American Journal of Physical Medicine & Rehabilitation Articles Ahead of Print

DOI: 10.1097/PHM.0000000000000866

Does a rehabilitation program of aerobic and progressive resisted exercises

influence HIV-induced distal neuropathic pain?

Dr Sonill S. Maharaj, B.Paed Sc (UDW); BEd(Unisa); B. Physio (UDW); M.Med Sc. Sports

Medicine(Natal); PhD(UKZN)

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Senior Lecturer: Department of Physiotherapy, School of Health Sciences, University of

KwaZulu-Natal, Durban, Republic of South Africa

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Abdulsalm M. Yakasai, Dip Physio; M Physio ;DPT (USA)

PhD Student c/o Department of Physiotherapy, University of KwaZulu-Natal Durban.

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The authors declare no conflict of interest and no funding was received for this study

Corresponding author
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Dr Sonill S. Maharaj

B.Paed Sc (UDW); BEd(Unisa); B. Physio (UDW); M.Med Sc. Sports Medicine(Natal);

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PhD(UKZN)

maharajss@ukzn.ac.za
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Senior Lecturer: Department of Physiotherapy, School of Health Sciences, University of

KwaZulu-Natal, Durban, Republic of South Africa

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ABSTRACT

Objective: Distal symmetrical polyneuropathy (DSPN) is a common neurological sequela

following HIV which leads to neuropathic pain and functional limitations. Rehabilitation

programs with exercises are used to augment pharmacological therapy to relieve pain but

appropriate and effective exercises are unknown. This study explored the safety and effect of

moderate intensity aerobic exercises (AE) and progressive resisted exercises (PRE) for HIV-

induced DSPN neuropathic pain.

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Design: A randomized pre-test, post-test of 12 weeks of AE or PRE compared to a control.

Outcome measures were assessed using the Subjective Periphery Neuropathy, Brief Peripheral

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Neuropathy Screening and Numeric Pain Rating Scale. Pain was assessed at baseline, 6 and

12weeks. Data between groups were compared using Kruskal Wallis, Mann Whitney U test and

within groups Friedman and Wilcoxon Signed Rank tests.

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Results: There were 136 participants (mean age 36.79±8.23years) and the exercise groups

completed the protocols without any adverse effects. Pain scores within and between AE and

PRE groups showed significant improvement (p<0.05) from baseline to 6 and 12 weeks

compared to the control (p>0.05).

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Conclusion: This study supports a rehabilitation program of moderate intensity AE and PRE
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being safe and effective for reducing neuropathic pain and is beneficial with analgesics for HIV-

induced DSPN.
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KEY WORDS: Neuropathic pain, HIV, Aerobic, Progressive resisted

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INTRODUCTION

Distal symmetrical polyneuropathy (DSPN) is a common neurological sequela following human

immunodeficiency virus (HIV) infection. More than 50% of HIV-infected individuals are

affected by the virus or from toxicity of antiretroviral therapy (ART). The clinical symptoms of

HIV-neuropathy are variable but DSPN and neuropathic pain are the most prevalent, disabling

and treatment-resistant complication of HIV.1 Pain is defined as an unpleasant sensory and

emotional experience associated with actual or potential tissue damage and presents in a third of

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those having DSPN.2

The neuropathic pain and sensory loss are due to distal symmetrical degeneration of peripheral

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nerves and impaired nerve regeneration of large and small nerve fibers.3 When nerve endings are

affected neuropathic pain occurs by primary lesion or dysfunction of the nervous system creating

positive and negative sensory phenomena.4 Neuropathic pain is uncomfortable with sensory loss
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contributing to impaired balance, gait and lower limb injury; these problems can then lead to a

vicious cycle of impairments and disability.5 Often the physical management of DSPN is

challenging, as the underlying cause can be idiopathic or genetic, with treatment available only

to ameliorate symptoms.6 The primary symptom is usually pain with the medical intervention
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being analgesics, which sometimes have limited efficacy or interact with other medication,

leading to toxicity or side effects.7 This deters individuals from taking prescribed medication and
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necessitates the study of non-pharmacological or alternative therapies.8 The overall effect of

