Frequency and Associated Factors of Dysphagia Diagnosed by Videofluoroscopic Swallow Study in Patients with Fragility Hip Fracture

Abstract

Background

Dysphagia after hip fracture is a common disease that causes malnutrition and aspiration pneumonia, which aggravate treatment outcome of patients. Therefore, the purpose of this study was to assess (1) the prevalence of dysphagia in elderly patients who underwent hip fracture surgery using videofluoroscopic swallow study (VFSS), (2) accuracy of screening test compared to VFSS, and (3) relationship between dysphagia and several factors, including sarcopenia.

Method

A total of 72 patients over the age of 60 who underwent a surgery for fragility hip fracture from February to September 2019 were included in this prospective study. Gugging Swallowing Screen (GUSS) and VFSS were performed in all patients to assess the swallowing function. Sarcopenia, history of various diseases, nutritional status, bone mineral density, and Koval grade, which can measure preoperative gait ability, were assessed to identify factors associated with dysphagia.

Results

VFSS results showed diagnosis of dysphasia in 55 (76.4%) patients, and penetration and airway aspiration were observed in 30 (41.7%) and 8 (11.1%) cases, respectively. The median value of GUSS was 19 points (range, 17–20) and 18 points (range, 14–20) in the dysphagia and non-dysphagia groups, respectively, and there was no statistically significant difference (p = 0.189). When dysphagia diagnosed by GUSS was compared to that of VFSS, the sensitivity and specificity of GUSS was 62% and 47%, respectively (positive predictive value 79%, negative predictive value 28%) Logistic regression analysis showed that dementia (OR10.56, CI 1.67 ~ 66.7) was associated with aspiration. SMI, grip strength, and sarcopenia were not associated with dysphagia; however, preoperative Koval grade was a factor that was associated with dysphagia (OR 2.36, CI 1.01–5.55).

Conclusions

GUSS showed mild dysphagia or normal findings in most patients, and the accuracy was not high. Therefore, VFSS is recommended to diagnose dysphagia and prevent complications for fragility hip fracture patients with a decreased gait ability who are likely to develop dysphagia.

Background

Fragility hip fracture in elderly patients is a serious disease that is associated with excess mortality.[1, 2] In particular, aspiration pneumonia is thought to be a major cause of increased mortality in this population; long-term intensive care, malnutrition, and delayed surgery after hip fracture are known to increase post-operative aspiration pneumonia.[3–5] Therefore, rapid surgery and sufficient nutrition after injury are important to prevent aspiration pneumonia.

Normal swallowing is essential for sufficient nutrient intake; it consists of a series of processes in which solid and liquid foods are delivered from the mouth to the stomach requiring approximately 50 pairs of muscles and various nerves working in combination.[6] Swallowing can be divided into 3 major phases: oral phase, pharyngeal phase, and esophageal phase. Dysphagia can occur at any of the three stages, causing delays and difficulties in swallowing, and there are many causes of dysphagia, one of which includes aging.[7] In general, oropharyngeal dysphagia refers to oral and pharyngeal dysphagia, excluding disorders such as esophageal stenosis or esophageal dyskinesia, which is classified as esophageal dysphagia.[8] Elderly hip fracture patients are known to have a high prevalence of dysphagia and this can lead to aspiration pneumonia, prolonged duration of hospitalization, and increased mortality and medical costs.[9, 10]

Sarcopenia is defined as a decrease in muscle mass, muscle strength, and physical activity by aging and other causes. It has been recently registered in the 10th clinical revision of the International Classification of Diseases (ICD) [11], and the European Working Group on Sarcopenia in Older People (EWGSOP) and the Asian Working Group for Sarcopenia (ASWG) suggested new diagnostic criteria. The recently revised diagnostic criteria by ASWG are: muscle mass of less than 7.0 kg/m² in men and 5.4 kg/m² in women by Dual Energy X-ray Absortiometry (DEXA), grip strength of less than 28kg in men and 18kg in women, and a 6m-gait speed of 1.0m/s.[12, 13] A decrease in muscle mass only, in muscle mass and muscle strength, and in muscle mass, muscle strength, and physical activity is defined as presarcopenia, sarcopenia, and severe sarcopenia, respectively.[14] Sarcopenia affects gait and physical activity, which leads to the increased hip fractures and negatively affects senility and mortality in elderly patients.[15, 16] In particular, the prevalence of sarcopenia in hip fracture patients is higher than that in healthy elderly people, and although there are differences in studies, sarcopenia is prevalent in 17–58% of hip fracture patients.[17–19]

