In our previous cross-sectional study, we evaluated the relationship between TT and MTP as a strength metric in DMD, DM1, and ALS patients. There was higher TT in the DMD group, lower MTP in the DM1 group, and a significant correlation between TT and MTP in the ALS group [4]. Thirteen of 21 ALS patients, 19 of 30 DM1 patients, 11 of 14 male DMD patients in this study overlapped with the previous one, and measurement values at the first measure of this study were close to the previous ones. In another study, we also revealed the distinctive features of dysphagia in DM1 and DMD patients using VFSS, hyoid bone movement during the pharyngeal phase of swallowing (excursion), or pharyngeal residue measurement [12], which also demonstrated distinct abnormalities in swallowing muscle function between DM1 and DMD. The study also showed the correlation between TT and BW, but not MTP, in the DM1 group [4], suggesting that, in DM1 patients, TT was associated with malnutrition and concomitant weight loss. However, long-term tongue muscle weakness is also thought to promote malnutrition, and further loss of muscle mass may lead to additional TT and BW reductions [13]. Therefore, we assessed TT, MTP, and BW at multiple times during disease progression in this study.
Van Den Engel-Hoek et al. reported that TT can be assessed, conveniently and reproducibly, in DMD patients using ultrasound [10, 14]. More recently, they reported increased tongue hypertrophy and dystrophic changes in masticatory muscles but did not report changes in tongue muscles [1]. Although we found “tongue pseudohypertrophy” in DMD patients by ultrasound assessment, there were no significant longitudinal changes as in the ALS group. We suggest that, in terms of TT progression, after the early stage of DMD that tongue muscle tissue is replaced by connective tissue or fat [15], the progression rate will become slower.
On the other hand, progressive bulbar palsy is rapidly linked to dysphagia, malnutrition, and BW loss which leads to poor survival time in ALS, but BW loss could be caused by rising energy consumption due to impairment of respiratory function [16]. Poor tongue strength is independently associated with shorter survival time in ALS patients [17], so measuring TT and MTP is critical for prognosis and adjustment of treatment. Tamburrini et al. examined tongue movement function among ALS patients using both ultrasonography and VFSS, but they did not conduct objective tongue atrophy assessment [18]. Nakamori et al. suggested an association between TT, disease progression, and tongue dysfunction [6], consistent with our previous study showing a significant correlation between TT and MTP in ALS [4]. The mean TT value of ALS patients in their study (41.9 ± 4.0 mm) was similar to our last measurement (40.0 ± 6.5 mm), while the mean TT value of their control volunteers (44.8 ± 3.0 mm) was closer to the first value in our ALS group (42.8 ± 6.8 mm), strongly suggesting tongue atrophy progressed during the roughly 2-year follow-up period. Nakamori et al. also found reduced TT over 15 months. In accordance with their study, the ALS group also included patients without TT reduction (Fig. 3a), possibly due to differences in time from onset or rate of disease progression between bulbar or limb onset types. The patients with limb onset types showed a greater reduction MTP than bulbar onset patients and limb onset patients were likely in an advanced clinical stage. Increased TT in few patients may be caused by measurement error which is expected about 10% one way or the other, due to the position of the ultrasound imaging probe. Alternatively, we found no association between TT and BW, in contrast to the linear association between TT and BMI reported by Nakamori et al. In our previous study, bulbar onset patients showed a stronger correlation between TT and MTP than limb onset patients, suggesting these measures especially important for monitoring bulbar paralysis patients [4], especially during the early clinical stages.
This study has several limitations, most notably the differences in mean age among groups, which is known to influence MTP [19]. However, age matching of DMD, ALS, and DM1 is difficult due to the differences in age at onset and course. Moreover, differences in gender or evaluation periods are also difficult to unify in the three groups. There are only male DMD patients and we considered that gender differences did not have a big effect on temporal changes of TT and MTP. The periodic evaluations were ordered depending on the disease progression and ALS patients underwent more examinations in the same term. In the initial stage, we often examined them once a year but increased the frequency of examinations depending on the deterioration of symptoms. Unfortunately, there is no uniform standard to assess the functional level or disease stage for NMD patients and ADL scales are not correlate well with their eating ability. Instead of functional level or disease stage, we used the score of FOIS to show their eating abilities. In the future, a further investigation with enough sample size is requested in order to confirm the distinctive characteristics of tongue dysfunction progression in NMD and to establish disorder-specific treatment plans for dysphagia. Nonetheless, these results suggest distinct dysphagia pathomechanisms and progression features of among neurogenic and myogenic disorder patients.
This longitudinal study revealed more rapid loss of tongue thickness and strength in ALS patients than DMD and DM1. Only the ALS patients also exhibited substantial weight loss over the observation period, a change strongly associated with shorter survival [16]. On the other hand, DM1 and DMD patients may show only slowly developing tongue dysfunction in the short term, although DM1 may have lower tongue strength and DMD patients enlarged tongues, respectively, both of which can contribute to dysphagia. These findings suggest that regular re-evaluation of TT and MTP could provide valuable information on tongue dysfunction progression in NMD.
