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The prognosis of dysphagia patients over 100 years old Hirotaka Shoji a, Ayako Nakane a,*, Yumiko Omosu b, Karin Sawashima b, Satoshi Teranaka a, Yoshiko Umeda a, Nobuhiro Inokuchi a, Shuhei Takeuchi a, Yutaka Kamikawatoko b, Shunsuke Minakuchi a a
Gerodontology and Oral Rehabilitation, Department of Gerontology and Gerodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8549, Japan Department of Rehabilitation, Isshin General Hospital of Nisshinkai Medical Corporation, 1-18-7 Kitaotsuka, Toshima-ku, Tokyo 170-0004, Japan
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A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 June 2013 Received in revised form 18 April 2014 Accepted 24 April 2014 Available online xxx
Several reports have recently been published regarding dysphagia in very elderly patients, and centenarian dysphagia patients have become more common in Japan. The aim of this study was to assess the prognosis of dysphagia in very elderly patients. Participants were 24 centenarian dysphagia patients. For each patient, we collected information on age, care level, past medical history, and changes in oral intake according to the Functional Oral Intake Scale (FOIS). Patients were divided into two groups based on the mode of food intake at the time of transfer or discharge: the per oral-only group (the PO-only group, i.e., oral intake alone) and the tube feeding-dependent group (the TF-dependent group, i.e., combination of oral intake and tube feeding, or tube feeding alone). In both groups, the FOIS score decreased significantly from pre-hospitalization to the time of transfer or discharge (p = 0.006 for both). The FOIS score at initial assessment was higher in the PO-only group with the TF-dependent group (p = 0.0004). Furthermore, the frequency of a FOIS score of 4 at initial assessment was significantly higher in the PO-only group, and the frequency of a FOIS score of 1 was significantly higher in the TF-dependent group (p = 0.0006). These findings collectively suggest that oral intake can be recovered if the FOIS score is 4 at initial assessment, is difficult if the score is 1, and may be possible with a FOIS score of 2. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Very elderly 100 Years old Aging Dysphagia Functional Oral Intake Scale
1. Introduction During the natural course of aging, people become more vulnerable to various illnesses and disorders, including dysphagia. In the elderly, dysphagia is the major pathophysiologic mechanism leading to aspiration pneumonia (Marik & Kaplan, 2003). In Japan, pneumonia ranks third among general causes of death (Ministry of Health, Labour, and Welfare, 2012), and is the most common cause of death in elderly males aged 90 years (The Committee for the JRS Guidelines in Management of Respiratory Infections, 2007, chap. 3). Aspiration pneumonia accounts for at least 80% of pneumonia cases in elderly people aged 70 years (Teramoto et al., 2008). Once infected, elderly people require considerably more time to return to their baseline state of mobility than young adults. This is particularly so among frail elderly people, and recovery may take several months for this population (Marrie, 2000). Indeed, even minor injuries can markedly impair activities of daily living
* Corresponding author. Tel.: +81 3 5803 5562; fax: +81 3 5803 5562. E-mail address: [email protected] (A. Nakane).
(ADL) and lead to various subtle, perhaps latent impairments to surface or become severe, such as decubitus ulcers, severe dry mouth, and deterioration of dementia. Disuse syndrome due to immobility is also an emerging issue, as is muscular atrophy due to inactivity from hospitalization. When reaching the age of 100, people suffer from several chronic conditions, which strongly suggests that healthy centenarians do not exist, or at least are extremely rare (Andersen-Ranberg, Schroll, & Jeune, 2001). In other words, centenarians are people who suffer from decreased functional reserve (Darviri et al., 2008). This phenomenon of atrophy from disuse is likely to be similar for swallowing and respiratory function, highlighting the importance of swallowing rehabilitation for very elderly people prone to aspiration. At present, swallowing rehabilitation is only occasionally performed for centenarians (Freeman, Kurosawa, Ebihara, & Kohzuki, 2010). In very elderly patients, perhaps due to their age, oral intake is often forgone without adequate efforts to rehabilitate swallowing function. Yet, substantial individual variation exists in physical function among elderly patients, and thus it is possible that even very elderly patients may be capable of oral intake with adequate swallowing rehabilitation. Given the
http://dx.doi.org/10.1016/j.archger.2014.04.009 0167-4943/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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prolongation of life expectancy, centenarians are becoming commonplace in society (Willcox, Willcox, & Poon, 2010). This inevitably implies that the number of centenarian patients with dysphagia will rise globally in the coming years, and underscores the need for specific measures to improve swallowing function in this population. To this end, an important consideration is the implementation of an appropriate system at the intervention stage of swallowing rehabilitation. Currently, a number of reports exist on dysphagia in elderly patients (Sheth & Diner, 1998; Tibbling & Gustafsson, 1991). However the age range of patients is wide in many studies and few have targeted very elderly patients. Importantly, no study has been performed in centenarian patients. To evaluate the prognosis of dysphagia in very elderly patients, we divided centenarian dysphagia patients into two groups after swallowing rehabilitation based on whether they were able to feed orally or were dependent on tube feeding. We also assessed factors affecting swallowing function from pre-hospitalization to the time of transfer or discharge. 