Academiejaar 2015 – 2016

'THE ULTRASOUND ‘POP-UP SIGN’ RELIABLY

PREDICTS CORRECT NASOGASTRIC TUBE

POSITION IN INTENSIVE CARE UNIT PATIENTS

Pieter VERSLYPE

Promotor: Prof. dr. P. Wouters

Co-promotor: Dr. W. Stockman

Masterproef voorgedragen in de master in de specialistische geneeskunde

Anesthesie en Reanimatie

Academiejaar 2015 – 2016

'THE ULTRASOUND ‘POP-UP SIGN’ RELIABLY

PREDICTS CORRECT NASOGASTRIC TUBE

POSITION IN INTENSIVE CARE UNIT PATIENTS

Pieter VERSLYPE

Promotor: Prof. dr. P. Wouters

Co-promotor: Dr. W. Stockman

Masterproef voorgedragen in de master in de specialistische geneeskunde

Anesthesie en Reanimatie

Abstract (English)

The ultrasound pop-up sign reliably predicts correct nasogastric tube position in ICU patients

Introduction:

Complications due to a malpositioned nasogastric tube (NGT) may have disastrous

consequences leading to prolonged length of stay or ultimately death. Therefore the correct

position must be confirmed before usage of the NGT. Although several methods have been

investigated, chest radiograph remains the golden standard to confirm correct position.

However, a chest X-ray in an ICU patient has disadvantages including radiation exposure,

cost and labor intensity.

Objective:

The aim of this study is to investigate the diagnostic accuracy of the ultrasound pop-up sign to

confirm correct position of a nasogastric tube in ICU patients compared with chest X-ray.

Material and methods:

In this single center prospective study, adult patients admitted to our ICU were included if a

NGT was placed. After placement the correct position was tested by ultrasound. The patient

remained in the dorsal decubitus position with the head of the bed elevated 30°. The antrum

was visualized by ultrasound and then NGT was rapidly insufflated with 60 ml of air. If a

sudden pop-up of air was identified in the stomach the sign was considered positive. A chest

X-ray was subsequently taken to confirm position.

Results:

Eighty patients were included. The mean patient age was 66 ± 14.6 years. The mean Body

Mass Index was 24.7 ± 5.5. Sixty-four patients (80%) were invasively ventilated. In 63/80

patients (79%) the pop-up sign could be identified. In all these 63 patients correct position of

the NGT was confirmed by chest X-ray (positive predictive value 100%). In 17 patients the

pop-up sign could not be identified. Of these the nasogastric tube was correctly placed in the

stomach in 14 patients (88%), while two (12%) were midesophageal and one postpyloric

(6%). The sensitivity of the method is thus 63/77 (=0.82).

Conclusion:

The ultrasound pop-up sign is a very reliable predictor of correct nasogastric tube position and

is present in 82% of correctly positioned nasogastric tubes. We believe a confirmatory chest

X-ray can be omitted after visualization of the pop-up sign.

Abstract (Nederlands)

Het ultrasound pop-up sign is een betrouwbare predictor van correcte nasogastrische tube

positie in intensieve zorg patienten.

Inleiding:

Complicaties ten gevolge van een verkeerd gepositioneerde nasogastrische sonde (NGS) kan

zeer ernstige gevolgen hebben leidend tot een verlengde hospitalisatie duur of overlijden. De

positie van de NGS dient geverifiëerd te worden voor het gebruik ervan. Verschillende

methodes zijn hiervoor reeds onderzocht, maar een thoraxfoto blijft de gouden standaard. Een

thoraxfoto op intensieve zorgen heeft wel nadelen zoals straling, kostprijs en werkintensiteit.

Doelstelling:

Het doel van deze studie is om de diagnostische performantie van het ultrasound pop-up sign

op intensieve zorgen te bepalen in vergelijking met de RX-Thorax voor de correcte positie

van de NGS.

