Foster, Elizabeth C. MS, PT, NCS1; Mulroy, Sara J. PT, PhD2
In order to more efficiently predict and advocate length of stay for individuals with Guillian Barre Syndrome (GBS), it is critical for the members of the rehabilitation team to understand the variables associated with the degree and speed of recovery of muscle strength and function. Guillian Barre Syndrome affects approximately 2 in 100,000 persons worldwide.1‐3 Mortality rate within 1 year is roughly 5% to 7% of cases, and most often associated with medical complications in patients with ventilator dependence, autonomic dysfunction, and severe axonal damage of the nerves.1,4 While the exact cause of GBS is unknown, almost half of cases are preceded by a mild respiratory or gastrointestinal infection.3‐5 This preonset event is thought to then trigger an autoimmune response that attacks the insulation of the peripheral nerves. Rees et al4 reported a 26% incidence of preceding Campylobacter jejuni infection in their study of 106 individuals with GBS or Miller Fisher variant of GBS. C. jejuni is associated with presence of the IgG1 subclass anti‐GM1 antibody in subjects with GBS.6 C, jejuni is the leading cause of gastroenteritis in developed countries and is acquired by ingestion of infected poultry products, commonly causing watery diarrhea. The GBS may also be preceded by viral infections such as mononucleosis.5
A few studies have focused on rehabilitation outcomes or length of stay for patients with GBS. Poor functional outcomes are associated with presence of axonal damage,1,4,7 absent tendon reflexes,7 ventilator dependence,8 more severe muscle weakness at nadir,1 increased time to reach nadir,8 absence of an antecedent respiratory infection,1 C. jejuni infection,4,7 presence of IgG1 subclass of the anti‐GM1 anti‐body,6 age over 50 years,1 and autonomic dysfunction.8 Measures of functional outcome in these studies included the Hughes Functional Grading Scale,1,4,7,9 FIM Rasch converted motor scores,8,10 or nonstandardized measures of limb weakness.3 While plasmapheresis and intravenous immuno‐globulins (IVIG) are common and effective medical treatments in GBS in the acute setting,11‐13 IVIG has been associated with better recovery in subjects with anti‐GM114 and anti‐GM1b antibodies.15
Length of stay (LOS) has rarely been reported for patients with GBS. In a retrospective chart review of 24 inpatients with GBS, Zelig et al5 reported 54% of patients stayed less than 3 months at the rehabilitation center. The remaining 46% had LOS of 3 months to 1 year. Meythaler et al8 found that 40% of all patients admitted with acute GBS at their facility were referred to rehabilitation. These 39 subjects stayed in the acute care setting 34 ± 47.1 days on average and in the rehabilitation unit 26 ± 18.6 days, Average total hospital stay for these patients averaged 61 ± 55.9 days.
Associations between LOS and clinical variables were reported by several authors.8,16 Clinical variables such as ventilator support, anemia, proprioception, vibratory, light touch, deep tendon reflexes, cranial nerve involvement, dysautonomia, electrodiagnostic findings, plasmapheresis, age and gender and their relationship to acute LOS, rehabilitation LOS, and total LOS were reported by Meythaler et al.8 They found that autonomic dysfunction was positively correlated with total LOS, cranial nerve involvement was associated with increased acute LOS and total LOS, and ventilator dependence was associated with increased LOS in all three settings. In a prospective descriptive study of 29 patients with GBS who were admitted to inpatient rehabilitation, Prasad et al16 found that longer lengths of stay were correlated with lower admission and discharge total Functional Independence Measure (FIM) scores. The study, however, did not report average length of stay or ranges.