Recent studies have reported on the relationship between sarcopenia and dysphagia, showing that dysphagia leads to insufficient intake of nutrients, which aggregates sarcopenia that further worsens dysphagia in a vicious cycle.[20, 21] Recently, dysphagia that occurs with systemic sarcopenia was named as sarcopenic dysphagia. Diseases and surgeries such as hip fractures that affect the systematic status of patient’s entire body lead to a decrease in the functional capacity of patients, which can weaken the swallowing actions and cause dysphagia.[7] The rate of dysphagia is already high in elderly patients admitted to hospitals, and aggravation of sarcopenia after hip fracture was reported as a risk factor for dysphagia.[22]

In this regard, the purpose of this study was to assess (1) the prevalence of dysphagia in elderly patients who underwent hip fracture surgery using videofluoroscopic swallow study (VFSS) which is the gold standard of diagnosis for dysphagia,[23] (2) accuracy of screening test for dysphagia compared to VFSS, and (3) the risk factors for dysphagia, including sarcopenia.

Methods

1. Subjects

This prospective observational study was approved by the Institutional Review Board (IRB) of Yeungnam University Hospital (YUMC 2018-10-026), and included 72 consecutive patients over the age of 60 who were hospitalized and underwent fragility fracture surgery of the femoral neck and intertrochanteric area of the hip joint from February to September 2019 were included in this study. Those patients with atypical and pathological fractures were excluded. Additionally, patients who were previously diagnosed with dysphagia or had traumatic inability to walk at all before injury were also excluded.

2. Assessment of dysphagia

Gugging Swallowing Screen (GUSS), which is a screening test for dysphagia, was performed on all subjects by an occupational therapist who specializes in dysphagia rehabilitation. [24] It is a well-validated tests whose sensitivity and specificity were reported to be high in many studies conducted for stroke patients and recently for healthy older people.[25] GUSS consists of indirect and direct swallowing tests; in indirect swallowing test, the vigilance of the patient, cough and/or throat clearing, and saliva swallowing are observed, while in the direct swallowing test, deglutition, involuntary cough, drooling, and voice change are observed when three types of foods with different consistency, namely semisolid, liquid, solid are provided to the patient. It classifies the subjects into four levels; 0–9 points: severe dysphagia and aspiration risk, 10–14 points: moderate dysphagia and aspiration risk, 15–19 points: mild dysphagia and aspiration risk, 20 points: normal. [24]

VFSS was performed by a rehabilitation medicine doctor specializing in dysphagia rehabilitation on an average of 1 week after surgery when the patients were able to sit and showed improved general conditions, using the same protocol in all patients. The test was performed using x-ray flat panel detector system (FPD, Zexira®, Canon Medical Systems, Ōtawara, Tochigi, Japan), and fluoroscopic images were saved as a digital medium at 30 frames per second using a scan converter. Bonorex 300 injection (iohexol 647 mg/mL, Central Medical Service, Seoul, Korea) was used as the contrast medium, and the test sequence was (1) 3ml of contrast medium, (2) 5ml of yogurt and contrast medium mixture (2ml of contrast medium mixed with 10g of yogurt), (3) 5ml of banana and contrast medium mixture (2ml of contrast medium mixed with 10g of banana), and (4) 10ml of contrast medium in a cup. For the safety of the patients, the test was stopped when the second aspiration was observed at any stage, and the time of entire fluoroscopy test did not exceed 5 minutes.