Methodologie

In deze single-center prospectieve studie werden volwassen patienten geïncludeerd die

werden opgenomen op intensieve zorgen als er een NGS werd geplaatst. Na de plaatsing werd

de positie bepaald met echografie: de patient was gepositioneerd in ruglig met 30° elevatie

van het bed. Het antrum werd met echografie in beeld gebracht en daarna werd snel 60 ml

lucht geinsuffleerd in de NSG. Als er een plotse pop-up van lucht zichtbaar werd, dan werd

het teken als positief beschouwd. Nadien werd een thoraxfoto genomen ter controle.

Resultaten:

Tachtig patienten waren geïncludeerd. De mean leeftijd was 66 ± 14.6 years en de mean Body

Mass Index 24.7 ± 5.5. Vierenzestig patiënten waren invasief geventileerd (80%). In 63/80

(79%) van de patiënten kon het pop-up sign opgemerkt worden. Een controle RX-thorax

bevestigde de correcte positie van de NGS bij alle patiënten met een positief pop-up sign

(Positive Predictive value = 100%) In 17 patiënten was het pop-up sign niet visualiseerbaar.

De positie van de maagsonde was van deze patienten correct geplaatst in 88 %. Twee NGS

waren midoesophagaal geplaatst en één postpyloor. De sensitiviteit is 82%

Conclusie:

Het ultrasound pop-up sign is een betrouwbare predictor van correcte nasogastrische tube

positie en is aanwezig in 82% van de correct gepositioneerde tubes. We zijn van mening dat

een controle RX-Thorax achterwege kan gelaten worden na een positief pop-up sign.

Introduction

In Intensive care medicine, the nasogastric tube has multiple purposes and is frequently

placed in the Intensive care unit in patients of all ages. A nasogastric tube is a flexible single

or double lumen tube that is passed proximally from the nose distally into the stomach or

small bowel. The gastric tube can also be placed orally in certain indications (e.g. basilar skull

fracture, …). (7) The most common indications for the placement of nasogastric tubes are

gastrointestinal decompression (e.g. ileus or bowel obstruction, or after gastric distension due

to bag-valve-mask ventilation or assisted ventilation), administration of medication, gastric

lavage or enteral nutrition. (2, 8)

The placement of a nasogastric tube is frequently considered a harmless procedure and is

placed on a daily basis and the complications may range from simple to disastrous

consequences leading to prolonged length of stay or ultimately death. Nasally inserted tubes

may cause nasal alar ulceration, epistaxis or sinusitis. (9,10) Nasal placement of a feeding

tube can obstruct breathing in patients of all ages although it is a greater problem in newborns

who are obligate nasal breathers due to partial nasal obstruction, an increase in airway

resistance and increased work of breathing. (9) The presence of a nasogastric tube impairs the

normal function of the lower esophageal sphincter making the patient more susceptible to

reflux of gastric contents which may lead to esophagitis, esophageal stricture, gastrointestinal

bleeding or pulmonary aspiration. (8) The most serious complications are related to

malpositioned tubes or perforation which can cause pneumothorax, pneumomediastinum,

subcutaneous emphysema, pulmonary hemorrhage, pulmonary abcess, aspiration by proxy,

mediastinitis. Nasogastric tube misplacement appears between 0.5-11% and intracranial or

intravascular placement has also been described in rare cases. (2, 3, 7, 9, 23, 28-31)

The standard of care requires verification of the placement of the gastric tube prior to its use

in order to minimize complications. (11) Several methods have been thoroughly investigated

(e.g. pH-metry, visual inspection of aspiration of gastric content, auscultation of air,

ultrasound of the stomach for direct visualization of the tip, capnography, … ) but

radiographic verification is considered the golden standard to confirm the correct position of

the nasogastric tube and is preferred by many. (11-17) However, radiological confirmation in

an ICU patient has several disadvantages including radiation exposure, cost, labor intensity

and is only a single point in time. (17-20)

