as JAMAR [7, 19,20,21, 24, 28, 31, 33, 41, 42], spring dynamometers such as Smedley [7, 18,19,20,21, 31] and pneumatic dynamometers such as Martin Vigorimeter [7, 19, 36, 42]. Two studies described that they measured the maximum handgrip strength [24, 29] and only one study described that they normalised the maximum handgrip strength to bodyweight (in kg) [29]. Lastly, one study described the use of a mechanical handgrip dynamometer that was adjusted for hand size [28].

Instruments for assessing knee extensor strength

For knee extensor strength, the most reported assessment tool was dynamometry [9, 15, 18, 21, 25, 26, 30, 32, 35,36,37], such as handheld dynamometry and Biodex systems [21]. Also, a hydraulic resistance system such as a leg press was reported to assess knee extensor strength [21, 34, 36, 37]. Different types of chair stand tests based on either the time needed to complete a specific number of repetitions (e.g. 5 repetitions) or the number of repetitions that can be performed within a specific amount of time (e.g. 30 s) were described for measuring knee extensor strength [9, 21, 22, 27, 34, 37, 38]. However, chair stand tests require not only isolated muscle strength but also other functions such as balance and endurance which makes them less suitable to measure neuromuscular function. Lastly, the single knee extension contractions [30] and manual muscle testing were described [9, 36]. However, the single knee extension contraction test is used to measure hamstring muscle length and the manual muscle testing protocol was not clarified, which makes them not suitable to measure neuromuscular function.

Instruments for assessing respiratory muscle strength

One systematic review reported the maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) [40] for assessing the respiratory muscle strength. They described the use of digital manometers, mechanical gauges, a gauge associated with a pneumotachograph and a gauge that was associated with a spirometry system. The assessment protocol varied but most studies performed measurements with the participants in a sitting position whilst using a nose clip. Whilst most studies measured MIP at residual volume and MEP at total lung capacity, also one study was reported that performed both MIP and MEP measurements at different volumes (percentage of vital capacity). The holding pressure varied from ≥ 1 s or > 2 s and the number of repetitions of the procedure varied between 2 and 10, with most studies reporting at least 3 repetitions.

The other study reported the phrenic nerve stimulation, the maximal voluntary inspiratory manoeuvre (Mueller), powerful sniff manoeuvre and electromyography to estimate the respiratory muscle strength [16]. The maximal voluntary inspiratory manoeuvre is referred to as MIP to measure the inspiratory muscle strength and the powerful sniff manoeuvre is commonly described as the sniff nasal inspiratory pressure.

Psychometric properties

A few included reviews described the psychometric properties of the assessments. For hand grip strength, the Takei dynamometer was found valid and the results for the validity of the DynEx dynamometer were inconclusive [24]. The JAMAR dynamometer was found less accurate than the Takei and DynEx dynamometer for estimating maximal isometric hand grip strength [24]. The handheld dynamometer for assessing knee extensor strength showed a high inter- and intra-rater reliability, as well as a good concurrent and construct validity [36]. Another study also reported a high intra-class correlation coefficient (ICC) of 0.90 and the minimal detectable change (MDC) was highly variable and ranged from 46.0 to 79.0 Newton in older adults [15]. One study investigated the psychometric properties of different chair stand tests. They described the 30 s sit to stand test with an ICC of 0.89 and moderate concurrent validity in community-dwelling adults with a mean age of 70.5 ± 5.5 years [30]. The ICC and construct validity of the 1RM leg press were described as ‘good’ as well [30]. There were no psychometric properties described for the assessments of respiratory muscle strength in the included reviews. The psychometric properties of the identified assessments are shown in Table 4.