Airway safety was evaluated using the Penetration-Aspiration Scale (PAS).[26] It is an 8-point scale scoring from 1 to 8 according to the severity of airway invasion of the food materials during the VFSS; a score of 1 represents no entry of material to the airway, scores of 2–5 represent penetration in which the materials enter the airway (Fig. 1a) and descend as far as the true vocal folds, and scores of 6–8 represent aspiration of the materials below the true vocal cords (Fig. 1b). The highest PAS score of any type of food tested in the VFSS was used for statistical analyses. In addition, we evaluated the swallowing status using the Functional Dysphagia Scale (FDS). It was originally developed for quantifying functional dysphagia in stroke patients[27] but it has also been used to evaluate swallowing function in patients with various diseases, including stroke, Parkinson’s disease, head and neck cancer, and patients with dysphagia due to frailty or general weakness.[28–31] Based on the aforementioned VFSS findings, dysphagia was diagnosed if any of the following three were present: 1) oral or pharyngeal delay, 2) pharyngeal residue after swallowing, and 3) penetration or aspiration at any food consistency on VFSS.

3. Assessment of sarcopenia

The lean body mass of the limbs excluding the torso was evaluated for muscle mass by using DEXA (Hologic, Marlborough, MA, USA) on the whole body about 3–5 days after surgery. The affected lower limbs were excluded as post-operative edema and metal implants decreased the reliability of the measurement results, and the lean mass of the unaffected lower extremities was measured and multiplied twice to calculate lower extremity lean body mass. This was adjusted by the square of the height to measure the skeletal muscle mass index (SM).

Muscle strength was assessed by measuring the grip strength. The posture and method of measuring the grip strength differs among studies, and thus, no standardized method is available.[32] Measurements can be made in a sitting position with the elbow bent at 90 degrees as suggested by the American Society of Hand Therapists (ASHT) or in a standing position with the elbow straightened as suggested by the Centers for Disease Control and Prevention (CDC). The patients in our study had hip fractures and difficulties standing. Therefore, the grip strength was measured as suggested by the ASHT on day 3–5 after surgery using a hydraulic grip strength meter (Jamar®, Patterson Medical Supply, Warrenville, IL, USA). The mean value of three measurements was calculated.

Assessment of physical activity was excluded as it was difficult to measure the gait speed after surgery. The above results were combined, and per the revised diagnostic criteria of AWGS, sarcopenia was diagnosed when the SMI was less than 7.0 kg/m2 in men and 5.4 kg/m2 in women and the grip strength was less than 28 kg in men and 18 kg in women.[13]

4. Assessment of risk factors for dysphagia

Residence status, respiratory and cerebrovascular diseases, motor neurological disease, dementia, autoimmune diseases, diabetes, and chronic renal failure before hospitalization were assessed to identify factors that affect dysphagia. The age and comorbidities of the patients were combined to calculate Charlson Comorbidity Index (CCI), and the patients' condition before surgery was evaluated using the American Society of Anesthesiologists (ASA) grade.[33, 34] The gait ability of the patients was assessed using Koval grade, and the grades of 1–3, 4–6, and 7 were classified as community ambulator, household ambulator, and nonfunctional ambulator, respectively.[35]

After injury, pre-operative pneumonia was assessed, and pneumonia and pressure ulcer that may occur due to long-term rest on bed were also assessed after surgery. On day 5–7 after surgery, DEXA was used to assess the bone mineral density (BMD) of the hip and spine as T-score, and albumin and vitamin D levels in the blood were checked to assess the nutritional status of the patients.

5. Statistical analysis

R software version 3.3.4 (R Foundation for Statistical Computing, Vienna, Austria) was used for statistical analysis. For continuous variables, independent t-test was performed to compare the mean and median values after normality test, and frequency analysis was performed for categorical variables by Chi-square test. Data of GUSS were entered in two-by-two table and analyzed for sensitivity and specificity using the formulas. In order to identify risk factors for dysphagia, univariate analysis was performed on each variable through logistic regression, followed by multivariate analysis including all variables with a p-value less than 0.1. Relevance was expressed as odds ratio (OR) and confidence interval (CI).

