Archives of Gerontology and Geriatrics 54 (2012) e83–e88

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Functional capacity of Brazilian patients with Parkinson’s disease (PD):Relationship between clinical characteristics and disease severity

Fabio A. Barbieri *, Natalia M. Rinaldi, Paulo Cezar R. Santos, Ellen Lirani-Silva, Rodrigo Vitorio,Claudia Teixeira-Arroyo, Florindo Stella, Lilian Teresa B. Gobbi

on behalf of the PROPARKI Group

UNESP – Sao Paulo State University at Rio Claro, Posture and Gait Studies Lab, SP, Brazil

A R T I C L E I N F O

Article history:

Received 12 May 2011

Received in revised form 6 July 2011

Accepted 19 July 2011

Available online 1 October 2011

Keywords:

Parkinson’s disease

Functional capacity

Disease severity

A B S T R A C T

The present study had three objectives: (a) to characterize the functional capacity of patients with PD, (b)

to assess the relationship between the physical fitness components of functional capacity with clinical

characteristics and disease severity, and (c) to compare the physical fitness components of functional

capacity with clinical characteristics according to disease severity. The study included 54 patients with

idiopathic PD who were distributed into two groups according to PD severity: unilateral group (n = 35);

and bilateral group (n = 19). All patients underwent psychiatric assessment by means of the Hoehn and

Yahr (HY) staging of PD, the Unified Parkinson’s Disease Rating Scale (UPDRS), the Hospital Anxiety and

Depression Scale (HADS-A and HADS-D, respectively), and The Mini-Mental State Examination (MMSE).

The physical fitness components of functional capacity were evaluated over a 2-day period, using

recommendations by the American Alliance for Health, Physical Education, Recreation and Dance, and

the Berg Balance Scale (BBS). Pearson correlation coefficients and multiple regressions were calculated to

test the correlation between functional capacity and clinical characteristics, and to predict clinical scores

from physical performance, respectively. Clinical variables and physical component data were compared

between groups using analysis of variance to determine the effects of disease severity. Patients with

advanced disease showed low levels of functional capacity. Interestingly, patients with good functional

capacity in one of the physical fitness components also showed good capacities in the other components.

Disease severity is a major factor affecting functional capacity and clinical characteristics. Medical

providers should take disease severity into consideration when prescribing physical activity for PD

patients, since the relationship between functional capacity and clinical characteristics is dependent on

disease severity.

� 2011 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

PD decreases the performance of daily activities, affecting thepatient’s quality of life (Stella et al., 2007; Shulman et al., 2008).The successful performance of daily activities requires the body tomake rapid changes from one position to another and to maintainbalance. Frequently, the absence of these abilities results in falls(Matinolli et al., 2009). The occurrence of motor injuries and bonefractures from such falls can negatively affect the quality of life ofthese patients (Hirayama et al., 2008). Therefore, PD symptoms

* Corresponding author at: Universidade Estadual Paulista – UNESP – IB – Rio

Claro, Laboratorio de Estudos da Postura e da Locomocao, Departamento de

Educacao Fısica, Avenida 24-A, 1515 Bela Vista, CEP: 13.506-900 Rio Claro, Sao

Paulo, Brazil. Tel.: +55 19 3526 4320; fax: +55 19 3534 6436.

E-mail address: barbieri_rc@hotmail.com (F.A. Barbieri).

0167-4943/$ – see front matter � 2011 Elsevier Ireland Ltd. All rights reserved.

doi:10.1016/j.archger.2011.07.008

include not only motor manifestations such as tremor, rigidity,bradykinesia, and postural instability, but, also, non-motorsymptoms such as cognitive deficits (Stella et al., 2007, 2009;Tanaka et al., 2009), depression (Mercury et al., 2007), sleepdisturbances (Hawkes et al., 2010), and impulse control disorders(Lopez-Morınigo et al., 2009).

Physical activity is an important factor for improving functionalcapacity in older individuals (Cyarto et al., 2008). According toBrach et al. (2004), any type of physical activity is better than noactivity for improving the level of functional capacity. However,functional capacity in people with PD has not been widelyinvestigated. Adequate levels of functional capacity (flexibility,coordination, agility, balance, aerobic resistance, and strength) arecrucial to perform daily activities and to prevent chronic diseases(Rantanen et al., 1999). In order to investigate functional fitness inolder individuals, the American Alliance for Health PhysicalEducation Recreation and Dance (AAHPERD) proposed using a

F.A. Barbieri et al. / Archives of Gerontology and Geriatrics 54 (2012) e83–e88e84

standardized test, the Physical Functional Ability Test for Adults 60Years of Age and Older (Osness et al., 1990). This instrument makesit possible to assess individual fitness components of functionalcapacity in PD patients, who may exhibit normal scores in somedomains and weak scores in others.

