Ipsilateral Deficits in Stroke

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Ipsilateral Involvement in Cerebral Hemisphere Strokes:

A Literature Review

Roy Barsola

University of Medicine and Dentistry of New Jersey

School of Health Related Professions

In partial fulfillment of the requirements for IDST 6400

Critical Literature Review and Scientific Writing

Craig Scanlan, EdD, RRT, FAARC

December 17, 2001

Ipsilateral Involvement in Cerebral Hemisphere Strokes: A Literature Review

Ipsilateral arm is generally considered unaffected or normal after a unilateral cerebral stroke resulting in contralateral side deficits. Therefore, rehabilitation is focused towards the recovery of function of the contralateral side of the stroke.

A long term outcome goal following hemiplegia is the attainment of independent living to the greatest extent possible. Independence in daily living is influenced by many factors, including motor function, perception, communication, memory, information processing, and cognition. When differences in functional outcomes are observed between right and left hemiplegia, the disparity can often be attributed to factors other than motor function. Left hemisphere specialization for language and right hemispheric specialization for visual, spatial, or perceptual processing often account for discrepancy in the outcomes among hemiplegic patients with unilateral lesions of either right or left hemisphere. As a result of these hemispheric asymmetries, the prediction of functional outcome is often difficult.

Major reasons for not detecting ipsilateral deficits in clinical practice are their relative subtlety, poor knowledge of the presence of deficits, failure to use sensitive tests, use of ipsilateral side as the reference for impairment in the hemiplegic/paretic side and the emphasis placed on contralateral in rehabilitation.

The purpose of this review is to examine the presence of ipsilateral deficits in cerebral hemisphere stroke and to explore the extent of involvement.

Context and Background of the Problem

Studies have reported conflicting and varying results as to the extent and the effects of unilateral hemisphere stroke to ipsilateral extremities. Several studies suggested bilateral control of each cerebral hemisphere, which causes ipsilateral deficits when one is affected. Some suggested the presence of deficits to right stroke subjects but not to left stroke subjects and vice versa. Some have looked at the complexity, and time constraint involved in the task performed by the ipsilateral limb.

Clinical practitioner must be knowledgeable in the different manifestation of cerebrovascular accidents (CVA), with consideration to the relative subtlety of the impairment in the ipsilateral side. The impairment must be effectively addressed in the evaluation and care planning since it had been shown to persists.

Smutok et al. (1989) has shown that damage to either hemisphere leads to long standing motor deficits in the ipsilateral upper extremity of Vietnam War Veterans. Although they considered it as mild, they do not completely recover even with the use of the ipsilateral arm. The results revealed decrease in simple visual reaction time, rapid alternating movement, and dexterity. Ipsilateral grip strength and visual-perceptual processing deficits are present in right hemispheric brain damage, while left hemispheric brain damage has shown decrease in pinch strength. Their study suggested that deficits in the ipsilateral UE after unilateral hemispheric lesion persist even after fourteen years later. The study was not included in this review because the subject’s brain lesions were from penetrating brain wounds and not from stroke.

Methods

An Ovid search was done using MEDLINE and CINAHL. MEDLINE produced 5,311 results and CINAHL produced 5,249 results using "cerebrovascular accidents" as the key word. Search was further limited to English language and to humans, with "stroke" and "ipsilateral" as Mesh words, which resulted to 34 possible studies.

Further results were expanded by manually searching for articles that were mentioned and cross-referenced by studies in the MEDLINE and CINAHL search results.

An Internet search was done using major web search engines. Google, Alltheweb, Northernlight, Altavista, and Go.com were used, with "cva", "stroke", and "ipsilateral" as key words. The search produced between 2,200 to 2,800 results. Search was further narrowed down by using the advance search option and using Boolean operators, "and" and "or". Names of the authors from studies that were included in the Medline search was also used to look for related articles. The Internet search added twelve possible studies.

