Is the nasopharynx warmer in children than in adults?

Journal of Clinical Forensic Medicine (1996)3, 157-160

© APS/PearsonProfessionalLtd 1996

ORIGINAL C O M M U N I C A T I O N

Is the nasopharynx warmer in children than in adults? N. C. Molony*, A. I. G. Kerr*, C. C. BlackwelF, A. BusuttiP *Department of Otolaryngology, Lauriston Building, The Royal Infirmary; ~Department of Medical Microbiology and ,~Forensic Science Unit, Medical School, University of Edinburgh, Edinburgh, UK SUMMARY Recent studies on the aetiology of the Sudden Infant Death Syndrome (SIDS) have suggested that some of these deaths are the consequence of an overwhelming inflammatory response to the production of pyrogenic toxins from bacteria colonizing the upper respiratory tract, particularly the nasopharynx? The pyrogenic toxins of Staphlococcus aureus, one of the likelier bacterial candidates, are only produced in temperatures of over 37°C. This study examined nasopharyngeal temperatures in children. It is a preliminary study to develop an accurate means to measure how close to 37°C the nasopharyngeal temperature lies in infants at the age when SIDS deaths occur. Following a pilot study and power calculation, measurements of nasopharyngeal temperature were made on 30 apyrexial children aged 4-10 years and 30 adults with no nasal pathology, undergoing surgery under general anaesthesia, using an accurately sited thermocouple probe. The mean temperature in children (35.64°C) was significantly higher than in adults (34.01 °C). Comparable measurements attempted with the same subjects awake gave similar results.

Journal of Clinical Forensic Medicine (1996) 3, 157-160

However, for Staphylococci to produce their toxins, temperature in excess of 37°C are required. 7Whatever the normal nasopharyngeal temperature, it is likely that it would be raised further by overheating of the body (e.g. overwrapping or intercurrent viral infections) and by blockage of a nostril (e.g. in the supine position), which are known to predispose to SIDS. Accurate nasal and nasopharyngeal temperatures are not well documented,8 although several methods have been used for temperature measurement at the anterior nares?-11 This study aimed to establish whether the nasopharyngeal temperature in children aged 4-10, undergoing general anaesthesia, was greater than adults undergoing a similar anaesthetic and, if possible, making corresponding measurements on the same subjects while awake. With regard to the proposed mechanism of SIDS, if the nasopharyngeal temperature was higher in these older children then it would be worthwhile repeating the study on infants young enough to be at risk of SIDS. The temperature probe was first tested extensively to validate its calibration. A pilot study was then carried out to make a power calculation assessing how large a study was required.

Over the last 3 years, deaths from the Sudden Infant Death Syndrome (SIDS) have fallen considerably2,3,4 but this condition still prevails as the commonest cause of post-perinatal mortality in the western hemisphere. ~ It has been suggested that an excessive production of pyrogenic bacterial toxins, formed by micro-organisms such as Staphlococcus aureus colonizing the nasopharynx in their role as superantigens, may produce an inflammatory response in some babies. This inflammation could be to such a degree as to overwhelm compensatory mechanisms and result in death from septic shock syndrome before it could be established clinically or at autopsy. Several features are known to coexist in infants who die from SIDS which may act synergistically in making such nasopharyngeal colonization more likely.5,6

N. C. Molony BSc FRCS, A. I. G. Kerr FRCS, Department of Otolaryngology, Lauriston Building, The Royal Infirmary, Edinburgh EH3 9EN, C. C. Blaekwell DSe, Department of Medical Microbiology, A. Busuttil MD, Forensic Science Unit, Medical School, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK. Correspondence to: Mr N. C. Molony Fax +44 (0)131 229 8769 157

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Journal of Clinical Forensic Medicine

