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4 4 &)4 4 4 4 4 6�6�J(�4 4 4 ��4 4 4 4 ���������������������������������������������������������������������4 4 4 4 4 4 4 4 4 �+	:CHARACTERIZATION OF SLEEP AND ITS INFLUENCE ON NEUROPHYSIOLOGICAL RECOVERY IN PATIENTS WITH POST-POLIO SYNDROME (SPP)
Adriano Rodrigues de Oliveira1*; Luis Vicente Franco de Oliveira2; Jo�o Carlos Ferrari Corr�a2  
1 Professor, Universidade Nove de Julho (UNINOVE), S�o Paulo, SP, Brazil
2 Professor of Master�s and Doctoral Programs in Rehabilitation Sciences, UNINOVE, S�o Paulo, SP, Brazil
Address for correspondence: Prof. Ms. Adriano Rodrigues de Oliveira*
Rua Josefina Arnoni, 115, apto 112, bl 01, Vila Irm�os Arnoni, S�o Paulo, SP, Brasil, CEP: 02374-050 E-mail:  HYPERLINK "mailto:adrianoro@ig.com.br" adrianoro@ig.com.br Tel: (11) 9517 0186
The authors declare no conflicts of interest related to the present study.
ABSTRACT
INTRODUCTION: Patients with motor impairment in the lower limbs stemming from poliomyelitis commonly experience sleep disorders, which can affect activities of daily living and have a negative impact on quality of life. OBJECTIVE: to assess quality of sleep the patients with post-polio syndorme using polysomnography. PATIENTS/METHODS: An analytical of the cross-sectional study was carried out involving 19 volunteers. RESULTS: Diminished sleep efficiency was found (74.73% � 18.47) and was credited to periodic movements of the lower limbs (index 9.21 � 15.26) as well as episodes of apnea and hypopnea (index: 14.41 � 12.86), which increased the number of micro-awakenings (93.26 � 67.02) and awakenings (12.31 � 7.08). CONCLUSION: The variables analyzed indicate abnormalities that favor sleep disorders. The consequent reduction in the period of neurophysiological recovery can have a negative effect on activities of daily living.
Keywords: Poliomyelitis; polysomnography; sleep disorders; fatigue; neurophysiological; activities of daily living.
INTRODUCTION
Until 1960, acute anterior poliomyelitis (polio) was the main cause of motor paralysis and death among children and young adults worldwide. This viral disease typically arises in a biphasic manner with headache, fever and gastrointestinal symptoms, which is soon followed by impairment of the motor neurons of the spinal cord, leading to asymmetric and disproportionate paralysis, especially in the lower limbs (1) .
The disease is caused by three serotypes of the poliovirus (PV1, PV2 and PV3), which induce paralysis. PV1 is the most prevalent, followed by PV3. PV2 exhibits the greatest degree of immunogenicity, followed by PV1 and PV3 (2). The virus is transmitted from person to person through nasopharyngeal secretions or from objects, food or water that have been contaminated by individuals with the disease (3).
The poliovirus is highly infectious and colonizes 100% of susceptible individuals who come into contact with it. Neurological impairment from poliovirus infection occurs in 1 to 1.6% of cases. The virus enters the human organism orally and reaches the oropharynx and intestinal tube, where it proliferates and invades the lymphatic tissues of the region. The virus first appears in the oropharynx and feces, with viral shedding into the environment and a shorter period of viremia, in which tissues of the reticuloendothelial system become affected. A number of patients experience a second period of viremia, also known as greater viremia, which is characterized by non-specific symptoms. This proliferation provides the infected individual with protective antibodies for life. Immunity is specific to the type of virus that causes the infection (4). 
The progression of paralysis generally ceases in less than one week and is followed by a period of stabilization and the gradual recovery of motor functions, leading to the return to basic and instrumental activities of daily living. However, individuals may experience asymmetrical paralysis, mainly in the lower limbs, due to the impairment of neurons in lamina 9 of the spinal cord (5).