Ultrasound use has gained its place in the Intensive care unit as a daily monitoring tool. Over

the past few years a multitude of protocols for standard evaluation of the Intensive Care

patient have been published such as the BLUE protocol (Bedside Lung Ultrasound in

Emergency), FALLS protocol (Fluid Administration Limited by Lung Sonography), FATE

protocol (Focused Assessed of Transthoracic Echocardiography), EFAST (Extended Focused

Assessment with Sonography for Trauma). (32-37) Ultrasound assessment of gastric content

and volume is also used in anaesthesia practice to help determine the aspiration risk. The

antrum of the stomach is the most tractable gastric region for ultrasound evaluation and its

evaluation accurately reflects the content of the entire organ. (5)

Several studies have already reported the use of ultrasound for the assessment of the correct

position of the nasogastric tube in the intensive care unit and the emergency department,

however to our knowledge no studies have been performed with to evaluate the diagnostic

accuracy of the ultrasound pop-up sign in the intensive care department. (2-4, 40, 41)

The objective of this study is to investigate the diagnostic accuracy of the ultrasound “pop-up

sign” to confirm correct position of a nasogastric tube in intensive care unit patients compared

with chest radiograph.

Material and methods

In this single centre prospective study, patients over the age of 18 with no previous history of

surgery to the stomach or esophagus, admitted to our mixed surgical and medical ICU were

included if a nasogastric tube was required for either enteral feeding and/or medication

administration, abdominal decompression or gastric lavage. The study was performed

between January 2012 until November 2014.

The length of the tube was estimated by using the distance from the tip of the nose to the tip

of the ear to the xiphisternum plus 10 centimeter. (see image 1) (24, 25, 38, 39) The

nasogastric tube was then lubricated with a water soluble lubricant to reduce friction. The

right nostril was usually preferred except when resistance was felt, then the contralateral

nostril was used.

.

In mechanically ventilated patients the nasogastric tube was either placed in the esophagus by

a trained anesthesiologist under direct vision with a laryngoscope and Magill forceps and

advanced in the esophagus until the premeasured length of the nasogastric tube was reached

or the head was maintained neutrally and by using two fingers inside the patients mouth the

tip of the nasogastric tube was guided between the two fingers to the esophagus. If resistance

was felt or coiling occurred in the mouth a laryngoscope was used. (8, 26)

When the patient was awake, the patient was seated with the head tilted towards the chest.

The tube was then introduced into one of the nostrils horizontally over the nasal floor. The

patient was given a small cup of water with a straw and was to drink while the nasogastric

tube was advanced. When the nasogastric tube reached the posterior nasopharynx and the

patient felt like gagging, then swallowing was encouraged to help guide the tube to the

stomach. If the patient became short of breath or had to cough then the nasogastric tube was

withdrawn and a new attempt was performed after a minute. (8, 27) Once the insertion of the

nasogastric tube was finished it was secured to the patient’s nose with adhesive tape.

After placement of the nasogastric tube the correct position was tested initially as follows.

The patient was placed in the dorsal decubitus position with the head of the bed elevated 30°.

The antrum of the stomach was visualized by ultrasound with a low-frequency (2-5 MHz)

curvilinear abdominal probe (Philips CX50 – probe C5-1). The probe was placed horizontally

in the epigastric area and oriented towards the left upper abdominal quadrant. The left lobe of

the liver was used as an internal landmark for optimal visualization of the antrum of the

stomach. The antrum appears flat with juxtaposed anterior and posterior walls in a fasted

stomach, with increasing volume, the antrum becomes round and distended with thin walls. In

the unfasted patient, the air/solid mixture creates multiple ring-down artifacts on the anterior

gastric wall which obscure the posterior wall due to scattering. (2, 5). (see image 2A)

When an optimal image was acquired, a nurse or second investigator was asked to rapidly

insufflate the nasogastric tube with 60 ml of air. The insufflated air causes a typical

appearance due to the scattering of the ultrasound waves at the interface of soft tissue and air.