Results

1. Patients Demographics and prevalence of dysphagia

A total of 72 patients (mean age 79.58 ± 6.5 years) were included in the study during the study period. The proportion of moderate and mild dysphagia was 2.8% and 56.9%, respectively. According to VFSS findings, dysphagia was diagnosed in 55 cases (76.4%), and penetration and airway aspiration were observed in 30 (41.7%) and 8 (11.1%) cases, respectively. When the subjects were divided into dysphagia and non-dysphagia groups based on the findings of VFSS, there was no significant difference in the sex, age, body mass index (BMI), duration of hospitalization, duration from fracture to surgery, preoperative residual status, duration from surgery to VFSS, ASA, CCI, surgical method, and the mean preoperative albumin level between the two groups. However, the rate of respiratory disease incidence in the past was significantly higher in the dysphagia group with 22 cases (40.0%) than in the non-dysphagia group (p = 0.019). (p = 0.019). Vitamin D deficiency was observed in both groups, however, there was no significant difference between the two groups. In addition, the median femoral T-score was − 3.8 (range, -4.4 to -3.1) and − 3.7 (range, -4.5 to -2.7) in non-dysphagia and dysphagia groups, respectively; the mean spine T-score was − 2.2 ± 0.9 in the non-dysphagia group and − 2.4 ± 1.3 in the dysphagia group, indicating that osteoporosis was observed in both groups, although there was no significant difference between the two groups. Also, there was no significant difference in the lean body mass, SMI, and group strength between the two groups. However, diagnosis of sarcopenia by SMI and grip strength was observed in 5 (29.4%) patients of the non-dysphagia group and 34 (61.8%) patients of the dysphagia group, and sarcopenia was significantly more frequent in the dysphagia group (p = 0.039) (Table 1).

2. Accuracy of GUSS compared to VFSS

The median value of GUSS was 19 points (range, 17–20) and 18 points (range, 14–20) in those without and with dysphasia, respectively, and there was no statistically significant difference between the two groups (p = 0.189). The sensitivity and specificity of GUSS was 62% and 47%, respectively (positive predictive value 79%, negative predictive value 28%).

3. VFSS findings

In 39 out of 72 (52.5%) patients, sarcopenia with reduced grip strength and SMI was diagnosed. To assess whether there was a difference in dysphagia by VFSS according to sarcopenia, VFSS results were compared by dividing the patients into sarcopenia and non-sarcopenia groups. The distribution of PAS scores of patients with and without sarcopenia is showed in Table 2. There was no statistically significant difference in the distribution of the PAS scores between the two groups. The mean value of the FDS scores was 8.48\(\pm\)7.84 in the patients without sarcopenia and 15.82\(\pm\)14.01 in the patients with sarcopenia, and the mean value of the FDS was significantly different between the two groups (p=0.007). In the analysis of FDS subscores, statistically significant differences were found in the ‘oral transit time’ (p=0.011), ‘residue in valleculae’ (p = 0.035), ‘residue in pyriform sinuses’ (p = 0.041), and ‘coating of pharyngeal wall after swallow’ (p = 0.023). (Table 2).

4. Risk factors for dysphagia, including sarcopenia.

Logistic regression analysis was performed to assess factors associated with penetration, aspiration, and dysphagia. Univariate analysis was performed to identify factors associated with penetration, and a p-value of less than 0.1 was observed for preoperative Koval grade, dementia, history of respiratory and cerebrovascular diseases, and SMI. Multivariate analysis of the above factors showed that preoperative Koval grade (OR 2.03, CI 1.67 ~ 66.7), history of respiratory diseases (OR 3.55, CI 1.06 ~ 11.84), history of cerebrovascular attack (OR 4.73, CI 1.15 ~ 19.48) were associated with penetration (Table 3, Fig. 2(a)). Univariate analysis was performed to identify factors associated with aspiration, and a p-value of less than 0.1 was observed for preoperative Koval grade, dementia, history of cerebrovascular diseases, postoperative delirium, grip strength, and SMI. Multivariate analysis showed that only dementia was associated with airway aspiration (OR 10.56, CI 1.67 ~ 66.7) (Table 3, Fig. 2(b))

In order to identify factors associated with dysphagia, multivariate analysis was performed on factors with a p-value of less than 0.1 in univariate analysis including sex, BMI, preoperative Koval grade, and history of respiratory diseases, and it was observed that only preoperative Koval grade was a factor associated with dysphagia (OR 2.36, CI 1.01 ~ 5.55) (Table 3, Fig. 2(c))