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DSPN is physical disability, psychological dysfunction and reduced quality of life (QOL) which

will require physical therapy and rehabilitation.9 Physical therapy encompasses rehabilitation

techniques, splints, orthotic and prosthetic devices which improve disabling symptoms.10 Some

rehabilitation modalities are functional or transcutaneous electrical stimulation, interferential

therapy, heat, ice, ultrasound, massage, manipulative therapy, acupuncture or therapeutic

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exercises. Studies show that participating in exercises increases blood circulation and reduces

pain by increasing endogenous opioids and transient anti-nociception.11 Additionally exercise

produces anti-nociception for a longer duration and increases the concentrations of plasma and

cerebrospinal fluid opioids reducing chronic neuropathic pain.12 Exercise also improves

neuropathic symptoms by promoting microvascular dilation, reducing oxidative stress and

increasing neurotrophic factors.13 Although various exercises are used to rehabilitate HIV-

infected individuals, aerobic exercises (AE) and progressive resisted exercises (PRE) are

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frequently used in the clinical environment. The primary action of AE is to facilitate oxygenated

blood flow from the heart to working muscles and is found to be safe at high intensities. When

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used for HIV-infected individuals there were improvements in cardiovascular fitness, body

composition and psychological status.14 The use of PRE increases body mass index, peripheral

girth, muscle bulk, strength and cardiovascular function in HIV-infected individuals.15 When
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individuals with HIV engaged in AE and PRE there were improvements in performance-oriented

mobility and reduction in neuropathic pain.16 However, to date there are no documented studies

that incorporated AE or PRE for HIV-induced DSPN. This study was designed to determine the

safety of AE and PRE for HIV-induced DSPN and the effect on neuropathic pain scores at
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baseline, 6 and 12weeks.

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METHODS
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Study design

This multi-centered randomized pre-test, post-test study recruited patients requiring physical

therapy and rehabilitation from four HIV-outpatient clinics in the Kano metropolis of Nigeria.

These clinics are attached to the Murtala Muhammed Specialist Hospital, Infectious Diseases

Hospital, Abdullahi Wase Specialist Hospital and International Clinic & Hospital. The Kano

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State Hospital Management Board gave permission to use the HIV-centers. Ethical clearance

conforming to the Helsinki Declaration of 1975 (revised 1983) was obtained from the

Biomedical Research Ethics Committee of the University of Kwazulu-Natal Durban, South

Africa. Duration of study was 1st April to the 31st December 2016. Participants were given

information of the procedures, risks and benefits of the study and signed informed consent in

Hausa which is the local language in Northern Nigeria. Data were coded and stored in a

computer using a secret password. Power analyses and sample size were determined using

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software (Pass15.0.3 NCSS, LLC USA) with Cohen indicating a minimum of 102 participants

for 80% power and 0.32 effect size. Kruskal-Wallis Test compared the control and exercise

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data.17 Exercise adherence was expressed as a percentage of sessions completed over 12 weeks

with 36 sessions equivalent to 100%. Participants completing 29(80%) of exercise sessions were

considered adherent.
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Medical officers supervising the clinics screened participants through medical records and a

physical examination for ability to engage in exercises. To ensure functional exercise capacity

participants completed a 6-minute walk test along a 30metre rectangular passage with no

obstructions.18 Inclusion criteria were participants being on ART for at least 6 months, referred
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for rehabilitation following HIV-related DSPN and ability to participate in weekly exercise
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sessions for 12 weeks. Participants were excluded if their DSPN was not HIV-related, if they had

central nervous system dysfunction, hemiparesis, cerebellar ataxia, myelopathy, if they were
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using a walking aid or were participating in other exercise programs. An administrator

independent of the study randomized participants into AE, PRE or control groups by an online

computer-generated randomization schedule. Data was collected at baseline, 6 and 12weeks, and

included medical parameters viz. blood pressure, heart rate, CD4 count and HIV medications;

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medications were a combination of tenofovir(300mg), lamivudine(300mg), efavirenz(600mg)

with co-trimoxazole and carnitine-combinations daily.

