Abstract

Background and Objectives: Acute and subacute stroke patients with dysphagia are at an increased risk of malnutrition and poor hydration. This study identified associations between dysphagia severity and the feeding method objectively selected based on videofluoroscopic swallowing study (VFSS) results, and the alteration of nutritional and hydration indicators after 2 months in stroke patients. Methods and Study Design: A retrospective chart review was completed including 120 patients with acute or subacute stroke who underwent VFSS in the Department of Physical Medicine between January 2010 and May 2017. For comparative analysis, we investigated the participants’ dysphagia severity using VFSS, nutrition and dehydration indicators, such as albumin, total protein, erythrocyte sedimentation rate, C-reactive protein, blood urea nitrogen, and creatinine at the time of admission and 2 months after admission. Results: The degree of poor hydration status increased with increasing severity of dysphagia at both time points. Furthermore, at 2 months after admission, as the severity of dysphagia increased, the frequency of malnutrition also increased. Albumin was significantly reduced in older adults with the same severity of dysphagia, especially in the aspiration group. Acute and subacute stroke patients with severe dysphagia had higher malnutrition and dehydration indicators 2 months after admission. Conclusion: Therefore, it is important to carefully monitor malnutrition and dehydration status in elderly patients with the same severity of dysphagia.

1. Introduction

It is well known that stroke is a leading cause of morbidity and mortality worldwide. Complications following stroke include infections, venous thrombosis, increased intracranial pressure, stroke recurrence, spasticity, depression, dysphagia, and malnutrition ^{1, 2}.

Dysphagia is commonly documented after stroke and has a negative impact on the oral intake of foods and liquids, potentially leading to malnutrition and dehydration ³. Compared with pneumonia, compromised nutrition, hydration, and poor quality of life caused by post-stroke dysphagia have attracted less clinical and research attention. In a systematic review by Foley et al., it was reported was the likelihood of malnutrition increased in patients with dysphagia, particularly in the post-acute phase ⁴. Patients with dysphagia are often afraid to eat or drink due to choking, and this may lead to dehydration and malnutrition ⁵. In clinical settings, modified consistency is commonly used to maintain oral intake, or a nasogastric (NG) tube or percutaneous endoscopic gastrostomy (PEG) tube is used to restrict oral intake. However, recent studies have noted that patients who consume modified food or thickened liquids may have inadequate intake of food or fluid ⁶.

A previous study showed that dehydration appears to be common in hospitalized stroke patients and is associated with severe stroke and poor outcomes at hospital discharge ⁷. A recent study reported that patients on clinically modified diets and liquids may be at increased risk of poor hydration during the post-acute stroke period. Furthermore, tube feeding was also significantly associated with poor hydration status at discharge ³.

The prevalence of malnutrition following stroke varies widely, with the reported frequency of malnutrition ranging from 6.1% to 62% ⁸.This might be due to varying definitions and prevalence of malnutrition. Malnutrition in hospital patients is a common and often unrecognized problem, especially in the elderly ^{9, 10}. Recently, an increased prevalence of swallowing difficulties in older healthy adults in the absence of disease has been noted. This disorder has been termed presbyphaigia ¹¹. For this reason, post-stroke dysphagia can occur more frequently in elderly patients. According to prior research, elderly patients with acute stroke have lower serum albumin levels ¹².

Numerous treatment guidelines for patients with acute stroke have been published, but there has been little clinical attention regarding nutritional support. Moreover, only a few studies have focused on the nutritional requirements of patients with stroke ¹³. Evaluation of nutritional indicators in acute stroke patients is important to prevent malnutrition, which is related to an increased hospitalization period and decreased functional improvement during rehabilitation ¹⁴.

In a previous study, strong predictors of malnutrition upon admission were the use of tube feeding and dysphagia ⁸. However, in previous studies concerning nutrition and feeding status, the selected feeding method, i.e., oral or tube feeding, was based on the clinical symptoms of dysphagia or a simple bedside screening test. In the neurorehabilitation process, the videofluoroscopic swallowing study (VFSS) is considered the gold standard for diagnosis of post-stroke dysphagia.