Several studies have established that pain is a common symptom in patients, and report a widely varying incidence from 17% to 85% of subjects with GBS.3,17,18 The origin of this pain is unclear. Ropper et al18 suggested that the muscle pain reported by 51% of their subjects may have been caused by neurogenic changes in the muscle. They ruled out pain related to inflammation of the peripheral nerve or spinal ganglia based on the absence of electrophysiological abnormalities and presence of elevated creatine kinase (CK) levels. In a prospective longitudinal survey of 55 patients with GBS, reported pain that was more variable.19 Myalgic pain characterized by local muscle tenderness similar to that described by Ropper et al18 was present in only 34.5% of subjects. Deep, aching back and leg pain, increasing with straight leg raising (SLR) was reported by 61.8% of subjects. Moulin et al19 suggested the positive SLR was indicative of inflamed nerve roots. No correlation was found between presence of pain (measured with the Visual Analog Scale and the McGill Pain Questionnaire) and subsequent neurologic disability as measured by the Disability Grading Scale for GBS.
Current management of GBS at Rancho Los Amigos National Rehabilitation Center (RLANRC) involves close monitoring of myalgic muscle belly tenderness (MBT) using the Pain Intensity Numerical Rating Scale (PI‐NRS) to protect weak musculature from overuse.19 This practice is based on the theory that over‐exercising painful, weak, and denervated muscles may delay recovery by further damaging the motor unit.
Studies of healthy subjects have shown that eccentrically induced delayed onset muscle soreness (DOMS) is associated with transitory weakness and elevated CK.20‐22 Creatine kinase also has been associated with muscle fiber damage in healthy muscle,23,24 individuals with post‐polio syndrome,25,26 and spinal cord injury.27 While exercise induced muscle fiber damage has been linked to beneficial remodeling of the healthy muscle, it is unclear if long‐term benefits exist for diseased states. Newham et a129 suggested that DOMS and delayed weakness occurs predominantly in eccentric compared to isometric or concentric exercise because of the relatively few muscle fibers that are active for a given resistance. In the diseased state then, when fewer muscle fibers are sufficiently innervated, overuse could result in soreness and decreased strength. In subjects with history of polio, symptoms of elevated CK and muscle pain have been associated with new weakness and fatigue.17,26 Fibrillations indicative of denervation were found more commonly in patients with history of polio who were experiencing delayed weakness compared to those who were not.30 High resistance exercise has shown some negative effects on strength compared to moderate exercise in subjects with slowly progressive neuromuscular disease.31 Following remyelination of the spinal cord in rats, strength improved and then stabilized for up to 9 months.32 Subsequently a gradual decline in motor function and motor neurons occurred. Strength declined earlier and to a greater degree in rats that were exercised on a treadmill compared to those who were not. Finally, long‐term follow‐up of individuals with GBS have shown residual weakness and fatigue to persist for years following apparent recovery.33,34
No prior studies on GBS have documented pain using the PI‐NRS commonly used in hospital settings. Nor have any prior studies reported using pain level to monitor therapeutic exercise progression in patients with GBS. Therefore in addition to confirming prior studies of predictive factors in GBS, this study sought to describe type and incidence of equipment issued; physical therapy treatment time; and the role of muscle soreness in strength, functional mobility, discharge setting, and lengths of inpatient rehabilitation stay. These areas are of particular interest to physical therapists as they seek to ensure cost‐effectiveness, maximize funcitonal outcomes, and prevent injury in treatment of clients with GBS.
Individuals were included in our study if they had a clearly documented diagnosis of GBS and were admitted to RLANRC for inpatient rehabilitation between March 1996 and August 1998. Of the 37 individuals who initially met our inclusion criteria, 2 patients were excluded because their charts were not available. In addition, 2 patients were excluded because their definitive discharge diagnoses were not GBS: one patient had chronic inflammatory demyelinating polyneuropathy and the other had chronic alcoholic neuropathy. The remaining 33 subjects were included in our study. This research project was approved by the Institutional Review Board at RLANRC.
The medical charts of all 33 patients were reviewed retrospectively to obtain demographic, disease course, and outcome variables (Table 1). Variables were chosen based on predictive variables found in the literature, cost‐management related to equipment issued, physical therapy treatment time, LOS, and interest in the role of current practice of monitoring MBT on LOS, strength, and function. Outcome measures of manual muscle testing (MMT) and Functional Independence Measure (FIM) were selected for measuring strength and functional impairment because these are the tests most consistently used in the physical therapy documentation at our facility.
