Dysphagia 7:142-147 (1992)
Dysphagia ,c~Springer-VcrlagNew York Inc. 1992
Periventricular White Matter Changes and Oropharyngeal Swallowing in Normal Individuals* Ross Levine, M.D., 1 Jo A n n e Robbins, Ph.D., 1 and A n d r e a Maser, M.S. 2 Departments of ~Neurology and 2Radiology, William S. Middleton Memorial Veterans Administration Hospital and University of Wisconsin Clinical Sciences Center, Madison, Wisconsin, USA
Cranial m a g n e t i c r e s o n a n c e imaging (MRI) has revealed patchy periventricular white m a t t e r lesions or "unidentified bright objects" (UBOs) in otherwise neurologically intact individuals. Q u a n t i t a t i v e v i d e o f l u o r o s c o p i c swallowing evaluations and cranial MRI examinations were studied in 49 neurologically normal volunteers (ages 43 to 79 years). Total swallowing duration (TSD) and its s u b c o m p o n e n t s o f oral transit duration (OTD), stage transition duration (STD), and pharyngeal response duration were measured for liquid and semisolid swallows. MRIs were graded from 0, or no UBOs, to 3, or multiple and confluent lesions. The effect o f the presence o f UBOs on swallowing durational measures and risk factors was analyzed with age differences accounted for statistically (ANCOVA). T S D and O T D for semisolids were significantly differentiated by M R I score (P < 0.009 and P < 0.047, respectively). T h a t is, a demonstrable effect was found for an increased n u m b e r o f UBOs on duration o f oropharyngeal swallowing in n o r m a l individuals. A b s t r a c t .
Key words: Deglutition -- Deglutition disorders -Deglutition durational measures -- Swallowing -Swallowing durational measures -- Magnetic resonance brain imaging -- Pefiventricular white matter lesions -- Videofluoroscopy.
* Supported in part by The National Institute of Health (NS24427). Address offprint requests to: Dr. Levine, Neurology Service/127, Middleton VAH, 2500 Overlook Terrace, Madison, WI 53705, USA
Basic to research on neurogenic dysphagia is the a t t e m p t to identify "site o f lesion" as accurately as possible. T o this end, a preliminary c o m p a r i s o n between neurological signs and cranial c o m p u t e r i z e d t o m o g r a p h y (CT) in a group o f unilateral ischemic stroke patients was reported [1]. M o r e recent exa m i n a t i o n o f the results oft2-weighted magnetic resonance imaging (MRI) o f unilateral stroke patients not only confirmed the C T - d e t e r m i n e d site o f ischemic infarction in those patients who u n d e r w e n t both C T and M R I scans, but also has indicated additional incidental M R I lesions o f the periventricular white matter, also known as "unidentified bright objects" (UBOs) [2]. T h e present investigation was designed to determine whether the presence o f UBOs has a demonstrable effect on measures o f swallowing duration in n o r m a l subjects. Cranial M R I has been r e c o m m e n d e d as the imaging procedure o f choice for evaluating neurogenic dysphagia [3]. Unfortunately, the authors did not clearly distinguish whether M R I lesions were incidental or clinically relevant. Several studies have a t t e m p t e d to correlate the presence o f U B O s with histopathological findings [4-10] and clinical findings such as stroke [11 ], cerebrovascular risk factors [12-15], cerebral blood flow decrements [16, 17], and age [6, 12, 18, 19]. A recent study using oxygen metabolic and blood measurements with positron t o m o g r a p h y showed that brains with severe periventricular hyperintensity had a b n o r m a l circulation but n o r m a l metabolism [20]. Little attention, however, was paid to the effect o f UBOs on performance o f specific neurological functions. Sarpel et al., in a study o f hospitalized veterans, found a significant
R. Levine et al.: Periventricular Lesions
but nonspecific relationship between periventricular hyperintensity and a b n o r m a l neurological findings on examination [21]. T h e y did not apparently measure swallowing ability. Robbins et aI., in a study o f 80 n o r m a l adults, found that several durational parameters o f oropharyngeal swallowing were significantly longer in the oldest subjects studied [22]. However, those subjects did not undergo cranial neuroimaging. Thus, in this study we investigate the effect o f M R I score, that is the presence o f UBOs, on swallowing durational measures as quantified with videofluoroscopy in selected neurologically n o r m a l individuals.