METHODOLOGY The temperature probe used was a TOR model 305 digital thermometer (TOR, Leicester, UK) which works on the thermocouple principle having 2 nickel alloys in the probe. Measurements are taken to the nearest 0.1 °C almost instantaneously. The instrument is factory-calibrated to be within 0.3% of the true temperature + 1 digit of the scale, and is periodically recalibrated to British Standard by the manufacturer. To assess the consistency of temperature measurements taken by this instrument, temperature readings were made on 20 unanaesthetized adult subjects (aged 18-55) during quiet mouth breathing. Five repeated measurements were made at the same site in each person over a period of about 1 minute, each reading being taken after the thermometer display had stabilized, usually within 3 seconds. Repeated readings were found to give an intra-subject variability of not more that 0.4 of a degree C in any of the 20 subjects tested, under the same conditions of ambient temperature (20°C) and humidity (60-65%). The temperature in the nasopharynx was measured using a 2.7 mm diameter, zero degree nasendoscope (Karl Storz & Co, Tuttlingen, Germany). This permits direct vision of the posterior wall of the nasopharynx at the level of the Eustachian tube and the thermometer's tip can be passed through the nose and applied directly and accurately to this area. Five steady state readings were obtained from each side of the nose and the mean of these 10 values was used as the value for that subject (Fig. 1). A pilot study was carried out prior to the main study. The children from whom nasopharyngeal

temperature recordings were obtained were aged 4-10 years and the adults, 16-52 years. All were undergoing elective ENT surgery. Excluded from this series were patients with pyrexia, known symptomatic nasal pathology, polyps, tumours, seasonal or perennial allergic rhinitis or a deviated nasal septum. Adenoid hypertrophy was not regarded as a symptomatic nasal pathology for the purposes of this study. The adults underwent such procedures as middle ear surgery, upper aerodigestive tract endoscopy or tonsillectomy. The children underwent tonsillectomy and/or adenoidectomy, sometimes with myringotomy. Ethical consent was obtained from the Lothian Ethics Committee. Adults and the parents of the child subjects gave written informed consent. Measurements were taken preoperatively under 10% xylocaine spray local anaesthetic (Astra Pharmaceuticals, Kings Longley, Herts, UK) (a single metered spray in both nostrils) on the adult subjects and, if possible, the children in the main study (not the pilot), and immediately after oral endotracheal intubation in the process of a standardized general anaesthetic (using thiopentone, halothane, suxamethonium and nitrous oxide). Benzodiazepines were used for premedication if required. Ambient temperature and humidity were recorded and were kept within carefully controlled limits for all measurements (20-24°C and 65-70% humidity, recorded with a hygrometer). For measurements made under local anaesthetic, the subjects were asked to breathe quietly through the mouth to minimize the effect of air flow. A pilot study was first made with 10 child subjects and 10 adults controls and it was planned to collect 30 readings in each group. A power calculation was

B

Fig. 1--The thermocouplethermometer(A) and the measuringtechnique(B)

Is the nasopharynx warmer in children

159

CI 35.265-36.035). These are also significantly different (P < 0.05) but the child sample size is small. The Table shows the individual results for the 2 groups under the 2 conditions.

made, assuming normal distribution of nasopharyngeal temperatures in each group, using the formula: Effect size = (mean group 1) - (mean group 2) standard deviation (SD) of the 2 groups This formula requires similar standard deviations in both groups. The pilot study found adult mean temperature under general anaesthesia to be 34°C (SD 0.571) and childrens' 35.7°C (SD 0.461) giving an effect size greater than three. Use of the appropriate table for 80% power at the 95% level (or P < 0.05) showed that groups of 10 would be sufficient for the main study. Nevertheless, sample sizes of 30 subjects in each group had originally been planned and were adhered to. In the main study, all adults had measurements under both local and general anaesthesia. All children had readings taken under general anaesthetic and, as experience with the technique grew, it was possible to obtain readings from 8 of the children under local anaesthetic. Two unpaired t-tests were carried out; one between the 2 groups of readings taken under general anaesthetic and the second between the 2 sets of local anaesthetic readings. 95% Confidence Intervals (CI) were calculated for the means.