Few studies have investigated the simultaneous effects of feeding methods and age on nutritional status. The primary aim of this study was to identify associations between dysphagia severity and the feeding method objectively selected based on VFSS results, and the alteration of nutritional and hydration indicators after 2 months in stroke patients. Also, we hypothesized that the change in nutritional and hydration status could show different trends according to age. There may be a greater impact of nutritional status in the older age group because of vulnerability and reduced reserves for body function. The secondary purpose of our study was to analyze the effects of age on nutritional and hydration status in patients with the same feeding method.

2. Materials and Methods

In the current study, we collected data from electronic medical records after approval was obtained from the Institutional Review Board of our institution (approval number RM17-09). The requirement for informed consent was waived due to the retrospective design of the study.

Acute and subacute patients with stroke who underwent VFSS in the Department of Physical Medicine between January 2010 and May 2017 were included in this study. VFSS was performed to screen for dysphagia or when a patient was referred for evaluation of swallowing difficulty. Diagnosis of stroke was limited to cases in which cerebral infarction or hemorrhage had been verified by computed tomography (CT) or magnetic resonance imaging (MRI).

Inclusion criteria were as follows: (1) all patients were diagnosed using MRI or CT, (2) completed the VFSS between 2010-2017, and (3) had laboratory tests conducted on the day of onset and 2 months later, including total protein, albumin, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), blood urea nitrogen (BUN), and creatinine. Exclusion criteria were as follows: (1) history of another neurologic disorder that could be the cause of dysphagia, such as Parkinson’s disease, brain tumor, advanced dementia, multiple sclerosis, inflammatory myopathies, myasthenia gravis, and muscular dystrophies; (2) missing medical records, brain imaging study, or laboratory results; and (3) duration between stroke onset and VFSS evaluation exceeded 30 days. Ultimately, a total of 120 patients satisfied the criteria and were chosen for analysis. Data from these patients were collected retrospectively.

The medical records and test results of patients were reviewed retrospectively. Patients’ demographic and clinical characteristics were recorded, including age, sex, brain lesion laterality (left or right), and duration between onset of stroke and VFSS evaluation (number of days). Laboratory data relating to nutritional status (albumin, total protein, ESR, and CRP level) and hydration status (blood urea nitrogen-to-creatinine (BUN/Cr) ratio) were recorded.

We defined malnutrition cut-off values for each nutritional indicator by referring to previous studies; the following cut-off values were used: serum albumin <3.5 g/dL, total protein <6.0 g/dL and body mass index (BMI) ≤18.5 kg/m². We defined the hypohydration cut-off value as BUN/Cr value >20:1 ^{15, 16, 17, 18, 19}.

Each VFSS was performed by physicians of the Department of Rehabilitation Medicine following a modified version of Logemann’s procedure ²⁰. Briefly, patients were seated, and fluoroscopy was performed as the patients swallowed barium mixed with juice, yogurt, thick gruel, or rice. For juice and yogurt, 2 different volumes were used (2 mL and 5 mL). Each food type was mixed with undiluted liquid barium to ensure proper bolus observation during the fluoroscopy procedure.

In the oral phase, functions such as lip sealing, bolus formation, mastication, early spillage, oral remnants, and oral transit time of the bolus were assessed. In the pharyngeal phase, laryngeal elevation and aspiration/penetration of the respiratory tract were assessed. The pharyngeal transit time of the bolus and swallowing response time until the swallowing reflex was initiated were also recorded. Each individual finding was assessed based on the presence or absence of an abnormal finding. When the food entered the respiratory tract but did not pass into the true vocal fold, it was recorded as penetration, whereas when the food passed into the true vocal fold, it was determined to be aspiration.

All patients were divided into 3 groups according to the penetration-aspiration scale (PAS) and age. PAS was determined based on VFSS results. Dysphagia severity was classified using the PAS score, as follows: the aspiration group was defined as a PAS score between 5 and 8, the penetration group as a PAS score from 2 to 4, and the normal group was defined as a PAS score of 1. In each group, patients were divided into subgroups according to age: <65 years, 65-75 years, and >75 years.