Table 4 Psychometric properties of the identified assessments
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Predictive validity for longevity

Low handgrip strength was associated with both worsening activities of daily living (ADL) and instrumental activities of daily living (IADL) (pooled odds ratio (95% CI) OR = 1.51 (1.34–1.70) and OR = 1.59 (1.04–2.31), respectively) [25]. Handgrip strength measured by hand dynamometry and adjusted for height is associated with mortality in older adults [23]. The summary hazard ratio for mortality comparing the weakest with the strongest quarter of grip strength was HR = 1.67 (95% CI 1.45 to 1.93) [39]. Weaker grip strength was associated with increased risk of future fractures, cognitive decline, hospitalisation [38], premature mortality and the development of disability [7]. Handgrip strength is also associated with the risk of type 2 diabetes: each standard deviation of higher muscular strength was associated with a 13% lower risk of type 2 diabetes (95% CI 6–19) [29]. Besides, handgrip strength may be a risk indicator for poor cognitive outcomes such as cognitive impairment, dementia, Alzheimer dementia [19] and depressive symptoms [20]. Regarding knee extensor strength, it is described that lower body muscle strength and the chair stand test performance were most associated with negative health outcomes [21, 22, 37]. Besides, the chair stand test time was associated with worsening ADL (OR = 1.90 (95% CI 1.63–2.21)) [25]. For lower extremity strength (measured with a dynamometer or a chair stand test), the combined odds ratio was OR = 1.76 (95% CI 1.31–2.37) for any fall and OR = 3.06 (95% CI 1.86–5.04) for recurrent falls [9]. Besides, knee extensor strength correlates significantly with age and disabilities when measured with a hydraulic or digital dynamometer [18]. Also, one systematic review indicated that knee extensor muscle weakness increased the odds of symptomatic knee osteoarthritis in adult women (OR = 1.85, 95% CI 1.29–2.64) and in adult men (OR = 1.43, 95% CI 1.14–1.78) [35]. For the respiratory muscle strength assessments, no information was available.

Neuromuscular assessments for implementation in vitality capacity

Based on the psychometric properties of the identified tools (see Tables 2 and 3) and the attributes and criteria of vitality capacity (see Table 4) [5], we found five assessment tools adequate for the measurement of neuromuscular function. The handheld dynamometer for hand grip strength and the handheld dynamometer for knee extensor strength were adequate. Regarding respiratory muscle strength, we found the sniff nasal inspiratory pressure, MIP and the MEP potentially adequate (Table 5). However, the psychometric properties of the assessments for respiratory muscle strength remain unclear. The Leg press, BIODEX, and electromyography were excluded from selection due to their impracticality in low-income countries, unacceptable costs, complexity in implementation and insufficient availability. Since chair stand tests do not measure a distinct attribute, these were also excluded from the selection (see Table 5).

Table 5 Implementation assessments’ vitality capacity
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Discussion

This umbrella review aimed to comprehensively summarise the available literature on assessment tools for neuromuscular function in community-dwelling older adults. The objective was to identify the available and most suitable assessment tools and their psychometric properties. Based on the criteria for vitality capacity, we have identified five assessment tools to measure neuromuscular function. The handheld dynamometer for handgrip strength, handheld dynamometer for knee extensor strength, sniff nasal inspiratory pressure, MIP and the MEP are adequate biomarkers of neuromuscular function within the context of vitality capacity.

We found that handgrip strength was assessed with a handheld dynamometer in all studies and different hydraulic (e.g. JAMAR or SEAHAN systems), pneumatic (e.g. Martin Vigorimeter system) or spring (e.g. Baseline system) dynamometers were described. The handheld dynamometer scored good on all the eight criteria to quantify handgrip strength as a biomarker for vitality capacity. Pneumatic handheld dynamometers, compared to hydraulic handheld dynamometers, have been found to be more sensitive in identifying participants with higher levels of muscle endurance, although both systems can be used [44,45,46,47]. The Eforto® system, which consists of a rubber bulb connected to a smartphone-based application, has been found to have good criterion validity and reliability in older community-dwelling persons for (self) measurement of grip strength and muscle fatigability [48]. The use of such assessments holds promise for practical healthcare implementation in the context of vitality capacity. For knee extensor strength, there were different assessment tools found in the literature. Based on the eight criteria for the biomarkers of vitality capacity, we found only the dynamometer for knee extensor strength excellent for assessing the knee extensor strength biomarker. The handheld dynamometer (e.g. Microfet system) showed a high inter- and intra-rater reliability, as well as a good concurrent and construct validity [36]. One study investigated the psychometric properties of different chair stand tests, which described the 30 s sit to stand test with an ICC of 0.89 and moderate concurrent validity in community-dwelling adults with a mean age of 70.5 ± 5.5 years [30]. For the other chair stand tests (e.g. five times sit to stand), the psychometric properties were not reported. However, chair stand tests require not only isolated muscle strength but also other functions such as balance and endurance. Therefore, the chair stand tests are not suitable as assessments to measure the neuromuscular function. Vitality capacity is closely linked with locomotor capacity, one of the other domains of intrinsic capacity. Locomotor capacity is a “state of the musculoskeletal system that encompasses endurance, balance muscle strength, muscle function, muscle power and joint function of the body’’ [49]. Therefore, the chair stand tests are not suitable for assessing vitality capacity but might be useful for assessing the locomotor capacity domain.

