Abstract
A growing concern in patients affected by Alzheimer’s disease (AD) is dysphagia, or swallowing impairment, which leads to malnutrition, dehydration, weight loss, functional decline and fear of eating and drinking, as well as a decrease in the quality of life. Thus the diagnostic assessment of dysphagia in patients with AD is imperative to ensure that they receive effective management, avoiding complications, and reducing comorbidity and mortality in such a growing population. Dysphagia management requires a multidisciplinary approach considering that no single strategy is appropriate for all patients. However, evidence for clinical diagnostic assessment, interventions, and medical management of dysphagia in these patients are still limited: few studies are reporting the evaluation and the management among this group of patients. Here we analyzed the most recent findings in diagnostic assessment and management of swallowing impairment in patients affected by AD.
INTRODUCTION
Alzheimer’s disease (AD) is the most prevalent cause of cognitive impairment, representing about 60% – 70% of all cases of dementia [1]. Clinically AD is a severe chronic neurodegenerative disorder characterized by a progressive cognitive impairment and functional decline. Along with population aging, AD is becoming one of the most important health and socioeconomic problem [1–3]. In 2012 the prevalence, significantly higher in women compared with men [3], was approximately 24 million worldwide while the frequency is expected to double every 20 years until 2050 [4, 5]. At present, one in nine people aged 65 and older has AD and more than one in three people aged 85 and older is affected [4]. By 2050, Alzheimer’s disease is predicted to affect 1 in 85 people worldwide, representing the most common cause of dementia among old age [5].
Patients affected by AD progressively lose their cognitive functions until the end-stage of disease characterized by the complete loss of body functions control [6, 7]. During illness, patients may start to have difficulty in swallowing leading to the progressive reduction in eating [8]. The deglutition process is significantly altered, resulting in delayed oral transit time trend and pharyngeal response duration [9]. Moreover, the incapability to recognize food visually, oral-tactile agnosia, swallowing and feeding apraxia [9], form a hindrance to food intake that can progressively lead to a wide spectrum of adverse consequences, ranging from weight loss, dehydration, malnutrition, and congestion as well as recurrent respiratory tract infections and reduced quality of life [10–12]. Thus, it is necessary to detect the initial signs of dysphagia and manage them at the earliest stages.
DYSPHAGIA, AGE-RELATED FACTORS AND AD
Swallowing is the efficient and safe movement of a bolus from the mouth to the stomach without aspiration. Normal swallowing involves the coordinated and synchronized contraction of muscles in the oropharynx, larynx, and esophagus regulated by the somatic-voluntary nervous and autonomic nervous system [10]. Dysphagia is the term used to describe the subjective sensation of difficulty or abnormality in moving food from the mouth to the stomach, including problems with behavioral, sensory, and preliminary motor acts in preparation for the swallow, as well as cognitive awareness of the upcoming eating situation, visual recognition of food, and all of the physiologic responses to the smell and presence of food. Dysphagia represents a common problem in the older population: age-related changes in swallowing physiology as well as age-related diseases are predisposing factors for dysphagia among old age subjects. In fact, swallow physiology changes along with aging: The muscle mass significantly decreases and connective tissue progressively loses its elasticity leading to the loss of strength and range of motion [13]. These age-related changes negatively impact the effective and efficient flow of swallowing materials from the mouth to the stomach. Oral preparation of food and material transits through the upper gastrointestinal tract become slower. Over time, these changes can contribute to the increased frequency of swallowed material penetrating into the upper airway and greater post-swallow residue during meals. Beyond motor changes, age-related decrements in oral moisture, taste, and smell acuity may contribute to reduced swallowing performance.