Validated questionnaires for data collection were the Subjective Periphery Neuropathy Screening

(SPNS), Brief Peripheral Neuropathy Screening (BPNS) and Numeric Pain Rating Scale

(NPRS).

The SPNS is a self-administered checklist for neuropathy. Participants tick responses of Yes or

No to questions relating to muscular cramping, ability to differentiate thermal sensation, burning,

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aching, sharp, stabbing, shooting or shock-like pain and allodynia. Foot sensation during walking

and dryness or cracking of the skin are also monitored.19 Participants having a SPNS score of 7

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or higher were screened using the BPNS to assesses intensity and clinical grade of neuropathy

related to „aching or burning pain, „pins and needles' or „numbness'. The intensity of these

symptoms was rated by each participant as 1- mild to 10- most severe. The extent of lower limb
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neuropathy was determined by: participants sitting on a chair with a vibrating 128 Hz tuning fork

placed over anatomical landmarks. Extent of decreased vibration sense was then identified as:-

toes to feet =1; extending to ankle=2; extending to above ankle but not knee=3, extending to the

knee=4, extending above knee or both limbs=5. The duration of vibration sensation in seconds
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was recorded to determine the clinical grade of peripheral neuropathy where: more than 10

seconds was considered “normal” and allocated a score 0; 6 to 10 seconds “mild” loss and
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clinical grade 1; less than 5 seconds “moderate” loss and clinical grade 2; no sensation severe”
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loss and clinical grade 3. The deep tendon reflex was also assessed with the participant seated

and ankle dorsiflexed to 90ᴼ. The Achilles tendon was struck with a reflex hammer to assess

plantar flexion and scored as: 0 if absent; 1 if hypoactive; 2 if normal; 3 if hyperactive and 4 if a

clonus. The BPNS is used by the AIDS Clinical Trial Group and is a valid neuropathy screening

tool for HIV infection and is easily applicable in resource-limited setting.20

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Pain intensity and distress were assessed with NPRS a valid and reliable tool for measuring such

symptoms.21 Participants ticked the number describing their level of pain experienced over 24

hours which was scored from 0 to 10 with; 0 no pain; 1-3 mild; 4-6 moderate and 7-10 severe

pain.

Procedure

Exercises were conducted in a rehabilitation gymnasium of the Murtala Mohammed Specialist

Hospital. Duration of AE and PRE was 30 minutes, on alternate days 3 times per week for 12

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weeks. Procedures for exercises were described and demonstrated to participants. The Tunturi E6

Heart Control Ergometer (Tunturi, USA) was used for AE with participants sitting with feet

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strapped onto the pedals. There were three phases: warm-up, aerobic and cool-down. During the

warm-up and cool-down phases of 5minutes each, participants pedaled without resistance.

During the aerobic phase for 20 minutes, a low resistance of 40% of maximal heart rate (220-
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age) was applied in the first 6 weeks and increased to 65% of maximal heart rate for the

remaining 6 weeks as prescribed by the American College of Sports Medicine.22

The PRE had three phases: warm-up, resisted exercises and cool-down. During warm-up and

cool-down of 5minutes each, participants stretched the quadriceps, hamstrings, tibialis anterior
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and gastrocnemius muscles bilaterally. These same muscle groups were used for the exercise
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phase. A quadriceps bench was used for resistance exercises for 20 minutes. The initial intensity

of exercise was set at 40% of 1-repetition maximum (1-RM) or the maximal weight that could be
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lifted once through full range. The 1-RM was measured at the first exercise session and weekly

for the first 6weeks with the absolute load increased to maintain the relative intensity of the

training effect. During this period, participants performed 2 sets of 10 repetitions of 5 minutes

with resting intervals of 3 to 5 seconds between repetitions. After 6 weeks, the relative intensity

of the exercise was increased to 65% of 1-RM and participants performed 3 sets of 10 repetitions

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for 5 minutes for each muscle group with resting intervals of 2 to 3 seconds between repetitions

as prescribed by the American College of Sport Medicine.22 During exercises blood pressure,

respiratory, heart and oxygen saturation rates were monitored. Heart rate was maintained at

moderate intensity of 40-65% calculated by (220-age) with an increase of systolic or diastolic

blood pressure above 30% from baseline an indication for stopping the activity. Additionally

participants were monitored for signs of subjective fatigue, dyspnea, respiratory distress, profuse

sweating or unsteady gait which showed they reached maximum exertion.23 The control group

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attended HIV-talks, video presentations and counselling when the other groups were exercising.

