Target insertion depth of nasopharyngeal temperature probes in children: A prospective observational study analyzing magnetic resonance images

Core temperature monitoring is indispensable to prevent children from perioperative thermal perturbations. Although nasopharyngeal measurements are commonly used in anesthesia and considered to reflect core temperature accurately, standardized target depths for probe insertion are unknown in children.


| INTRODUC TI ON
Perioperative temperature perturbations are common in neonates, infants, and young children. 1 Continuous core temperature measurement is essential in guiding temperature management and preventing hypo-and hyperthermia in such a susceptible patient population.
Although a precise core temperature measurement is of utmost importance, only few methods and measurement sites have proven accurate enough. 1 While exact core temperature is best measured in the pulmonary or iliac artery, those sites are usually not feasible in noncardiac surgery. 2 Alternatively, esophageal probes give accurate temperature core estimates when placed in the distal third between the left atrium and the descending aorta, even though they still carry the risk of complications such as tracheal displacement and consequent respiratory adverse events. 3,4 When the use of esophageal probes is precluded because of interference with the surgical field or because laryngeal mask anesthesia is planned, 2 nasopharyngeal probes present a widely used, minimally invasive, and accurate alternative method of core temperature measurement in children. 5 It is recommended to position the nasopharyngeal probe tip where the mucosa is in closest proximity to the internal carotid artery, 6 since temperature measurements at this location in the upper nasopharynx correlates well with core temperature values. 7 While in adults, the optimal insertion depth from the nostrils to the nasopharynx-carotid-point (NCP) is 9 to 10 cm, 6 in children, the ideal insertion depth for nasopharyngeal probes remains to be established. 1 Primary goal of the current research was to prospectively determine a target depth of nasopharyngeal temperature probe insertion in children by measuring the distance from nostril to the NCP through magnetic resonance imaging (MRI). Secondary aims were to correlate these measurements with biometric variables and facial landmark-distances in order to derive practical formulas that could easily estimate the targeted depth.

| ME THODS
The current research was approved by the Institutional Review were enrolled from March to September 2020. The study methodology is a secondary analysis planned a priori from our previously published research that determined the optimal targeted nasopharyngeal airway insertion depths in children through MRI. 8 We adhered to the STROBE guidelines for reporting observational studies. 9 Detailed study methodology has been reported previously, 8 and written parental or legal guardians informed consent was obtained before enrolment. We included children up to and including 12 years of age, requiring procedural sedation or monitored anesthesia care whenever MRI was indicated to rule out or follow-up a variety of brain pathologies. Exclusion criteria were facial, nasal, or airway pathologies that would have altered distance measurements.

| Protocol
We collected the following variables for each patient: age, sex, height, weight, American Society of Anesthesiologists physical status classification and indication for MRI. The following distance measurements of facial landmarks were performed with a tape measure (Skin Marker, Symmetry Surgical®) and recorded by investigators involved in this study: • Nostril-mandible-from the middle of the nostril to the angle of the ipsilateral mandible; • Nostril-tragus-from the middle of the nostril to the ipsilateral tragus of the ear; Conclusions: Height-based formulas could be a valuable proxy for the insertion depth of nasopharyngeal temperature probes. Further clinical trials are necessary to investigate their measurement accuracy.

K E Y W O R D S
anesthesia, body temperature, child, nasopharynx, temperature

Clinical Implications
What is already known?
Nasopharyngeal temperature probes are minimally invasive and routinely used to monitor perioperative core temperature.

What this article adds?
Based on biometric variables, landmark-distances and magnetic resonance imaging measurements in 120 children aged 0 to 12 years, we determined a target insertion depth of nasopharyngeal probes in children and derived a formula to estimate optimal insertion depth.
• Philtrum-tragus-from the philtrum to the tragus of the ear.
Magnetic resonance imaging was performed with T1-3D-MPRAGE (Magnetization Prepared Rapid Acquisition with Gradient Echoes) and sagittal T2-weighted Turbo-Spin-Echo sequences. No additional sequences were required for study purposes.

| Imaging analysis
The nasopharynx-carotid-point was defined as the closest spot of the nasopharyngeal mucosa to the internal carotid artery. We measured the distance of the nostril to the NCP on MRI using the proprietary measurement tool of General Electric PACS® (version 6.0, General Electric). First, the NCP was determined on transversal T1 axis. After triangulation of this point to sagittal T1 axis, the distance of the nostril to the NCP was measured through the inferior nasal meatus and defined as target insertion depth (see Figure 1 for an illustration).