2. Materials and methods 2.1. Participants and study design We conducted a retrospective cohort study of 24 centenarian patients with dysphagia (5 males, 19 females; mean age, 103.3 2.8 years; age range, 100–109 years) hospitalized between January 2007 and April 2012. Table 1 summarizes their reasons for hospitalization. All patients were introduced to rehabilitation department after admission to internal medicine and orthopedics due to dysphagia. After the initial assessment, all patients received rehabilitation therapy. The rehabilitation program ranged from direct swallowing therapy to indirect therapy (Neumann, Bartolome, Buchholz, & Prosiegel, 1995). Direct rehabilitative exercises included diet adjustments and were supervised by speech language pathologist, nurse, and dental hygienist. Indirect therapy involved oral care, electrical stimulation, and physical exercises addressing range of movement, joint mobility, and posture. Oral care was provided by dental hygienist and physical exercises by physical therapists. Other swallowing rehabilitation methods, such as supraglottic swallowing and Mendelsohn maneuver (Ding, Larson, Logemann, & Rademaker, 2002), were not performed. Patients were divided into two groups based on the mode of food intake at the time of transfer or discharge: the per oral-only group (the PO-only group, i.e., oral intake alone without tube feeding) and the tube feeding-dependent group (the TF-dependent group, i.e., combination of oral intake and tube feeding or tube feeding alone). Each survey item was compared between the two groups. This study was approved by the Ethics Committee of the Tokyo Medical and Dental University Faculty of Dentistry (approval number 875) and the Ethics Committee of the Isshin General Hospital of Nisshinkai Medical Corporation.
of hospitalization and swallowing rehabilitation, form of food intake before hospitalization, at the initial assessment, and at the time of transfer or discharge, were obtained from medical records. During the initial assessment, videofluoroscopic (VF) and/or videoendoscopic (VE) swallowing examinations were performed in almost all patients. Patients who could not undergo the examinations underwent one or more of the following tests: repetitive saliva swallowing test (RSST; Oguchi et al., 2000), cough test (CT; Wakasugi et al., 2008), water test (WT; Tohara, Saitoh, Mays, Kuhlemeier, & Palmer, 2003), and food test (FT; Tohara et al., 2003). When the general condition of the patients was stable, some tests were carried out. VF was performed in seven patients (29.2%), VE in 11 (45.8%), RSST in 12 (50%), CT in 14 (58.3%), WT in eight (33.3%), and FT in seven (29.2%). FOIS (Crary, Mann, & Groher, 2005) (FOIS) score was used to assess swallowing function. FOIS consists of 7 rank-ordered scales to evaluate changes in the swallowing function of stroke patients. Levels 1 through 3 relate to varying degrees of nonoral feeding; levels 4 through 7 relate to varying degrees of oral feeding without nonoral supplementation. Its validity and reliability have been established (Crary et al., 2005). In fact, Crary et al. suggest that other assessment scales (e.g., Dysphagia Outcome and Severity Scale (O’Neil, Purdy, Falk, & Gallo, 1999) and Functional Outcome Swallowing Scale for Staging Oropharyngeal Dysphagia; Salassa, 1999) are less valid or reliable. Moreover FOIS was assessed retrospectively on the basis a chart review (Crary et al., 2005; Hansen et al., 2008). FIOS has also been used in populations other than stroke patients, such as patients with head and neck cancer (Crary, Carnaby (Mann), Groher, & Helseth, 2004). A partially modified version has been used in patients with Zenker’s diverticulum (Adam, Paskhover, & Sasaki, 2013). FOIS score before hospitalization was estimated based on the form of food ingested. Furthermore, FOIS scores at initial assessment and at the time of transfer or discharge were estimated based on the form of food intake determined by results of several tests and examinations and clinical symptoms. We adopted this scale given its adequate reliability and validity to assess changes in swallowing function and applicability across various diseases. 2.3. Statistical analysis The Wilcoxon signed-rank test was used for within-group analyses and the Mann–Whitney U and Fisher’s exact tests were used for analyses between the PO-only and TF-dependent groups. SPSS11.0J for Windows (SPSS Inc, Chicago, IL, USA) was used for statistical analysis. P < 0.05 was considered statistically significant. 3. Results 3.1. Characteristics of the PO-only group
2.2. Data collection 3.1.1. Changes in FOIS score (Fig. 1) Information regarding past medical history, age, care level (Tamiya et al., 2002), number of days to initial assessment, length Table 1 Reasons for hospitalization. Respiratory Orthopedic Gastrointestinal Cerebrovascular Circulatory Endocrine
11 patients (pneumonia, 10; acute bronchitis, 1) 4 patients (femoral neck fracture, 3; femoral fracture, 4 patients (acute gastroenteritis, 2; gastric ulcer, 1; choledocholithiasis, 1) 2 patients (cerebral infarction, 1; hydrocephalus, 1) 2 patients (heart failure, 2) 1 patient (dehydration, 1)
The pre-hospitalization FOIS score was 7 for eight patients, 5 for one patient, and 4 for six patients. At initial assessment, the FOIS score was 5 for one patient, 4 for eight patients, and 2 for six patients, and at the time of transfer or discharge, 5 for four patients and 4 for 11 patients. The pre-hospitalization FOIS score significantly differed from the FOIS score at the time of transfer or discharge (p = 0.006; Wilcoxon signed-rank test). The FOIS score at the time of transfer or discharge significantly differed from the FOIS score at initial assessment (p = 0.016; Wilcoxon signed-rank test). The FOIS score decreased for all nine patients who had pre-hospitalization FOIS scores of 5, and did not return
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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Table 2 Comparison between groups PO-only group TF-dependent group (n = 15) (n = 9).