Discussion

In our study, the prevalence of dysphagia diagnosed with VFSS in fragile hip fracture patients was 76.4%, which was higher than that of previous studies. The prevalence of dysphagia in hip fracture patients was ranged between 5.3%-34% in previous studies, which greatly varied.[7, 22, 36] The prevalence of dysphagia observed in our study was approximately twice as high as in previous studies, and it is thought that the design of studies and different methods for assessment of dysphagia led to such differences. GUSS, which is a screening test for dysphagia, does not have high sensitivity and specificity for identifying airway aspiration, penetration, and dysphagia. Frank et al. reported that the sensitivity and specificity of GUSS for diagnosis of airway aspiration was 50% and 51.35%, respectively, when comparing the accuracy of GUSS results in patients with Parkinson's disease. Additionally, the sensitivity and specificity of GUSS for diagnosis of penetration/dysphagia were 72.97% and 35.71%, respectively.[37] In our study, the sensitivity and specificity of GUSS for diagnosis of dysphagia were 62% and 47%, respectively, and the accuracy was not high. In two patients (2.8%) who had a moderate risk of dysphagia with a score of 14 points on GUSS, airway aspiration was not observed, and those 8 patients with airway aspiration showed mild risk of dysphagia. In addition, there was no significant difference in GUSS score between the dysphagia and non-dysphagia groups that were classified based on VFSS results. Therefore, additional tests other than GUSS are required for groups with a high-risk dysphagia such as hip fracture patients, and among those tests, VFSS is the most standardized test. [38]

In a study by Byun et al., VFSS was performed retrospectively to assess the prevalence of dysphagia in hip fracture patients with dysphagia symptoms who drank 30ml of water as a screening test.[36] In such cases, patients with asymptomatic airway aspiration that do not have reflexes such as coughing and suffocation may not have been included in the VFSS. Moreover, it is possible that the prevalence was underestimated due to a selection bias that did not include patients with dysphagia such as pharyngeal delay and pharyngeal residue which can only be identified through a VFSS. In a study by Love et al., the prevalence of dysphagia was prospectively evaluated using clinical characteristics such as symptoms in swallowing food without imaging tests such as VFSS.[7] In such cases, evaluation is likely to vary according to the judgement of the examiner. In a study by Nagano et al., food oral intake scale (FOIS) was used to assess dysphagia.[22] FOIS is divided into 7 levels according to the level of oral food intake, and levels of 5 or less are defined as dysphagia. FOIS is a test with a relatively high reliability between examiners; however, the results may vary depending on the skill level of the evaluator, and there is a limitation in that the test measures the level of food intake through a tube or oral cavity.[39] Unlike the studies mentioned above, our study prospectively included all hip fracture patients within a certain period to eliminate selection bias, and VFSS was performed to objectively assess asymptomatic airway aspiration, pharyngeal delay, and pharyngeal residues in order to accurately assess the prevalence of dysphagia compared to previous studies.

The prevalence of dysphagia in hip fracture patients is considered to be significantly high even though most hip fracture patients are elderly. In a study by Mulheren et al., 31 elderly subjects with a mean age of 76.2 years who have no history of dysphagia and resided in a local community were compared with younger subjects using VFSS and Dysphagia Handicap Index (DHI).[40] DHI showed that 9 elderly subjects (29%) were suspected to have dysphagia; however, VFSS results showed no difference in the rate of aspiration between the two groups. In our study, the rate of airway aspiration in elderly hip fracture patients was 11.1%, and hip fracture is thought to increase the risk of airway aspiration. In particular, history of dementia was assessed as a factor associated with airway aspiration. Dementia increased dysphagia in previous studies, and airway aspiration in hip fracture patients with dementia may increase the duration of hospitalization and mortality through aspiration pneumonia. Therefore, VFSS needs to be performed for more active diagnosis of dysphagia.[3, 41, 42]