Studies included were subjects with cerebral hemisphere stroke from anterior circulation system involvement and more particularly in the middle cerebral artery. Testings were done on the ipsilateral or the unaffected side of stroke. The subjects were ambulatory and independent in self-care, home care, and community living skills. Most of the studies included used either age-matched, gender-matched, and/or hand dominance-matched controls, except for the studies by Desroisers, Bourbonnais, Bravo, Roy, and Guay (1996) and Spaulding, McPherson, Strachota, Kuphal, and Ramponi (1988). All studies are of quasi-experimental designs.

Studies that examined the roles of the cerebral hemisphere in motor control, which used the ipsilateral side after stroke, were also included. (Robinson, Fitts and Kraft, 1990; Spaulding et al., 1988; Winstein and Pohl, 1995) A total of ten studies were included in the review.

Literature Review

A study by Desroisers et al. (1996) showed significant deficits in the unaffected upper extremity of hemiplegic subjects compared with normal subjects on the following parameters: gross manual dexterity, fine manual dexterity, motor coordination, global performance, and kinesthesia (p<.01 to p<.0001). No significant clinical or statistical difference was found for grip strength (p<.81), static and moving two-point discrimination (p=.21 and p=.12) or touch/pressure threshold (p<.91). Subjects were compared to a normative a data of 360 subjects that was collected from a previous study, which used the same sensorimotor tests given in the same order as those used in the study. Gross manual dexterity was measured by use of the Box and Block Test in a 60-second time period. Fine manual dexterity was measured by the use of Purdue Pegboard in a 30-second time period. The four unilateral task of Tempa (pick up and move a coffee jar, pick up a pitcher and pour water into a glass, handle coins, and pick up and move small subjects) were used to evaluate upper extremity global performance. Motor coordination was assessed by Finger-Nose test. Jamar dynamometer was used to measure grip strength.

The role of sensorimotor areas in the specification of kinematic parameters for aiming movements was studied by Velicki, Winstein , and Pohl (2000). Six stroke subjects with unilateral sensorimotor involvement were tested and compared to 6 matched controls. Lesion locations were obtained from a computed tomography (CT) or magnetic resonance imaging. The perimeter of each lesion site was outlined using a hand digitizer, and the area was measured to obtain an index of lesion volume. Rapid arm movements were made to one of four targets by rotating the forearm in a short (20° ) or long (45° ) arc of motion using a lever. Four targets were represented: two directions (flexion and extension), and distance (short and long). The onset of lever movement was timed with the last in the series of four audible tones presented by the computer. A timed-response paradigm was used to differentiate response initiation and specification. Targets were presented in a fixed sequence or random sequence. Three dependent variables were measured: constant error, absolute error, and direction error. Absolute error to the long targets was greater for the stroke group than the control group (p.05), whereas absolute error to the short targets was similar between the groups (p=.05).

The results showed no significant differences in performance between stroke and control groups in the predictable condition. In the unpredictable condition, subjects with stroke produced more production errors and were less accurate in extent than the control subjects (p=.05). The results show that ipsilateral sensorimotor areas contribute to the planning of an optimal motor program, especially when an imperative programming of unimanual goal directed aiming movements is required.

Sunderland, Bowers, Sluman, Wilcock, and Ardron (1999) investigated whether impairment of ipsilateral dexterity is common early after middle cerebral artery stroke and explored the relationship to cognitive deficit. A slightly modified Jebsen Hand Function Test was performed on four subtests (card turning, picking up small common objects, simulated feeding, and stacking checkers). Williams door was used to assess dexterity in opening and closing small doors. All dexterity tests were performed for 3 trials and speed and accuracy was evaluated. Task performance was recorded by a video camera for assessment of quality and speed. Apraxia assessment was done by asking subjects to produce each of 9 actions and scored by the examiner on 3-point scales. Test for visual neglect was done using Line cancellation. Benton Line Test was used to test visuospatial perception in which the subject has to identify short oblique lines that are matching angles to the horizontal. Finally, a Jamar dynamometer was used to measure grip strength over 3 trials. All patients were able to complete all dexterity tests, but video analysis showed that performance was slow and clumsy in the stroke group compared with that of controls (p<0.001). Impairment was most severe after left hemisphere damage, and apraxia was a strong correlate of increased dexterity errors (p<0.01), whereas reduced ipsilateral grip strength correlated with slowing (p<0.05). Patients with right hemisphere damage showed no correlation between grip strength and slowing, while dexterity errors appeared to be due to visuospatial problems. The degree of paresis of the contralateral arm as measured by the Extended Motricity index was not a correlate of ipslateral dexterity speed or accuracy for the LCVA or RCVA group (r<.3, not significant, for all). A comparison of the seven patients who have posterior frontal and no parietal damage with the remainder showed no significant differences for dexterity speed or errors (Mann Whitney U tests, p>.01).