Poliomyelitis can have visible lasting effects. Post-polio syndrome (PPS) is the most common late-onset effect of the disease. PPS is a neurological condition that causes new muscle weakness and/or abnormal muscle fatigability in individuals who have experienced poliomyelitis in the past (over 15 years ago) and leads to limitations in the performance of activities of daily living (1). This syndrome is also characterized by symptoms such as pain, new atrophy, breathing and swallowing difficulties, periodic limb movement disorder (PLMD) and sleep disorders. The frequency of sleep disorders is high due to the increase in sleep latency and number of awakenings (6).
There are a number of hypotheses regarding the cause of PPS, but the most accepted is that the syndrome is not caused by new activity of the disease, but rather by the excessive use of motor neurons over a period of years. In the acute phase of poliomyelitis, the virus may damage up to 95% of the motor neurons in the anterior horn of the spinal cord, leading to the death of at least 50% of the neurons. Consequently, the muscles in the affected region are no longer innervated, which causes paralysis and atrophy. Although damaged, the remaining neurons offset the losses by forming new connections to activate these �orphaned� muscles. Neuromuscular function is partially or totally recovered, depending on the number of neurons involved in the �adoption�. A single neuron can send branches to connect five to 10 times more neuromuscular fibers than it normally would, thereby restoring motor function. However, the excessive load over many years of functional stability can lead to further degeneration, followed by new symptoms (7).
Sleep is characterized by two distinct phases: non-rapid eye movement sleep (non-REM) and rapid eye movement sleep (REM). In healthy individuals, the beginning of non-REM sleep (stages 1, 2, 3 and 4) is associated with reductions in metabolic rate, sympathetic nervous system (SNS) activity, heart rate and blood pressure. REM sleep is associated with intermittent increases in metabolic rate, SNS activity, heart rate and blood pressure, often at levels equal to or greater than those recorded during waking hours, and is characterized by a period of low voltage electrical activity as well as mixed frequency electroencephalography, high electromyographic activity and frequent involuntary eye movement (8).
Sleep stages are evaluated by polysomnography, which is a generic term for the simultaneous recording of physiological variables during sleep, such as electroencephalogram (EEG), electrooculogram (EOG), electromyogram (EMG), electrocardiogram (ECG), airflow (nasal and oral), respiratory effort (thoracic and abdominal), other body movements (by EMG), blood gases (oxygen saturation, concentration of carbon dioxide) and body temperature (9). Moreover, polysomnography in post-poliomyelitis patients may reveal sleep apnea, which is defined as a complete lack of airflow for a minimum of 10 seconds, and hypopnea, which is a 50% reduction in baseline airflow for a minimum of 10 seconds combined with a 3% decrease in oxyhemoglobin saturation, leading to micro-awakenings. Apnea and hypopnea are classified as obstructive due to the presence of respiratory effort. The apnea-hypopnea index is defined as the number of apnea/hypopnea episodes per hour of sleep (10).
A large number of variables are directly related to sleep disorders, which affect sleep efficiency and lead to a reduction in quality of life. The aim of the present study was to analyze these variables and draw a parallel with patterns of normality in order to determine the most frequent sleep disorders that affect the daily living of patients with sequelae stemming from poliomyelitis.

