Skip to main content
NCBI home page
Medicine logoLink to Medicine
. 2023 Jul 28;102(30):e34298. doi: 10.1097/MD.0000000000034298

Association between successful weaning from nasogastric tube feeding and thoracic muscle mass in patients with aspiration pneumonia

Hyun Woo Lee a, Dong Hyun Kim b, Kwang Nam Jin b, Hyo-Jin Lee a, Jung-Kyu Lee a, Tae Yeon Park a, Deog Kyeom Kim a, Eun Young Heo a,*
PMCID: PMC10378740  PMID: 37505164

Abstract

Nasogastric tube feeding is often used to provide optimal nutrition and hydration in patients with aspiration pneumonia. However, evidence regarding radiologic indicators for successful nasogastric tube weaning is lacking. We investigated whether thoracic skeletal muscle assessment can be useful for predicting successful weaning from nasogastric tube feeding in patients with aspiration pneumonia. This longitudinal, observational study included subjects with aspiration pneumonia who underwent a videofluoroscopic swallowing study (VFSS) and chest computed tomography (CT) in Boramae Medical Center, from January 2012 to December 2019. We estimated the area under the receiver operating characteristics curve (AUC) to evaluate the predictive performance of skeletal muscle and visceral fat parameters and VFSS results for successful weaning from nasogastric tube feeding. A board-certified radiologist measured muscle and fat areas. Muscle and fat volumes were segmented and measured using an externally validated convolutional neural network model. Among the 146 included patients, nasogastric tube feeding was successfully transitioned to oral feeding in 46.6%. After adjusting for covariables related to successful weaning, skeletal muscle areas, indices, and volume indices were positively associated with successful nasogastric tube weaning. Although VFSS results and skeletal muscle parameters alone showed suboptimal performance for predicting successful weaning, a prediction model combining skeletal muscle index at the T4 level and VFSS results improved the prediction performance to an acceptable level (AUC ≥ 0.7). Skeletal muscle index measured at the T4 level may be a useful supplementary indicator for predicting successful weaning from nasogastric tube feeding in patients with aspiration pneumonia.

Keywords: deglutition disorders, feeding and eating disorders, feeding, tube, pneumonia, aspiration, sarcopenia

What is known

Although nasogastric tube feeding is a good option for nutrition and hydration in patients with aspiration pneumonia, the evidence on radiologic indicators for successful weaning from nasogastric tube to oral feeding is lacking.

What is new

VFSS had a higher specificity than the skeletal muscle parameters, but still showed a suboptimal performance to predict successful weaning from nasogastric tube. In the prediction model combining skeletal muscle index (−29 to 150 HU) measured at T4 level and VFSS, the predictive performance was significantly improved to an acceptable level.

1. Introduction

Aspiration pneumonia is a lower respiratory tract infection caused by accidental inhalation of oral or gastric contents, which has a higher mortality than other forms of pneumonia.[1] One of the most prevalent comorbid conditions in patients with aspiration pneumonia is oropharyngeal dysphagia, a disorder that affects 30% to 47% of elderly patients.[2,3] Dysphagia is a significant contributing factor to malnutrition.[4] Providing adequate nutritional support without enteral feeding can be challenging for patients hospitalized with aspiration pneumonia. In one study, over half of the elderly patients hospitalized for aspiration pneumonia required parenteral nutrition, and only 5% to 6% of patients receiving total parenteral nutrition were able to receive an adequate amount of nutrients.[5]

Nasogastric tube feeding is a strategy for providing optimal nutrition and hydration in patients with swallowing problems. In a randomized controlled trial of 5033 patients with a recent stroke, early tube feeding was associated with improved survival, compared with no tube feeding.[6] However, it is uncertain whether nasogastric tube feeding prevents further aspiration events.[7–9] Several studies have even reported that prolonged nasogastric tube feeding may increase the risk of aspiration pneumonia and negatively impact swallowing function.[10–12] Therefore, unnecessarily prolonged use of a nasogastric tube should be avoided, and timely transition to oral feeding should be initiated when feasible. Several clinical and functional parameters have been evaluated as a predictor for successful weaning from tube feeding in adults.[13–23] However, little is known about useful radiologic indicators for predicting successful weaning from nasogastric tube feeding in adults.

Sarcopenia has been associated with an increased risk of aspiration pneumonia and may contribute to mortality related to aspiration pneumonia.[24,25] Recent studies have explored the potential influence of systemic sarcopenia on swallowing dysfunction.[26] In a systematic review and meta-analysis, dysphagia was more prevalent in patients with sarcopenia.[27] In elderly patients, mid–upper arm circumference was positively correlated with swallowing function.[28] In addition, tongue muscle force was related to grip strength.[29] Current evidence suggests that skeletal muscle volume may have a role as a clinical indicator of successful weaning from nasogastric tube feeding.

Therefore, we conducted a study to investigate whether thoracic skeletal muscle measured by chest computed tomography (CT) can help predict successful nasogastric tube weaning in patients hospitalized for aspiration pneumonia.