Motor and non-motor manifestations and disease severity,which also can affect the performance of daily activities, have beenassessed using clinical instruments such as the UPDRS (Fahn andElton, 1987); the HY scale (Goetz et al., 2004); MMSE (Folsteinet al., 1975); and the HADS-A and HADS-D (Mondolo et al., 2006).Motor functions, also, are associated with cognitive function, anddepression and anxiety. Cognitive decline in PD patients appears tobe associated with worsening motor symptoms (Van Spaendoncket al., 1996). Depression and anxiety levels are related not only tocognitive impairment, but, also, to motor symptoms, dyskinesias,the prodromal period, and moderate HY stages (Hawkes et al.,2010). Thus, depression and cognitive impairment could beconsidered main predictors of poor quality of life in PD patients(Rahman et al., 2008).

In PD patients, this strong relationship between motor andcognitive functions affects quality of life. For example, depressionand anxiety symptoms can negatively affect quality of life,resulting in impaired cognitive function. Conversely, a higherlevel of functional capacity can ensure a better quality of life.Therefore, the present study had three objectives: (a) tocharacterize the functional capacity of patients with PD, (b) toassess the relationship between the physical fitness components offunctional capacity with clinical characteristics and diseaseseverity, and (c) to compare the physical fitness components offunctional capacity with clinical characteristics according todisease severity.

2. Materials and methods

2.1. Study population

The participants consisted of 54 patients with idiopathic PD,who participated in a multidisciplinary PD project conducted atSao Paulo State University at Rio Claro (UNESP-RC). These patientsregularly attended the neurology clinic at UNESP-RC. The inclusioncriteria included both men and women who have had a clinicallyconfirmed diagnosis of PD and were able to walk independently.The patients were interviewed from February 2004 to December2008.

2.2. Clinical evaluation

Data were collected using demographic and anthropometricguidelines that included: gender, age, disease duration, educationlevel, and body weight and height. All patients underwentpsychiatric evaluation as follows: (a) PD symptoms and signswere assessed in all subsections of the UPDRS, and includedmental, activities in daily living (ADL), and motor examinations(Fahn and Elton, 1987). This scale ranges from 0 to 176 points(mental: 16 points, ADL: 52 points, motor: 108 points), and a highscore indicates greater impairment; (b) mental status was assessedusing the MMSE (Folstein et al., 1975), which is a brief 30-pointquestionnaire, in which values up to 24 points are considered asmentally ‘‘intact’’ (Brucki et al., 2003); (c) PD severity wasevaluated using the modified HY scale (Hoehn and Yahr, 1967;Goetz et al., 2004). This scale ranges from 0 (no signs of disease) to5 (needing a wheelchair or bedridden unless assisted) in order toindicate a relative level of disability; and (d) anxiety anddepression symptoms were assessed using the HADS-A andHADS-D (Mondolo et al., 2006). It consists of 14 items (sevenfor assessing anxiety, and seven for depression), ranging from 0 (no

problem) to 3 (severe problem). Values of up to 9 points in eachscale are representative of symptoms of anxiety and depression(Zigmond and Snaith, 1983).

2.3. Functional capacity evaluation

All patients were evaluated in the morning—in the ‘‘onmedication’’ state, one hour after taking the first morning dose ofanti-Parkinson medications. The physical fitness components wereassessed over 2 days, using the test proposed by the AAHPERD(Osness et al., 1990), and the BBS (Scalzo et al., 2009). The AAHPERDtest includes measures of flexibility, muscular strength, agility,coordination, and aerobic endurance. It provides a set of standard-ized instructions, which were used with the participants inpreparation for the assessment of the test items (Osness et al., 1990):

(a) F

lexibility test: a standard sit-and-reach test in whichparticipants are seated, with their heels 12 in apart and overa line that runs perpendicular to a measuring tape. They areasked to reach with both hands as far along the measuring tapeas they comfortably can while keeping both knees straight. Thescore is their highest tape measure mark for three attempts.

(b) M

uscular strength: requires female participants to lift a 4-lbobject, and male participants to lift an 8-lb object, using abiceps curl motion, as many times as possible in 30 s.

(c) A

gility: patients start from a seated position and are asked torise from a chair, walk to the right around a cone, and return tothe seat and sit down, stand again, walk to the left around acone, return to their seat and sit down, and then repeat theentire procedure. The participants are given two attempts, andthe raw score represents the faster of the two.