DISCUSSION This study found the nasopharyngeal temperature to be higher in children than in adults under identical conditions, both with local and general anaesthetic. Two reasons for this could be the small dimensions of the nasopharynx in the child compared to the adult, or greater blood flow and hence warming in the child. The question which arises is how far this may differ from the waking (or sleeping) subject breathing normally with no anaesthetic of any kind. A number of techniques have been used over many years to measure nasal temperature81l but nasopharyngeal temperatures are much less well documented. The most accurate instruments appear to be thermocouples (used in his study), thermistors, and infrared thermometers. An inherent problem in a thermometer measuring by contact, such as the thermocouple probe, is that the tip sinks into the mucosa, and the mucosal secretions could react with the metal alloys8(Prof. A. S. Jones, University of Liverpool, personal communication.). Infrared thermometers have the advantage of not making mucosal contact and being unaffected by air flow, but all those available at present are too large to use in a child's nose or to reach an adult's nasopharynx. It is hoped to repeat this study with an infrared temperature probe when a suitable one becomes available. The present technique has, however, given consistent, repeatable nasopharyngeal readings. Children have more lymphoid tissue in the nasopharynx than adults. It is possible that if the thermocouple sinks into crypts in children's adenoid tissue,

RESULTS The pilot study found an adult mean nasopharyngeal temperature of 34°C (SD 0.571) and a childrens' nasopharyngeal temperature of 35.7°C (SD 0.461). Under general anaesthetic, the adult mean was 34.01°C (SD 0.69, 95% CI 33,801-34.219) and the childrens' mean was 35.64°C (SD 0.469, 95% CI 35.44~35.808). These are significantly different (P < 0.01). The readings taken under local anaesthetic gave an adult mean of 34.03°C (SD 0.756, 95% CI 33.76-34.3) and a childrens' mean of 35.65°C (SD 0.555, 95%

Table Results from the main study, nasopharyngeal temperature in 30 subjects

(A) Adult readings under general anaesthetic 35.4 33.8

34.3 34.1

32.6 32.6

34.1 34.9

33.1 34.5

33.9 34.0

(°C) 34.6 33.9

33.9 34.2

34.1 34.2

34.3 34.1

33.9 33.9

35.1 34.2

34.1 34.6

33.8 34.0

34.1 32.8

34.9 36.1

36.0 36.1

35.9 35.6

36.0 35.8

35.8 36.1

35.9 34.7

35.7 34.9

35.8 36.0

34.2 33.2

33.9 34.1

33.9 34.6

34.0 34.0

33.0 32.7

35.2 34.2

35.1 34.2

32.8 33.8

(B) Child readings under general anaesthetic (°C) 36.1 36.1

36.1 35.5

35.6 35.3

35.8 35.5

35.8 35.2

36.1 34.8

34.7 35.1

(c) Adult readings under local anaesthetic (°C) 32.7 35.3

24.7 34.9

24.7 34.1

34.1 33.9

32.5 34.1

34.5 34.9

33.9 33.7

(D) Child readings under local anaesthetic (°C) (only 8 managed technique) 36.1

36.1

35.6

35.9

36.1

34.7

34.9

35.8

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this might give a warmer reading than a 'true' surface reading. However, many adults have folds of tissue on the nasopharyngeal wall and some of the younger adults in this study had visible adenoid remnants which could have the same effect. The thermocouple was applied as lightly as possible to obtain a reading and was not observed to be sinking into the mucosa. Warming and humidifying inspired air are regarded as functions of the nose in normal respiration. Airflow and blood flow may lead to cyclical temperature changes on the surface of the nasal and nasopharyngeal mucosa. This has been described previously in the nose. 8s For example a recent study 8 found inspiratory temperature at the anterior nasal septum to be 32. l°C and expiratory temperature to be 33.6°C. The nasopharynx may be expected to undergo some cyclical changes but these are likely to be smaller, partly because the nasopharynx is deeper in the head but also because it lacks the complex blood vasculature that the nose has to enable it to warm and humidify air. How far nasopharyngeal temperature varies with respiration is to be addressed in a subsequent study in adults. The present readings have been taken in the absence of airflow as far as possible. Clearly the local and general anaesthetic agents used could have affected nasal blood flow. The same agents were given to the adults as to the children to attempt to standardize any effect from this. In many of the children, backflow of gases when an uncuffed endotracheal tube was used was a possible confounding variable. Measurements were taken as soon as possible after intubation before regular ventilation was established to minimize this. It could be argued that the temperature of the nasopharyngeal mucosal surface might rise to core body temperature in the absence of airflow. This was not found to be the case. Previous work on the nasal lining found a steady temperature to be reached, below core temperature, in the absence of breathing? This is because heat loss occurs whether there is air flow or not. The difference in recorded temperatures in the same subjects when awake and when under anaesthetic was found to be small in most cases. Some of the children were having their adenoids removed. Large or frequently infected adenoids could have an effect on local temperature but, to be undergoing surgery, all children had to be free of known upper respiratory infection at the time the readings were taken. Readings were being taken from children undergoing non-ENT surgery to look at this. However, it is normal to have a fair amount of nasopharyngeal lymphoid tissue at the age range studied. Ambient temperature and humidity were further potential confounding variables which were kept within as narrow limits as possible.