Baskett, Marshall, Broad, Owen, and Green (1996) evaluated the ipsilateral side of twenty stroke patients with the use of a repetitive side to side movement by tapping two touch-sensitive target plates 25cm apart for 30s. The test was both done to the upper and lower limbs ipsilateral to the cerebral infarct, and measured at 10s and 30s. Motor disability was also assessed using the Motor Assessment Scale, which includes eight items representing seven areas of motor function and one item relating to general tone. Each test is scored on a seven-point scale (from 0 to 6). A score of six represents optimal motor behavior in each test, to a total maximum combined score of 48. The results were compared to 20 stroke subjects, who were studied from another study 2-192 poststroke. Both stroke groups were compared with forty-one healthy subjects of similar age as that of the subjects. The result of the study showed significantly worse performance (p<0.005), using student t-test, on the right ipsilateral side, but not the left ipsilateral side. The finding was consistent with the result of a different group of stroke from previous study that was used for comparison. A multivariate analysis showed no relationship between the severity of the motor deficits and the performance of the ipsilateral extremities. The authors were very quick to conclude that ipsilateral sensorimotor deficit occurs after stroke but only on the right side, even with just one simple motor task tested.

Pohl, Luchies, Stoker-Yates, and Duncan (2000) investigated whether motor deficits are present in the ipsilateral upper extremity when contralateral extremity impairment is mild, since studies have suggested an ipsilateral involvement after a cerebral hemisphere stroke. Mild residual impairment was defined as Fugl-Myer score of 49/66 or greater. Thirty right-handed adults (10 controls, 10 right stroke, 10 left stroke) performed rapid continuous aiming movements to small and large objects. Temporal measures of movement were defined, including movement time, and its three components: acceleration, deceleration, and dwell time. Participants with right stroke had prolonged movement time only with the left upper extremity, primarily due to longer dwell times. Participants with left stroke had prolonged movement time with both upper extremities as a result of longer dwell times. The results indicate the control deficits of the ipsilateral arm are evident in individuals with left but not right brain damage who have minimal impairment of the contralateral arm. These findings are consistent with the role of the left hemisphere in the control of both upper extremities.

Another study tested manual tracking control of the ipsilateral side poststroke to examine the depth of information processing,accomplished through different levels of stimulus-response compatibility. Carey, Baxter, and DiFabio (1998). Subjects were asked to track four cycles of fixed sine wave, which were displayed in a computer. Two tracking tests were done, under stimulus-response compatible and incompatible conditions, followed by a handgrip test. The order of the two tests was randomized. For each scored tracking trial, the computer calculated an accuracy index. The score was based on the root mean square error between the target line and the response line. Previous works have shown that the accuracy index has good reliability with intraclass correlation coefficient ranging from .88 to .95 for stroke subjects and .90 for healthy subjects. In stimulus response-compatible condition, the accuracy index of subjects with stroke was not significantly different from controls (F (1, 89) =1.73, p=.19). In stimulus-response compatible condition, accuracy index of control subjects was significantly better than subjects with stroke (F (1, 89) =14.3, p=.0003). The ANOVA on handgrip strength revealed a significant difference between the control subjects and stroke subjects (F (1, 89) =4.97, p=.03). Stroke subjects have a lower mean grip strength score. The results showed that manual tracking is impaired in the ipsilateral hand of stroke subjects, suggesting that information processing, separate from motor weakness, may be a problem impairing controlled movements in individuals with stroke.