The reverberations of the ultrasound waves between the transducer and the air increase the

echogenicity and cause posterior artifactual reverberation echoes with characteristic comet-

tail echo appearance. (43) If a sudden pop-up of air, also known as dynamic fogging was

identified in the stomach in a maximum of four attempts, then the sign was considered

positive. (see image 2B)

The investigator was asked to only identify the pop-up sign as positive if he was absolutely

certain of visualization of the sign.

After the ultrasound investigation a chest radiograph was taken to confirm the position of the

nasogastric tube and to determine the precise location of the tip of the nasogastric tube in the

upper gastrointestinal tract. (see image 3) (42) Chest radiographs were interpreted by a

radiologist who did not perform the ultrasound visualization.

Statistical methods:

Observed data were entered into Microsoft Excel Workbook 2010. All analyses were

conducted using Statistical Package for the Social Sciences (SPSS) for Windows (IBM SPSS

Statistics version 23. Inc., Chicago, IL, USA). Continuous variables were reported in terms of

the mean and standard deviation, and categorical variables were reported in terms of

frequency and percentage. Student’s t-test was used for continuous variables and Fisher’s

exact test for categorical variables. A P-value under 0.05 was considered to be of statistical

significance for all tests. Indicators of the performance of a diagnostic test, sensitivity,

specificity, positive predictive value, and negative predictive value were determined.

Results

Eighty patients were included in this study, of which 47 were male (58.8%). The mean age

was 66.3 years (Standard deviation (=SD) 14.6 years). The height and weight of the patient

were used to calculate the Body Mass Index. The mean BMI was 24.7 (SD 5.5). The

placement of the nasogastric tube was indicated for either abdominal decompression or

medication administration and/or enteral feeding in respectively 62.5% and 37.5% of the

cases. There were no indications for nasogastric tube placement for gastric lavage during the

study.

The nasogastric tube was inserted in awake patients in 16/80 cases (20%). In mechanically

ventilated patients, the nasogastric tube was inserted blind in 30 of 64 cases (46.9%) and with

the aid of the laryngoscope and Magill forceps in 34 of 64 cases (53.1%). (Table 1) The p-

value of the mean BMI and mean age between the group with a positive ultrasound pop-up

sign and a negative ultrasound pop-up sign when using a student’s t-test was >0.05 and was

not considered statistically significant. Fisher’s exact test showed no statistically significant

difference between a positive pop-up sign for either the indication for the nasogastric tube or

the method of insertion.

Table 1: Patient characteristics

Sexe Male 47/80 (58.8%)

Age (years) 66,3 ± 14,6 *

Body Mass Index1 24,7 ± 5,5*

Indication for nasogastric tube

Abdominal decompression 50/80 (62,5%)

Medication administration/enteral feeding 30/80 (37,5%)

Gastric lavage 0/80 (0%)

Method of nasogastric tube insertion

Awake patient 16/80 (20%)

Laryngoscope and Magill forceps 34/80 (42,5%)

Blind insertion 30/80 (37,5%)

*mean ± standard deviation 1: kg/m²

Three different types of nasogastric tubes were inserted, with each varying external diameters.

Thirty small bore enteral feeding tubes were inserted with an external diameter of 8 F

(French). The ultrasound pop-up sign was positive in 18/30 cases. Six 14 F Salem-sump tubes

were inserted with a positive pop-up sign in 83.3% of the cases. Forty Levin tubes were

inserted with four different diameters. One 10 F Levin tube was inserted with a positive pop-

up sign. Eight 12 F Levin tubes were inserted with a positive pop-up sign in 7/8 (87.5%) of

the cases. The majority of the inserted Levin tubes had a diameter of 14 F and had a positive

pop-up sign in 30/33 (90.9%). There were two 16 F Levin tubes inserted with both had a

positive pop-up. (Table 2) A Fisher’s exact test was performed and showed there was a

significant difference (p=0.031) between the external diameter of the nasogastric tube and the

visualization of the ultrasound pop-up sign.