The data were analyzed using the Statistical Package Software for Social Sciences Version 18.0 (SPSS Inc., Chicago, IL, USA). The basic information of participants was presented using descriptive statistics. One-way ANOVA, Kruskal-Wallis, and Mann Whitney-U tests were used to analyze differences in their clinical characteristics, albumin, total protein, ESR, and CRP levels to indicate nutritional status, and the BUN/Cr ratio for hydration, measured at admission and 2 months. Furthermore, we calculated the proportion of patients with dehydration and malnutrition according to dysphagia severity using the linear by linear association method. Statistical significance was defined as p<0.05.

3. Results

Among 120 patients, 70 were men and 50 were women. The mean patient age was 65.95±12.18 years. The mean duration from onset of stroke to VFSS was 18.28±9.99 days. Lesions were focused in the supratentorial region (n=106) and the infratentorial region (n=14). The demographic and clinical characteristics of all subjects are shown in Table 1.

Differences between patients without penetration or aspiration (group I), patients with penetration (group II), and patients with aspiration (group III) are shown in Table 2. There were no statistically significant differences between the groups according to swallowing function by VFSS in age, height, body weight, BMI, lesion of stroke, and duration from onset of stroke to VFSS.

Table 3 shows the comparison between the total protein, albumin, BUN/Cr, ESR, and CRP level on the day of onset and 2 months after onset according to dysphagia severity. No significant difference was found between groups. Using the linear by linear association method, as the severity of dysphagia increased, the degree of poor hydration status, as measured using BUN/Cr ratio, increased on the day of onset and 2 months after onset (Table 4). Furthermore, as the severity of dysphagia increased, the frequency of malnutrition increased 2 months after onset only, not on the day of onset.

Table 3 shows the comparison between the albumin level, total protein, CRP, ESR, and BUN/Cr ratio on the day of onset and 2 months after onset in the subgroups according to age with the same severity of dysphagia. As expected, albumin was significantly reduced in older adults with the same severity of dysphagia. In group I, there was no difference in albumin level according to age at the time of admission, but 2 months later, there was a significant difference (p<0.001) in albumin level according to age. Albumin levels were lower in older groups. In group II and group III, no age differences were observed in albumin, total protein, ESR, CRP, and BUN/Cr ratio both at admission or after 2 months.

4. Discussion

The present study demonstrated that the older age group had a lower albumin level and that the frequency of malnutrition increased as the severity of dysphagia increased 2 months after admission for stroke. In particular, the older age group had a lower albumin level in the dysphagia group who were fed via a tube 2 months later. The frequency of dehydration increased as the severity of dysphagia increased at both admission and after 2 months. To the best of our knowledge, few studies have evaluated the simultaneous effect of feeding methods and age on the nutritional and dehydration status of stroke patients classified by dysphagia severity based on VFSS results.

During the rehabilitation period after acute stroke, more than half of patients experience a swallowing disorder and have an increased risk of malnutrition. However, establishing a patient’s true nutritional state can be difficult, as there is not a universally accepted definition of malnutrition or a gold standard for nutritional assessment. Furthermore, it remains unclear whether malnutrition was pre-existing at the time of the initial assessment or had developed as a consequence of stroke, as the pre-stroke nutritional status of patients from previous studies is unknown ²¹.

Previous studies have commonly placed a strong emphasis on equating low albumin levels to malnutrition. Hepatic proteins, such as albumin, prealbumin, and transferrin are commonly used as markers to evaluate nutritional status. Serum albumin level can be a fair marker of nutrition status in the absence of inflammation and infection. Given its long half-life, it may only be ideal for long-term care or rehabilitation settings ⁸. In our study, we used albumin, total protein, ESR, and CRP as nutritional markers. A recent study showed that nutritional indicators drastically change in patients with severely impaired swallowing ability between onset and 7 days after admission ¹⁴. However, Foley et al. reviewed 8 studies with the aim of clarifying the relationship between nutrition status and dysphagia in both the acute and rehabilitation stages following stroke. Of the included trials, 5 were conducted within the first 7 days following stroke, while 3 were conducted during the rehabilitation phase. In subgroup analysis, the odds of malnutrition were significantly increased during the rehabilitation stage but not during the first 7 days of hospital admission ⁴. In this study, we investigated changes in the nutritional status of the 3 groups during the 2-month rehabilitation period. Similar to the results from Foley et al., the frequency of malnutrition was found to increase after 2 months from admission for stroke.