Previous studies have shown manual muscle testing to be a reliable and valid measure of muscle strength.35‐37 In our study, composite scores for lower extremity manual muscle tests (LE MMT) were obtained by summing MMT scores for bilateral hip flexors, hip extensors, knee extensors, ankle dorsiflexors, and plantarflexors at admission and again at discharge (maximum possible score = 50). Hip abduction and knee flexion strength values were not included due to the scarcity of documentation in the medical records. Upper extremity MMT scores and self‐care FIM subscores were not included in the scope of this study as a concurrent study looking at these variables was being conducted through the Occupational Therapy Department.
In the present study, FIM mobility subscores (6 items: bed/chair transfers, toilet transfers, tub/shower transfers, walking ability, wheelchair ability, and stairs) were recorded upon admission and discharge. Prasad et al17 found that the mobility domain of the Functional Independence Measure (FIM) Motor subscore was sufficiently sensitive in detecting disability and change over the rehabilitation period. It should be noted that the walking/wheelchair item, typically a single item in the FIM, was separated into 2 categories, each given a maximum score of 7. If a patient was not using a wheelchair upon discharge, he was automatically given a wheelchair score of 7 to indicate independence from a wheelchair. Therefore, the maximum possible FIM subscore = 42, minimum = 6.
Pain data were extracted using the PI‐NRS scores and muscle belly tenderness (MBT). The reliability and validity of an 11 point numerical rating scale as a measure of clinical pain intensity has been established.38‐40 Regarding clinical sensitivity of the PI‐NRS, Farrar et al41 concluded that a reduction of 2 points represented a clinically important difference in a review of 2724 subjects in placebo controlled clinical trials of patients with diabetic neuropathy, post herpetic neuralgia, chronic low back pain, fibromyalgia, and osteoarthritis. In the physical therapy notes of the medical records in this study, pain described as muscle belly tenderness (MBT) was monitored and documented.
The Muscle Belly Tenderness (MBT) test was developed at RLANRC. It is performed by applying gentle pressure with the palmar surface of the hand and fingers to the relaxed muscle bellies of all major muscle groups and asking the patient to subjectively report his/her pain using the PI‐NRS (Figure 1). The reliability and validity of MBT testing has not been established. For analysis purposes, presence of muscle belly tenderness in this study was defined as bilateral tenderness to manual pressure in 2 or more lower extremity muscles for over one week.
Independent t‐tests using Mann‐Whitney Rank Sums were used to determine differences in outcomes for categorical variables (Table 2). Spearman correlations determined associations between LOS and noncategorical variables (Table 3).
Alpha levels of 0.05 were used to test for significance for Spearman correlations. Bonferroni corrected alpha levels of 0.01 were used to test for significance for Mann‐Whitney Rank Sums. This correction is used in pairwise groupings when more than 1 outcome variable is tested in order to reduce Type I error. Corrected alpha levels were obtained by dividing alpha by the number of outcome measures used.
Average age of subjects was 34.1 years (range = 8.1‐79.3 years). The ratio of men to women in our study (21:12) closely resembled the 2:1 ratio reported by Meytheler8 in 1997. Fifty‐five percent of our subjects had comorbidities (Table 4). Sixteen subjects exhibited signs of depression or depressed mood during their rehabilitation, as documented in psychology and social work evaluations. The onset of depression, whether before or after illness was not captured during data collection. Average time from onset of symptoms to admission to rehabilitation was 23 ± 15 days. Average LOS for all subjects was 63 ± 47 days (range = 7‐203 days).
Disease Course Data
Eleven subjects had a gastrointestinal infection, 4 had respiratory infection, and 7 had other or no infections prior to the onset of GBS. Twelve subjects had axonal damage documented by either EMG or NCV testing. Four patients were initially ventilator dependent and later weaned. Twenty‐one received plasmapheresis while only 7 underwent IVIG treatments during their acute hospitalization. Eleven subjects had MBT that fit our criteria (Table 5).