Age (years) Care levela FOIS scoreb Before hospitalization At initial assessment** Number of days to initial assessment Length of hospitalization (days)** Length for swallowing rehabilitation**
PO-only group (n = 15)
TF-dependent group (n = 9)
103.6 2.7 3.0 (3.0–5.0)
102.7 2.8 4.0 (4.0–5.0)
7.0 (4.0–7.0) 4.0 (2.0–4.0) 9.5 14.5 32.6 21.9 23.1 14.6
5.0 (4.0–5.0) 1.0 (1.0–2.0) 18.6 24.6 71.9 23.0 53.3 27.0
Data are expressed as mean SD or median (IQR). a Care Levels are range from the lowest (care level 1) to the most severe (care level 5) needs (Tamiya et al., 2002). Levels were determined before hospitalization. b FOIS levels 1–7. ** Significant difference in length of hospitalization and swallowing rehabilitation and FOIS score at initial assessment between groups (p < 0.01 for both). Fig. 1. Change in FOIS score at each stage (N = 15 for each evaluation). **FOIS score at pre-hospitalization was significantly lower than that at transfer or discharge (p < 0.01). *FOIS score at transfer or discharge was significantly higher than that at initial assessment (p < 0.05).
to the pre-hospitalization score. The remaining patients with a prehospitalization FOIS score of 4 maintained this score or returned to their pre-hospitalization score. 3.2. Characteristics of the TF-dependent group 3.2.1. Changes in FOIS score (Fig. 2) The pre-hospitalization FOIS score was 5 for five patients and 4 for four patients. The FOIS score at initial assessment was 2 for four patients and 1 for five patients, and at the time of transfer or discharge, 2 for one patient and 1 for eight patients. The pre-hospitalization FOIS score significantly differed from the FOIS score at the time of transfer or discharge (p = 0.006; Wilcoxon signed-rank test). The FOIS score at the time of transfer or discharge did not differ significantly from the FOIS score at initial assessment (p = 0.25; Wilcoxon signed-rank test).
of the following: cerebrovascular disease, dementia, and pneumonia. There were no other disease known to impair swallowing in both groups. 3.3.2. Age, care level, number of days to initial assessment and length of hospitalization and swallowing rehabilitation The mean age of the PO-only group was 103.6 years (SD, 2.7), and the median care level was 3.0 (IQR, 3.0–5.0). The mean number of days to initial assessment and the mean length of hospitalization and swallowing rehabilitation were 9.5 days (SD, 14.5), 32.6 days (SD, 21.9) and, 23.1days (SD, 14.6) respectively. The mean age of the TF-dependent group was 102.7 years (SD, 2.8), and the median care level was 4.0 (IQR, 4.0–5.0). Moreover, the mean number of days to initial assessment and the mean length of hospitalization and swallowing rehabilitation were 18.6 days (SD, 24.6), 71.9 days (SD, 23.0) and 53.3 days (SD, 27.0), respectively. 3.3.3. Comparison of each of the items between groups (Table 2)
3.3.1. Past medical history Two patients had no history of neurologic or respiratory disease known to affect swallowing function between the PO-only and TFdependent groups. The remainder of the patients had one or more
There were no significant differences in age, care level, prehospitalization FOIS score, or the number of days to initial assessment between the PO-only and TF-dependent groups (p = 0.48, p = 0.14, p = 0.14, p = 0.08, respectively; Mann–Whitney U test). In contrast, there were significant differences in the length of hospitalization and swallowing rehabilitation and FIOS score at initial assessment between the two groups. Specifically, compared with the TF-dependent group, the length of hospitalization and swallowing rehabilitation were shorter (p = 0.002, p = 0.006, respectively) and FOIS score at initial assessment was higher in
Fig. 2. Change in FOIS score at each stage (N = 9 for each evaluation). **FOIS score at pre-hospitalization was significantly lower relative to that of the score at transfer or discharge (p < 0.01).
Fig. 3. FOIS score frequency at initial assessment in the PO-only and TF-dependent groups (PO-only group, 15; TF-dependent group, 9). **Significant difference between PO-only and TF-dependent groups (p < 0.01).