In addition to older age, a variety of other health conditions can contribute to the development of dysphagia in this population, including neurological diseases, stroke, and dementia. Thus, advanced age together with cognitive disorders inevitably predispose to dysphagia susceptibility. The prevalence of dysphagia in moderate to severe AD is up 84% to 93% [7–14]. However, dysphagia may also occur early in AD associated with functional changes in the cortical swallowing network as measured using functional magnetic resonance imaging [15, 16]. Oropharyngeal swallowing abnormalities, including aspiration, have been reported to be as high as 45% among institutionalized persons with dementia [10]. The most of patients with AD presents a gradual regression in appetite, food intake, feeding and alimentation skills in addition to cognitive and physical decline, which places these individuals at increased risk for aspiration [7]. This condition is serious and can lead progressively to death. Furthermore, swallowing difficulties cause weight loss, malnutrition and dehydration creating a vicious circle worsening the cognitive and functional impairment in this patients group.
Thus, AD patients, mostly elderly and affected by multiple diseases, may become dependent for feeding, which further impacts negatively on their quality of life [13]. Weight loss can reflect the decreased nutritional status that increases the patient’s risk of opportunistic infections such as pneumonia, which represents the most common cause of mortality in patients with dementia [17]. Dementia, dysphagia, and related feeding impairments can lead to nutritional deficit, which, in turn, contributes to pneumonia and mortality. Thus the diagnostic assessment of dysphagia in AD patients is imperative to ensure that patients receive effective dysphagia management that is tailored to their needs.
DIAGNOSTIC APPROACHES
The assessment of dysphagia in AD patients can be performed with a wide variety of methods; however, there are two methods currently considered the gold standard: 1) the clinical evaluation of dysphagia or feedings impairments, and 2) the instrumental swallowing assessment by videofluoroscopic swallow studies (VFSS) or fiberoptic endoscopic evaluation of swallowing (FEES). Occasionally an electromyography (EMG) after water injection into the pharynx has been reported [18].
Clinical evaluation of dysphagia
The clinical swallow evaluation (CSE) represents a wide, swallowing assessment based on both questionnaires on swallowing problems (appetite modification, food predilection and other nutritional behaviors) administered to “caregivers” of patients with AD, and a motor and sensory exam of all oral structures involved in bolus formation including the evaluation of swallowing of solid and liquid foods at various consistencies [8]. Oral praxis, laryngeal elevation initiation, pharyngeal and gag reflexes, dysphonia and swallow attempt are some of the evaluated parameters. Collectively, the prevalence estimates of dysphagia in AD based on clinical assessments are lower than estimates based on instrumental swallowing assessments.
Volicer and colleagues [18] reported a prevalence of 32% for swallowing impairments in AD patients living in a long-term care facility [19]. Similarly, a dysphagia prevalence of 45% among institutionalized AD individuals has been described [20], suggesting a correlation with death due to aspiration pneumonia. Particularly, among the common evaluated symptoms and signs suspicious for aspiration risk (like cough after swallowing, dysphonia, and abnormal gag reflex) [21], only the voice quality assessment (dysphonia) resulted of limited specificity in the diagnosis. In this regard, Horner and colleagues [7] demonstrated an abnormality of voice quality assessment in 52% of AD patients evaluated with CSE. As far as the dysphagia’s time of onset based on CSE, strong evidences document dysphagia in later stage of AD [22]. However, a study [23] also described swallowing disruption in all stages throughout AD evolution, with an upward linear trend related to the advanced stages. Accordingly, another study [24] found signs of dysphagia in moderate to severe AD, suggesting that behavioral eating difficulties may occur in all stages of AD. Strikingly, the severity of dysphagia may be related to the AD advanced stages, even if such an association is still unclear. Wada and colleagues [25] reported that subjects with severe AD demonstrated greater pharyngeal swallow delay than those with mild and moderate AD.
A comprehensive geriatric assessment (CGA) should also be considered as a diagnostic tool for the diagnosis of dysphagia in AD patients [26]. CGA is defined as a multidisciplinary diagnostic process that identifies medical, psychosocial, and functional limitations in older persons in order to develop a coordinated plan to maximize overall health with aging. CGA is based on the assumption that a systematic evaluation of older persons by a team of health professionals may identify a variety of treatable health problems and lead to better outcomes. Dysphagia assessment in older subjects with AD is best provided by the multidisciplinary team approach because of the complexities and interrelated nature of their needs. A multidisciplinary team working together may ensure a comprehensive geriatric approach in relation to dysphagia management. A coordinated approach is essential for patients with dementia to ensure consistent transfer of care between different care settings.