A study by Yelnik et al. (1996) analyzed the changes in the execution of a complex manual task of ipsilateral extremity after an ischemic cerebral hemisphere stroke. The stroke subjects were further grouped according to their brain lesions as determined by CT. Patients with lesions in the lenticulostriate arteries territory formed one group called "deep lesions". The other group called "superficial" (with or without deep lesions), had lesions in the hemispheric branches of the middle cerebral artery. The Nine Hole Peg Test (NHPT) and the "Pig Tail" Test (PTT) were utilized. For the NHPT, patients were required to place nine wooden dowels in nine holes within 50 seconds for one trial. The subjects were asked to run a 3cm diameter copper ring, attached to a wood handle, along the wire 5mm in diameter with two curves. Bonferroni adjustment was done to control the overall error rate fixed at .05, when multiple tests were done. Both right CVA and left CVA performed worse than controls in the NHPT (p<.05) and in the PTT (<.05). Right CVA performed faster but clumsy compared to left CVA. Deep lesion group and the Superficial lesion group were not significantly different in both tests, except for the PTT for LCVA. Performance was significantly lower for Deep than for the Superficial (Mann-Whitney U test, p<.05).The study confirmed that there are ipsilateral motor disturbances in a complex manual task after hemispheric stroke, even without speed constraint, and regardless of the hemisphere damaged.

Jones, Donaldson, and Parkin (1989) tested the subjects initially at 11 days and at 12 months poststroke and compared. Results showed decrease in performance of the ipsilateral arm in all quantitative tests compared with matched controls at 11 days. At 12 months it has shown significant improvement in performance, but it still remained impaired. The improvement was attributed to normal learning and neurological recovery. Arm strength, speed and random tracking were marginally impaired (P<0.1). Three tracking task (random, step, and combination), arm strength, reaction time, speed, steadiness, steady movement were performed. The results indicated that all cerebral hemisphere areas involved in sensorimotor functions can exert some degree of bilateral motor control and the proportion of ipsilateral to contralateral control is closely related to the degree of continuous sensory feedback required by the particular task.

Winstein and Pohl (1995) examined the role of each cerebral hemisphere by evaluating the effects of unilateral cerebral hemisphere damage on the control of rapid, reciprocal aiming movements under different conditions of task complexity. The performance of the limb ipsilateral to the lesion was evaluated to control for the effector problems caused by sensory loss and hemiparesis of the contralateral limb, which was compared to controls using the same limb. It was included in the review because the study examined the unaffected side after CVA. The study found that movement time in stroke subjects to be longer compared to their controls in medium and high Index of Difficulty.

Finger tapping and grip strength represents two distinct aspects of motor control, rapid repetitive movement versus sustained contraction. Robinson, et al. (1990) evaluated the laterality of performance in finger tapping rate and grip strength by hemisphere of stroke and gender. Both were tested on the contralateral and ipsilateral side of stroke, using JAMAR hand-held dynamometer for grip strength squeezed for 6 seconds, and a finger tapping device with a mechanic lever with most. Performance was compared to 19 right-handed age and gender-matched controls. All subjects had CT or clinical evidence of vascular lesions in the territory of middle cerebral artery. The results showed that right hand grip of rightCVA survivors was inferior to right group of controls (p<.05), Left finger tapping in left CVA subjects was inferior to left finger tapping in controls (p<.01). Two-tailed t-test showed that contralateral-to-lesion arms performed significantly worse on both tests than the control arms (p<.01). Further, male right CVA subjects were superior to right finger tapping than controls (p<.05), and left hand grip in left CVA men was superior to controls (p<.01). The results supported their hypothesis that the right cerebral hemisphere specializes in sustained contractions and the left cerebral hemisphere specializes in rapid movements. Therefore, ipsilateral involvement in CVA may be attributed to hemispheric specialization in motor tasks.