MATERIALS AND METHODS
Patients:
After screening and the statistical calculation of the sample size, 19 patients (mean age: 52.36 � 6.83 years) with motor sequelae in the lower limbs stemming from poliomyelitis were selected from the Laboratory of Cardiopulmonary Sleep Disorders of the Universidade Nove de Julho (UNINOVE), S�o Paulo, Brazil. All patients had a previous medical diagnosis of paralytic poliomyelitis and had experienced a period of partial or complete functional recovery, followed by an interval of stable neurological function and the subsequent emergence of further neurological complications (new persistent muscle atrophy and weakness) with symptoms lasting more than a year. The individuals selected were informed as to the procedures and objectives of the study as well as the possibility of withdrawal at any stage without penalty and signed a statement of informed consent agreeing to participate. The study received approval from the UNINOVE Human Research Ethics Committee under process number 274010/2009.

Sleep assessment 
All patients were submitted to standard level 1 polysomnography. This level involves the analysis of at least seven physiological parameters, including monitoring electrodes of the EEG, EOG, EMG signals of the submental and tibialis anterior muscles, ECG, nasal cannula pressure, thermistor, snoring sensor, thoracic and abdominal belts, body position sensor and digital pulse oximeter. The Somnologica Studio � Embla A10, version 3.1.2 (Flaga, Hs. Medical Devices, Iceland) was used for the polysomnography in compliance with the manufacturer�s recommendations. Polysomnography was performed following the patient�s habitual sleep schedule. The sites at which the electrodes were attached with conductive paste were cleaned with an exfoliating agent prior to fixation. 
The examination commenced when the polysomnography system was in place, all transducers were calibrated and all channels were operational. A technical specialist in polysomnography was present during the entire examination, which was concluded when the patient awoke in the morning. The polysomnographic tracings were studied manually by a technical expert using the standard manual by Rechtschaffen and Kales (11). Sleep stages were analyzed every 30 seconds (1 epoch), whereas the analysis of respiratory parameters was performed every 120 seconds (4 epochs) due to the slower occurrence of respiratory events. The report of the results was drafted by a specialist in sleep medicine. The following variables were calculated: total recording time (TRT), total sleep time (TST), sleep efficiency (TST/TRT), sleep latency, latency of REM sleep, percentage of time awake and of each stage of non-REM (1-4) and REM sleep, number of micro-awakenings per hour of sleep, apnea/hypopnea index per hour of sleep, time in sleeping position, oxygen desaturation index per hour, blood oxygen saturation (SpO2) and heart rate. 
Sleep was initially broken into stages using EEG channels (C4-A1, O1-A2 and O2-A1), EOG and EMG signals of the submental and tibialis anterior muscles, characterizing waking time, phases 1, 2, 3 and 4 of non-REM sleep and REM sleep. For the detection of respiratory events, airflow amplitude was analyzed through the nasal cannula signal and a thermistor positioned in the mouth to record the airflow of the region through alterations in temperature. The amplitude of thoracic and abdominal movements was analyzed using Xtrace belts, which consist of a flexible sealed tube filled with an electric conductor (usually mercury) submitted to an electric current, which, combined with stretching of the cell, alters its length and conduction area, resulting in a proportional increase in resistance. SpO2 was analyzed using digital pulse oximetry. Continuous monitoring of SpO2 is essential, as it provides important information on the severity of the respiratory disorder (12). 
 A complete lack of airflow for a minimum of 10 seconds was classified as apnea, whereas a 50% reduction in baseline airflow for a minimum of 10 seconds combined with a 3% decrease in oxyhemoglobin saturation leading to micro-awakenings was classified as hypopnea, as described by the AASM TASK FORCE (13). Apnea and hypopnea episodes are also classified as obstructive due to the presence of respiratory effort. The apnea-hypopnea index was defined as the number of apnea/hypopnea episodes per hour of sleep. 
Micro-awakenings were defined as a sudden change on the tracing to faster frequencies with a minimal duration of three seconds and a maximal duration of 15 seconds, based on the analysis of the EEG signals (13). Data from the snoring sensor, body position sensor and EMG signals of the submental and tibialis anterior muscles were collected in order to measure the quantity and intensity of snoring and lower limb movements per hour as well as the patient�s body position (supine, prone, right lateral or left lateral decubitus) during the examination. ECG signals were recorded from a single channel by placing one electrode on the right upper anterior region and one on the left upper anterior region of the thorax. 

