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Dysphagia https://doi.org/10.1007/s00455-018-9894-7

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ORIGINAL ARTICLE

Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and Literature Review Gowun Kim1 • Sora Baek1

•

Hee-won Park1,2 • Eun Kyoung Kang1 • Gyuhyun Lee1

Received: 16 January 2017 / Accepted: 29 March 2018  Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract Nasogastric tube (NGT) is a common feeding strategy for patients at risk of endotracheal aspiration with an oral diet. With NGT feeding, however, swallowing of small amounts saliva cannot be avoided. We investigated whether the aspiration rate when swallowing 1 mL of fluid increased in patients using an NGT in different dysphagia severities. One hundred fortyseven patients who had been receiving NGT feeding underwent a videofluoroscopic swallowing study (VFSS). During VFSS, subjects were offered 1 mL of fluid twice: initially, with the tube inserted (NGT-in) and, subsequently, with the tube removed (NGT-out). Aspiration depth was determined using the 8-point Penetration–Aspiration Scale (PAS) (0 points, no aspiration/penetration; 8 points, aspiration passing the vocal cords with no ejection efforts). PAS-diff was computed (PASNGT-in - PASNGT-out), and a positive PAS-diff (PAS-diff [ 0) meant increased aspiration depth in the presence of NGT. After VFSS, diet recommendations were made according to dysphagia severity assessment: non-oral feeding (n = 59), diet modification (n = 74), and diet as tolerated (n = 13). Cognitive level (mini-mental state examination, MMSE) and general functional level (Modified Barthel Index, MBI) were compared between the PAS-diff [ 0 and PASdiff B 0 groups. Aspiration severity did not significantly change after NGT removal (PASNGT-in, 2.45 ± 2.40; PASNGT-out, 2.57 ± 2.58; P = .50). Regardless of recommended diet, PAS-diff values were not significantly different (P = .49). MMSE and MBI were not significantly different (P = .23 and .94) between subjects with PAS-diff [ 0 (n = 25) and PAS-diff B 0 (n = 121). In conclusion, the risk of aspirating a small amount of fluid was not significantly different before and after NGT removal, regardless of swallowing function, cognitive level, or general functional level. Keywords Deglutition
Deglutition disorder
Nasogastric tube
Aspiration
Rehabilitation

Introduction Nasogastric tube (NGT) is widely used for enteral feeding access because it is simple and inexpensive [1]. An estimated 271,000 NGTs were used annually in the United Kingdom alone [2]. NGTs vary in bore size, from small bore (8-12Fr) to large bore (C 14Fr) [1], and large bore NGTs can be used more often than small bore NGTs for

& Sora Baek [email protected] 1

Department of Rehabilitation Medicine, Kangwon National University Hospital, Kangwon National University School of Medicine, Baengnyeong-ro 156, Chuncheon, Gangwon 24289, South Korea

2

Gangwon-do Rehabilitation Hospital, Chuncheon, South Korea

feeding purposes [3]. NGT is frequently used to improve nutritional intake for patients with impaired mental status or patients with inadequate oral intake [1, 3]. It is also used for patients with dysphagia for oropharyngeal bypass feeding to avoid endotracheal aspiration during oral feeding and secondary pulmonary complications such as aspiration pneumonia in patients [3]. Pneumonia is related to prolonged hospital stay and increased mortality. According to mortality reports in the United States, pneumonitis due to aspirated solids and liquids is one of the leading causes of death [4]. For patients with dysphagia, prevention of aspiration pneumonia is one of the therapeutic goals, and NGTs are often placed to prevent aspiration pneumonia [3]. The role of NGT, however, seems to be limited in its protective effects against aspiration pneumonia. The incidence of aspiration pneumonia is still high in patients fed by NGT [5]. In 100