In previous studies, the prevalence of sarcopenia in hip fracture patients was high, and in our study, sarcopenia was diagnosed in 39 out of 72 patients (52.5%).[17, 18, 43]Univariate analysis in our study also showed that the rate of sarcopenia was significantly higher in the dysphagia group with 61.8% than in the non-dysphagia group. However, logistic regression analysis demonstrated that sarcopenia, SMI, and grip strength were not associated with dysphagia. Only preoperative Koval grade was associated dysphagia. Preoperative gait ability of patients is highly associated with sarcopenia, and the level of physical activity at the time of diagnosis of sarcopenia is evaluated by the gait speed. Therefore, dysphagia observed in hip fracture patients may be sarcopenic dysphagia, which is associated with the gait ability and physical activity.[22] Additionally, although there was no statistical significance, vitamin D deficiency was observed in both the dysphagia and non-dysphagia groups. Vitamin D plays various roles in the human body, affects both bone and muscle metabolism, maintain muscle strength, and prevent falls.[44]

Penetration was associated with preoperative Koval grade and history of respiratory and cerebrovascular diseases. Preoperative Koval grade and airway aspiration were not significantly associated although there is a tendency (adjusted OR 95% CI 0.98–3.06). Dementia was found to be a strong risk for dysphagia, and the dementia and cerebrovascular diseases showed stronger association with dysphagia than sarcopenia and preoperative gait ability. It is known that dementia and cerebrovascular diseases were highly associated with dysphagia,[45] and dysphagia rehabilitation is one of the important rehabilitations for patients with these conditions.

Recent studies have reported that osteoporosis and sarcopenia interact via various substances and hormones and that osteoporosis and sarcopenia are closely related by not only the mechanical load between muscles and bones, but also through endocrine cross talking.[46, 47] Thus, osteoporosis and osteopenia accompanied by sarcopenia is defined as osteosarcopenia.[48] In hip fracture patients, severe osteoporosis is often accompanied, and in our study, severe osteoporosis with a T-score of -3.5 or less was observed in all patients. If proper weight-bearing gait becomes impossible due to hip fractures, cross talking between bones and muscles might lead to aggravation of osteoporosis and sarcopenia, and this suggests that preoperative gait ability in our study could be a risk factor for dysphagia as well as sarcopenia.

The limitations of this study are as follows. First, long-term follow-ups of the patients were not performed in this study, which prevents measuring the long-term prognosis such as aspiration pneumonia and mortality. Additional studies with longer follow-up on the frequency of postoperative aspiration pneumonia and on the level of improvement after dysphagia rehabilitation in patients with dysphagia would be necessary in the future.

Second, there was no control group in this study, therefore, it was difficult to assess the impact of hip fractures on dysphagia because the incidence of dysphagia increases with aging. However, the prevalence of dysphagia observed in our study was remarkably high even compared to healthy elderly subjects in previous studies, which suggest that hip fracture might impact developing dysphagia, at least partially.

Despite those limitations, our study estimated more accurate prevalence using standard test methods of dysphagia evaluation, VFSS, and showed that that it might not be sufficient to use bedside screening test, such as GUSS, instead of VFSS to evaluate the swallowing ability in this population. In addition, our study found that preoperative gait ability, as well as the history of dementia and cerebrovascular diseases identified in previous studies, might be a risk factor for dysphagia in elderly hip fracture patients.

Conclusion

In this study, GUSS showed mild dysphagia or normal findings in most patients, and the accuracy was not high. Therefore, VFSS is recommended to diagnose dysphagia and prevent complications for fragility hip fracture patients with a decreased gait ability who are likely to develop dysphagia.

Declarations

Ethics approval and consent to participate

Institutional Review Board Statement: The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of Yeungnam University Hospital (YUMC 2018-10-026). Informed consent was obtained from all subjects involved in the study.

Consent for publication

Not applicable.

Availability of data and material

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Competing interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding 

This work was supported by the 2019 Yeungnam University Research Grant (Grant No.219A580049)

Authors' contributions

S.K., S.J.P. and C.H.P. conceived and designed the study, recruited the study subjects, and planned and performed the statistical analysis. S.K. and C.H.P. contributed to study supervision and critical revision of the manuscript. All authors have read and approved the final manuscript.

Acknowledgements

None

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