(d) C

oordination: involves the movement of three 12-oz soda cans,using the dominant hand. The cans are placed on a table, top-side-up and on a line indicated by a 30-in. length of maskingtape. The cans are located at 10-in. intervals. The participantsare seated at the table with the line of cans well within theirgrasp and they are then asked to perform two attempts inwhich they are asked to place each can top-side-down in aspace adjacent to its original position. Then they return thecans to their original top-side-up position. Each trial consists ofperforming these movements twice, and the raw score reflectsthe faster of two trials.

(e) A

erobic endurance: an 880-yd walk, at the participant’smaximum speed.

The BBS was used to assess global functional balance ability.This test rates performance from 0 (cannot perform) to 4 (normalperformance) on 14 different tasks, which involve functionalbalance control (transfer, turning, and stepping).

2.4. Study procedures

All procedures described were approved by the Research EthicsCommittee at UNESP-RC. Participants gave their written informedconsent and were screened. Those eligible to participate in the studyunderwent a clinical evaluation. All who met the inclusion criteriawere invited to participate in two additional testing sessions. Duringthe first testing session, each participant performed balance,flexibility, coordination, strength, and agility tests. Aerobic resis-tance was evaluated on the second day. Both sessions were held inthe morning between 8:00 a.m. and 11:00 a.m.

2.5. Statistical analysis

Demographic, anthropometric, and clinical characteristics andphysical components of PD patients were described as means and

[(Fig._1)TD$FIG]

Fig. 1. Relationships between physical fitness components (r-value, p-value).

*p < 0.05, **p < 0.01 and ***p < 0.001.

F.A. Barbieri et al. / Archives of Gerontology and Geriatrics 54 (2012) e83–e88 e85

standard deviations (S.D.). The Shapiro–Wilk test was used to testthe normal distribution. Pearson correlation coefficients werecalculated to test the correlation of functional capacity withclinical characteristics. Multiple regressions (step-wise model)were used to predict the main functional capacity outcomevariables, while controlling for clinical PD characteristics. Theregression analysis model included physical fitness components asa predictive variable relative to all of the other variables (Field,2005).

The participants were assigned to two groups according to PDseverity: unilateral group (HY stages 1 and 1.5) (n = 35); andbilateral group (HY stages 2–3) (n = 19). The Student’s t-test wasused to test for differences between the two PD severity groups(unilateral and bilateral). Pearson coefficients and multipleregressions (the same models noted previously) were calculatedto assess the correlation and to predict the clinical scores byphysical performance in each group, respectively. Statisticalanalyses were carried out using SPSS for Windows 10.01 (thesignificance level was set at p < 0.05).

3. Results

The PD patients showed mild-to-moderate disease. Thecharacteristics of the sample studied are shown in Table 1. Allcomponents of physical fitness, except flexibility, were correlated(Fig. 1). The strongest correlations were found for balance/agility,aerobic resistance/agility, balance/aerobic resistance, and balance/coordination.

The Pearson correlation showed a strong relationship betweenall physical fitness components and clinical variables (Table 2),except for flexibility, which did not reveal a significant relationshipwith clinical variables. The multiple regressions revealed thatsome of the physical fitness components are predictors of theclinical PD characteristics (Table 2). The most notable results forthe regression were for the UPDRS-motor, which was predicted in67.8% by coordination (R2 = 0.29; b = 0.44; p < 0.003) and strength(R2 = 0.38; b = �0.31; p < 0.003).

As for PD severity (Fig. 2), the analysis of variance showed thatthe PD patients with unilateral impairment scored significantly

Table 1Demographic, anthropometrical, clinical and physical characteristics of the

participants (mean� S.D.).