Factors that may have affected the results were considered. Student t-tests comparing the two control groups revealed a small but statistically significant difference in finger tapping, which favored the results obtained. The lesion depth was confounded with hemisphere of stroke. Computed tomography showed that six of the eight left CVA individuals had subcortical lesions (plus one cortical and one unknown), while four of twelve right CVA subjects had cortical lesions (plus two subcortical and six unknown). Grip strength was always measured before finger tapping, which may have favored the findings for individuals with left CVA due to the onset of fatigue.

The study by Spaulding et al.(1988) used the Jebsen Hand Function Test, to evaluate the performance of the involved and uninvolved hand of CVA subjects with consideration to hand dominance, hemisphere of stroke, age, and gender. Multiple t-test was used to compare subject’s performance with normative data that was collected by Jebsen et al. (1969), on performance of the same test of 360 normal individuals. The test is a measure of speed, consisting of seven sub-tests (writing, card turning, small objects, simulated feeding, checkers, light objects, and heavy objects). The authors tried to control for type II errors by dividing the 0.05 level to seven subtests, which is .007 and rounded to .01. Twenty-six of the 28 t-tests comparing the uninvolved hand of the subjects to the norms for adults 60 years and older were significantly slower in the performance of the test, at p£ 0.001 for a two-tailed test. In comparison to the uninvolved hands of right handed RCVA and LCVA, only writing was found to be of significant difference at p£ 0.01 of two-tailed test.

Table 1

Subject Comparison

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Authors/Study Country Hemisphere of Lesion Mean Age Onset of CVA

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Velicki, Winstein, USA 3 RCVA, 3 RCVA 62.7± 8.9 4.2± 2.9 years

& Pohl

Desroisers et al. Canada 29 RCVA, 14 LCVA 72 6 mos-4 years

Sunderland et al. UK 15 RCVA, 15 LCVA 67 <1 month

Baskett et al. New Zealand 9 RCVA, 11 LCVA 70 4-6 weeks

Pohl et al. USA 10 RCVA, 10 LCVA R-71.7, L-67.2 5 mos-1 year

Carey, Baxter, & USA 20 RCVA, 20 LCVA R-68.6, L-65.2 L=5.3± 1.6,*

Difabio R = 8± 1.6**

Yelnik et al. France 18 RCVA, 18 LCVA 54± 13 2 mos

Jones et al. New Zealand 5 RCVA, 3 LCVA 63.9± 7.9 11days to 1yr†

Winstein & Pohl USA 10 RCVA, 10 LCVA R-60.3± 8.2, RCVA=4.2yrs

L-62.1± 8.9 LCVA=4.2yrs

Robinson et al. USA 12 RCVA, 8 LCVA 64 29 mos

Spaulding et al. USA 27 RCVA, 22LCVA 66± 15 acute adm. ‡

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RCVA-right cerebrovascular accidents

LCVA-left cerebrovascular accidents

* right-handed

** left -handed

† testing was done at 11 days and 1 year poststroke

‡ the study did not mention the onset of stroke, but testing was done few days upon admission to hospital

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Table 1 compares the subjects that were included in the review. It shows varying differences in the onset of stroke but a fairly homogenous age. The onset of CVA is the length time since the stroke when the tests were done.

Discussion

Results of the studies in this review have confirmed the presence of ipsilateral deficits after unilateral cerebral hemisphere stroke in varying degrees of involvement.

Sunderland et al and Baskett et al. have shown the presence of ipsilateral deficits even at less than one month poststroke.

Carey et al. (1998) have shown that information processing is impaired globally and may contribute to the deficit of movement in the paretic side in performing perceptual motor tasks, as demonstrated by abnormal tracking behavior under stimulus-response compatible conditions on the non-paretic side in subjects with stroke.

