Edited by: Andrew S. Day, University of Otago, New Zealand
Reviewed by: Selen Serel Arslan, Hacettepe University, Turkey; Matjaž Homan, University Medical Centre Ljubljana, Slovenia
This article was submitted to Pediatric Gastroenterology, Hepatology and Nutrition, a section of the journal Frontiers in Pediatrics
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It has been suggested that oral feeding trial has therapeutic implications for improving oral-motor and swallowing function in infants and young children fed via an enteral tube or gastrostomy. This study aimed to investigate whether oral feeding challenges in children with tracheostomy could improve feeding outcomes, even with the finding of aspiration compared to those who did not receive oral feeding at all. Children (age <7 years) with tracheostomy who had thin fluid aspiration on videofluoroscopic swallowing study (VFSS) were included in this retrospective study. Enrolled children were then divided into two feeding method groups according to the physician's decision at the time of VFSS: oral feeding (OF) group and non-oral feeding (NOF) group. Data were obtained from 47 children (median age: 49.75 months, interquartile range [IQR]: 24.08–79.42). The incidence of pneumonia within 1 year after the VFSS was not different between NOF (
In children with swallowing difficulties, aspiration of food and fluid is commonly observed and is associated with a wide range of diseases. Current management decisions for aspiration generally include tube feeding, restricting aspirated diets, and providing texture-modified foods and thickened fluids (
With regard to starting tube feeding during the first few years of life, it has been reported that the feeding outcome could be poor although the pharyngeal phase of swallowing is well preserved (
In 2016, McSweeney et al. reported that oral feeding of nectar or honey-thickened liquids instead of tube feeding via gastrostomy reduced the hospitalization frequency in children with aspiration or penetration findings on their videofluoroscopic swallow study (VFSS) (
In this study, we hypothesized that swallowing function could improve over time if infants or young children attempted oral feeding before the aero-digestive centers are fully established.
Thus, this study aimed to investigate whether oral feeding challenges in children with tracheostomy can improve feeding outcomes, even with the finding of aspiration compared to group that did not receive oral diets at all.
All study-related procedures were performed in accordance with the ethical standards of the institutional and/or national research committee and the 1964 Declaration of Helsinki. Ethical approval for the study was obtained from our institutional review board (Approval No. 1803-115-932), which waived the requirement for informed consent due to the retrospective nature of the study. The following inclusion criteria were applied to potential subjects: (1) confirmed aspiration of fluid in a VFSS at <7 years of age between 2011 and 2017, (2) had a tracheostomy at the time of VFSS, and (3) medical records were available at least 1 year after the initial VFSS. When performing VFSS, foods with fluid consistency (e.g., water, juice) were always used, but foods with different consistencies (e.g., Yoplait, puree, cookies) were also used depending on individual eating habits. In many cases, parents brought foods that the children commonly ate at home and we tested these diets. VFSS results when using the diets other than fluid ones were not included in the inclusion or exclusion criteria. Patients with fluid swallowing of <2 times on VFSS records and those who refused food during VFSS were excluded from the analysis.
Enrolled children were then divided into two groups according to the feeding method received, per physician's decision at the time of VFSS: (1) oral feeding group (OF group), who were recommended partial oral feeding (POF) or full oral feeding (FOF) and (2) non-oral feeding (NOF) group, who were recommended exclusive tube feeding.
The caregiver played an important role in the oral feeding challenge. Oral feeding trial was conducted only when the parents were skillful and cooperative in suctioning during and immediately after the oral feeding. The oral feeding trial tended to be not applicable in school-age children, because parents were not able to perform suction while the children were in school. Therefore, we only included preschool children (<7 years of age) for the analysis. The oral diet was started at a low dose of 0.1–0.2 cc for the first time and gradually increased. The physician recommended the rate of increase considering the results of VFSS. Suction was carried out using portable equipment for home use. The depth and frequency of suctioning were not specified, but caregivers were instructed to perform shallow and gentle suctioning.
Primary outcome was defined as the feeding status (FOF, POF, or NOF) 1 year after the VFSS. The feeding status at the time and 1 year after the VFSS was recorded for all children through a medical record survey. Secondary outcomes included the occurrence of pneumonia and days of hospitalization related to pulmonary complications within 1 year after the VFSS.