Longer lengths of stay were associated with muscle belly tenderness, lower FIM subscores and LE MMT scores on admission, lower FIM subscores upon discharge, and total PT hours received. Subjects with axonal damage, ventilator dependence, and need for ankle foot orthoses at discharge tended to have longer LOS (See Tables 2 and 3).
Axonal damage and requiring wheelchair at discharge were significantly associated with decreased LE strength and functional independence at discharge. There was a non‐significant tendency for MBT to be associated with greater overall change in both LE strength and FIM subscores. This reflects a lower FIM subscore upon admission when MBT tends to be greatest, and an achievement of similar FIM subscores by discharge.
There was no significant association between the overall change in FIM or MMT scores and LOS. A longer rehabilitation stay allowed weaker and more functionally dependent patients to make similar gains in function by discharge.
Trends observed included subjects with depression having lower FIM subscores at discharge and lower overall gain in FIM subscores. Finally, those subjects requiring AFOs at discharge tended to have decreased LE muscle strength.
Mean individual FIM item scores for transfer and locomotion are reported in Table 5. On average, subjects were admitted to rehabilitation requiring maximum assistance for bed and toilet transfers and required total assistance for bath transfers, walking, stairs, and maneuvering a wheelchair. Upon discharge, subjects improved on average to requiring approximately minimal to no assistance for transfers, minimum assistance for walking and stairs, and were modified independent using a wheelchair. All subjects were discharged to home.
The average length of stay for subjects who were admitted with a diagnosis of Guillain Barre Syndrome and underwent rehabilitation was 63 days, By discharge, subjects required minimal to no assistance for mobility and locomotion, compared with maximum assistance upon admission. Lengths of stay roughly doubled when subjects had axonal damage, ventilator dependence, or MBT. The length of time MBT persisted varied greatly, but resolved by discharge in all but 2 of the 11 subjects who reported MBT. In the 2 subjects where MBT persisted, it was very mild at discharge, approximately 1 on a 0 to 10 pain scale. Of the 11 subjects with MBT, 5 also had axonal damage, 8 required AFOs at discharge, 4 required power wheelchairs, and 1 required a manual wheelchair. Three of these subjects required maximum to total assistance for ambulation at discharge, while the other 8 required no assistance.
We found that longer LOS was correlated with lower admission and discharge mobility FIM subscores, which is similar to Prasad's findings.16 In comparison to Prasad's study,16 our subjects had lower mobility/locomotor FIM subscores on admission (averaging 1.88 per mobility item in our study versus Prasad's 3.38) but only slightly lower scores on discharge (averaging 5.10 in our study versus Prasad's 5.76 per item), indicating our patients had more disability upon admission but this discrepancy waned by discharge. Decreased strength upon admission and need for AFOs were also significantly associated with increased rehabilitation stay. Therefore, these factors are important to consider when estimating LOS.
In contrast to Meythcyler,8 we found ventilator dependence was not associated with LE MMT or mobility FIMs at discharge. Unlike our pool of patients, all subjects in Meytheyler's study were weaned from the ventilator prior to rehabilitation. This may be one reason our rehabilitation length of stay was longer than that reported in other studies.8,16
Over half of the individuals with GBS in our study experienced muscle belly tenderness. We have described a means of evaluating such symptoms and have shown how presence of MBT is associated with increased LOS but not functional mobility or strength at discharge. The increased LOS for patients with MBT at our facility may partially be explained by our approach to rehabilitation progression. At RLANRC, daily assessment of MBT and muscle strength guides the rehabilitation progression in order to prevent muscle damage from overwork or overstretch.20 This approach is based on the theory that denervated or reinnervating muscle units can be overworked to the point where weakness is irreversible, At our facility, if a patient with GBS reported an increase in MBT or demonstrated decreased strength in the gastroc‐soleus muscle on a given day, activity in that muscle would be reduced. Once the strength/MBT returned to the previous level, the program would again be progressed with close monitoring. Therefore, the LOS would likely be longer for a patient who experienced increased MBT or weakness following minimal exercise compared to a patient who did not experience these symptoms. In addition, presence of MBT may have artificially lowered the strength and FIM scores upon admission, when MBT tends to be highest and resistive muscle testing would be contraindicated.