Some researchers found differences in upper extremity performance between left and right CVA patients compared with healthy subjects. (Winstein, & Pohl, 1995; Spaulding et al., 1988; and Robinson et al., 1990)

Baskett et al. found ipsilateral deficits on the right CVA subjects but not the left CVA subjects in alternate continuous tapping test for both upper extremity and lower extremity. Further, they suggested the role of the left and right hemisphere in the control of open-loop and closed-loop movement. Open-loop movements are thought to be sensory independent, rapid and programmed, and under the control of left hemisphere. Closed- loop movement are thought to be slower, modified by sensory input, and under the control of right cerebral hemisphere.

Differences between studies may be explained in part by the side of the lesion, the length of time since the stroke, the types of task performed, and the level of independence of the subjects. Studies have varied greatly in sampling procedures and have seldom focused on well-defined groups of stroke patients at a fixed time after stroke. There has been inconsistency in dealing with the dependence of manual dexterity on cognitive functioning. Some studies have excluded patients who showed clinically obvious apraxia or visuospatial problems, while others have regarded these cognitive deficits as major causes of ipsilateral impairment. Sunderland et al., (1999) have shown that mild deficits in cognition are sufficient to impair dexterity.

An exclusion of criteria in the study by Desroisers et al., (1996) may have significantly eliminated other right CVA subjects. The exclusion criterion was: no important visual perceptual deficits. There was no mention of exact number of possible subjects out of the 13 excluded, who did not met the criterion, which is mainly related to visual perception.

Laterality of cerebral processes implies that each hemisphere exerts a degree of bilateral control over its specialized functions. Therefore, damage to one hemisphere may produce bilateral deficits in performance of lateralized functions. Robinson et al. (1990)

Bilateral cortical activation has been reported in healthy controls during the performance of right upper extremity movements. (Colebatch, et al., 1991; and Dieber et al., 1991) It is particularly associated with performance of difficult task as examined by Winstein, Grafton, and Pohl (1997).

Chen, Gerloff, Hallert, & Cohen (1997a) study on 15 healthy adults using repetitive transcranial magnetic stimulation has shown ipsilateral involvement of motor cortex, in fine finger movements, and that the left hemisphere plays a greater role in timing ipsilateral complex sequences than the right hemisphere and may be more involved in the processing of complex motor programs. This has been confirmed in stroke patients by Baskett et al. (1996).

Some suggest that the ipsilateral involvement is a by-product of plasticity in the unaffected hemisphere. A negative effect in the plasticity of motor output organization could be a decreased or disordered organization of the contralateral and the ipsilateral sensorimotor areas involved in the motor planning and higher organization.

A review of a neuro-anatomy text has pointed a concern in the role of the ipsilateral projection of the corticospinal tract. The anterior corticospinal tract is a smaller group of uncrossed fibers originating from the giant pyramidal Betz cells of layer V in the primary motor cortex of the precentral gyrus (Area 4), which continues to the cervical spinal cord and ending by synapsing with motor neurons in the anterior horn of the spinal cord. The functional role of anterior corticospinal tract is uncertain, although its endings in lamina VIII suggest that it may be involved in the cortical control of axial muscles Netter, (1986). Although, studies using Transcranial magnetic stimulation found no evidence in that the ipsilateral fast corticospinal tract was responsible for recovery of affected limb functions (Netz et al., 1997; Palmer et al., 1992; and Turon et al., 1996), indicating a negative role in the control of sensorimotor function of ipsilateral side.

It is also possible that a vascular lesion in one hemisphere interrupts corticobulbar and corticoreticular projections and consequently affects subcortical structures involved in motor control. Kuypers, (1981)

Conclusion

The review confirmed the presence of impairment to the "unaffected side" in stroke. The studies have shown conflicting results which may be attributed a lot of factors, such as the different set up of instruments, different testing and procedures, the role of each cerebral hemispheres, size of lesion, presence of perceptual deficits, and the onset of stroke.

The puzzling intricacy and the obscure functions of some parts of the mid-brain level structures may hold the answer to the question.

As a clinical practitioner, being knowledgeable of the presence of these deficits in stroke patients and be able to address it, will make us more effective and successful in attaining the functional goals.

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