Patient records were reviewed for the sex and age of the patients at the time of their first VFSS. Initial feeding status before the VFSS was recorded for all children. The penetration-aspiration scale (PAS) on VFSS was rated by one of the authors. PAS scale is an 8-point scale developed to characterize the severity of airway invasion events viewed during VFSS, capturing the location to which material is observed to travel and then qualifying that information based on whether the material remains there at the end of the swallow or is ejected to safer (anatomically higher) locations (
For children who underwent both initial VFSS and 1 year follow-up VFSS, the pharyngeal transit time (PTT) as well as the PAS scale (
Differences in continuous variables between the two groups were analyzed using the Wilcoxon rank sum test. In case of categorical variable, statistical significance was calculated by using Chi-square or Fisher's exact test. Main diagnoses were categorized as brain lesion as well as neuromuscular, cardiac, gastrointestinal, pulmonary, and otolaryngeal comorbidities for univariate and multivariate analyses; the comorbidities were not considered to be mutually exclusive. Given that the primary outcome comprised three categorical nominal variables (POF, FOF, and NOF), multinomial logistic regression was used to estimate the odds ratio (OR). Mann-Whitney U-test was used to compare initial PTT and follow-up PTT between groups. Analyses were performed using SAS statistical software (SAS system for Windows, version 9.4; SAS institute, Cary, NC).
Data were obtained for 47 children (median age: 49.75 months, interquartile range [IQR]: 24.08–79.42) who had tracheostomies and confirmed aspiration of fluid on initial VFSS between 2011 and 2017 (
Flowchart of children with tracheostomy younger than 7 years of age with definite fluid aspiration confirmed via VFSS. VFSS, videofluoroscopic swallowing study.
Characteristics of subjects at the time of the videofluoroscopic swallowing study.
Female sex, |
4 (23.53) | 14 (46.67) | 18 (38.30) | 0.117 |
Age, median (IQR), months | 61.75 |
35.42 |
49.75 |
0.257 |
Main diagnosis | ||||
Myopathy/motor neuron disease | 7 (41.18) | 5 (16.67) | 12 (25.53) | 0.064 |
Brain lesion | 6 (35.29) | 14 (46.67) | 20 (42.55) | 0.449 |
Others |
4 (23.53) |
11 (36.67) |
15 (31.91) |
0.517 |
CHARGE syndrome | 2 (11.76) | 0 (0) | 2 (4.26) | |
Initial feeding status, |
0.152 |
|||
NOF | 11 (64.71) | 10 (33.33) | 21 (44.68) | |
Partial OF | 4 (23.53) | 13 (43.33) | 17 (36.17) | |
Full OF | 2 (11.76) | 7 (23.33) | 9 (19.15) | |
Initial PAS, median (IQR) | 8 (8–8) | 8 (8–8) | 8 (8–8) | 0.631 |
In children with tracheostomies, there was a significant difference in feeding status after 1 year between the OF and NOF groups (
Outcome assessment 1 year after videofluoroscopic swallowing study in each group.
Feeding status after 1 year, |
<0.0001 |
|||
NOF |
11 (64.71) |
1 (3.57) |
12 (26.67) |
|
Pneumonia presence within 1 year, |
8 (47.06) | 9 (30) | 17 (36.17) | 0.242 |
Pulmonary inpatient days within 1 year, mean (SD) | 5 (8.3) | 3.93 (7.59) | 4.32 (7.78) | 0.304 |
The presence of neuromuscular disease was different between the two groups, with 8 (47.06%) in the NOF group and 5 (16.67%) in the OF group having a neuromuscular disease (
Univariate and multinomial logistic regression analysis was conducted to calculate the OR of each factor affecting the feeding status after 1 year. Compared with the NOF group, the OF group showed an OR of 35.714 (
Univariate analysis via multinomial logistic regression for feeding status (full oral feeding, partial oral feeding, or non-oral feeding) 1 year after the initial VFSS.
Age (years) | 0.9366 | ||||
NOF |
1.0 | ||||
POF | 0.924 | 0.595 | 1.435 | 0.7242 | |
FOF | 0.938 | 0.57 | 1.543 | 0.8009 | |
Group |
0.0022 | ||||
NOF | 1.0 | ||||
OF vs. NOF group |
POF | 35.714 | 3.597 | 333.33 | 0.0022 |
OF vs. NOF group |
FOF | 125 | 6.711 | >999.999 | 0.0012 |
Sex | 0.8757 | ||||
NOF | 1.0 | ||||
Female vs. male | POF | 1 | 0.222 | 4.502 | 1.000 |
Female vs. male | FOF | 1.429 | 0.271 | 7.518 | 0.6738 |
Initial feeding status | 0.1408 | ||||
NOF | 1.0 | ||||
OF vs. NOF | POF | 2.2 | 0.504 | 9.611 | 0.2946 |
OF vs. NOF | FOF | 6.0 | 1.018 | 35.374 | 0.0478 |
Neuromuscular | 0.9031 | ||||
NOF | 1.0 | ||||
No vs. yes | POF | 1.25 | 0.271 | 5.765 | 0.7748 |
No vs. yes | FOF | 1.5 | 0.254 | 8.844 | 0.6542 |
Brain | 0.693 | ||||
NOF | 1.0 | ||||
No vs. yes | POF | 0.75 | 0.181 | 3.115 | 0.6921 |
No vs. yes | FOF | 1.4 | 0.279 | 7.015 | 0.6824 |
Otolaryngeal | 0.5287 | ||||
NOF | 1.0 | ||||
No vs. yes | POF | 1.067 | 0.205 | 5.543 | 0.9388 |
No vs. yes | FOF | 0.467 | 0.082 | 2.656 | 0.3904 |
Respiratory | 0.1914 | ||||
NOF | 1.0 | ||||
No vs. yes | POF | 0.7 | 0.162 | 3.023 | 0.6328 |
No vs. yes | FOF | 2.8 | 0.532 | 14.735 | 0.2243 |
Cardiac | 0.2192 | ||||
NOF | 1.0 | ||||
No vs. yes | POF | 2.5 | 0.572 | 10.932 | 0.2235 |
No vs. yes | FOF | 5 | 0.753 | 33.213 | 0.0957 |
Gastrointestinal | 0.9784 | ||||
NOF | 1.0 | ||||
No vs. yes | POF | 0.85 | 0.131 | 5.505 | 0.8643 |
No vs. yes | FOF | 1 | 0.117 | 8.561 | 1.000 |
For 29 children with follow-up VFSS (
The change in the penetration-aspiration scale (PAS) between the first VFSS and follow-up VFSS.