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Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and…

patients with stroke, 40% of patients fed by NGT developed aspiration pneumonia [6]. Several mechanisms have been suggested for the relatively high pneumonia incidence in patients with NGT feeding. NGT occupies some space in the nasopharynx, oropharynx, and hypopharynx and may interfere with pharyngeal swallowing in both healthy individuals and those with dysphagia. In normal subjects, the presence of NGT is associated with temporal slowing, delayed initiation of maximal hyolaryngeal excursion, or a longer duration of upper esophageal sphincter opening and total swallowing [7, 8]. In previous studies of subjects with impaired swallowing function, the presence of NGT in the pharynx did not result in changes in aspiration rate. However, the severity of impaired swallowing function was not considered in the analysis of the effect of NGT. Severe dysphagia could compromise the swallowing to a greater degree than less severe. We aimed to investigate whether the aspiration risk would increase with an NGT inserted compared to removed when swallowing a small amount of fluid, and to determine the effect of NGT on swallowing function in patients with different severities of dysphagia.

Fig. 1 Inclusion flow diagram

Materials and Methods Subjects We retrospectively reviewed the medical records of 591 patients who presented to the Department of Rehabilitation Medicine at Kangwon National University Hospital for videofluoroscopic swallowing study (VFSS) for suspected swallowing difficulties from January 2014 to June 2015. Among the 591 patients, 221 patients were receiving NGT feeding. Sixty-five patients were excluded because NGT had been removed at the ward just before VFSS. Nine patients failed to complete the study after tube removal. Finally, 147 patients were included in the final analysis, and their medical records were retrospectively reviewed (Fig. 1). We did not insert an NGT for the purpose of the study. Only subjects with an NGT inserted before the study were tested. This study protocol was approved by our institutional review board. Age, sex, and underlying disease were reviewed.

Evaluation of Severity of Dysphagia VFSS was used to assess swallowing function. It permits collection of detailed information regarding the structure and function of the oropharynx, pharynx, and larynx as well as the upper esophageal swallowing complex. It also

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Fig. 2 Nasogastric tube inserted state

permits assessment of the potential benefits of compensatory and treatment strategies [9]. The VFSS was performed to patients in their upright sitting posture by a doctor in a fluoroscopy room. Patients arrived at the fluoroscopy room with an NGT inserted. The NGT was a 16-Fr all-silicone tube (Levin tube, Sewoon Medical Co., Ltd., Cheonan, Korea) in 116 subjects who had the NGT inserted in our hospital. The size of the NGT was not recorded in 31 patients that had their NGTs inserted in other hospitals, but most NGTs were inserted for the purpose of feeding, and thus the size would be 16-Fr in most cases. Swallowing of 1 mL thin fluid was evaluated as a part of the standard clinical evaluation of VFSS at our hospital. To

Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and…

evaluate the effect of NGT on swallowing function, patients were evaluated while swallowing 1 mL of thin fluid with the NGT in place (NGT-in) (Fig. 2). Then the NGT was removed, and the swallowing of 1 mL of fluid was re-evaluated (NGT-out). The thin fluid was offered to the subjects in a spoon. After completion of the 1 mL fluid tests, patients subsequently attempted to swallow barium-impregnated boluses of different volumes and consistencies with the NGT removed: 2 mL thin fluid, 5 mL thin fluid, yogurt, pudding, solids, and thick liquid. The fluoroscopic images of the studies were recorded as a video file. For the thin fluid test, diluted barium fluid was prepared as 43% weight/ volume barium sulfate (Solotop sol 130, Tae Joon Pharmaceutical, Seoul, Korea). Chest radiographs were taken after the study and reviewed to look for aspiration. After VFSS, the dysphagia severity was assessed, and a decision about the proper diet for each patient was made based on it: tube feeding, diet modification, or diet as tolerated. Tube feeding was recommended for patients with severe dysphagia. Diet modification using viscosity change was recommended in patients with moderate dysphagia. Diet as tolerated was recommended in patients without evidence of aspiration or penetration during VFSS.

Cognitive Function and General Function To assess the patients’ cognitive function, the Korean version of the Mini-Mental State Examination (MMSE-K) was used [11]. The Korean version of the Modified Barthel Index (K-MBI) was reviewed to assess the patients’ general function and ability to perform activities of daily living [12]. Among the 147 patients, MMSE-K and K-MBI were investigated in 135 and 125 subjects, respectively.