Range

Demographic characteristicsMen/women (number of patients) 29/25

Age (years) 66.48�9.04 48–84

Education (years) 7.56�4.62 2–18

Age at onset (years) 61.74�10.81 41–83

Duration of disease (age) 5.40�6.04 0.5–30

Anthropometrical characteristicsBody weight (kg) 67.52�12.49 39.5–91.6

Body height (m) 1.61�0.09 1.42–1.79

Clinical characteristicsUPDRS mental score (pts) 3.84�2.38 0–10

UPDRS ADL score (pts) 12.98�7.59 1–32

UPDRS motor score (pts) 25.24�14.33 5–64

MMSE score (pts) 24.91�4.72 17–30

HY scale 1 (median) 1–3

HADS-A score (pts) 7.02�4.63 0–17

HADS-D score (pts) 7.57�5.02 0–20

Physical components characteristicsBalance (pts) 49.87�6.89 30–56

Flexibility (cm) 48.48�11.74 16–71.5

Coordination (s) 22.00�13.44 10.02–86

Agility (s) 44.01�43.93 18.66–285

Strength (rep.) 19.24�6.10 8–37

Aerobic resistance (min) 10.32�2.36 6.25–17.24

better in the UPDRS ADL (p < 0.0001) and motor (p < 0.0001), andHADS-D (p < 0.01) than did those with bilateral impairment.HADS-A showed a difference trend (p < 0.06) between the groups,with fewer anxiety signs for the unilateral group. For physicalfitness, the unilateral group performed significantly better forbalance (p < 0.0001), agility (p < 0.0061), and coordination(p < 0.007) than their bilateral group counterparts. The unilateralgroup showed a tendency toward a better performance forflexibility (p < 0.07).

Table 2 illustrates that the severity of PD impairment affects therelationship of the physical components relative to the otherclinical variables. This is true, also, for the results in the multipleregression analysis. The unilateral group showed a strongerrelationship between physical fitness components and indicatorsof disease severity. Coordination was an important predictor ofscores on the MMSE (R2 = 0.42; b = �0.65; p < 0.001). In thebilateral group, the physical fitness components were strongpredictors for clinical variables (more than 22%). Muscle strengthwas a predictor for scores on the UPDRS ADL (R2 = 0.41; b = �0.64;p < 0.003) and motor (R2 = 0.42; b = �0.65; p < 0.003), whileflexibility was a predictor of scores on both the HADS-A (R2 = 0.40;b = 0.64; p < 0.01) and the HADS-D (R2 = 0.22; b = 0.47; p < 0.03).

4. Discussion

The purposes of this study were (a) to investigate the functionalcapacity of PD patients, (b) to assess the relationship between thephysical fitness components of functional capacity with clinicalcharacteristics and disease severity, and (c) to compare thephysical fitness components of functional capacity with clinicalcharacteristics according to disease severity. The PD patients inthis study showed mild to moderate levels of the disease as definedby the UPDRS and HY stages assessments. Patients presented signsof anxiety and depression, and high variability relative to durationof disease. These clinical characteristics can explain the wide rangebetween the minimum and maximum values found for thefunctional capacity components, particularly for agility andcoordination.

Some functional capacity components decline with PD severity.PD patients have cognitive deficits (manifested in tasks that

Table 2Pearson correlations and multiple regressions results between physical fitness components with clinical variables for overall and according disease severity.

UPDRS mentation UPDRS ADL UPDRS motor MMSE HY scale HADS-A HADS-D

OverallAerobic resistance r = 0.43*,+ r = 0.37** r = 0.41** r = 0.31* r = 0.43**,+ r = 0.39**,+

Strength r = 0.33*** r =�0.52***,+ r =�0.45***,+ r = 0.37** r = 0.44***

Coordination r = 0.31* r = 0.49***,+ r =�0.41** r = 0.41** r = 0.32***

Balance r =�0.44* r = 0.51*** r = 0.37**,+ r =�0.61***,+

Agility r = 0.38** r = 0.35** r = 0.44***

Unilateral groupAerobic resistance r = 0.45**,+

Strength r =�0.46**,+ r =�0.34*,+ r = 0.38*

Coordination r =�0.65***,+

Bilateral groupAerobic resistance r = 0.54*

Strength r =�0.47*,+ r =�0.58**,+ r =�0.53*,+

Flexibility r = 0.58**,+ r = 0.55**,+

* p<0.05.** p<0.01.*** p<0.001.+ Significant multiple regressions.

[(Fig._2)TD$FIG]

Fig. 2. Comparisons between the PD severity groups (mean � SD). (A) Clinical variables; (B) physical fitness components. * Unilateral group 6¼ bilateral group; + difference trend

between unilateral and bilateral groups.

F.A. Barbieri et al. / Archives of Gerontology and Geriatrics 54 (2012) e83–e88e86

demand mental flexibility), which subsequently may lead to motordysfunction and poor performance in the physical tests. In PDpatients, personal, motor, and cognitive characteristics affectwalking speed, mainly during complex dual tasks (i.e., motor andcognitive tasks performed simultaneously) (Rochester et al., 2009).Our results also illustrated that the participants who performedwell in one of the functional capacity components also performedwell in all the other components, with the exception of flexibility. Itappears that during the successful performance of daily livingactivities, these components have an interdependent relationship.It should be noted that independent living requires a high level offunctional capacity (Okamoto et al., 2006).