3.3. Comparison between groups
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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the PO-only group (p = 0.0004). Moreover, the frequency of a FOIS score of 4 at initial assessment was significantly higher in the PO-only group, and the frequency of a FOIS score of 1 was significantly higher in the TF-dependent group (p = 0.0006, Fisher’s exact test; odds ratio, 0.4 (95% Confidence Interval, 0.21–0.74); Fig. 3). 4. Discussion In this study, we examined swallowing function in very elderly patients from pre-hospitalization to the time of transfer or discharge using FOIS, assessed changes in swallowing function, and evaluated the prognosis of dysphagia in very elderly patients. 4.1. Changes in FOIS score from pre-hospitalization to transfer or discharge Pre-hospitalization FOIS scores and FOIS scores at the time of transfer or discharge significantly differed between the two groups (p < 0.01). The pre-hospitalization FOIS score was 7 for eight patients in the PO-only group and oral intake became possible for all of these patients. However, FOIS scores of these eight patients at the time of transfer or discharge did not return to pre-hospitalization scores. Although statistically significant, pre-hospitalization FOIS score and FOIS score at the time of transfer or discharge may be different in a strict sense. Comparability between pre-hospitalization FOIS score and FOIS score at the time of transfer or discharge may not be correct. Though our results suggest that dysphagia in very elderly patients may be associated with poor recovery, it is impossible to relate these results in this study. Since criteria for assigning FOIS scores could have been different. Therefore, further studies are needed to evaluate swallowing function from pre-hospitalization to the time of transfer or discharge strictly. Meanwhile, Hattori et al. (2008) reported that the mode of food intake did not necessarily correlate with the swallowing abilities of homebound and institutionalized dysphagia patients. Additionally, Ekberg and Feinberd (1991) reported that swallowing studies with imaging in 56 elderly people without dysphagia symptoms revealed normal swallowing function in only 16% of them. In the present study, swallowing function was not assessed prior to hospitalization. However, the effects of aging on swallowing have been recently reported (Achem & Devault, 2005; Nogueira & Reis, 2013; Sura, Madhavan, Carnaby, & Crary, 2012), and the effects are likely to be more pronounced in very elderly people. That is, patients who had been eating a normal diet orally prior to hospitalization may have had undetected problems with swallowing to begin with. This suggests the need for a swallowing assessment system for very elderly people. 4.2. FOIS scores at initial assessment 4.2.1. FOIS scores of 1 and 4 A statistically significant difference in FOIS score at initial assessment was observed between the PO-only and TF-dependent groups (p < 0.01). The frequency of a FOIS score of 4 was significantly higher in the PO-only group, as was the frequency of a FOIS score of 1 in the TF-dependent group (p < 0.01 for both). Swallowing rehabilitation was performed for all patients with a FOIS score of 1. However, these patients refused rehabilitation or had an unstable general medical status. They showed poor progress and their FOIS score never increased. By contrast, previous studies reported that elderly dysphagia patients with a FOIS score of 3 at initial assessment recovered after swallowing rehabilitation (Bogaardt, Grolman, & Fokkens, 2009; Sun et al., 2013). Compared with the PO-only group, FOIS
score at initial assessment is lower in these groups. Although some patients with a FOIS score of 1 at initial assessment were included, oral intake was recovered in these studies. Altogether, oral intake may be recovered even if the FOIS score is 1 at initial assessment in elderly patients. These suggest that if swallowing function had not been reserved enough to obtain FOIS score of 4 at initial assessment, oral intake would become impossible in very elderly patients. Though the underlying medical condition in that studies differ from that of ours, active interventions should be performed for very elderly patients with FOIS scores 4 in the early stages of disease. Furthermore, oral intake may no longer be possible for a very elderly patient with a FOIS score of 1 at initial assessment. 4.2.2. FOIS score of 2 In the PO-only and TF-dependent groups, six and four patients had a FOIS score of 2 at initial assessment, respectively (not statistically significant). Patients in the PO-only group remained medically stable, and all six patients became capable of oral intake by the time of transfer or discharge (FOIS score of 4, five patients; FOIS score of 5, one patient). However, the FOIS score of one patient in the TF-dependent group remained unchanged, the general medical status for two patients deteriorated (one died), and the FOIS score of the remaining patient decreased to 1 because the patient refused to continue training due to worsening dementia. Thus, those in the TF-dependent group tended to have deteriorating medical status and dementia, which was not the case in the PO-only group. Although not statistically significant, a FOIS score of 2 at initial assessment may indicate that oral intake is recoverable. Thus, it may make sense to closely monitor the progress of dementia and the general condition of patients with this FOIS score. 4.3. Study limitations This study has some limitations worth noting. First, this study did not include a control group with elderly dysphagia patients. Further studies are needed to determine the difference between centenarians and the elderly patients. Second, swallowing assessment before hospitalization was not strictly performed. Further studies are still needed to examine swallowing function from pre-hospitalization to the time of transfer or discharge. Other limitations include the retrospective nature of data collection and the relatively small sample size. 5. Conclusions In this study, we examined the prognosis of dysphagia in centenarian patients. Our results suggest that oral intake can be recovered to some extent in patients with FOIS scores 4 at the time of initial assessment, but may be difficult for patients with a FOIS score of 1. Moreover, general medical status and degree of dementia are likely to influence whether oral intake can be achieved later on for patients with a FOIS score of 2 at the time of initial assessment.
Conflict of interest None declared by any author. Acknowledgements This study was supported by a Grant-in-Aid for Young Scientists (B) (23792503 and 25862074) from the Japan Society for the Promotion of Science.