Statistics SPSS for Windows, version 21.0 (IBM Corp., Armonk, NY) was used for statistical analysis. Wilcoxon signed rank test and Friedman test analyses were used to compare PAS between the NGT-in and NGT-out states. PAS-diff was calculated from the difference of PAS in NGT-in and NGT-out. The PAS-diff value was analyzed according to the types of recommended diet after VFSS using analysis of variance. Chi square and t test were used to compare the baseline characteristics, MMSE-K, and K-MBI between the PAS-diff [ 0 and PAS-diff B 0 groups.

Penetration–Aspiration Scale in 1 mL Tests The aspiration/penetration status on the video clip was reviewed by 2 medical doctors who are experienced in VFSS. The aspiration severity in both NGT-in and NGTout patients was assessed using the 8-point penetration– aspiration scale (PAS). PAS was determined by the depth of material invasion to the airway and by whether or not material entering the airway was expelled. A higher value indicates more severe aspiration: 0 points, no aspiration/ penetration; 8 points, aspiration passing the vocal cords with no ejection efforts [10]. Aspiration depths in the 1 mL fluid tests for both NGT-in and NGT-out were compared between subjects with the 3 different recommended diets. The difference in PAS between the NGT-in and NGTout state (PAS-diff = PASNGT-in - PASNGT-out) was calculated. Positive PAS-diff (PAS-diff [ 0) represents the increase in aspiration depth in the presence of NGT. PASdiff was compared between subjects with 3 different recommended diets to determine the effect of NGT on swallowing function in patients with different severities of dysphagia. Then, patients were divided into two groups, PAS-diff [ 0 and PAS-diff B 0, to evaluate any differences in demographic characteristics, severity of dysphagia, cognitive level, and general functional level between groups. Patients with PAS-diff [ 0 were considered to have compromised swallowing function in the presence of NGT.

Table 1 Basic characteristics of subjects (N = 147) Variable Sex, N (%) Men Women Age, mean (SD), years

90 (61.2) 57 (38.8) 74.2 (9.2)

Cause of dysphagia, N (%) Stroke Hemorrhage Infarction

96 (65.3) 35 (36.4) 61 (63.5)

Traumatic brain injury

13 (8.8)

Parkinson disease

15 (10.2)

Dementia

8 (5.4)

Cervical spine operation

4 (2.7)

Myopathy

1 (0.7)

Hypoglycemic encephalopathy

1 (0.7)

Uremic encephalopathy

1 (0.7)

Viral encephalitis

1 (0.7)

Recurrent laryngeal nerve injury

1 (0.7)

Unknown

6 (4.1)

SD standard deviation

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Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and…

Results

Discussion

The demographic characteristics and causes of dysphagia of the 147 patients are summarized in Table 1. The mean (standard deviation, SD) age was 74.2 (9.2) years, 90 patients were men, and 57 patients were women. The most common causes of dysphagia were stroke (n = 96, 65.8%), Parkinson disease (n = 15, 10.2%), and traumatic brain injury (n = 13, 8.8%). Diet recommendations were determined based on dysphagia severity as assessed by VFSS: tube feeding for 59 patients, diet modification for 75 patients, and diet as tolerated for 13 patients. Mean (SD) PAS values in the NGT-in and NGT-out states were 2.5 (2.40) and 2.6 (2.58) and were not statistically different (P = .50) (Table 2). The mean (SD) value of PAS-diff was - 0.1 (2.53). PAS values between recommended diet groups were significantly different in NGTin (P \ .01) and NGT-out (P \ .01) states and were highest in patients who were recommended to continue non-oral feeding (Table 3). Mean (SD) values of PAS-diff were - 0.4 (2.79), 0.0 (2.47), and 0.3 (1.11) in patients recommended to have tube feeding, diet modification, and diet as tolerated, respectively, and were not statistically different between the 3 recommended diet groups (P = .49). The basic characteristics of the PAS-diff [ 0) and PASdiff B 0 groups are summarized in Table 4. There was no difference in sex, age, or recommended diet between the two groups (P = .45). MMSE-K and K-MBI were not significantly different between the 2 groups (P = .23 and .94, respectively) (Table 5).