On the other hand, our findings suggest that in PD patients,flexibility is an independent component. It is possible that theevaluation method for flexibility is not as sensitive as those forthe other components. It is also possible that the flexibility levels ofthe patients in this study simply are not sufficient to promoteimprovements in other functional capacity components and

clinical variables. This seems evident, since no general relationshipwas found between flexibility and the other functional capacitycomponents. Specifically, the results suggest that patients withadvanced disease and high flexibility scores had more signs ofanxiety and depression, which indicates that flexibility, is animportant predictor for anxiety and depression. Motor symptomsdo not have an association with cognitive decline, but depressionsymptoms can be a strong predictor of cognitive decline (Kandiahet al., 2009). Our findings with regard to flexibility suggest thatfurther research is needed on this subject.

Functional capacity components can predict the clinicalcharacteristics of PD. Patients in the unilateral group (initialstages of the disease) showed high levels of functional capacity.The relationship between functional capacity components andclinical characteristics may help medical providers better assessearly physical functional impairment (Song et al., 2009) in thesepatients. Functional capacity components seem to be an effectiveparameter in the determination of UPDRS ADL and motor scores,

F.A. Barbieri et al. / Archives of Gerontology and Geriatrics 54 (2012) e83–e88 e87

MMSE scores, HY stages, and depression. Non-motor symptomsmore negatively affect the quality of life of PD patients than domotor symptoms (Qin et al., 2009). Motor impairment is commonin PD patients and can be associated with increased risk ofcognitive decline, dementia and depression symptoms (Camicioliet al., 2007). It is important to note that some clinicalcharacteristics are particularly dependent on functional capacitycomponents. For example, high levels of coordination and musclestrength can lead to improved UPDRS motor scores. For theunilateral group, better coordination implies more favorableMMSE scores. Therefore, the clinical characteristics of the bilateralgroup appear to be highly dependent on muscle strength andflexibility, which were the main predictors for this group.

Disease severity is a modifier of physical performance andcauses disability in PD patients, affecting their ability to performdaily living activities (Shulman et al., 2008). The unilateral groupshowed higher levels of functional capacity (balance, agility, andcoordination) than the bilateral group. Balance problems in PDpatients can cause falls, and, consequently, fear of falling(Franchignoni et al., 2005) and reduced gait velocity (Carpinellaet al., 2007). Slowness of movement arising from bradykinesia andakinesia can explain lower performance in the bilateral group inagility and coordination. Functional capacity in PD patients isinfluenced by clinical variables (as reflected in the UPDRS, HADSand MMSE scores). A reduction in their functional capacity andcognitive function impairs the performance of daily activities, and,consequently, affects their quality of life. These findings alsosupport the differences between the two groups studied relative toclinical variables, as assessed by the UPDRS (ADL and motorsubsections) and the HADS instruments (depression and anxiety).

Motor and non-motor symptoms arise from frontal-basalganglia damage, pigmented neurons loss in the substantia nigra,and a decrease in striatal dopamine transport, even in theprodromal period and early stages of the disease (Hawkes et al.,2010). Due to a longer disease course, the bilateral group had agreater loss of dopamine neurons than did the unilateral group.Poor performance in the physical and clinical tests in the bilateralgroup can also be explained by a more extensive Lewy bodyformation, and disease progression from the brainstem to thelimbic system and cerebral neocortex (Drag et al., 2009). PDpatients experience impaired executive function due to adysfunction of connections between the striatum and the frontallobes. The bilateral group, who received dopaminergic drugs for alonger period of time, showed higher HADS scores than theirunilateral counterparts, which supports Fahn (2005) results. Ourresults illustrate the progression of motor and non-motorsymptoms.

Several limitations of this study are evident. The importance ofevaluating functional capacity and its relationship to quality of lifehas been well documented. However, the instruments used toevaluate the PD patients in the current study have not been validatedfor use in this population. In future studies, tests should be designedspecifically to determine the functional capacity of PD patients.Additionally, it might prove useful to include other motor and non-motor variables in the regression model: for example, gait velocity,executive function, and memory, to determine the extent to whichfunctional capacity components can predict disease severity.

5. Conclusion

In conclusion, PD patients appear to have decreases infunctional capacity performance that are related to the severityof the disease. Interestingly, patients with a greater capacity inone of the physical fitness components also showed a greatercapacity in the other components. The impairment severity of PDis a major factor affecting patients’ functional capacity and clinical

characteristics. Therefore, medical providers should take diseaseseverity into consideration when prescribing physical activity toPD patients.

Conflict of interest statement

All authors have disclosed any financial and personal relation-ships, with other people or organizations, that could inappropri-ately influence (bias) this work.

Acknowledgments

The authors thank each movement disorder specialist in thePROPARKI Group. The authors thank CNPq, CAPES and PROEX forfinancial support. Author responsible for all correspondence andcorrection of proofs.

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