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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Contents lists available at ScienceDirect
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The prognosis of dysphagia patients over 100 years old Hirotaka Shoji a, Ayako Nakane a,*, Yumiko Omosu b, Karin Sawashima b, Satoshi Teranaka a, Yoshiko Umeda a, Nobuhiro Inokuchi a, Shuhei Takeuchi a, Yutaka Kamikawatoko b, Shunsuke Minakuchi a a
Gerodontology and Oral Rehabilitation, Department of Gerontology and Gerodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8549, Japan Department of Rehabilitation, Isshin General Hospital of Nisshinkai Medical Corporation, 1-18-7 Kitaotsuka, Toshima-ku, Tokyo 170-0004, Japan
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 June 2013 Received in revised form 18 April 2014 Accepted 24 April 2014 Available online xxx
Several reports have recently been published regarding dysphagia in very elderly patients, and centenarian dysphagia patients have become more common in Japan. The aim of this study was to assess the prognosis of dysphagia in very elderly patients. Participants were 24 centenarian dysphagia patients. For each patient, we collected information on age, care level, past medical history, and changes in oral intake according to the Functional Oral Intake Scale (FOIS). Patients were divided into two groups based on the mode of food intake at the time of transfer or discharge: the per oral-only group (the PO-only group, i.e., oral intake alone) and the tube feeding-dependent group (the TF-dependent group, i.e., combination of oral intake and tube feeding, or tube feeding alone). In both groups, the FOIS score decreased significantly from pre-hospitalization to the time of transfer or discharge (p = 0.006 for both). The FOIS score at initial assessment was higher in the PO-only group with the TF-dependent group (p = 0.0004). Furthermore, the frequency of a FOIS score of 4 at initial assessment was significantly higher in the PO-only group, and the frequency of a FOIS score of 1 was significantly higher in the TF-dependent group (p = 0.0006). These findings collectively suggest that oral intake can be recovered if the FOIS score is 4 at initial assessment, is difficult if the score is 1, and may be possible with a FOIS score of 2. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Very elderly 100 Years old Aging Dysphagia Functional Oral Intake Scale
1. Introduction During the natural course of aging, people become more vulnerable to various illnesses and disorders, including dysphagia. In the elderly, dysphagia is the major pathophysiologic mechanism leading to aspiration pneumonia (Marik & Kaplan, 2003). In Japan, pneumonia ranks third among general causes of death (Ministry of Health, Labour, and Welfare, 2012), and is the most common cause of death in elderly males aged 90 years (The Committee for the JRS Guidelines in Management of Respiratory Infections, 2007, chap. 3). Aspiration pneumonia accounts for at least 80% of pneumonia cases in elderly people aged 70 years (Teramoto et al., 2008). Once infected, elderly people require considerably more time to return to their baseline state of mobility than young adults. This is particularly so among frail elderly people, and recovery may take several months for this population (Marrie, 2000). Indeed, even minor injuries can markedly impair activities of daily living
* Corresponding author. Tel.: +81 3 5803 5562; fax: +81 3 5803 5562. E-mail address: [email protected] (A. Nakane).
(ADL) and lead to various subtle, perhaps latent impairments to surface or become severe, such as decubitus ulcers, severe dry mouth, and deterioration of dementia. Disuse syndrome due to immobility is also an emerging issue, as is muscular atrophy due to inactivity from hospitalization. When reaching the age of 100, people suffer from several chronic conditions, which strongly suggests that healthy centenarians do not exist, or at least are extremely rare (Andersen-Ranberg, Schroll, & Jeune, 2001). In other words, centenarians are people who suffer from decreased functional reserve (Darviri et al., 2008). This phenomenon of atrophy from disuse is likely to be similar for swallowing and respiratory function, highlighting the importance of swallowing rehabilitation for very elderly people prone to aspiration. At present, swallowing rehabilitation is only occasionally performed for centenarians (Freeman, Kurosawa, Ebihara, & Kohzuki, 2010). In very elderly patients, perhaps due to their age, oral intake is often forgone without adequate efforts to rehabilitate swallowing function. Yet, substantial individual variation exists in physical function among elderly patients, and thus it is possible that even very elderly patients may be capable of oral intake with adequate swallowing rehabilitation. Given the
http://dx.doi.org/10.1016/j.archger.2014.04.009 0167-4943/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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prolongation of life expectancy, centenarians are becoming commonplace in society (Willcox, Willcox, & Poon, 2010). This inevitably implies that the number of centenarian patients with dysphagia will rise globally in the coming years, and underscores the need for specific measures to improve swallowing function in this population. To this end, an important consideration is the implementation of an appropriate system at the intervention stage of swallowing rehabilitation. Currently, a number of reports exist on dysphagia in elderly patients (Sheth & Diner, 1998; Tibbling & Gustafsson, 1991). However the age range of patients is wide in many studies and few have targeted very elderly patients. Importantly, no study has been performed in centenarian patients. To evaluate the prognosis of dysphagia in very elderly patients, we divided centenarian dysphagia patients into two groups after swallowing rehabilitation based on whether they were able to feed orally or were dependent on tube feeding. We also assessed factors affecting swallowing function from pre-hospitalization to the time of transfer or discharge. 2. Materials and methods 2.1. Participants and study design We conducted a retrospective cohort study of 24 centenarian patients with dysphagia (5 males, 19 females; mean age, 103.3 2.8 years; age range, 100–109 years) hospitalized between January 2007 and April 2012. Table 1 summarizes their reasons for hospitalization. All patients were introduced to rehabilitation department after admission to internal medicine and orthopedics due to dysphagia. After the initial assessment, all patients received rehabilitation therapy. The rehabilitation program ranged from direct swallowing therapy to indirect therapy (Neumann, Bartolome, Buchholz, & Prosiegel, 1995). Direct rehabilitative exercises included diet adjustments and were supervised by speech language pathologist, nurse, and dental hygienist. Indirect therapy involved oral care, electrical stimulation, and physical exercises addressing range of movement, joint mobility, and posture. Oral care was provided by dental hygienist and physical exercises by physical therapists. Other swallowing rehabilitation methods, such as supraglottic swallowing and Mendelsohn maneuver (Ding, Larson, Logemann, & Rademaker, 2002), were not performed. Patients were divided into two groups based on the mode of food intake at the time of transfer or discharge: the per oral-only group (the PO-only group, i.e., oral intake alone without tube feeding) and the tube feeding-dependent group (the TF-dependent group, i.e., combination of oral intake and tube feeding or tube feeding alone). Each survey item was compared between the two groups. This study was approved by the Ethics Committee of the Tokyo Medical and Dental University Faculty of Dentistry (approval number 875) and the Ethics Committee of the Isshin General Hospital of Nisshinkai Medical Corporation.