The ultrasound pop-up sign was present in 63/80 cases (78.8%). The pop-up sign could be

identified after a single insufflation of air in 24/63 (38.1 %) patients, after two insufflations in

15/63 (24%) patients, after three insufflations in 9/63 (14%) and after four insufflations in

5/63 (8%) patients. In the remaining 10 patients (16%), the data of the number of attempts are

missing. (Table 3)

Table 2. Type of nasogastric tube

Ultrasound pop-up sign

Diameter Positive Negative

Small bore nasogastric tube 8 F1 18 (60%) 12 (40%)

Salem-sump tube 14 F 5 (83.3%) 1 (16.7)

Levin tube

Black 10 F 1 (100%) 0 (0%)

White 12 F 7 (87.5%) 1 (12.5%)

Green 14 F 30 (90.9%) 3 (9.1%)

Orange 16 F 2 (100%) 0 (0%) 1 F= External Diameter (mm) * 3

The nasogastric tube position was confirmed by chest radiograph in all patients with no cases

of serious complications. In all 63 patients with a positive pop-up sign, the correct position of

the nasogastric tube was confirmed by chest radiograph. On chest X-ray, the nasogastric tube

was identified in the corpus in 49/63 (77.8%), in the cardia in 4/63 (6.3%), in the antrum in

3/63 (4.8%) and in the fundus in 7/63 (11.1%). In 17 patients the pop-up sign could not be

identified. Of these the nasogastric tube was correctly placed in the stomach in 14 patients

(82.3%), while two (11.8%) were midesophageal and one was located postpyloric 1/17

(5.9%). (Table 4)

Table 4: Location of tip of nasogastric tube on chest radiograph

Ultrasound pop-up sign

Tip location on chest radiograph Positive Negative

Corpus 49/63 (77.8%) 7/17 (41.1%)

Cardia 4/63 (6.3%) 2/17 (11.8%)

Antrum 3/63 (4.8%) 0/17 (0%)

Fundus 7/63 (11.1%) 5/17 (29.4%)

Midesophageal 0/63 (0%) 2/17 (11.8%)

Postpyloric 0/63 (0%) 1/17 (5.9%)

Table 3: Insufflation of air until appearance of pop-up sign

Positive ultrasound pop-up sign 63/80 (78,8%)

Attemps of insufflation

One insufflation 24/63 (38,1%)

Two insufflations 15/63 (23,8%)

Three insufflations 9/63 (14,3%)

Four insufflations 5/63 (7,9%)

Unknown 10/63 (15,9%)

The ultrasound pop-up sign has a sensitivity of 81.8% with 95% confidence interval [71.4%-

89.7%] and a specificity of 100%, 95% CI [29.2%-100%]. The positive predictive value is

100%, 95% CI [94.3%-100%] and a negative predictive value of 17.6%, 95% CI [3.8%-

43.4%]. The Youden’s index is 0.81. (Table 5)

Table 5: Diagnostic accuracy of ultrasound pop-up sign for confirming correct position

of nasogastric tube

Confirmation chest radiograph of nasogastric tube

Correct Position Incorrect Position Total

Pop-up sign

Positive 63 0 63

Negative 14 3 17

Total 77 3 80

Discussion

The frequency of malposition varies between 0.5-11%. The incidence of tracheopulmonary

complications are approximately 2% and 0.3% died from the complications. Therefore it is

necessary to verify the correct position of the nasogastric tube. (3) Although many

verification methods have been described the most common used techniques are monitoring

for signs of respiratory distress, observing the aspirate of the nasogastric tube and the ‘whoosh

test’(auscultation over the epigastrium following the rapid insufflation of air). (48-49)

The ‘whoosh’ test however has proven to be unreliable and widely used despite

recommendations to the contrary. PH measures are used in combination with visual inspection

of the aspirate, a pH lower than 5.5 indicates gastric placement however the use of H2-

blockers and proton pump inhibitors in the intensive care unit confounds the usefulness of

assessing the pH. Enteral feeding, certain medications and sterile water (pH 5.5-7) can also

alter the pH. It is often difficult to obtain an aspirate and small bore tubes may collapse when

negative pressure is applied. (50)

Other methods exist to confirm the correct position such as pepsin and trypsin concentrations

in the aspirate, capnography, bilirubin testing of the aspirate or with an electromagnetic

device for special nasogastric tubes.