2. Methods

This study followed the ethical guidelines outlined in the Declaration of Helsinki of 1975. The Institutional Review Board Committee of Boramae Medical Center approved the study protocol and waived the requirement for informed consent from study participants to access their electronic medical records (institutional review board No. 30-2018-12). This study is reported in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology guidance.[30]

2.1. Study design and eligibility criteria

In this longitudinal, observational study, we retrospectively reviewed data from subjects hospitalized for aspiration pneumonia in Boramae Medical Center, from January 2012 to December 2019. We evaluated the performance of skeletal muscle parameters, visceral fat parameters, and videofluoroscopic swallowing study (VFSS) results for predicting successful weaning from nasogastric tube feeding. In addition, we elucidated whether models combining skeletal muscle indices and VFSS results have better predictive performance for successful weaning. The inclusion criteria were as follows: diagnosis of aspiration pneumonia based on clinical history of swallowing dysfunction or oropharyngeal aspiration, risk factors, and the presence of radiologic infiltrates in dependent lung regions on chest CT; nasogastric tube inserted for nutritional support; and severity of dysphagia evaluated by VFSS. All included patients underwent chest CT at admission or in the emergency department. The exclusion criteria were as follows: feeding through a gastrostomy tube; dependence on total or partial parenteral nutrition; severe cognitive impairment or neurodegenerative disease; deteriorating medical condition, other than aspiration pneumonia; and documented refusal of diagnostic work-up or medical treatment.

2.2. Clinical variables

We collected information at the time of admission, including age, sex, body mass index (BMI), Eastern Cooperative Oncology Group performance status, and comorbidities. Pneumonia severity was assessed using the CURB-65 score. We also collected patient laboratory data, including blood test results (hemoglobin, C-reactive protein, sodium, urea nitrogen, creatinine, cholesterol, protein, and albumin), microbiologic profiles, and blood culture results. After the improvement of aspiration pneumonia, we conducted VFSS and assessed the penetration-aspiration scale (PAS) to evaluate the depth of material penetration or aspiration into the airway and the patient response to such material.[31] PAS was classified into 3 ordinal categories: no penetration or aspiration (PAS 1), penetration (PAS 2–5), and aspiration (PAS 6–8).[32] Information was also recorded for clinical outcomes, including antibiotic treatment duration, bronchoscopic toileting, mechanical ventilation, duration of diet training, duration of rehabilitation, hospital length of stay, in-hospital mortality, and re-admission within 1 year.

2.3. Outcomes

The primary outcome was successful weaning from nasogastric tube feeding. Patients successfully weaned during hospitalization were defined as the weaning success group, whereas those who were not successfully weaned during hospitalization were defined as the weaning failure group.

2.4. Skeletal muscle and visceral fat parameters

Skeletal muscle areas and volumes, as well as visceral fat areas and volumes, were estimated using chest CT imaging. A board-certified radiologist measured skeletal muscle or visceral fat area at the T4 vertebra level using threshold-based manual segmentation (−29 to + 150 Hounsfield unit [HU] or −29 to + 100 HU for skeletal muscle; −190 to −30 HU for visceral fat). Skeletal muscle volumes and visceral fat volumes at T1 through T12 vertebrae levels were segmented and measured using the internally developed convolutional neural network model called DeepCatch, which is an externally validated tool for automated segmentation or measurement of skeletal muscle and visceral fat. Detailed information on the model architecture, data preprocessing, data augmentation, weight initiation process, and training process for DeepCatch were previously described.[33] A board-certified radiologist visually checked the measured volume and modified it manually, if necessary. Skeletal muscle index was calculated as skeletal muscle area (cm2)/(height [m])2. Skeletal volume index and fat volume index were calculated as volume (cm3)/length of the thoracic spine from T1 to T12 (cm)/ (height [m])2.

2.5. Statistical analysis

Student t test or the Wilcoxon rank-sum test was used to evaluate continuous variables. The chi-square test or Fisher exact test was used to evaluate categorical variables. Univariable and multivariable logistic regression analyses were used to identify clinical factors and skeletal muscle parameters and visceral fat parameters associated with successful weaning. Receiver operating characteristics curves were used to estimate cutoff values of skeletal muscle parameters and visceral fat parameters for predicting successful weaning. The predictive performance for successful nasogastric tube weaning of different skeletal muscle and visceral fat volumes and volume indices, as well as VFSS results, were assessed by determining the sensitivity, specificity, and area under the receiver operating characteristic curve (AUC). DeLong test was used to compare the predictive performances for weaning success among the different skeletal muscle parameters, VFSS results, and combined models (a skeletal muscle parameter + VFSS results). P value < .05 were considered to have statistical significance. A variance inflation factor of > 4.0 was considered indicative of significant multicollinearity. We considered an AUC < 0.7 as suboptimal performance, 0.7 to 0.79 as acceptable performance, 0.8 to 0.89 as excellent performance, and ≥ 0.9 as outstanding performance.[34] R statistical software, version 4.1.0 (R Core Team [2020], Vienna, Austria), was used for all statistical analyses.

3. Results

Among the 312 patients diagnosed with aspiration pneumonia during the study period, VFSS was performed in 213 patients with a nasogastric tube. After excluding 67 of these patients, we included the remaining 146 in this study (Fig. 1). During hospitalization, successful weaning from nasogastric tube feeding was documented in 68 (46.6%) patients, whereas weaning failure was documented in 78 (53.4%) patients.

Figure 1.

Figure 1.

Open in a new tab

Flow diagram for inclusion and exclusion of study patients. VFSS = video fluoroscopic swallowing study.