For respiratory muscle strength, we found three different assessment tools. Unfortunately, data on the psychometric properties of these tools were scarcely reported in the included review papers. Some systematic reviews reported spirometry as assessment tools for lung function. Spirometry is a test used to measure the ability of a person to inhale and exhale air respective to time, and the forced expiratory volume in one second (FEV1) and forced volume capacity (FVC) are main results of spirometry [50]. A decrease in FEV1 of 10% is associated with a 20% (95%CI 17%–23%) increase in lung cancer risk [51]. Besides, in non-diabetic participants, every 10% decrease in baseline predicted FVC% value was associated with a 13% higher risk of incident diabetes (HR: 1.13, 95% CI: 1.09–1.17) and a similar conclusion could be drawn for FEV1 (HR: 1.10, 95% CI: 1.06–1.14) [52]. However, the spirometry outcomes are useful to categorise the severity of obstructive lung diseases, such as asthma and chronic obstructive pulmonary disease (COPD) [50]. Spirometry does not assess the respiratory muscle strength, which is why the FEV1 and FVC are not eligible as assessments for neuromuscular function. Therefore, we only suggested the use of the MIP, MEP and sniff nasal inspiratory pressure to assess respiratory muscle strength in older adults. Volitional tests such as the MIP and MEP are commonly used to assess the respiratory muscle strength. The MIP measures upper airway pressure during a maximal voluntary inspiratory effort against an occluded mouthpiece and the MEP measures upper airway pressure during a maximal voluntary expiratory effort [53]. Measurement of MIP and MEP can be made with an analogue or digital pressure manometer. The MIP tends to decrease around 40 to 60 years and continues to fall progressively with age, and men tend to have higher MIPs than women [54]. The sniff nasal inspiratory pressure is another non-invasive assessment for the measurement of inspiratory muscle strength. It uses pressure monometers which are inexpensive, and the sniff nasal inspiratory pressure is easy to perform. The digital manovacuometre UFMG has been found to be a reliable and valid instrument for assessing MIP, MEP and sniff nasal inspiratory pressure in adults [55].

The loss of neuromuscular function will lead to a drop of the functional ability of older adults, and an adequate understanding of the underlying mechanisms in skeletal muscle structure is important to understand these age-related changes. Loss of muscle mass is largely due to the progressive loss of motoneurons, which is associated with reduced muscle fibre number and size [56]. The neuromuscular function declines because the motoneuron loss is not compensated by re-innervation of muscle fibres by the remaining motoneurons [6]. At the intracellular level, the ageing process leads to changes in post-translational modifications of muscle proteins and the loss of coordinated control between contractile, mitochondrial and sarcoplasmic reticulum [6]. This loss of muscle strength during the ageing process [57] is a significant contributor of the rising prevalence of frailty and mobility limitations amongst older adults. Notably, functional ability limitations are more pronounced in women compared to men [58]. Women lose muscle mass at a slower rate than men [59] which is intriguing, considering that women experience a higher prevalence of physical disabilities [60]. However, men tend to have a higher muscle mass which protects them during the ageing process since they can lose relatively more muscle mass compared to women. The knee extension peak torque declines 25 years earlier in women, which contributes to the explanation why functional decline occurs more often in women than men [61]. The higher fat mass percentages in women might also contribute to the explanation of the discrepancy in physical functioning between men and women [62]. Interventions that help alleviate muscle mass loss in older adults would be of great benefits in maintaining a better neuromuscular function and reducing the risk of negative health outcomes. Therefore, the assessments as identified in this current umbrella review might allow to identify those persons that are at risk for a declined neuromuscular function and are in need for those interventions to improve their muscle mass.