The HIV-talks covered the prevention and management of HIV. Videos showed the anatomy of

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muscles of the upper and lower limbs, correct posture, patterns of movement and gait

rehabilitation. Counselling related to relevance of diet, benefits of exercises and a healthy

lifestyle for a good quality of life following HIV-infection. Activities for groups are shown in
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Table 4. At the end of the study there was a cross- over of groups where the control group was

given the opportunity to participate in the exercise program that showed maximal benefit, while

the exercise groups received HIV-talks, video presentations and counselling. All data and

exercise monitoring were conducted by senior therapists experienced in neurology and exercise
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programs and blinded to the aims of the study. As this was the first study participants continued
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with their medication during participation but were to inform the researchers of any changes to

their medication.
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Data analysis

The Statistical Package for the Social Science (Version 20.0, Inc., Chicago IL, USA) was used to

analyze data. These were depicted in figures, tables and descriptive statistics using means and

standard deviations. Inferential statistics by means of Friedman test was used to determine the

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differences within groups. Pain scores between groups were compared using Kruskall Wallis test

with post-hoc analysis using the Wilcoxon Signed Rank test for differences at baseline, 6 and

12weeks post-intervention. Mann Whitney U-test was used to determine pain differences

between groups at baseline, 6 and 12 weeks. All statistical analyses were performed at a

probability level of p<0.05 indicating significance.

RESULTS

Demographic characteristics of the participants

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During the study period 233 HIV-infected individuals were referred for physical therapy and

rehabilitation with 165 satisfying the inclusion criteria but 11 refused to sign consent. The 154

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participants were randomized into the three groups with 136 (88%) completing the study. Gender

distribution was 79 females: [27(34%) in AE, 23(29%) in PRE and 29(37%) in the control] and

57 males: [18(31%) AE, 21(37%) PRE and 18(32%) in the control]. Retention and adherence in
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the AE and PRE groups was 99 (96%). The reasons for the 18 (12%) participants not completing

their group allocation were: getting “tired” 5(28%); “bored” 3 (17%) and 10(55%) unknown. The

Consort flow of the study is shown in Figure 1. The number of BPNS scores having clinical

grade 1 was 85 (55%) and 69 (45%) had clinical grade 2. Inferential statistics using ANOVA and
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Kruskall Wallis showed no significant differences between groups for age, gender, weight,
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height, marital status and CD4 count (Table 1).

Differences in pain scores within groups at baseline, 6 and 12weeks post intervention.
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The Friedman test indicated significant differences (p<0.05) from baseline, 6 and 12 weeks post-

intervention for AE and PRE groups (Table 2). Post hoc analysis using Wilcoxon Signed Rank

Test revealed significant differences (p<0.001) with large effect sizes in the AE group from

baseline to 6weeks (r=0.72); 6 to 12weeks (r=0.62) and baseline to 12weeks (r=0.88). Significant

differences (p<0.001) with large effect sizes were also noted post-intervention for PRE from

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baseline to 6weeks (r =0.71); 6 to 12 weeks (r =0.60) and baseline to 12 weeks (r=0.82). No

significant difference (p>0.05) was noted for the control at baseline to 6 and 12weeks.

Differences in pain scores between groups at baseline, 6 and 12weeks post intervention.