3.1. Demographic and clinical features

Of the baseline characteristics, BMI was higher in the weaning success group than in the weaning failure group, whereas there was no significant difference in age, sex, eastern cooperative oncology group performance status, or comorbidities between the 2 groups (Table 1). The weaning success group had a lower proportion of patients with a high CURB-65 score (≥3), as well as a higher mean hemoglobin and cholesterol level. Drug-resistant pathogens, such as methicillin-resistant Staphylococcus aureus, extended-spectrum β-lactamase-producing gram-negative pathogens, and vancomycin-resistant Enterococcus, were detected more frequently in the weaning failure group than in the weaning success group. In addition, bacteremia was more frequent in the weaning failure group. Regarding VFSS results, 53% of patients in the weaning success group exhibited no penetration or aspiration, whereas aspiration or penetration were observed in 40% of patients in the weaning failure group.

Table 1.

Baseline characteristics and clinical features of the patients diagnosed with aspiration pneumonia.

Weaning failure group (n = 78) Weaning success group (n = 68) P value
Age, mean (SD) 72.9 (11.0) 72.3 (14.2) .774
Male, n (%) 50 (64.1) 45 (66.2) .930
BMI, mean (SD) 18.4 (2.8) 20.6 (4.4) <.001
ECOG performance status ≥ 3, n (%) 28 (35.9) 24 (35.3) 1.000
Comorbidities
 Hypertension, n (%) 37 (47.4) 33 (48.5) 1.000
 Diabetes mellitus, n (%) 34 (43.6) 23 (33.8) .300
 Cerebrovascular disease, n (%) 38 (48.7) 39 (57.4) .381
 Chronic kidney disease, n (%) 15 (19.2) 6 (8.8) .121
 Active cancer, n (%) 17 (21.8) 10 (14.7) .375
 Dementia, n (%) 21 (26.9) 13 (19.1) .359
 Parkinson disease, n (%) 4 (5.1) 5 (7.4) .832
CURB-65 ≥ 3, n (%) 37 (47.4) 20 (29.4) .040
Blood examination
 Hemoglobin, mean (SD) 10.6 (2.2) 11.6 (1.9) .004
 C-reactive protein, mean (SD) 11.3 (10.3) 11.0 (10.9) .846
 Sodium, mean (SD) 136.4 (5.8) 136.2 (6.2) .824
 Urea nitrogen, mean (SD) 30.3 (22.7) 27.7 (23.2) .498
 Creatinine, mean (SD) 1.20 (0.88) 1.61 (1.85) .079
 Cholesterol, mean (SD) 129.3 (36.4) 148.6 (43.0) .004
 Protein, mean (SD) 5.84 (0.84) 5.94 (0.88) .499
 Albumin, mean (SD) 3.12 (0.58) 3.27 (0.58) .123
Microbiologic examination
 Methicillin resistant Staphylococcus aureus, n (%) 23 (29.5) 3 (4.4) <.001
 Extended spectrum β-lactamase-producing gram-negative pathogens, n (%) 19 (24.4) 4 (5.9) .005
 Carbapenem-resistant enterobacteriaceae, n (%) 20 (25.6) 12 (17.6) .335
 Vancomycin-resistant enterococcus, n (%) 15 (19.2) 4 (5.9) .032
 Mycobacterium tuberculosis, n (%) 2 (2.6) 6 (8.8) .196
 Streptococcus pneumoniae urinary antigen, n (%) 2 (2.6) 0 (0.0) .538
Blood culture positivity, n (%) 13 (16.7) 3 (4.4) .036
Video fluoroscopic swallowing study
 No penetration or aspiration (PAS 1), n (%) 16 (20.5) 36 (52.9) <.001
 Penetration (PAS 2-5), n (%) 31 (39.7) 21 (30.9) .346
 Aspiration (PAS 6-8), n (%) 31 (39.7) 11 (16.2) .003
Open in a new tab

BMI = body mass index, ECOG = Eastern Cooperative Oncology Group, PAS = penetration-aspiration scale, SD = standard deviation, VFSS = video fluoroscopic swallowing study.

Management and outcomes differed between groups. Bronchoscopic toileting and mechanical ventilation were more frequent in the weaning failure group than in the weaning success group (Supplementary Material S1, http://links.lww.com/MD/J280). Durations of antibiotic treatment, diet training, and rehabilitation were longer in the weaning failure group. In-hospital mortality was higher, and hospital LOS was longer in the weaning failure group.

3.2. Area and volume of skeletal muscle and fat

Examples of measured skeletal muscle area and volume and fat area and volume are depicted in Supplementary Material S2, http://links.lww.com/MD/J281. In the analysis of axial muscle and fat areas at the T4 level, skeletal muscle area and index, as well as visceral fat area and index, were significantly higher in the weaning success group than in the weaning failure group (Supplementary Material S3, http://links.lww.com/MD/J282). In the analysis of muscle and fat volumes at levels T1 through T12, the weaning success group had a higher total skeletal muscle volume and volume index. However, there was no association between weaning success and visceral fat volume or volume index. Regarding segmented muscle volumes, volume and volume indices of the erector spinae, pectoralis major, and pectoralis minor muscles were significantly higher in the weaning success group.