Instrumental swallowing assessment: Videofluoroscopic swallow studies
VFSS represents a radiological procedure which allows to explore the impaired oral and pharyngeal stages of swallowing administering a radio-opaque material barium mixed with liquids and foods of varying consistencies. The analyzed parameters are the time of bolus preparation and the oral transit time as well as the pharyngeal swallows initiation time, the reduced hyolaryngeal excursion, the laryngeal penetration and tracheal aspiration [27]. The prevalence of dysphagia in AD based on the VFSS is higher as compared with other diagnostic assessment methods, accounting in 84–93% of moderate to severe AD patients [7, 9]. Mild AD patients as compared with age-matched healthy controls had significant differences in terms of prolonged duration as regard the oral transit time, the swallowing pharyngeal phase and the total swallow time [7, 9]. Furthermore Humbert [15] described a statistically significant in effective hyoid and laryngeal elevation movements in AD patients with mild dementia (MMSE score 23) as compared with healthy controls (MMSE score 28). The disruption of oral bolus preparation as well as the starting swallowing phase might allow the bolus to enter in unprotected airway, with higher aspiration risk. Interestingly the aspiration incidence can be related to the AD in advanced stages. In the prospective study by Horner and colleagues [7] patients with severe AD showed an incidence of aspiration of 44% as compared with moderate AD patients (12,5% ), resulting the oral praxis and the global videofluoroscopic examination score significantly correlated with severity of dementia.
Instrumental swallowing assessment: Fiberoptic endoscopic evaluation of swallowing
Endoscopic examination provides information on the assessment of larynx and soft palate mobility and the evaluation of secretion using a flexible fiberoptic scope. It can also be used to indirectly assess the oral preparation, oral transit, and pharyngeal phases of swallowing [28]. One of the most significant advantages of endoscopic assessment of swallowing is the possibility of providing results for foods of different consistencies and that it can be performed bedside thus increasing its range in the diagnostic and follow-up settings [28]. Nevertheless, only one study has evaluated the employment of this diagnostic tool to investigate dysphagia in AD patients [29]. The purpose of this retrospective study conducted in the acute-care setting of patients with altered mental status as a result of such different etiologies, including dementia, was to investigate if answering specific orientation questions (What is your name? Where are you right now? What year is it?) and following specific single-step verbal commands (Open your mouth. Stick out your tongue. Smile) are predictive of aspiration status prior to dysphagia testing with FEES. The odds of liquid aspiration were 31% greater for subjects not oriented. Similarly, if orientation and command-following are impaired, the clinician should be aware that the odds of aspiration for any oral intake were 69% . This may help identify subjects at risk for swallowing impairment by means of orientation questions and simple verbalcommands [29].
Instrumental swallowing assessment: Electromyography and other instrumental assessments of swallowing
Considering that deglutition is a complex action involving twenty-six muscles and five cranial nerves, electromyography, a well-known diagnostic method, would appear especially suitable for screening and early diagnosis of dysphagia, since it provides information on the timing of selected muscle contraction patterns [30] and on the amplitude of muscles’ electric activity [31, 32] during swallowing. Nevertheless, due to the lack of standard requirements that negatively impacts the value of this noninvasive radiation-free diagnostic tool, only two reports dealing with cough/swallowing reflexes in patients with dementia are reported in medical literature [25, 33]. In a comparative study, Mizushima and colleagues [33] found a lower response rate difference of swallowing reflex as well as cough reflex between patients with dementia (vascular type dementia and AD dementia) and age-matched healthy controls, and between vascular and Alzheimer types of dementia. On the other hand, Wada and colleagues [25] showed a significantly poorer swallowing reflex rate in severe AD patient group as compared with mild and moderate AD group. Although the videofluoroscopy combined with manometry, videofluoromanometric assessment significantly increased the ability to investigate the dysphagia, there are not published data of its employment in patients with AD [34].