Subjects and Methods Age- and sex-matched normal individuals were recruited as paid volunteers in order to match previously studied patients with unilateral ischemic stroke [1]. Subjects had no history o f dysphagia, speech or hearing problems, head trauma, head or neck surgery, neurological disorders, or ischemic cerebrovascular symptomatology. Subjects had normal neurological examinations and scores o f 27 or higher on each o f two Mini Mental Status Exams (MMSE) [23]. They were from wide-ranging socioeconomic backgrounds. Each subject underwent a neurological examination, MMSE, swallowing evaluation, and cranial MRI within a 3-day period. MRI scans were obtained on a 1.5 tesla General Electric Signa scanner. The /:-weighted MRI scans were graded according to the scale published by Awad et al. [4, 12] and were scored either 0 (no UBOs), 1 (focal, limited to one lobe or posterior fossa), 2 (multiple, extending beyond one or lobe or posterior fossa), or 3 (multiple and confluent, forming multiple and large patches). The terms MR! score and U B O s are s y n o n y m o u s in this paper..Cerebral atrophy was scored as 1 (atrophy present) or 0 (no atrophy). The volume o f individual lesions and the extent o f atrophy were not quantified, nor was an attempt made to correlate exact n u m ber or location o f UBOs with other study variables. Out o f an original group o f 50 subjects, one subject was excluded based on MRI evidence o f an old cortical hemorrhage. This left 49 subjects for data comparisons.
Methods Each subject was given a score for their n u m b e r o f cerebrovascular risk factors (RISK; m a x i m u m score o f 9) including prior history o f TIA or stroke, arterial hypertension, coronary artery disease, diabetes mellitus, hyperlipidemia, cigarette smoking, obesity, gout, and familial history o f premature cardiovascular disease. Subjects underwent videofluoroscopic oropharyngeal swallowing evaluation according to a standard research protocol [1,221. Each subject swallowed 2 ml liquid and 2 ml semisolid material three times each. Values were reported as the mean o f each set o f three. Swallowing measures consisted o f oral transit duration (OTD), from beginning o f posterior bolus m o v e m e n t to arrival at top o f pharynx; stage transition duration (STD), from arrival o f bolus at top o f pharynx to initiation o f maximal hyolaryngeal excursion; pharyngeal response duration (PRD), from
143 Table 1.
MRI score in normals ~ (N = 49)
MRI
N
Mean age (years)
Range (years)
0 I 2 3
21 4 19 5
63 70 68 72
43-78 57-75 59-75 61-79
"~For statistical purposes, subjects grouped as M R I score 0 plus 1 versus 2 plus 3.
initiation o f maximal hyoid excursion to hyoid return to rest, which is a measure o f pharyngeal stage duration that is not bolus dependent: and total swallowing duration (TSD) or sum o f O T D plus STD plus PRD. Table 1 presents the MR1 scores for the subjects. Because o f the unequal distribution resulting in two cells o f small n u m b e r s (scores o f 1 or 3), subjects with MRI scores o f 0 and I were grouped together and subjects with scores o f 2 and 3 were grouped together for statistical analysis. In order to account for the effect o f age [22], univariate A N C O V A s were performed with age as the covariate, MRI score as the independent variable, and durational measures as the d e p e n d e n t variables. This was done using SYSTAT (version 4.0, SYSTAT) [24] and eight swallowing measures, OTD, STD, and P R D for both liquids and semisolids, as welt as TSD for liquids and semisolids, were studied. The effect o f MRI score on RISK was examined in the same manner. Since cerebral atrophy in this particular study was a binary measurement, atrophy or no atrophy, a Wilcoxon two-sample rank testing was performed to relate atrophy to MRI score. MRI scores and swallowing measures were generated using a numerical identification system in a fashion blinded to specific subject identity. Site o f UBO was not dealt with at this time. Lesions were frontal, parietal, or occipital in location for the most part and separated data resulting in too m a n y small n u m b e r samples.