3.3. Clinical factors related to successful weaning

Univariable regression analyses were conducted to evaluate clinical factors associated with successful weaning from nasogastric tube feeding. Of the demographic factors, higher BMI was associated with successful weaning (Supplementary Material S4, http://links.lww.com/MD/J283). Of the clinical features, a lower CURB-65 (<3), higher hemoglobin, and higher cholesterol were associated with successful weaning. Methicillin-resistant S. aureus, carbapenem-resistant Enterobacteriaceae, vancomycin-resistant Enterococcus, and positive blood cultures were negatively associated with successful weaning. Aspiration (PAS 6–8) during VFSS was negatively associated with successful weaning. The probability of successful weaning was lower in patients who underwent bronchoscopic toileting or mechanical ventilation. Successful weaning was related to shorter durations of antibiotic treatment, diet training, and rehabilitation.

In univariable logistic regression analyses for muscle and fat areas at the T4 level, skeletal muscle area and index, as well as visceral fat area and index, were positively associated with successful weaning (Table 2 and Supplementary Material S5, http://links.lww.com/MD/J284). In univariable logistic regression analyses for muscle and fat volumes at levels T1 through T12, total skeletal muscle volume and volume index, as well as segmented skeletal muscle volume and volume index, were positively associated with successful weaning. After adjusting for clinical factors associated with successful weaning, skeletal muscle area and index, total skeletal muscle volume index, and erector spinae volume index were positively associated with successful weaning. There was no significant association between skeletal muscle measurements and VFSS results.

Table 2.

Muscle areas or volumes significantly related with successful weaning from nasogastric tube.

Univariable analysis Multivariable analysisa
Odds ratio (95% CI) P value Odds ratio (95% CI) P value
Muscle or fat area at T4 vertebrae level
 Skeletal muscle area, cm2 (−29 to 150 HU) 1.002 (1.001–1.003) <.001 1.002 (1.001–1.003) .002
 Skeletal muscle index, cm2/m2 (−29 to 150 HU) 1.006 (1.003–1.009) <.001 1.006 (1.002–1.010) .004
 Skeletal muscle area, cm2 (−29 to 100 HU) 1.002 (1.001–1.004) .006 1.003 (1.001–1.005) .009
 Skeletal muscle index, cm2/m2 (−29 to 100 HU) 1.006 (1.002–1.011) .005 1.007 (1.002–1.013) .012
Muscle or fat volume at T1 through T12 vertebrae levels
 Total skeletal muscle volume index, cm3/cm/m2 1.085 (1.033–1.138) .001 1.067 (1.003–1.136) .041
 Both erector spinae volume index, cm3/cm/m2 1.860 (1.326–2.610) <.001 1.585 (1.021–2.459) .040
  Left erector spinae volume index, cm3/cm/m2 3.191 (1.648–6.181) <.001 2.965 (1.186–7.413) .020
  Right erector spinae volume index, cm3/cm/m2 4.692 (2.232–9.861) <.001 3.587 (1.369–9.396) .009
Open in a new tab
a

Variables including BMI, CURB-65, hemoglobin, cholesterol, methicillin resistant staphylococcus aureus, carbapenem-resistant enterobacteriaceae, vancomycin-resistant enterococcus, blood culture positivity, aspiration (PAS 6-8) in VFSS, treatment duration of antibiotics, duration of diet training and/or exercise and rehabilitation, bronchoscopic toileting, and mechanical ventilation were adjusted for multivariable logistic regression analyses.

Skeletal muscle index was calculated as skeletal muscle area/(height)2. Skeletal muscle or visceral fat volume index was calculated as volume/length of thoracic spine (T1-T12)/(height).2

HU = Hounsfield unit, PAS = penetration-aspiration scale.

3.4. Prediction of successful weaning

The cutoff values and AUC for predicting successful weaning were determined for each parameter (Table 3). Among the muscle and fat measurement parameters, skeletal muscle index (−29 to 150 HU) at the T4 level had the highest AUC: 0.697 (95% confidence interval [CI], 0.612–0.782); however, this was considered suboptimal performance. VFSS results also exhibited suboptimal performance, with an AUC of 0.691 (95% CI, 0.610–0.772). In a combined prediction model consisting of skeletal muscle index (−29 to 150 HU) and VFSS results, the AUC for predicting successful nasogastric tube weaning improved to 0.796 (95% CI, 0.721–0.870), which was at the high end of the range considered acceptable performance (Fig. 2). However, prediction models combining skeletal muscle volumes or volume indices and VFSS results did not show additional benefits for predicting successful weaning (Supplementary Material S6 and S7, http://links.lww.com/MD/J285).

Table 3.

cutoff value and area under the ROC curve to predict successful weaning from nasogastric tube.