What is the relevance of these findings to cot death? If the nasopharynx of the child in this age range is warmer than that of the adults then so too, presumably, is that of the infant at risk of SIDS. It has been suggested above that the nasopharyngeal temperature is unlikely ever to reach core body temperature. However, if the child is pyrexial, the higher core temperature could cause the nasopharyngeal mucosal temperature to rise, perhaps reaching 37°C. Sites within the nasopharynx which become acutely inflamed might have further local temperature increases due to the exothermic chemical reactions occurring. It is known that the incidence of SIDS has declined since parents were discouraged from leaving their babies lying prone. The prone baby may have a warmer nasopharynx than the supine, particularly if the nose is blocked. If this combination of circumstances allows the nasopharyngeal temperature to reach, or exceed, 37°C, then the conditions are there to allow overgrowth of bacteria and the release of toxins. In the future it is intended to repeat the study on children up to a few months old who are more of the age to be at risk of SIDS. We also hope to examine the effects of prone position, upper respiratory infection and prolonged nasal blockage. REFERENCES

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Blackwell CC, Weir DM, Busuttil A et al. Infection, inflammation and the developmental stage of infants: A new hypothesis for the aetiology of SIDS. Molecular Medicine Today 1995; 1:72-78 2. Chief Medical Officer's Expert Group. The sleeping position of infants and Cot Death. London: HMSO, 1993 3. Fleming PJ, Cooke M, Chantler SM, Golding J. Fire retardants, biocides, plasticisers, and sudden infant deaths. Br Med J 1994; 309:1594-1595 4. Fleming PJ. Understanding and preventing sudden infant death syndrome. Curr Opin Paed 1994; 6:158-162 5. Saadi AT, Blackwell CC, Raza MW, James VS, Stewart J, Elton RA. Factors enhancing adherence of toxigenic Staphylococcus aureus to epithelial cells and their possible role in Sudden Infant Death Syndrome. Epidemiol Infect 1993; 110:507-517 6. Blackwell CC, Saadi AT, Weir DM et al. Infectious agents and SIDS: A new concept involving interactions between microorganisms, the immune system and developmental stage of infants. In: Rognum T O (ed) Sudden Infant Death Syndrome: New Trends in the 1990's. Oslo: Scand Univ Press, 1996:189-199 7. Bohach GA, Fast DJ, Nelson RD, Schlievert PM. Staphyloccocal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit Rev Microbiol 1990; 17:251-272 8. Willatt DJ. Temperature and the Nasal Lining. [thesis] Liverpool: University of Liverpool, 1995 9. Cole P. Some aspects of temperature, moisture and heat relationships in the upper respiratory tract. J Laryngol 1953; 67:449-456 10. Drettner B: Vascular reactions of the human nasal mucosa on exposure to cold. Acta Otolaryngol Supp 1961; 166:1-109 11. Kus J, Krakowa E The effectiveness of nasal provocation tests for the diagnosis of atopic bronchial asthma. Allergol Immunopath 1983; 11:233-241