Results All subjects were right-handed. T h e group comprised 20 w o m e n and 29 men, with a mean age o f 66 years and an age range o f 43 to 79 years. The group with M R I scores o f 0 or 1 had 26 subjects, and 23 subjects comprised the group with M R I scores o f 2 or 3 (Table 1). Higher M R I scores were graphically related to increasing age (Fig. 1). Otherwise, age was covaried out o f this analysis. A significant effect between M R I score and R I S K was found (P < 0.001). T h e group had a m e a n R I S K o f 1.4 with a range o f 0 (N = 15) to 6 (N = 1; Fig. 2). While 26 subjects had a history o f arterial hypertension, it was not factored into the statistical analysis. We also found a significant effect for M R I score on swallowing durational measures. T S D o f semisolid material was significantly longer (P < 0.009)
144
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Dysphagia ,c~Springer-VcrlagNew York Inc. 1992
Periventricular White Matter Changes and Oropharyngeal Swallowing in Normal Individuals* Ross Levine, M.D., 1 Jo A n n e Robbins, Ph.D., 1 and A n d r e a Maser, M.S. 2 Departments of ~Neurology and 2Radiology, William S. Middleton Memorial Veterans Administration Hospital and University of Wisconsin Clinical Sciences Center, Madison, Wisconsin, USA
Cranial m a g n e t i c r e s o n a n c e imaging (MRI) has revealed patchy periventricular white m a t t e r lesions or "unidentified bright objects" (UBOs) in otherwise neurologically intact individuals. Q u a n t i t a t i v e v i d e o f l u o r o s c o p i c swallowing evaluations and cranial MRI examinations were studied in 49 neurologically normal volunteers (ages 43 to 79 years). Total swallowing duration (TSD) and its s u b c o m p o n e n t s o f oral transit duration (OTD), stage transition duration (STD), and pharyngeal response duration were measured for liquid and semisolid swallows. MRIs were graded from 0, or no UBOs, to 3, or multiple and confluent lesions. The effect o f the presence o f UBOs on swallowing durational measures and risk factors was analyzed with age differences accounted for statistically (ANCOVA). T S D and O T D for semisolids were significantly differentiated by M R I score (P < 0.009 and P < 0.047, respectively). T h a t is, a demonstrable effect was found for an increased n u m b e r o f UBOs on duration o f oropharyngeal swallowing in n o r m a l individuals. A b s t r a c t .
Key words: Deglutition -- Deglutition disorders -Deglutition durational measures -- Swallowing -Swallowing durational measures -- Magnetic resonance brain imaging -- Pefiventricular white matter lesions -- Videofluoroscopy.
* Supported in part by The National Institute of Health (NS24427). Address offprint requests to: Dr. Levine, Neurology Service/127, Middleton VAH, 2500 Overlook Terrace, Madison, WI 53705, USA
Basic to research on neurogenic dysphagia is the a t t e m p t to identify "site o f lesion" as accurately as possible. T o this end, a preliminary c o m p a r i s o n between neurological signs and cranial c o m p u t e r i z e d t o m o g r a p h y (CT) in a group o f unilateral ischemic stroke patients was reported [1]. M o r e recent exa m i n a t i o n o f the results oft2-weighted magnetic resonance imaging (MRI) o f unilateral stroke patients not only confirmed the C T - d e t e r m i n e d site o f ischemic infarction in those patients who u n d e r w e n t both C T and M R I scans, but also has indicated additional incidental M R I lesions o f the periventricular white matter, also known as "unidentified bright objects" (UBOs) [2]. T h e present investigation was designed to determine whether the presence o f UBOs has a demonstrable effect on measures o f swallowing duration in n o r m a l subjects. Cranial M R I has been r e c o m m e n d e d as the imaging procedure o f choice for evaluating neurogenic dysphagia [3]. Unfortunately, the authors did not clearly distinguish whether M R I lesions were incidental or clinically relevant. Several studies have a t t e m p t e d to correlate the presence o f U B O s with histopathological findings [4-10] and clinical findings such as stroke [11 ], cerebrovascular risk factors [12-15], cerebral blood flow decrements [16, 17], and age [6, 12, 18, 19]. A recent study using oxygen metabolic and blood measurements with positron t o m o g r a p h y showed that brains with severe periventricular hyperintensity had a b n o r m a l circulation but n o r m a l metabolism [20]. Little attention, however, was paid to the effect o f UBOs on performance o f specific neurological functions. Sarpel et al., in a study o f hospitalized veterans, found a significant
R. Levine et al.: Periventricular Lesions
but nonspecific relationship between periventricular hyperintensity and a b n o r m a l neurological findings on examination [21]. T h e y did not apparently measure swallowing ability. Robbins et aI., in a study o f 80 n o r m a l adults, found that several durational parameters o f oropharyngeal swallowing were significantly longer in the oldest subjects studied [22]. However, those subjects did not undergo cranial neuroimaging. Thus, in this study we investigate the effect o f M R I score, that is the presence o f UBOs, on swallowing durational measures as quantified with videofluoroscopy in selected neurologically n o r m a l individuals.