Cutoff value Sensitivity Specificity AU-ROC (95% CI)
Muscle or fat area at T4 vertebrae level
 Skeletal muscle area, cm2 (−29 to 150 HU) 102 73.4% 57.4% 0.679 (0.591–0.766)
 Skeletal muscle index, cm2/m2 (−29 to 150 HU) 39 74.7% 57.4% 0.697 (0.612–0.782)
 Skeletal muscle area, cm2 (−29 to 100 HU) 44 84.8% 42.6% 0.613 (0.518–0.707)
 Skeletal muscle index, cm2/m2 (−29 to 100 HU) 18 86.1% 41.2% 0.614 (0.521–0.708)
 Visceral fat area, cm2 (−190 to −30 HU) 61 63.3% 67.6% 0.667 (0.578–0.756)
 Visceral fat index, cm2/m2 (−190 to −30 HU) 21 57.0% 73.5% 0.653 (0.563–0.743)
Muscle or fat volume at T1 through T12 vertebrae levels
 Total skeletal muscle volume, cm3 3511 84.6% 38.8% 0.612 (0.517–0.706)
 Total skeletal muscle volume index, cm3/cm/m2 35.8 67.9% 62.7% 0.677 (0.589–0.766)
 Visceral fat volume, cm3 412 62.8% 50.0% 0.558 (0.464–0.653)
 Visceral fat volume index, cm3/cm/m2 7.9 79.5% 35.3% 0.561 (0.466–0.657)
 Both erector spinae, cm3 645 96.2% 20.9% 0.597 (0.504–0.691)
 Both erector spinae volume index, cm3/cm/m2 6.1 69.2% 59.7% 0.676 (0.588–0.764)
  Left erector spinae, cm3 272 78.2% 39.7% 0.590 (0.494–0.686)
  Left erector spinae volume index, cm3/cm/m2 3.2 74.4% 54.0% 0.658 (0.567–0.749)
  Right erector spinae, cm3 222 53.8% 65.1% 0.623 (0.529–0.716)
  Right erector spinae volume index, cm3/cm/m2 3.0 69.2% 60.3% 0.698 (0.612–0.785)
 Both pectoralis major volume, cm3 344 89.7% 33.8% 0.625 (0.532–0.718)
 Both pectoralis major volume index, cm3/cm/m2 5.2 64.1% 61.8% 0.640 (0.549–0.731)
  Left pectoralis major volume, cm3 134 70.5% 51.5% 0.607 (0.5130.701)
  Left pectoralis major volume index, cm3/cm/m2 2.9 80.8% 48.5% 0.630 (0.538–0.722)
  Right pectoralis major volume, cm3 142 80.8% 47.1% 0.640 (0.548–0.732)
  Right pectoralis major volume index, cm3/cm/m2 2.2 48.7% 77.9% 0.659 (0.570–0.748)
 Both pectoralis minor volume, cm3 54 74.4% 52.9% 0.635 (0.543–0.727)
 Both pectoralis minor volume index, cm3/cm/m2 1.4 92.3% 26.5% 0.615 (0.523–0.707)
  Left pectoralis minor volume, cm3 27 69.2% 52.9% 0.633 (0.552–0.733)
  Left pectoralis minor volume index, cm3/cm/m2 0.8 47.4% 76.5% 0.657 (0.568–0.746)
  Right pectoralis minor volume, cm3 28 76.9% 51.5% 0.642 (0.551–0.733)
  Right pectoralis minor volume index, cm3/cm/m2 0.9 78.2% 50.0% 0.661 (0.571–0.751)
Video fluoroscopic swallowing study Aspiration (PAS 6-8) 39.2% 83.8% 0.691 (0.610–0.772)
Open in a new tab

Skeletal muscle index was calculated as skeletal muscle area/(height)2.

HU = Hounsfield unit, PAS = penetration-aspiration scale, ROC = receiver operating characteristic curve.

Figure 2.

Figure 2.

Open in a new tab

Prediction model for successful nasogastric tube weaning combining skeletal muscle index and video fluoroscopic swallowing study results. AUC = area under the ROC curve, ROC = receiver operating characteristic, SMI = skeletal muscle index, VFSS = video fluoroscopic swallowing study.

4. Discussion

In this study, we investigated whether thoracic skeletal muscle parameters determined by chest CT were associated with successful weaning from nasogastric tube in patients with aspiration pneumonia. Better nutritional indices (such as higher BMI and higher cholesterol), lower pneumonia severity, and lower drug-resistant microbiologic profiles, were found in the weaning success group. More patients in the weaning success group had a lower PAS during VFSS. In multivariable regression analyses adjusted for clinical variables related to successful weaning, skeletal muscle areas, skeletal muscle indices, and skeletal muscle volume indices were positively associated with successful weaning from nasogastric tube feeding. VFSS results had a higher specificity than skeletal muscle parameters but still showed suboptimal performance for predicting successful weaning. However, predictive performance improved to an acceptable level using a prediction model combining skeletal muscle index (−29 to 150 HU) measured at the T4 level and VFSS results. Our study therefore suggests that skeletal muscle index measured at the T4 level may be a useful supplementary indicator for predicting successful nasogastric tube weaning.

Dysphagia, sarcopenia, and aspiration pneumonia are intertwined and create a vicious cycle. Dysphagia and sarcopenia are important risk factors for aspiration pneumonia, while aspiration pneumonia contributes to dysphagia and sarcopenia.[35] Dysphagia increases the risk of malnutrition and the development of sarcopenia, while sarcopenia decreases swallowing strength and contributes to dysphagia.[28,36] Sufficient nutritional support and prevention of additional aspiration are essential to break this cycle in patients with aspiration pneumonia. Tube feeding has been considered an appropriate intervention to avoid additional aspiration from oral feeding, while maintaining adequate enteral nutrition.[37] However, unnecessarily prolonged nasogastric tube feeding should be avoided because of its negative impact on clinical outcomes.[10–12]