THERAPEUTIC INTERVENTIONS
The presence of a strong relationship between swallowing ability, nutritional status, and health outcomes in AD patients suggests the importance of dysphagia management in such a population. Successful swallowing interventions not only benefit individuals with reference to oral intake of food/liquid, but also have extended benefits to nutritional status and prevention of related morbidities such as pneumonia. A variety of dysphagia management tools are available depending on the characteristics of swallowing impairment and individual patient. The main studies evaluating management of dysphagia in patients with AD are summarized in Table 1.
Diet and postural modifications
Despite the studies investigating the effect of various therapies on the outcomes of dysphagic AD patients are poor, the modification of the consistency of food may represent an effective solution to improve the dysphagia and to avoid aspiration. Chouinard and colleagues [35] demonstrated the decrease of the aspiration rate in AD patients fed with honey-thickened liquids compared to thin or nectar-thickened liquids. Similarly, a randomized clinical trial showed that demented patients aspirated more with a thin-liquids and nectar-thickened liquids than honey- thickened liquids [36]. However, Robbins and colleagues [37] showed no statistically significant difference in the incidence of pneumonia between nectar-thickened and honey- thickened liquid feeding groups in patients with a diagnosis of AD, reporting instead a decrease in the overall incidence of pneumonia (20–40% ) compared to the expected rate in AD patients. Another randomized controlled study [38] investigated also the feasibility of cervical spine mobilization by physiotherapists in individuals with severe AD, altered neck posture, and dysphagia, evaluating the “dysphagia limit” (the maximum volume of water that can be swallowed in a single movement). After a one-week treatment of three cervical spine mobilization sessions of 20 minutes, a significant improvement in swallowing capacity was observed. Indeed, a more recent prospective cohort study [39] showed that a feeding intervention among AD patients with dysphagia significantly improved patient’s food intake, and increased eating and swallowing ability. The feeding intervention consisted of appropriate assistance, patient monitoring, psychological care, and nursing care after eating.
Enteral feeding
Enteral feeding in patients with advanced dementia is controversial. The clarified benefits of tube-feeding by physicians include improved survival, better nutritional status, and reduced risk of complications are hindered by numerous studies that fail to demonstrate the accomplishment of these outcomes [40–42]. Kuo and colleagues [43] reported that in patients with advanced dementia the majority of feeding tube positioning were requested in an acute care setting, with a one-year follow up mortality of 64.1% , a median survival of 56 days, and a significant rate of health care utilization post insertion (average hospitalization of 9 days). Similarly, it has been reported an aspirated pneumonia rate of 58% in enterally fed demented patients compared to 16% of those fed orally [44]. However, an important limitation of these studies is the non-categorizations of demented patients, thus we cannot rule out the difference related to the various types of dementia. Finally an interesting retrospective study showed a higher 30-day mortality rate and 12 month mortality rate for enteral fed with percutaneous endoscopic gastrostomy (PEG) demented patients compared to other patients (oropharingeal cancer, stroke and other neurological injuries) [45].
Pharmacologic therapy
Recently, dopamine agonists and angiotensin-converting enzyme inhibitors (ACEIs) were reported to be effective at preventing aspiration pneumonia through increasing substance P levels, which enhances swallowing and cough reflexes [46]. Yamaguchi and colleagues [47] reported three cases where the use of dopamine agonists and angiotensin converting enzyme inhibitors exhibited prolonged oral intake for a period of seven months up to two years. However, evidence of their utility is still poor, and further studies are needed to validate and support this data.
CONCLUSION AND FINAL REMARKS
Normal swallowing involves a series of complex, coordinated muscular movements, which are directed by the brain and require participation of the mouth, throat, and esophagus. Dysphagia is a common problem in patients with AD, leading to negative health outcomes, morbidity, and mortality, thus the early identification as well as the correct management represents the best strategy to avoid its complications. However, still limited is the evidence available for clinical diagnostic assessment, interventions, and medical management. Comprehensive feeding interventions may improve food intake, eating compliance and nutritional status in AD patients with dysphagia and may prevent further decline in swallowing functions.
DISCLOSURE STATEMENT
Authors’ disclosures available online (http://j-alz.com/manuscript-disclosures/15-0931r1).