In the OF group, there was a tendency for follow-up PTT (median 0.701 s, IQR: 0.600–0.984) to be shorter than the initial PTT (median 0.901s, IQR: 0.784–1.517), although the difference was not statistically significant (
There have been few reports regarding the effects of oral feeding trial on the development of swallowing function in children with aspiration. The results of this study suggest that swallowing function might improve over time if infants or young children attempt oral feeding before the aero-digestive centers are fully established despite aspiration findings on VFSS. Moreover, improvement in follow-up PAS was observed only in the group that received oral feeding.
From birth to 3 years of age, children learn to adapt the swallowing mechanism to accommodate different foods, fluids, and textures (
In adults with stroke, it was reported that patients with tracheostomies had inferior swallowing function and kinematics compared to those without tracheostomies (
Although tracheostomy interferes with swallowing function, it has the potential to promote oral feeding challenge (
Although in the present study there was a difference in the frequency of neuromuscular disease between those who received oral feeding and those who did not, this seemed not to be a factor affecting feeding outcome after 1 year according to the multinomial logistic regression analysis. Among the OF group, 5 children were diagnosed with neuromuscular disease, 3 with congenital myopathy, and 2 with muscular dystrophy. Among them, 3 achieved FOF and 2 achieved POF after 1 year. Two children developed pneumonia within 1 year. Among the NOF group, 8 children were diagnosed with neuromuscular disease, 5 with congenital myopathy, 2 with muscular dystrophy, and 1 with motor neuron disease. Among them, 4 achieved POF and 4 remained at NOF status. Four of them developed pneumonia within 1 year. These results suggest that the swallowing function could be improved at least in the short term by the growth of the pharyngeal muscles (
Firstly, frequent suctioning may cause laryngeal wall irritation and tracheal wall injury. Injurious prolapse of the tracheal mucosa may occur by suctioning (
Secondly, many parents of children who underwent an oral feeding trial reported that food was expelled through the tracheostomy during feeding without suctioning (for example, when the grape juice was fed, the purple liquid came out). Suction should be considered to be an incomplete method of removing all aspirates. If the aspirate not removed by suction or drainage through the tracheostomy exceeds a certain threshold, respiratory complications, such as aspiration pneumonia might occur. However, aspirates below a certain amount may not cause problems. Weiss (
There are several limitations to this study. Firstly, this was a single-center study with a small number of subjects, which may have led to a selection bias. Secondly, because this study retrospectively obtained information from the medical records, it is possible that patients were regarded as having no respiratory complications if they had been previously treated for pneumonia in another hospital. Moreover, we could not clearly distinguish whether pneumonia was related to aspiration or not; thus, we analyzed pulmonary admission days and occurrence of pneumonia, as performed in the previous studies (
In infants and young children with tracheostomy, oral feeding challenge improved the feeding outcome without an increased risk of pneumonia, although aspiration was confirmed by VFSS. These results suggest that oral feeding challenges might be attempted if aspirates can be removed through the tracheostomy even with the findings of aspiration.
The datasets generated for this study are available on request to the corresponding author.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Ethical approval was obtained from the Seoul National University Hospital Institutional Review Board (IRB) No. 1803-115-932, which waived the requirement for informed consent due to the retrospective nature of the study.
YY: acquisition of data, analysis and interpretation of data, writing, and critical revision of manuscript. B-MO: analysis and interpretation of data, and critical revision of manuscript. SY: critical revision of manuscript. H-IS: study concept and design, acquisition of data, analysis and interpretation of data, study supervision, and critical revision of manuscript for intellectual content.
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.
We appreciate the statistical advice of the Medical Research Collaborating Center, Seoul National University Hospital.