Several studies have investigated various approaches to identify clinical factors related with successful transition from tube feedings to oral feedings.[13–21] Younger age was associated with a successful transition to oral nutrition from gastrostomy tube feeding in adults diagnosed with cancer.[19] Stroke and aspiration pneumonia are known as important clinical factors that make the removal of NG tubes difficult.[20] In patients with stroke and dysphagia, functional status was a significant clinical factor in nasogastric tube removal.[16] In a large-scale study that aimed to identify factors predicting oral intake in elderly patients with aspiration pneumonia, it was found that not only functional status but also underweight was an important factor in the delayed initiation of oral intake.[18] When evaluating functional status using 4 different methods including functional dysphagia scale (FDS) score and PAS score, the prediction AUC for nasogastric tube removal showed a good predictive power of 0.820.[14] In other studies, FDS score and PAS score showed significant predictive power for gastrostomy tube removal.[15] A recent prospective cohort study reported that decreased skeletal muscle index was an independent predictor for dysphagia.[21] When considering that a decrease in muscle mass often accompanies reductions in both body weight and functional performance, it becomes plausible to explain the association between decreased muscle mass and successful nasogastric tube weaning. The findings from our study supported the importance of monitoring and addressing muscle mass as a key factor in achieving nasogastric tube weaning.

There have been attempts to predict tube feeding withdrawal using tools that visualize swallowing function. Videoendoscopic examination may be a useful tool for predicting the successful recovery of oral intake, with AUC values ranging from 0.774 to 0.826.[22] Experts have suggested that VFSS can be the most useful tool for making decisions regarding transitioning to oral feeding.[23] Measurement of muscle mass index in chest CT images can be considered as an indirect visualization method that reflects swallowing function. Our results suggest that skeletal muscle index measured at T4 level is a potentially useful clinical indicator of successful weaning from nasogastric tube feeding. In predicting successful weaning, skeletal muscle index had a high sensitivity, while VFSS results had a high specificity. Combining VFSS results and skeletal muscle index was therefore expected to have complementary benefits for predicting successful transition from tube to oral feeding, which was confirmed by the improved predictive performance of our combined model.

Mechanisms for the association between reduced systemic skeletal muscle and problems with oral feeding have not been clearly identified, but several plausible hypotheses have been suggested. As a generally accepted causal relationship, dysphagia potentially contributes to malnutrition, which causes secondary sarcopenia.[38] On contrary, dysphagia can be induced or aggravated by systemic sarcopenia, which has been explained as the concept of sarcopenic dysphagia.[28] Dysphagia resulted in weakened tongue strength and motion and reduced swallowing muscle contractions and endurance.[39] Malfunctioning satellite cell activation, oxidative stress, and changes in general muscle metabolism are possible pathophysiologic mechanisms of sarcopenic dysphagia.[40] Another hypothesis is that sarcopenia and dysphagia are common conditions affected by the aging process. Aging independently contributes to progressive loss of systemic skeletal muscle, as well as swallowing muscles, in older adults.[38,41] Presbyphagia refers to the characteristic age-related reduction in physiologic reserves for swallowing function.[42] A final hypothesis is that aspiration pneumonia may cause secondary sarcopenia in systemic and swallowing muscles, which worsens dysphagia. In a mouse model, aspiration pneumonia was shown to increase the expression of inflammatory cytokines and enhance muscle proteolytic pathways in swallowing muscles.[35]

Our study has several limitations. First, this cohort study was conducted retrospectively and included a relatively small number of patients from a single medical center. Despite the small number of the include patients, we used a large number of explanatory variables as covariables to identify independently significant muscle parameters for successful weaning from nasogastric tube. Secondly, the possibility of selection bias should be considered when interpreting our results. Lastly, skeletal muscle strength was not measured in our study.

5. Conclusion

Skeletal muscle index measured at the T4 level may be a useful supplementary indicator for predicting successful weaning from nasogastric tube feeding. A model combining VFSS results with skeletal muscle index at the T4 level may have an acceptable level of performance for predicting successful nasogastric tube weaning.

Author contributions

Conceptualization: Hyun Woo Lee, Eun Young Heo.

Data curation: Hyo-Jin Lee, Jung-Kyu Lee, Tae Yeon Park, Deog Kyeom Kim.

Formal analysis: Hyun Woo Lee, Dong Hyun Kim, Kwang Nam Jin.

Investigation: Hyun Woo Lee, Eun Young Heo.

Methodology: Hyun Woo Lee, Dong Hyun Kim, Kwang Nam Jin.

Project administration: Hyun Woo Lee, Eun Young Heo.

Resources: Hyun Woo Lee, Dong Hyun Kim, Kwang Nam Jin.

Software: Hyun Woo Lee, Dong Hyun Kim, Kwang Nam Jin.

Supervision: Eun Young Heo.

Visualization: Hyun Woo Lee.

Writing – original draft: Hyun Woo Lee, Dong Hyun Kim.

Writing – review & editing: Eun Young Heo.

Supplementary Material

medi-102-e34298-s001.pdf (172.3KB, pdf)
medi-102-e34298-s002.pdf (221.8KB, pdf)
medi-102-e34298-s003.pdf (207.9KB, pdf)
medi-102-e34298-s004.pdf (281.9KB, pdf)
medi-102-e34298-s005.pdf (280.3KB, pdf)
medi-102-e34298-s006.pdf (445.8KB, pdf)

Abbreviations:

AUC
area under the roc curve
BMI
body mass index
CT
computed tomography
HU
Hounsfield unit
PAS
penetration-aspiration scale
VFSS
video fluoroscopic swallowing study

HWL and DHK contributed equally to this work.

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Supplemental Digital Content is available for this article.

The authors have no funding and conflicts of interest to disclose.