In particular, in our study, the older age group had a lower albumin level in the dysphagia group with aspiration 2 months later. Recently, an increased prevalence of swallowing difficulties in older healthy adults in the absence of disease has been noted ¹², as swallow physiology changes with advancing age. Reductions in muscle mass and connective tissue elasticity result in loss of strength and range of motion. Over time, these factors can contribute to an increased frequency of swallowed material penetrating into the upper airway and greater post-swallow residue during meals. Beyond subtle motor changes, age-related decrements in oral moisture, taste, and smell acuity may contribute to reduced swallowing performance in the elderly. Therefore, the presence of age-related disease is the primary factor contributing to clinically significant dysphagia in the elderly ²². Previous studies also reported that elderly patients with acute stroke have a lower serum albumin level. Elderly patients have an increased risk of malnutrition because of reduced nutritional reserves and prolonged hospital stays. Furthermore, older stroke patients are vulnerable to dehydration for reasons including immobility and reduced sensitivity to thirst due to old age. Moreover, the clinical signs of dehydration are also not as reliable in older patients ¹⁵. Therefore, it is important to carefully assess the nutritional status of elderly patients.

Dehydration is also associated with recurrent strokes, venous thromboembolism, and increased mortality risk ⁷. Based on the BUN/Cr level, the prevalence of dehydration in this study was high at baseline (36.4%) and even higher at discharge (51.5%). Beyond that result, the degree of dehydration reflected in the BUN/Cr levels was significantly greater in patients with dysphagia than in those without dysphagia at baseline and at discharge. In previous studies, tube fed patients were expected to be sufficiently hydrated and may be over hydrated in some situations ^{23, 24}. However, Leibovitz et al. reported that 18% of tube fed, long-term care patients demonstrated multiple markers of dehydration ²⁵. Additionally, a recent study revealed that tube fed patients had higher BUN/Cr values at discharge and that this was significantly associated with the number of tube fed days ³. Therefore, it is not a surprising result that the frequency of dehydration increased with increasing severity of dysphagia at both admission and after 2 months in our study. Since patients with dysphagia demonstrate dehydration at admission and BUN/Cr levels increase (though not significantly) during hospitalization, acute ischemic stroke patients with dysphagia should be considered at risk for dehydration upon admission and monitored for adequate hydration during hospitalization.

In this study, we used VFSS as an assessment tool; this requires a higher level of patient consciousness and cooperation to complete than a simple water swallow test, which can be done at the bedside easily but can miss up to 50% of patients with aspiration ²⁶. Therefore, defining dysphagia severity based on objective VFSS results was one of the strengths of our research.

There are several limitations to this study. First, the retrospective nature of this study prevented the control of confounding factors, such as lesion size and stroke severity. Second, VFSS could not be performed at the same time from admission for each patient, and other factors could not be controlled. Third, we did not evaluate the parenteral fluid supplementation, which may have directly impacted hydration status.

Given these limitations, the study had multiple strengths. First, we enrolled not only patients with hemispheric lesions, who tended to report lower dysphagia incidence (39% to 40%), but also patients with mixed lesions (51% to 55%) ⁹. Second, this study assessed the presence of dysphagia after stroke in acute stroke patients with cortical lesions as well as brain stem lesions using VFSS, which is the most common instrumental test to assess swallow function and is often used as the gold standard. Third, our study showed changes in nutritional and hydration status according to age and dysphagia severity over a 2-month period. Given the serious consequences of malnutrition and inadequate hydration in these patients with dysphagia, clinical strategies to appropriately support nutrition and enhance hydration have potential to significantly modify and improve acute stroke care guidelines.

5. Conclusion

In this retrospective study, there was no correlation between dysphagia severity and malnutrition frequency at admission. However, as the severity of dysphagia increased at both admission and after 2 months, the frequency of dehydration increased. In clinical settings, we suggest that hydration status should be monitored carefully in patients with dysphagia. In addition, this study demonstrated poor nutritional status of patients with severe dysphagia in the older age group after 2 months. Therefore, it is important to evaluate the presence of swallowing disorders in stroke patients and monitor nutritional and hydration status carefully, especially in elderly patients.

Acknowledgements

None.

Conflict of Interest and Funding Disclosure

The authors have no potential conflicts of interest to declare with respect to the research, authorship and/or publication of this article.

References