Our reported LOS, as well as that reported by Zelig et al5 and Meythaler et al8 far exceed the expected 6 to 24 physical therapy visits suggested in the Guide to Physical Therapist Practice for individuals with acute or chronic polyneuropathies.21 However, this practice pattern suggests factors that may alter the duration of care. These include several that are applicable to the GBS population: severity of current condition, level of impairment and physical function, potential discharge destinations, comorbidities/secondary impairments, and probability of prolonged impairment, function limitation, and disability. Pain was a frequent secondary impairment in our subjects, and associated with increased LOS. Also, all subjects were discharged to home. For the patients with more severe disability, an alternative discharge placement with more skilled care was likely unaffordable for our patient population, most of whom do not have health insurance. As a result, longer LOS in our subjects may have been required for caregiver instruction, and progressing function to a level that could be managed at home.
As is common with retrospective chart reviews, this study was limited by the amount of documentation available in the medical chart. Some patients had very thorough documentation in our areas of interest, while others were sparse. As a result, the total values in Table 2 vary. We initially hoped to obtain weekly FIM and MMT from the chart review in order to obtain a picture of when patients displayed the most rapid recovery. We felt that this would identify the best window of opportunity for active rehabilitation (at least 3 hours per day of 2 or more therapies), and times when a lower level of rehabilitation would be recommended, especially when some patients were limited by MBT. Unfortunately, weekly data were inconsistently recorded in the chart and therefore not included. In retrospect regarding the statistical analysis, the use of a regression model would have been a better choice for offering the most robust conclusions possible. While our use of Mann‐Whitney Rank Sums is appropriate for comparing pairwise groupings of categorical variables to linear outcomes, the large number of outcome measures we chose required us to perform a Bonferroni correction on the alpha level of significance to reduce Type I error and therefore making our tests very conservative.
This study described muscle belly tenderness in patients with GBS and the role of monitoring this pain in determining functional progression during the rehabilitation stay. Future studies that specifically look at measuring the validity or reliability of MBT testing in the Guillain Barre population are needed. It would be interesting to compare length of stay and outcome of patients with MBT where the program does not use MBT and strength monitoring to modify the therapy plan. Our study placed all patients who met our criteria for presence of MBT into one group, regardless of severity. Future studies that differentiate levels of pain severity may show that those with minimal pain are similar to those without MBT.
Another need is to look at the long‐term outcome of individuals with GBS. What are the predictors of whether they achieve community level ambulation, and return to prior roles and function? What is the role of the PT in this transition?
In light of changes in health care over recent years resulting in shortened lengths of stay, it is helpful to identify factors related to recovery and prognosis in order to determine and justify lengths of stay for our patients with Guillain Barre Syndrome. Our study supports prior works that found axonal degeneration to be predictive of worse functional outcome. In addition, we found that presence of muscle belly tenderness, lower FIM subscores at admission and discharge, and LE strength on admission were significantly associated with longer LOS. Overall change in LE strength and FIM mobility subscores were not correlated with LOS, suggesting that subjects with severe weakness and functional impairment required more time to improve but were able to make similar gains in both areas by discharge compared to stronger counterparts. In terms of strength and function, patients with MBT tended to ‘catch up’ to MBT free counterparts by discharge.
There was a tendency for those with axonal damage, ventilator dependence, and prescription of AFOs to also have longer LOS. Forty‐seven percent of subjects required manual wheelchairs at discharge, while 22% required power wheelchairs. As would be expected, wheelchair use was significantly associated with decreased strength and functional independence at discharge. This study provides new information regarding clinical factors, pain, equipment usage, functional mobility, and length of stay that can assist the clinician in prognostication and discharge planning for patients with GBS.
A special thank you to those PT students who assisted with this research project as part of their internship at RLANRC. Thank you Jocelyn Blaskey, Jan Furumasu, Walt Weiss, and the Neurology Department at RLANRC for your valuable feedback and expertise in the field of Neurologic Physical Therapy.
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