RESULTS 
The initial sample consisted of 33 volunteers. However, 14 individuals were excluded � eight for being unable to climb stairs (the laboratory is located on the top floor and there was no elevator) and six for not appearing on the date of the scheduled assessment and data collection. Thus, a total of 19 volunteers took part in the study (Table 1).
----------------- TABLE 1 -----------------------------
Table 2 displays the sleep characteristics (expressed as mean and standard deviation) of the 19 volunteers.
---------------- TABLE 2 --------------------------------

Table 3 displays the polysomnographic variables of the 19 volunteers alongside normal values. 
----------------- TABLE 3 ---------------------------------


DISCUSSION
The prevalence of sleep abnormalities in individuals with sequelae stemming from poliomyelitis is high, with noticeably diminished sleep efficiency and frequent awakenings. This diminished sleep quality can be caused by different extrinsic factors such as working hours and daily stress or intrinsic factors such as spontaneous muscle contractions during sleep, known as periodic limb movement disorder (PLMD), which predominantly occurs in the lower limbs (3,16). In order to describe these sleep abnormalities and their influence on the quality of life of patients with sequelae from poliomyelitis more objectively, the present study prioritized the characterization of variables collected during the polysomnographic examination of 19 volunteers.
The results demonstrated a decrease in sleep duration (316.14 � 61.43), sleep efficiency (74.73 � 18.47) and REM sleep (15.11 � 8.48), which is the period in which neurophysiological recovery is achieved. These findings were related to the increase in awakenings (12.31 � 7.08), which in turn was associated with PLMD (9.21 � 15.26), thereby corroborating findings described by Bruno (17), who found that 52% of volunteers with a history of poliomyelitis reported involuntary limb movements at night that negatively affected sleep efficiency.
PLMD associated with micro-awakenings was found in 12 volunteers (63.15%), which is similar to findings described in studies carried out by Bruno (17, 18) ,who reports that PLMD may be present in 63% of patients with PPS characteristics and can occur after poliomyelitis. In the present study, PLMD was most noticeable during non-REM sleep (58.27 � 38.94), characterized by more superficial sleep in which the individual enters deeper sleep at each stage (I, II, III and IV), becoming progressively less reactive to sensory stimuli. After these stages, the individual enters REM sleep, which is characterized by dreams, high levels of electrical activity in the brain and a lack of muscle activity and is important to musculoskeletal recovery (15, 19, 20). Therefore, patients with PLMD cannot enter deep sleep due to awakenings and micro-awakenings, leading to a low degree of sleep efficiency and a sensation of tiredness upon waking (21).
The participants exhibited a significant increase in apnea and hypopnea episodes (14.41 � 12.86) in comparison to individuals with normal sleep architecture. This result is similar to findings described by Mesquita and Silva et al. (22), who analyzed 60 volunteers and found that cardiopulmonary abnormalities are common and caused by an increase in obstructive apnea (mean of 19.2 � 54.9 p/h) and hypopnea (mean of 13.4 � 26.3 p/h), forming an index of 6.2 � 14.5 p/h. The authors report that these abnormalities lead to oxyhemoglobin desaturation, increased carbon dioxide and consequent fluctuations in heart rate. In an attempt to clarify the association of respiratory abnormalities, one may suggest that these conditions also lead to an increase in the number of awakenings and thus negatively affect sleep efficiency. 
Using a similar approach in the analysis of 98 polysomnographic tracings of volunteers with PPS characteristics, Dahan et al. (23) found that 65% of the participants experienced respiratory disorders associated with sleep. The authors state that age, time of onset of acute poliomyelitis and type of viral involvement exert an influence, with higher values for these demographic characteristics denoting a greater likelihood of respiratory distress.
The polysomnographic findings are in agreement with those reported in other studies conducted with the intention of characterizing the sleep of a population with sequelae of poliomyelitis. The results demonstrate that complaints of sleep disorders are relevant, despite the fact that the mean score on the Epworth Daytime Sleepiness scale (4.64 � 3.73) was non-significant in the present study. This scale consists of eight situations and the volunteer attributes a score regarding four possibilities of dozing (0 = no chance, 1 = slight chance, 2 = moderate chance and 3 = high chance), in which a score equal to or greater than 8 suggests the individual is affected by daytime sleepiness. However, some of the situations addressed on the scale may not be relevant to the daily lives of the volunteers in the present study, which could affect the final result.

ConclusION
The variables analyzed indicate abnormalities that lead to sleep disorders. The consequent reduction in the period of neurophysiological recovery can have a negative effect on activities of daily living. 	 

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