of hospitalization and swallowing rehabilitation, form of food intake before hospitalization, at the initial assessment, and at the time of transfer or discharge, were obtained from medical records. During the initial assessment, videofluoroscopic (VF) and/or videoendoscopic (VE) swallowing examinations were performed in almost all patients. Patients who could not undergo the examinations underwent one or more of the following tests: repetitive saliva swallowing test (RSST; Oguchi et al., 2000), cough test (CT; Wakasugi et al., 2008), water test (WT; Tohara, Saitoh, Mays, Kuhlemeier, & Palmer, 2003), and food test (FT; Tohara et al., 2003). When the general condition of the patients was stable, some tests were carried out. VF was performed in seven patients (29.2%), VE in 11 (45.8%), RSST in 12 (50%), CT in 14 (58.3%), WT in eight (33.3%), and FT in seven (29.2%). FOIS (Crary, Mann, & Groher, 2005) (FOIS) score was used to assess swallowing function. FOIS consists of 7 rank-ordered scales to evaluate changes in the swallowing function of stroke patients. Levels 1 through 3 relate to varying degrees of nonoral feeding; levels 4 through 7 relate to varying degrees of oral feeding without nonoral supplementation. Its validity and reliability have been established (Crary et al., 2005). In fact, Crary et al. suggest that other assessment scales (e.g., Dysphagia Outcome and Severity Scale (O’Neil, Purdy, Falk, & Gallo, 1999) and Functional Outcome Swallowing Scale for Staging Oropharyngeal Dysphagia; Salassa, 1999) are less valid or reliable. Moreover FOIS was assessed retrospectively on the basis a chart review (Crary et al., 2005; Hansen et al., 2008). FIOS has also been used in populations other than stroke patients, such as patients with head and neck cancer (Crary, Carnaby (Mann), Groher, & Helseth, 2004). A partially modified version has been used in patients with Zenker’s diverticulum (Adam, Paskhover, & Sasaki, 2013). FOIS score before hospitalization was estimated based on the form of food ingested. Furthermore, FOIS scores at initial assessment and at the time of transfer or discharge were estimated based on the form of food intake determined by results of several tests and examinations and clinical symptoms. We adopted this scale given its adequate reliability and validity to assess changes in swallowing function and applicability across various diseases. 2.3. Statistical analysis The Wilcoxon signed-rank test was used for within-group analyses and the Mann–Whitney U and Fisher’s exact tests were used for analyses between the PO-only and TF-dependent groups. SPSS11.0J for Windows (SPSS Inc, Chicago, IL, USA) was used for statistical analysis. P < 0.05 was considered statistically significant. 3. Results 3.1. Characteristics of the PO-only group
2.2. Data collection 3.1.1. Changes in FOIS score (Fig. 1) Information regarding past medical history, age, care level (Tamiya et al., 2002), number of days to initial assessment, length Table 1 Reasons for hospitalization. Respiratory Orthopedic Gastrointestinal Cerebrovascular Circulatory Endocrine
11 patients (pneumonia, 10; acute bronchitis, 1) 4 patients (femoral neck fracture, 3; femoral fracture, 4 patients (acute gastroenteritis, 2; gastric ulcer, 1; choledocholithiasis, 1) 2 patients (cerebral infarction, 1; hydrocephalus, 1) 2 patients (heart failure, 2) 1 patient (dehydration, 1)
The pre-hospitalization FOIS score was 7 for eight patients, 5 for one patient, and 4 for six patients. At initial assessment, the FOIS score was 5 for one patient, 4 for eight patients, and 2 for six patients, and at the time of transfer or discharge, 5 for four patients and 4 for 11 patients. The pre-hospitalization FOIS score significantly differed from the FOIS score at the time of transfer or discharge (p = 0.006; Wilcoxon signed-rank test). The FOIS score at the time of transfer or discharge significantly differed from the FOIS score at initial assessment (p = 0.016; Wilcoxon signed-rank test). The FOIS score decreased for all nine patients who had pre-hospitalization FOIS scores of 5, and did not return
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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Table 2 Comparison between groups PO-only group TF-dependent group (n = 15) (n = 9).