Subjects and Methods Age- and sex-matched normal individuals were recruited as paid volunteers in order to match previously studied patients with unilateral ischemic stroke [1]. Subjects had no history o f dysphagia, speech or hearing problems, head trauma, head or neck surgery, neurological disorders, or ischemic cerebrovascular symptomatology. Subjects had normal neurological examinations and scores o f 27 or higher on each o f two Mini Mental Status Exams (MMSE) [23]. They were from wide-ranging socioeconomic backgrounds. Each subject underwent a neurological examination, MMSE, swallowing evaluation, and cranial MRI within a 3-day period. MRI scans were obtained on a 1.5 tesla General Electric Signa scanner. The /:-weighted MRI scans were graded according to the scale published by Awad et al. [4, 12] and were scored either 0 (no UBOs), 1 (focal, limited to one lobe or posterior fossa), 2 (multiple, extending beyond one or lobe or posterior fossa), or 3 (multiple and confluent, forming multiple and large patches). The terms MR! score and U B O s are s y n o n y m o u s in this paper..Cerebral atrophy was scored as 1 (atrophy present) or 0 (no atrophy). The volume o f individual lesions and the extent o f atrophy were not quantified, nor was an attempt made to correlate exact n u m ber or location o f UBOs with other study variables. Out o f an original group o f 50 subjects, one subject was excluded based on MRI evidence o f an old cortical hemorrhage. This left 49 subjects for data comparisons.
Methods Each subject was given a score for their n u m b e r o f cerebrovascular risk factors (RISK; m a x i m u m score o f 9) including prior history o f TIA or stroke, arterial hypertension, coronary artery disease, diabetes mellitus, hyperlipidemia, cigarette smoking, obesity, gout, and familial history o f premature cardiovascular disease. Subjects underwent videofluoroscopic oropharyngeal swallowing evaluation according to a standard research protocol [1,221. Each subject swallowed 2 ml liquid and 2 ml semisolid material three times each. Values were reported as the mean o f each set o f three. Swallowing measures consisted o f oral transit duration (OTD), from beginning o f posterior bolus m o v e m e n t to arrival at top o f pharynx; stage transition duration (STD), from arrival o f bolus at top o f pharynx to initiation o f maximal hyolaryngeal excursion; pharyngeal response duration (PRD), from
143 Table 1.
MRI score in normals ~ (N = 49)
MRI
N
Mean age (years)
Range (years)
0 I 2 3
21 4 19 5
63 70 68 72
43-78 57-75 59-75 61-79
"~For statistical purposes, subjects grouped as M R I score 0 plus 1 versus 2 plus 3.
initiation o f maximal hyoid excursion to hyoid return to rest, which is a measure o f pharyngeal stage duration that is not bolus dependent: and total swallowing duration (TSD) or sum o f O T D plus STD plus PRD. Table 1 presents the MR1 scores for the subjects. Because o f the unequal distribution resulting in two cells o f small n u m b e r s (scores o f 1 or 3), subjects with MRI scores o f 0 and I were grouped together and subjects with scores o f 2 and 3 were grouped together for statistical analysis. In order to account for the effect o f age [22], univariate A N C O V A s were performed with age as the covariate, MRI score as the independent variable, and durational measures as the d e p e n d e n t variables. This was done using SYSTAT (version 4.0, SYSTAT) [24] and eight swallowing measures, OTD, STD, and P R D for both liquids and semisolids, as welt as TSD for liquids and semisolids, were studied. The effect o f MRI score on RISK was examined in the same manner. Since cerebral atrophy in this particular study was a binary measurement, atrophy or no atrophy, a Wilcoxon two-sample rank testing was performed to relate atrophy to MRI score. MRI scores and swallowing measures were generated using a numerical identification system in a fashion blinded to specific subject identity. Site o f UBO was not dealt with at this time. Lesions were frontal, parietal, or occipital in location for the most part and separated data resulting in too m a n y small n u m b e r samples.
Results All subjects were right-handed. T h e group comprised 20 w o m e n and 29 men, with a mean age o f 66 years and an age range o f 43 to 79 years. The group with M R I scores o f 0 or 1 had 26 subjects, and 23 subjects comprised the group with M R I scores o f 2 or 3 (Table 1). Higher M R I scores were graphically related to increasing age (Fig. 1). Otherwise, age was covaried out o f this analysis. A significant effect between M R I score and R I S K was found (P < 0.001). T h e group had a m e a n R I S K o f 1.4 with a range o f 0 (N = 15) to 6 (N = 1; Fig. 2). While 26 subjects had a history o f arterial hypertension, it was not factored into the statistical analysis. We also found a significant effect for M R I score on swallowing durational measures. T S D o f semisolid material was significantly longer (P < 0.009)
144
R. Levine et al.: Periventricular Lesions 80
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