We attempted to investigate whether the presence of NGT would increase the aspiration risk when swallowing a small volume, mimicking normal saliva swallowing. In this study, the risk of aspirating a small amount of fluid was not significantly different before and after NGT removal, regardless of swallowing function, cognitive level, or general functional level. In many cases, NGT is used for nutrition and prevention of pneumonia in patients with dysphagia. However, NGT feeding has not been shown to reduce the risk of aspiration or pneumonia in many studies [5, 13]. Some researchers suspect that the oropharyngeal swallowing mechanism would be disturbed by the NGT in the pharynx and has been suggested that NGTs are related to gastrointestinal complications and local irritation [14]. There are normally produced secretions in the oropharyngeal space [15]. Swallowing of saliva and/or regurgitated gastric contents occurs continuously during NGT feeding, which could be related with aspiration pneumonia with NGT-fed patients. The volume of daily secretions in the subglottic space was 10–15 mL in patients receiving mechanical ventilation [16]. The major source of subglottic secretions is saliva. The amount of saliva in the oral space is about 1 mL, and the volume of a single swallow is about 0.3 mL [17]. For patients with stroke, the saliva flow rate (0.09 ± 0.05 mL/ min) was less than in the normal group (0.73 ± 0.37 mL/ min) [18]. Besides salivary secretions, gastric contents are another source of aspiration. In patients with NGT, the chance of gastroesophageal reflux of the gastric contents could be increased compared to that in patients without NGT [19, 20]. On a pepsin immunoassay analysis, at least one tracheal secretion was pepsin positive in 88.9% (n = 320) of the subjects who were tube-fed and mechanically ventilated [21].

Table 2 The 8-grade penetration–aspiration scale before and after nasogastric tube removal (NGT-in and NGT-out) (N = 147) NGT-in

NGT-out

P

PAS, mean (SD)

2.5 (2.40)

2.6 (2.58)

.50

PAS scale, N (%) 1 Material does not enter the airway

95 (64.6)

96 (65.3)

.50

2 Material enters the airway, remains above the vocal folds, and is ejected from the airway

9 (6.1)

7 (4.8)

3 Material enters the airway, remains above the vocal folds, and is not ejected from the airway

10 (6.8)

8 (5.4)

4 Material enters the airway, contacts the vocal folds, and is ejected from the airway

4 (2.7)

4 (2.7)

5 Material enters the airway, contacts the vocal folds, and is not ejected from the airway

10 (6.8)

9 (6.1)

6 Material enters the airway, passes below the vocal folds, and is ejected into the larynx or out of the airway

0 (0.0)

0 (0.0)

7 Material enters the airway, passes below the vocal folds, and is not ejected from the trachea despite effort

3 (2.0)

1 (0.7)

8 Material enters the airway, passes below the vocal folds, and no effort is made to eject

16 (10.9)

22 (15.0)

NGT Nasogastric tube, PAS penetration–aspiration scale, SD standard deviation

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Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and… Table 3 PAS-diff according to type of diet recommendation after videofluoroscopic swallowing study Recommended diet

Subjects, N (%)

PASNGT-in, mean (SD)

P

PASNGT-out, mean (SD)

P

PAS-diff, mean (SD)

F

P

Non-oral feeding

59 (40.1)

3.4 (2.74)

\ .001

3.8 (2.95)

\ .001

-0.4 (2.79)

0.715

.491

Diet modification

77 (52.4)

1.9 (1.98)

1.9 (2.03)

0.0 (2.47)

Diet as tolerated

11 (7.5)

1.3 (1.11)

1.0 (0.00)

0.3 (1.11)

PAS Penetration–aspiration scale, SD standard deviation

Table 4 Baseline characteristics of subjects in the PAS-diff [ 0 group (N = 25) and the PASdiff B 0 group (N = 122)

PAS-diff [ 0 group

PAS-diff B 0 group

P

Men

14 (56.0)