| Outcomes
Our primary outcome parameter was the target insertion depth to reach the NCP from the nostril according to age. Secondary outcomes included correlations of this distance with patients' characteristics age, sex, height, and weight as well as with the measured nostril-mandible, nostril-tragus, or philtrum-tragus landmarkdistances. We additionally derived formulas to best predict insertion depth by calculating their probabilities of tip placement at the NCP. Successful placement of the temperature probe was defined as probe tip located within a range of 10% around NCP. 6

| Statistics
Since we collected data as part of our previously published trial, 8 no power analysis or sample size calculation was needed.
Outcomes are reported as mean and standard deviation according to age. Differences between females and male patients were assessed using the t-test with unequal variances. Exploratory analysis was performed to assess the correlations between the target insertion depth to reach the NCP from the nostril and the patient's characteristics using Pearson's correlation coefficient (ρ) and univariate linear regression. Correlation coefficients are reported with 95%-confidence interval (CI) and regression lines are shown with 95%-pointwise CI. Parameters of the linear regression are reported with estimate and SE. Multiple linear regression analysis with stepwise backward selection, based on Akaike's information criterion (AIC), was used to derive a formula for the insertion depth to reach the NCP using all measured variables as independent variables. Data were analyzed using R version 4.0.5 (The R Foundation for Statistical Computing).

| RE SULTS
Data of 120 children were analyzed (see Figure 2), whose characteristics are presented in Table 1 Table 2 shows mean measurements according to age. No significant difference in targeted insertion depth was found between females and males (p = .509).   Table 3).
Using stepwise analysis (n = 102), the formula to best predict the target depth measured from the nostrils to the NCPs in millimeters was "33. 3

| DISCUSS ION
The target depth of nasopharyngeal temperature probe insertion, Defining NCP and measuring the distance from nostrils on radiologic images has been mainly used in adults. 6 Its advantage is to be noninvasive compared with nasal endoscopy or insertion of a gadolinium-filled gastric tube as previously reported. 10,11 The plausibility of our results is supported by studies in adults, where NCP was found in the upper nasopharynx at a depth of 91 to 94 mm in females and 97 to 101 mm in males from the nostrils. 6,10 In contrast, we did not find any sex-specific difference, although those are known for growth rate of nasopharyngeal length during early childhood. 12 We consider as the most relevant finding, that in children the distance from the nostrils to NCP has a moderate to strong correlation with height. It is unclear whether identifying stronger correlations in children is even possible due to their different proportions, interindividual growth and development stages of the upper airway. [13][14][15][16] This is especially true for a younger age, smaller height or lower weight. 8 Since we are missing measurements of landmark-distances in 18 children for our multiple analysis, its correlation coefficient could be underrated, but likely not to a clinically meaningful extent. Since the multiple regression formula including philtrum-tragus improved the AIC only by 0.01, we consider it equally accurate to use the univariate formula with the height only.
Application of complex formulas, even though potentially useful in clinical trials, seems unlikely to be implemented in daily pediatric anesthesia practice. While distances for esophageal temperature probe insertion were reported to be more precisely predictable  After cardiac arrest 2 Other 24 by a formula, 17  that more than half of anesthesia providers did not place nasopharyngeal probes appropriately. 6 Since one can expect that the rate of correctly placed temperature probes in children with their smaller proportions 8 would be even worse, a simple and pragmatic recommendation for clinicians could potentially lead to a clinical improvement. Our suggestion according to height categories (see Table 3) seems accurate enough to justify this simplification and allow adoption into routine clinical practice.
In comparison with other routes, the nasal insertion has several advantages: First, it is easily accessible and may be more convenient than rectal measurement, which also lags core temperature over time of the measurements, particularly during rapid thermal perturbations. 2 Second, placement of a nasopharyngeal temperature probe is feasible in conjunction with laryngeal masks as well as

| LI M ITATI O N S
We included children with potential or previously diagnosed cerebral pathology, resulting in a potential bias against a "healthy" TA B L E 2 Target insertion depth measured from the nostrils to the NCPs according to age. Values are numbers or mean (SD)

ACK N OWLED G M ENTS
We are grateful to Iris Herzberg and Heike Bodmann for supporting our enrolment process, to Carlo Pancaro for language review and to our team of anesthesiologists, anesthesia nurses, and neuroradiological technicians for their continuous support.

FU N D I N G I N FO R M ATI O N
We conducted this research with institutional resources only.
Publication was funded by the Open Access Publication Funds of the Göttingen University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

DATA AVA I L A B I L I T Y S TAT E M E N T
The study data are not publicly available due to institutional policy.
Data are available upon reasonable request from the corresponding author.