Age (years) Care levela FOIS scoreb Before hospitalization At initial assessment** Number of days to initial assessment Length of hospitalization (days)** Length for swallowing rehabilitation**
PO-only group (n = 15)
TF-dependent group (n = 9)
103.6 2.7 3.0 (3.0–5.0)
102.7 2.8 4.0 (4.0–5.0)
7.0 (4.0–7.0) 4.0 (2.0–4.0) 9.5 14.5 32.6 21.9 23.1 14.6
5.0 (4.0–5.0) 1.0 (1.0–2.0) 18.6 24.6 71.9 23.0 53.3 27.0
Data are expressed as mean SD or median (IQR). a Care Levels are range from the lowest (care level 1) to the most severe (care level 5) needs (Tamiya et al., 2002). Levels were determined before hospitalization. b FOIS levels 1–7. ** Significant difference in length of hospitalization and swallowing rehabilitation and FOIS score at initial assessment between groups (p < 0.01 for both). Fig. 1. Change in FOIS score at each stage (N = 15 for each evaluation). **FOIS score at pre-hospitalization was significantly lower than that at transfer or discharge (p < 0.01). *FOIS score at transfer or discharge was significantly higher than that at initial assessment (p < 0.05).
to the pre-hospitalization score. The remaining patients with a prehospitalization FOIS score of 4 maintained this score or returned to their pre-hospitalization score. 3.2. Characteristics of the TF-dependent group 3.2.1. Changes in FOIS score (Fig. 2) The pre-hospitalization FOIS score was 5 for five patients and 4 for four patients. The FOIS score at initial assessment was 2 for four patients and 1 for five patients, and at the time of transfer or discharge, 2 for one patient and 1 for eight patients. The pre-hospitalization FOIS score significantly differed from the FOIS score at the time of transfer or discharge (p = 0.006; Wilcoxon signed-rank test). The FOIS score at the time of transfer or discharge did not differ significantly from the FOIS score at initial assessment (p = 0.25; Wilcoxon signed-rank test).
of the following: cerebrovascular disease, dementia, and pneumonia. There were no other disease known to impair swallowing in both groups. 3.3.2. Age, care level, number of days to initial assessment and length of hospitalization and swallowing rehabilitation The mean age of the PO-only group was 103.6 years (SD, 2.7), and the median care level was 3.0 (IQR, 3.0–5.0). The mean number of days to initial assessment and the mean length of hospitalization and swallowing rehabilitation were 9.5 days (SD, 14.5), 32.6 days (SD, 21.9) and, 23.1days (SD, 14.6) respectively. The mean age of the TF-dependent group was 102.7 years (SD, 2.8), and the median care level was 4.0 (IQR, 4.0–5.0). Moreover, the mean number of days to initial assessment and the mean length of hospitalization and swallowing rehabilitation were 18.6 days (SD, 24.6), 71.9 days (SD, 23.0) and 53.3 days (SD, 27.0), respectively. 3.3.3. Comparison of each of the items between groups (Table 2)
3.3.1. Past medical history Two patients had no history of neurologic or respiratory disease known to affect swallowing function between the PO-only and TFdependent groups. The remainder of the patients had one or more
There were no significant differences in age, care level, prehospitalization FOIS score, or the number of days to initial assessment between the PO-only and TF-dependent groups (p = 0.48, p = 0.14, p = 0.14, p = 0.08, respectively; Mann–Whitney U test). In contrast, there were significant differences in the length of hospitalization and swallowing rehabilitation and FIOS score at initial assessment between the two groups. Specifically, compared with the TF-dependent group, the length of hospitalization and swallowing rehabilitation were shorter (p = 0.002, p = 0.006, respectively) and FOIS score at initial assessment was higher in
Fig. 2. Change in FOIS score at each stage (N = 9 for each evaluation). **FOIS score at pre-hospitalization was significantly lower relative to that of the score at transfer or discharge (p < 0.01).
Fig. 3. FOIS score frequency at initial assessment in the PO-only and TF-dependent groups (PO-only group, 15; TF-dependent group, 9). **Significant difference between PO-only and TF-dependent groups (p < 0.01).