Vitality capacity has been suggested as an essential domain of intrinsic capacity, since it represents the conditional physiological aspects of intrinsic capacity. A decline in intrinsic capacity amongst older adults is associated with a wide range of adverse outcomes, including impairments in cognitive function, functional ability, sensory perception, physical and mental health, and living standards [63]. Dysfunction of vitality capacity might, therefore, influence various domains of intrinsic capacity, including locomotion, sensory, cognition and psychological capacity. Lower neuromuscular function, higher feelings of fatigue and higher levels of inflammation can negatively influence activities such as walking or raising from a chair [64]. Therefore, a lower vitality capacity can have a negative effect on the locomotor capacity as well. To assess the sensory domain, the most important biomarkers are the hearing and vision abilities. Older people with hearing loss report more disabilities in daily living compared to older people without hearing loss, with older people that contend both hearing and visual problems having the greatest disabilities in daily living [65]. Further research should investigate the relationship of sensory impairment, neuromuscular function and functional declines in daily living. Furthermore, research indicates strong connections between neuromuscular function and cognition, and neuromuscular function is a risk indicator for poor cognitive outcomes such as cognitive impairment, dementia and Alzheimer dementia [19]. In addition, depressive symptoms, recognised as one of the biomarkers of the psychological domain, have been shown to correlate with reduced neuromuscular function as well [20]. Hence, it is essential to adequately assess the vitality capacity domain to gain insights into the intrinsic capacity reserves rather than focussing solely on the vitality capacity domain itself.

This umbrella review has some strength and limitations. We conducted a broad search strategy to identify all assessments for handgrip, knee extension and respiratory muscle strength in the literature. Therefore, the included studies reported on participants that were 18 years and older, even though most studies included older adults. However, the included assessments might not be all validated specifically in older adults, but the results are promising. Furthermore, we have only searched for articles in English, which might have increased the risk of missing relevant research papers. Besides, we did not conduct an additional search for the psychometric characteristics of the assessment tools to prevent any potential bias in the selection process. This decision, however, introduces a limitation to our review, as our discussion on the psychometric properties of these tools is limited to the information provided by the studies that were included in this umbrella review. In particular, we were not able to appraise the psychometric properties of the tools to assess respiratory muscle strength. Moreover, this umbrella review contributes to a better understanding of neuromuscular function assessment in older adults. Whenever we can identify people that are at risk for a decrease in neuromuscular function, we might be able to prevent further decline and functional losses. In doing so, we can encourage healthy ageing by focussing on prevention of adverse health outcomes, rather than treating the clinical manifestations in older adults. Consequently, it is crucial to conduct a validation study of assessments for neuromuscular function and measure the correlation between vitality capacity, healthy ageing and the various domains of intrinsic capacity. Further research could investigate the trajectories of vitality capacity and how to maintain or improve vitality capacity in older adults.

Conclusion

This umbrella review gives an overview of the available and suitable assessment tools for neuromuscular function for community-dwelling older adults. Five assessments are suitable for measuring the neuromuscular function domain of vitality capacity in community-dwelling older adults: the handheld dynamometer for hand grip strength, dynamometer for knee extensor strength, and the sniff nasal inspiratory pressure, MIP and MEP for respiratory muscles. Further research is necessary to validate these biomarkers and investigate the trajectories of vitality capacity. This study highlights the need of measuring vitality capacity to enhance healthy ageing of community-dwelling older adults. By comprehensively synthesising the available literature and identifying relevant assessment tools, this umbrella review contributes to a better understanding of neuromuscular function assessment in older adults and supports future research and clinical applications.