76 (62.3)

.705

Women

11 (44.0)

46 (37.7)

73.6 (7.40)

74.4 (9.54)

.559

Non-oral feeding

11 (44.0)

48 (39.3)

.449

Diet modification

13 (52.0)

62 (50.8)

Diet as tolerated

1 (4.0)

12 (9.8)

Sex, N (%)

Age, [mean (SD), years] Recommended diet, N (%)

PAS Penetration–aspiration scale, SD standard deviation

Table 5 MMSE-K and K-MBI in patients in the PAS-diff [ 0 group (N = 25) and PASdiff B 0 group (N = 122)

PAS-diff [ 0

PAS-diff B 0

t

P

MMSE-K, mean (SD)

16.7 (8.71)

14.4 (8.57)

-1.200

.232

K-MBI, mean (SD)

23.0 (17.41)

22.6 (22.48)

-0.077

.939

MMSE-K Korean version of mini-mental state examination, K-MBI Korean Version of Modified Barthel Index, PAS penetration–aspiration scale, SD standard deviation

Some of the temporal components of swallowing were changed in the presence of NGT. Robbins et al. reported the effect using a manometry tube in swallowing 2 mL of liquid barium and 2 cm3 of semi-solid barium in normal subjects [7]. In the manometry tube-in condition, the velar duration was shorter, and durations of hyoid maximum elevation, hyoid maximum anterior excursion, and upper esophageal sphincter opening were longer than the tube out state. However, there was no aspiration in any subjects. A similar trend was seen in studies using NGT. The report by Huggins et al. revealed that pharyngeal transit time was prolonged with NGT in normal subjects, but there was no aspiration [8]. There was also prolonged transit time during NGT-in for patients with stroke, but the difference was not statistically significant [22]. However, there were no obvious changes in pharyngeal clearance or airway protection in normal subjects [8]. Several previous studies have investigated the effect of NGT on the swallowing mechanism and aspiration (Table 6) [7, 8, 22–24]. Four of five papers we reviewed used NGT, and one study used manometry. A manometry

catheter was guided through the patient’s nose into the esophagus and positioned in a similar location to the NGT. The size of the tube, the amount of food studied, and the subjects varied. In the 4 previous studies using NGTs, 16 Fr tubes were used in one study, and the other 3 studies used 2 tubes with different bore sizes. Most studies evaluated the effects of diet with a volume of 5 mL, and only one study tested a 2 mL volume. In 22 stroke patients with minor or no aspiration, NGT placement did not affect temporal and non-temporal components of 5 mL fluid swallowing [22]. There were similar trends in 2 other studies on subjects who were referred for dysphagia evaluation. In both studies, NGTs did not affect the aspiration status of 5 mL of fluid or purees [23, 24]. Like previous studies, our results demonstrated that the aspiration risk for 1 mL of fluid was not significantly different with or without NGT. We used PAS to grade the depth of aspiration. There was no statistical difference in PAS values when swallowing 1 mL of fluid when comparing NGT-in and NGT-out states and reaffirmed the previous results that there is no significant impact of NGT on aspiration risk [22–24].

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Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and… Table 6 Review of literature Type of tube

Size of tubes

Subjects

No. of subjects

Design (sequence of tube in and out)

Swallowing function of subjects

Studied diets

Main changes in presence of NG tube

Reference

Manometry

NR

Normal

80

In/out

Normal

2 mL liquid barium and 2 cm3 semisolid barium

Slowed swallowing

Robbins [7]

NGT

8 Fr and 16 Fr

Normal

10

In (8 Fr)/in (16 Fr)/out

Normal

5 mL of 96% (w/ v) barium sulfate

Slowed swallowing

Huggins [8]

NGT

16 Fr

Stroke patients

22

In/out

Minor or no aspiration of barium on VFSS

5 mL of thin and thick barium

No significant changes in temporal and nontemporal measurements

Wang [22]

NGT

Group 1: 8 Fr or 18 Fr

Patients referred for dysphagia evaluation

630

Group 1: in

NR

(Group 1: 630,

Group 2: out

5 mL of thin liquid and pureed food

No change in aspiration status

Leder [24]