Kruskall Wallis test showed significant differences (p<0.05) between groups from baseline to 6

and 12 weeks post-intervention (Table 3). Mann Whitney U-test post-hoc analysis showed

significant difference (p= 0.046) with small effect size (r=0.21) at 6 weeks between AE and

PRE; between AE and control (p<0.001) with effect size (r=0.38); PRE and control (p<0.001)

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with effect size (r =0.52). Data also showed significant differences between groups at 12weeks

post-intervention, as follows: between AE and PRE groups (p=0.014) and effect size (r =0.26);

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AE and control (p<0.001) and effect size (r=0.75); PRE and control (p<0.001) and effect size (r

=0.83). A few participants reported missing collection dates for medication but none reported

changes to medication.
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DISCUSSION

The purpose of this study was to determine the safety and effect of AE and PRE for HIV-induced

DSPN and neuropathic pain. Results from this short-term 12weeks study of moderate intensity

AE and PRE showed these exercises to be safe and to reduce neuropathic pain for individuals
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with HIV-induced DSPN. This conclusion was supported by the participant‟s compliance,
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occurrence of no adverse effects post-exercise and data showing positive outcomes for pain. The

control group had no changes for pain scores at all time points of the study. The data from this
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study is supported by other studies which show that moderate intensity exercises reduce risk

factors and improves many health conditions.24 It was noted that regular aerobic and resisted

exercises had positive benefits because these exercises enhanced peripheral nerve conduction

velocity, increased density of nerve fibers and neurogenic branching.25 This study is consistent

with other studies showing positive benefits following exercises. There is support that engaging

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in exercises have favorable adaptions to the nervous system through plasticity mechanisms,

retraining the neural pathways, improving sensation, increasing circulation and reducing

neuropathic pain.7,26 Similarly studies with rodents showed that aerobic exercises delayed the

onset of pain, tactile hypersensitivity, reduced mechanical allodynia and hyperalgesia following

injury.11 The significant decrease in pain scores following AE and PRE in this current study also

correlates with another study in which aerobic and resisted exercises alleviated neuropathic pain,

increased plantar cutaneous sensation and the ability to perceive vibrations.27 A hypothesized

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reason for the positive benefits for pain in this study could be based on two ways in which

exercises reduce neuropathic pain. First, norepinephrine, which is increased systemically during

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exercise by enhanced adrenal sympathetic activity may inactivate GSK-3β. This inactivation

reduces the proliferation of microglia and the release of pro-inflammatory cytokines from

microglia and astrocytes.28 Second, during exercises contracting skeletal muscles secrete
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cytokines, mainly myokines which have anti-inflammatory properties and prevent or reduce low-

grade systemic inflammation.29 Additionally, there is support for the finding that the use of AE

and PRE is highly effective in enhancing the recovery from some of the distressing symptoms

associated with peripheral neuropathy.7 This finding correlates with the data in this study as
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neuropathic pain could be regarded as a distressing symptom and was reduced following AE and

PRE. However, this study is in contrast to the study by Mkandla16 who found that neuropathic
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pain was also reduced in their control group. On review of Mkandla‟s16 study it was noted that
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PRE was a component of the control‟s home exercise program.

As there were no adverse effects following AE and PRE these exercises appear safe for

individuals presenting with HIV-induced DSPN and neuropathic pain provided they have no

contra-indications for engaging in exercise programs. As this was an initial study the researchers

allowed participants to continue with analgesics. The improvements following AE and PRE

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support their use by therapists as an adjuvant to pharmacological therapy to rehabilitate

individuals with HIV-induced neuropathic pain to improve their function, and to improve their

quality of life.

Further studies are recommended in which the use of analgesic be reduced or terminated during

exercise programs because the long-term goal is to replace analgesics use by exercises. If

successful such studies would support exercise as an alternative to medication, and would ensure

that the medical management does not only deal with the health problem but allows for the

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patient‟s personal treatment of pain.30 Exercise prescription as „self-care‟ would reduce the side

effects associated with medication and the dependency on public health especially in resource

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constrained environments.

Although, this study showed positive benefits for AE and PRE there were limitations. Firstly, as

an initial study the researchers allowed participants to continue with medication during
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participation. Secondly, some participants may have walked long distances to access the

hospitals and this was not considered during group allocation, nonetheless, they could have been

allocated to any group. Finally, although participants were required to notify the researchers of

changes to medication there may have been instances where this was not reported.
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This study supports a rehabilitation program of moderate intensity AE and PRE for HIV-induced
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DSPN. The exercises are safe and with analgesics is effective in reducing neuropathic pain.
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ACKNOWLEDGEMENTS

The authors express their appreciation to staff of the hospitals for their assistance and

participants for engaging in the study.