This study followed the ethical guidelines outlined in the Declaration of Helsinki of 1975. The Institutional Review Board (IRB) Committee of Seoul Metropolitan Government-Seoul National University (SMG-SNU) Boramae Medical Center approved the study protocol and waived the requirement for informed consent from study participants to access their electronic medical records (IRB No. 30-2018-12).

How to cite this article: Lee HW, Kim DH, Jin KN, Lee H-J, Lee J-K, Park TY, Kim DK, Heo EY. Association between successful weaning from nasogastric tube feeding and thoracic muscle mass in patients with aspiration pneumonia. Medicine 2023;102:30(e34298).

Contributor Information

Hyun Woo Lee, Email: jk1909@empas.com.

Dong Hyun Kim, Email: kimdkmd@gmail.com.

Kwang Nam Jin, Email: wlsrhkdska@gmail.com.

Hyo-Jin Lee, Email: jk1909@empas.com.

Jung-Kyu Lee, Email: jk1909@empas.com.

Tae Yeon Park, Email: cally0329@hanmail.net.

Deog Kyeom Kim, Email: kimdkmd@gmail.com.

References

  • [1].Mandell LA, Niederman MS. Aspiration pneumonia. N Engl J Med. 2019;380:651–63. [DOI] [PubMed] [Google Scholar]
  • [2].Lin LC, Wu SC, Chen HS, et al. Prevalence of impaired swallowing in institutionalized older people in Taiwan. J Am Geriatr Soc. 2002;50:1118–23. [DOI] [PubMed] [Google Scholar]
  • [3].Carrión S, Cabré M, Monteis R, et al. Oropharyngeal dysphagia is a prevalent risk factor for malnutrition in a cohort of older patients admitted with an acute disease to a general hospital. Clin Nutr (Edinburgh, Scotland). 2015;34:436–42. [DOI] [PubMed] [Google Scholar]
  • [4].Namasivayam AM, Steele CM. Malnutrition and dysphagia in long-term care: a systematic review. J Nutr Gerontol Geriatr. 2015;34:1–21. [DOI] [PubMed] [Google Scholar]
  • [5].Maeda K, Murotani K, Kamoshita S, et al. Nutritional management in inpatients with aspiration pneumonia: a cohort medical claims database study. Arch Gerontol Geriatr. 2021;95:104398. [DOI] [PubMed] [Google Scholar]
  • [6].Dennis MS, Lewis SC, Warlow C, et al. Effect of timing and method of enteral tube feeding for dysphagic stroke patients (FOOD): a multicentre randomised controlled trial. Lancet (London, England). 2005;365:764–72. [DOI] [PubMed] [Google Scholar]
  • [7].Mamun K, Lim J. Role of nasogastric tube in preventing aspiration pneumonia in patients with dysphagia. Singapore Med J. 2005;46:627–31. [PubMed] [Google Scholar]
  • [8].Dziewas R, Ritter M, Schilling M, et al. Pneumonia in acute stroke patients fed by nasogastric tube. J Neurol Neurosurg Psychiatry. 2004;75:852–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [9].Leder SB, Suiter DM. Effect of nasogastric tubes on incidence of aspiration. Arch Phys Med Rehabil. 2008;89:648–51. [DOI] [PubMed] [Google Scholar]
  • [10].Gomes GF, Pisani JC, Macedo ED, et al. The nasogastric feeding tube as a risk factor for aspiration and aspiration pneumonia. Curr Opin Clin Nutr Metab Care. 2003;6:327–33. [DOI] [PubMed] [Google Scholar]
  • [11].Luk JK, Chan DK. Preventing aspiration pneumonia in older people: do we have the “know-how?”. Hong Kong Med J. 2014;20:421–7. [DOI] [PubMed] [Google Scholar]
  • [12].Wang ZY, Chen JM, Ni GX. Effect of an indwelling nasogastric tube on swallowing function in elderly post-stroke dysphagia patients with long-term nasal feeding. BMC Neurol. 2019;19:83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [13].Crary MA, Groher ME. Reinstituting oral feeding in tube-fed adult patients with dysphagia. Nutr Clin Pract. 2006;21:576–86. [DOI] [PubMed] [Google Scholar]
  • [14].Lee KC, Liu CT, Tzeng IS, et al. Predictors of nasogastric tube removal in patients with stroke and dysphagia. Int J Rehab Res. 2021;44:205–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [15].Jang BS, Park JY, Lee JH, et al. Clinical factors associated with successful gastrostomy tube weaning in patients with prolonged dysphagia after stroke. Ann Rehab Med. 2021;45:33–41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [16].Chuang ST, Yen YH, Hsu H, et al. Predictive factors for nasogastric tube removal in post-stroke patients. Medicina (Kaunas, Lithuania). 2023;59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Lee JH, Kim SB, Lee KW, et al. Associating factors regarding nasogastric tube removal in patients with Dysphagia after stroke. Ann Rehab Med. 2014;38:6–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [18].Momosaki R, Yasunaga H, Matsui H, et al. Predictive factors for oral intake after aspiration pneumonia in older adults. Geriatr Gerontol Int. 2016;16:556–60. [DOI] [PubMed] [Google Scholar]
  • [19].Naik AD, Abraham NS, Roche VM, et al. Predicting which patients can resume oral nutrition after percutaneous endoscopic gastrostomy tube placement. Aliment Pharmacol Ther. 2005;21:1155–61. [DOI] [PubMed] [Google Scholar]