3.3. Comparison between groups
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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the PO-only group (p = 0.0004). Moreover, the frequency of a FOIS score of 4 at initial assessment was significantly higher in the PO-only group, and the frequency of a FOIS score of 1 was significantly higher in the TF-dependent group (p = 0.0006, Fisher’s exact test; odds ratio, 0.4 (95% Confidence Interval, 0.21–0.74); Fig. 3). 4. Discussion In this study, we examined swallowing function in very elderly patients from pre-hospitalization to the time of transfer or discharge using FOIS, assessed changes in swallowing function, and evaluated the prognosis of dysphagia in very elderly patients. 4.1. Changes in FOIS score from pre-hospitalization to transfer or discharge Pre-hospitalization FOIS scores and FOIS scores at the time of transfer or discharge significantly differed between the two groups (p < 0.01). The pre-hospitalization FOIS score was 7 for eight patients in the PO-only group and oral intake became possible for all of these patients. However, FOIS scores of these eight patients at the time of transfer or discharge did not return to pre-hospitalization scores. Although statistically significant, pre-hospitalization FOIS score and FOIS score at the time of transfer or discharge may be different in a strict sense. Comparability between pre-hospitalization FOIS score and FOIS score at the time of transfer or discharge may not be correct. Though our results suggest that dysphagia in very elderly patients may be associated with poor recovery, it is impossible to relate these results in this study. Since criteria for assigning FOIS scores could have been different. Therefore, further studies are needed to evaluate swallowing function from pre-hospitalization to the time of transfer or discharge strictly. Meanwhile, Hattori et al. (2008) reported that the mode of food intake did not necessarily correlate with the swallowing abilities of homebound and institutionalized dysphagia patients. Additionally, Ekberg and Feinberd (1991) reported that swallowing studies with imaging in 56 elderly people without dysphagia symptoms revealed normal swallowing function in only 16% of them. In the present study, swallowing function was not assessed prior to hospitalization. However, the effects of aging on swallowing have been recently reported (Achem & Devault, 2005; Nogueira & Reis, 2013; Sura, Madhavan, Carnaby, & Crary, 2012), and the effects are likely to be more pronounced in very elderly people. That is, patients who had been eating a normal diet orally prior to hospitalization may have had undetected problems with swallowing to begin with. This suggests the need for a swallowing assessment system for very elderly people. 4.2. FOIS scores at initial assessment 4.2.1. FOIS scores of 1 and 4 A statistically significant difference in FOIS score at initial assessment was observed between the PO-only and TF-dependent groups (p < 0.01). The frequency of a FOIS score of 4 was significantly higher in the PO-only group, as was the frequency of a FOIS score of 1 in the TF-dependent group (p < 0.01 for both). Swallowing rehabilitation was performed for all patients with a FOIS score of 1. However, these patients refused rehabilitation or had an unstable general medical status. They showed poor progress and their FOIS score never increased. By contrast, previous studies reported that elderly dysphagia patients with a FOIS score of 3 at initial assessment recovered after swallowing rehabilitation (Bogaardt, Grolman, & Fokkens, 2009; Sun et al., 2013). Compared with the PO-only group, FOIS
score at initial assessment is lower in these groups. Although some patients with a FOIS score of 1 at initial assessment were included, oral intake was recovered in these studies. Altogether, oral intake may be recovered even if the FOIS score is 1 at initial assessment in elderly patients. These suggest that if swallowing function had not been reserved enough to obtain FOIS score of 4 at initial assessment, oral intake would become impossible in very elderly patients. Though the underlying medical condition in that studies differ from that of ours, active interventions should be performed for very elderly patients with FOIS scores 4 in the early stages of disease. Furthermore, oral intake may no longer be possible for a very elderly patient with a FOIS score of 1 at initial assessment. 4.2.2. FOIS score of 2 In the PO-only and TF-dependent groups, six and four patients had a FOIS score of 2 at initial assessment, respectively (not statistically significant). Patients in the PO-only group remained medically stable, and all six patients became capable of oral intake by the time of transfer or discharge (FOIS score of 4, five patients; FOIS score of 5, one patient). However, the FOIS score of one patient in the TF-dependent group remained unchanged, the general medical status for two patients deteriorated (one died), and the FOIS score of the remaining patient decreased to 1 because the patient refused to continue training due to worsening dementia. Thus, those in the TF-dependent group tended to have deteriorating medical status and dementia, which was not the case in the PO-only group. Although not statistically significant, a FOIS score of 2 at initial assessment may indicate that oral intake is recoverable. Thus, it may make sense to closely monitor the progress of dementia and the general condition of patients with this FOIS score. 4.3. Study limitations This study has some limitations worth noting. First, this study did not include a control group with elderly dysphagia patients. Further studies are needed to determine the difference between centenarians and the elderly patients. Second, swallowing assessment before hospitalization was not strictly performed. Further studies are still needed to examine swallowing function from pre-hospitalization to the time of transfer or discharge. Other limitations include the retrospective nature of data collection and the relatively small sample size. 5. Conclusions In this study, we examined the prognosis of dysphagia in centenarian patients. Our results suggest that oral intake can be recovered to some extent in patients with FOIS scores 4 at the time of initial assessment, but may be difficult for patients with a FOIS score of 1. Moreover, general medical status and degree of dementia are likely to influence whether oral intake can be achieved later on for patients with a FOIS score of 2 at the time of initial assessment.
Conflict of interest None declared by any author. Acknowledgements This study was supported by a Grant-in-Aid for Young Scientists (B) (23792503 and 25862074) from the Japan Society for the Promotion of Science.
Please cite this article in press as: Shoji, H., et al., The prognosis of dysphagia patients over 100 years old. Arch. Gerontol. Geriatr. (2014), http://dx.doi.org/10.1016/j.archger.2014.04.009
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