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FIGURE LEGENDS

Figure 1: Consort Flow of Study

Table 1: Demographic Characteristics of Participants

Table 2: Differences in pain level scores within groups at baseline, 6 and 12weeks post-

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intervention

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Table 3: Differences between groups on pain scores at baseline, 6 and 12weeks post-intervention

Table 4: Duration and activities for the Groups

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Table 1: Demographic Characteristics of Participants

Variable Aerobic (n=45) Progressive resisted Control (n=47) P-

(n=44) value
Age (years) 38.29±8.06 35.98±8.53 36.13±8.10 0.331
Height (cm) 1.67±0.11 1.67±0.11 1.67±0.12 0.959
Weight (kg) 64.07±16.00 70.96±15.81 70.20±16.21 0.091
Gender (%)
Female 34.18 29.11 36.71 0.773
Male 31.58 36.84 31.58 0.812
Marital status
(%)

D
married 82.04 63.61 60.11 0.111
HIV-status
Mean CD4 362 401 396 0.451
(cell/mm2 )

TE
Key: *Significant at p<0.05.
EP
C
C
A

19

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Table 2: Differences in pain level scores within groups from the baseline, 6 and 12 weeks post-
intervention

Variable Group N Baseline 6 weeks 12 weeks X2 p-value

Mdn (IQR) Mdn (IQR) Mdn (IQR)
Pain level Aerobic 45 2.0(1.0) 2.0(0.5) 1.0(1.0) 62.373 <0.001*
Progressive 44 2.0(1.0) 2.0(1.0) 1.0(0.0) 55.590 <0.001*
Control 47 2.0(1.0) 2.0(1.0) 3.0(1.0) 5.549 0.062

Key:

Significant at p<0.05

D
X2 = Chi square of Friedman test

N= number of participant in group

TE
Mdn (IQR) = Median inter-quartile range
EP
C
C
A

20

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Table 3: Differences between groups for pain scores at baseline, 6 and 12 weeks post-
intervention

Group Aerobic Progressive Control

Variables Time period AE (N) Mdn PRE Mdn CG (N) Mdn X2 p-value
(IQR) (N) (IQR) (IQR)
Pain level Baseline 45 2.0(1.0) 44 2.0(1.0) 47 2.0(1.0) 3.183 0.204
6 weeks 45 2.0(0.5) 44 2.0(1.0) 47 2.0(1.0) 28.20 <0.001*
12 weeks 45 1.0(1.0) 44 1.0(0) 47 3.0(1.0) 81.84 <0.001*

Key:

*Significant at p<0.05.

D
AE(N) - number of participants in aerobic exercise group

PRE(N) - number of participants in progressive resisted exercise group

TE
CG(N) - number of the participants in control group

Mdn(IQR) - median inter quartile range

X2 - Chi square of Kruskal-Wallis test.

Refer to text for detail pairwise comparison and effect size

EP
C
C
A

21

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Table 4: Duration and activities for the Groups

Time period Aerobic Progressive Control group.

exercise resisted
group(AE) exercise
group(PRE)
Aerobic Stretching of The HIV-talks
exercise using quadriceps, covered the
1 to 6weeks cycle hamstrings, prevention and
ergometer at gastrocnemius management
intensity of and tibialis of HIV. Videos

D
40% maximum anterior showed the
heart rate for bilaterally for anatomy of
30 minutes. 10 minutes. muscles of the

TE
Strength upper and
exercise with lower limbs,
40% of 1RM correct
with 2 sets of posture,
repetitions for patterns of
20 minutes. movement and
gait
EP
rehabilitation.
The intensity of Stretching as Counselling
the aerobic above. related to
6 to12weeks. exercise was Intensity relevance of
increased to increased to diet, benefits of
65% maximum 65% of 1RM exercises and a
C

heart rate for with 3 sets of healthy lifestyle

30 minutes. repetitions for for a good
20 minutes. quality of life
following HIV-
C

infection
A

22

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