NR

5 mL of thin liquid and pureed food

No change in aspiration status

Fattal [23]

Group 2: no tube NGT

Group 1: 8 Fr or 18 Fr Group 2: 8 Fr

Group 2: 630) Patients referred for dysphagia evaluation

62 (Group 1: 21 Group 2: 41)

Group 1: in ? out Group 2: out ? in

NR not recorded, VFSS videofluoroscopic swallowing study, NGT nasogastric tube

In this study, we also aimed to determine the effect of NGT on swallowing function in patients with different severities of dysphagia. Diet recommendations were determined based on the dysphagia severity assessed by VFSS: tube feeding for 59 patients, diet modification for 75 patients, and diet as tolerated for 13 patients. We found that PAS-diff values were not statistically different between the 3 diet recommendation groups, which showed that the effect of NGT on swallowing function was also equally negligible among different severities of dysphagia. Patients with NGT feeding tend to be more cognitively and functionally impaired [13]. Previous studies demonstrated that poor functional status and cognitive function were associated with poorer swallowing outcomes [25, 26]. These previous researches imply that functional status and cognitive function are strongly associated with swallowing function. Among the 147 patients in this study, 25 patients had a PAS-diff [ 0 and 122 patients had a PAS-diff B 0. When comparing these groups, MMSE-K and K-MBI were not significantly different, demonstrating that the risk of aspiration of a small amount of fluid was not significantly different before and after removal of NGT regardless of

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swallowing function, cognitive level, or general functional level. Strengths of our study include the relatively large number of subjects evaluated. Most studies’ sample size was 10–80 subjects. There was one study with a larger sample size than this study, but the design was 630 patients with NGT matched with controls without NGT [24]. We evaluated the same subjects with and without NGT. There were limitations to our study. The order of the various swallowing tests was not randomized. Our subjects were already solely tube-fed, and we did not insert NGT for the purpose of the study. We did not evaluate any hindering effects of NGT from a kinematic aspect. Even though rate of aspiration was not increased, temporal change of swallowing was observed in the presence of NGT in previous studies [7, 8], and kinematic analysis of hyoid bone or epiglottis movement could have identified the reason of those temporal changes. Prospective development of pneumonia after VFSS was not reviewed in this study. In the future, the effect of NGT on the long-term development of pneumonia between subjects with similar swallowing difficulty could be needed. Finally, we did not include

Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and…

semi-solid or solid foods to evaluate the effect of NGT. In most patients, oral diets are provided in semi-solid or solid form. NGT has been suspected to disrupt normal swallowing and NGT is commonly removed before starting oral diets in patients that are NGT-fed. Oral diet studies involving semi-solid diets for patients with in situ NGT should be considered to provide the basis to allow additional oral feeding in patients with NGT.

7.

8.

9.

10.

Conclusion NGT is a widely used tool to administer nutrition, but there are misunderstandings about the role of NGT. NGT is believed by many to reduce aspiration events and pulmonary complications. On the other hand, NGT is considered to be a risk factor for pneumonia in population studies and NGT has been suspected to disrupt normal swallowing. This study showed that the aspiration risk of swallowing a small amount of fluid was not significantly different before and after removal of NGT, regardless of swallowing function, cognitive level, and general functional level. We hope that these results will be valuable for diet prescription and dysphagia management in patients that are NGT-fed.

11.

12.

13.

14.

15.

16.

17.

Compliance with Ethical Standards

18.

Conflict of interest The authors declare that they have no conflict of interest.

19.

Ethical Approval None of the authors has any proprietary interests in the materials described in this article. This study protocol was approved by our institutional review board.

20.

Informed Consent We retrospectively reviewed the medical records, and informed consent was waived. 21.

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Effect of Nasogastric Tube on Aspiration Risk: Results from 147 Patients with Dysphagia and… Eun Kyoung Kang MD, PhD Gowun Kim MD Gyuhyun Lee MD Sora Baek MD, PhD Hee-won Park MD, MA

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