Chest radiograph remains the golden standard by which all tests are compared. Although the

radiation exposure is small for the a single chest radiograph, repeated exposures may result in

high cumulative doses which can be associated with cancer. Ultrasound examination requires

little patient manipulation, whereas a chest radiograph can be more time consuming and labor

extensive. We believe that ultrasound may become another verification method with a

widespread accessibility in the intensive care unit. (18, 19, 21, 50)

The use of ultrasound has become a standard of care in the intensive care unit. The objective

of this study was to evaluate the ultrasound pop-up sign compared with the golden standard to

determine the correct position of the nasogastric tube in the intensive care unit. The sensitivity

was 81.8% and specificity 100% confirm the diagnostic performance of the ultrasound pop-up

sign. The diagnostic odds ratio cannot be calculated since the positive likelihood ratio is

infinite (sensitivity/1-specificity). To approximate the diagnostic odds ratio, 0.5 was added in

each cell in table 5. The diagnostic odds ratio is 242 and indicates a high discriminatory test

performance which is independent of prevalence. (51)

Our study shows that the pop-up sign becomes less visible with a smaller diameter. This could

be due to the inability to rapidly insufflate the air through a smaller diameter.

Bedside sonography for confirming the tip of nasogastric tubes can rapidly taught and

although we only studied the ultrasound pop-up sign, ultrasound can also be used as an

adjuvant method during the insertion of the nasogastric tube to confirm the location of the

nasogastric tube in the cervical esophagus or it can be used to directly visualize the location of

the tip in the stomach. The larger the nasogastric tube is, the easier the direct visualization. (2-

4, 21). Weighted-tip nasogastric tubes are easily identified and appear as an hyperechogenic

line. (21) Ultrasound verification of the correct position of the nasogastric tube by direct

visualization has also been performed in children. Other studies have also used the ultrasound

pop-up sign but they only used it as an adjuvant technique when the tip was not visible. (2-4,

41, 46-47) Kim et al (4) described one case in which dynamic fogging was false positive. The

nasogastric tube was located midesophageal and dynamic fogging could be seen in the

stomach. However they used a solution of 40 ml normal saline and 10 ml of air, whereas in

our study only air was used.

Limitations

The time required to perform the ultrasound examination was not measured and could not be

compared with chest radiograph. A recent study by Brun however showed that the insufflation

of air and echographic verification can be performed in one minute. (3)

There is no report on whether the patient was fasted or ‘unfasted’. It seems likely that the

ultrasound pop-up sign could not be visualized in certain cases due to gas interposition which

remains a major limitation for ultrasound. (2) The duration of the study was almost three

years and this is due to the fact that only a single examiner included the patients and

performed the ultrasound examination. It is possible that a selection bias occurred.

Conclusion

Bedside ultrasound examination is becoming standard of care in the intensive care unit and

sonography for confirming the correct location of the nasogastric tube can be easily and

rapidly taught. The combination of ultrasound techniques to confirm the correct position of

the nasogastric tube supplement one another and we believe the ultrasound pop-up sound is an

essential part of this examination. The ultrasound pop-up sign is a very reliable predictor of

correct nasogastric tube position and is present in 82% of correctly positioned nasogastric

tubes. We believe a confirmatory chest X-ray can be omitted after visualization of the pop-up

sign and should be reserved for when the examination is indecisive.

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