  • [20].Moon J-B, Kim J-H, Kim Y-H, et al. Predictive factors associated with achieving oral intake in patients with dysphagia. 2022;12:35–44. [Google Scholar]
  • [21].Maeda K, Takaki M, Akagi J. Decreased skeletal muscle mass and risk factors of sarcopenic dysphagia: a prospective observational cohort study. J Gerontol A Biol Sci Med Sci. 2017;72:1290–4. [DOI] [PubMed] [Google Scholar]
  • [22].Kimura M, Nakayama E, Ogawa Y, et al. Prediction of oral intake recovery for inpatients with aspiration pneumonia by videoendoscopic evaluation using the Hyodo-Komagane score in Japan. J Oral Rehabil. 2021;48:55–60. [DOI] [PubMed] [Google Scholar]
  • [23].Stroud M, Duncan H, Nightingale J, et al. Guidelines for enteral feeding in adult hospital patients. Gut. 2003;52(Suppl 7):vii1–vii12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [24].Okazaki T, Ebihara S, Mori T, et al. Association between sarcopenia and pneumonia in older people. Geriatr Gerontol Int. 2020;20:7–13. [DOI] [PubMed] [Google Scholar]
  • [25].Endo K, Ueno T, Hirai N, et al. Low skeletal muscle mass is a risk factor for aspiration pneumonia during chemoradiotherapy. Laryngoscope. 2021;131:E1524–9. [DOI] [PubMed] [Google Scholar]
  • [26].Clavé P, Shaker R. Dysphagia: current reality and scope of the problem. Nat Rev Gastroenterol Hepatol. 2015;12:259–70. [DOI] [PubMed] [Google Scholar]
  • [27].Zhao WT, Yang M, Wu HM, et al. Systematic review and meta-analysis of the association between sarcopenia and dysphagia. J Nutr Health Aging. 2018;22:1003–9. [DOI] [PubMed] [Google Scholar]
  • [28].Kuroda Y, Kuroda R. Relationship between thinness and swallowing function in Japanese older adults: implications for sarcopenic dysphagia. J Am Geriatr Soc. 2012;60:1785–6. [DOI] [PubMed] [Google Scholar]
  • [29].Sakai K, Nakayama E, Tohara H, et al. Tongue strength is associated with grip strength and nutritional status in older adult inpatients of a rehabilitation hospital. Dysphagia. 2017;32:241–9. [DOI] [PubMed] [Google Scholar]
  • [30].von Elm E, Altman DG, Egger M, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4:e296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [31].Rosenbek JC, Robbins JA, Roecker EB, et al. A penetration-aspiration scale. Dysphagia. 1996;11:93–8. [DOI] [PubMed] [Google Scholar]
  • [32].Borders JC, Brates D. Use of the penetration-aspiration scale in dysphagia research: a systematic review. Dysphagia. 2020;35:583–97. [DOI] [PubMed] [Google Scholar]
  • [33].Lee YS, Hong N, Witanto JN, et al. Deep neural network for automatic volumetric segmentation of whole-body CT images for body composition assessment. Clin Nutr. 2021;40:5038–46. [DOI] [PubMed] [Google Scholar]
  • [34].Mandrekar JN. Receiver operating characteristic curve in diagnostic test assessment. J Thorac Oncol. 2010;5:1315–6. [DOI] [PubMed] [Google Scholar]
  • [35].Komatsu R, Okazaki T, Ebihara S, et al. Aspiration pneumonia induces muscle atrophy in the respiratory, skeletal, and swallowing systems. J Cachexia Sarcopenia Muscle. 2018;9:643–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [36].Chen KC, Jeng Y, Wu WT, et al. Sarcopenic dysphagia: a narrative review from diagnosis to intervention. Nutrients. 2021;13:4043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [37].Finucane TE, Bynum JP. Use of tube feeding to prevent aspiration pneumonia. Lancet (London, England). 1996;348:1421–4. [DOI] [PubMed] [Google Scholar]
  • [38].Fujishima I, Fujiu-Kurachi M, Arai H, et al. Sarcopenia and dysphagia: Position paper by four professional organizations. Geriatr Gerontol Int. 2019;19:91–7. [DOI] [PubMed] [Google Scholar]
  • [39].Wakabayashi H. Presbyphagia and sarcopenic dysphagia: association between aging, sarcopenia, and deglutition disorders. J Frailty Aging. 2014;3:97–103. [DOI] [PubMed] [Google Scholar]
  • [40].Dellis S, Papadopoulou S, Krikonis K, et al. Sarcopenic dysphagia. A narrative review. J Frailty Sarcopenia Falls. 2018;3:1–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [41].Kamel HK. Sarcopenia and aging. Nutr Rev. 2003;61(5 Pt 1):157–67. [DOI] [PubMed] [Google Scholar]
  • [42].McCoy YM, Varindani Desai R. Presbyphagia versus dysphagia: identifying age-related changes in swallow function. 2018;3:15–21. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

medi-102-e34298-s001.pdf (172.3KB, pdf)
medi-102-e34298-s002.pdf (221.8KB, pdf)
medi-102-e34298-s003.pdf (207.9KB, pdf)
medi-102-e34298-s004.pdf (281.9KB, pdf)
medi-102-e34298-s005.pdf (280.3KB, pdf)
medi-102-e34298-s006.pdf (445.8KB, pdf)

Articles from Medicine are provided here courtesy of Wolters Kluwer Health

RESOURCES