Archives ofDisease in Childhood 1996; 74: 427-431

Breathing, sleep state, and rectal temperatureoscillations

David M Tappin, Rodney P K Ford, Kerrie P Nelson, Brent Price, Paul M Macey,Richard Dove, Janine Larkin, Beryl Slade

AbstractOverheating may cause terminal apnoeaand cot death. Rectal temperature andbreathing patterns were examined innormal infants at home during the first 6months of life. Twenty one infants hadcontinuous overnight rectal temperatureand breathing recordings for 429 nights(mean 20*4 nights, range 7-30) spacedover the first six months of life. Periodswhen breathing was 'regular' weredirectly marked on single night records.Sleep state was determined from respira-tory variables. 'Regular' breathing was areliable marker of 'quiet' sleep (specificity93%/o). The duration of 'quiet' sleep in-creased from 6 to 22 minutes from twoweeks to three months of age and thenremained static, as did the proportion ofsleep spent in the quiet phase (9%/o to 34%/o).Rectal temperature fell during 66% ofquiet sleep and usually rose during rapideye movement (REM) sleep. The drop inrectal temperature was maximal at thestart ofquiet sleep, whereas the maximumrise during REM sleep was reached after10 to 15 minutes. Oscillations in rectaltemperature are associated with changesin sleep and breathing state. The matura-tion ofrectal temperature patterns duringthe first six months of life are closelyrelated to a maturation of sleep state andbreathing patterns.(Arch Dis Child 1996; 74: 427-431)

Keywords: body temperature, respiration, sleep stages,sudden infant death.

There is evidence of a link between the suddeninfant death syndrome (SIDS or cot death)and overwrapping or raised environmentaltemperature. ' Infant thermoregulation andrespiratory control are closely linked and thereare some hypotheses as to how this link maylead to cot death.

Infant thermoregulation is related to coretemperature, in that failure of thermoregula-tion will lead to an abnormally high or low coretemperature. We have described a regularoscillation of rectal temperature in overnightrecordings of infants who have previouslyexperienced an apparent life threatening event(ALTE).2This work has now been extended to record

temperature and breathing ofnormal infants intheir home environment during the first sixmonths of life, when 80% of cot deaths occur.In this paper we explore the relations between

sleep state, breathing patterns, and oscillationsof rectal temperature.

MethodsENROLMENTEthics committee approval allowed con-tinuous overnight temperature and respira-tory patterns to be recorded on infants athome. Recruiting of normal infants was madethrough newspaper articles asking women inlate pregnancy to volunteer their infants fortemperature and respiration recording duringthe first six months after birth. We specifiednon-smoking mothers with full term deliveriesand no neonatal problems. The studyresearch nurse explained the study anddemonstrated the HomeLog3 equipment andrecording procedures in the home. Parentswere then asked to phone her once their babywas born if they still wanted to join the study.At the first recording at two weeks of age theresearch nurse delivered the equipment andasked for written consent. She was availableby telephone in case of equipment breakageor other problems.

PATIENTSBetween 1 September 1993 and the 31August 1994, 21 infants had at total of 429(mean 20-4, range 7 to 30) nights of datarecorded, using four HomeLog systems.3 Allinfants (12 male and nine female) were bornat term and had no neonatal problems. Meanbirth weight was 3850 g (range 3000 to4300). Twenty infants were breast fed.Twenty infants were put down to sleep ontheir back or side, one infant was placedprone to sleep. No mothers smoked during orafter pregnancy. Twenty infants thrivedthroughout their first six months; the otherinfant, who started on the 90th weight centile,fell to the 10th at three months, in associationwith failure of lactation; he started formulafeeds and soon returned to the 75th centile.Each infant was recorded over four predeter-mined periods during the first six months oflife: 2-3 weeks of age for three nights; at thefirst vaccination at 6 weeks for seven nights(three nights before the vaccination, the nightof the vaccination, and three nights after-wards); and similarly for seven nights at eachof the routine vaccinations at 3 and 5 monthsof age. One infant had only a 5-month record-ing, two had a 3-month and a 5-monthrecording, three had a 6-week, a 3-month,and a 5-month recording, and 15 had a com-plete set.

Community PaediatricUnit, HealthLinkSouth, PO Box 1475,Christchurch, NewZealandD M TappinR P K FordK P NelsonB SladeJ Larkin

Department ofMedical Physics andBioengineering,Christchurch Hospital,Christchurch, NewZealandB PriceRDove

Department ofElectrical andElectronicEngineering,University ofCanterbury,Christchurch, NewZealandP M Macey

Correspondence to:Dr D M Tappin,Department of Child Health,Royal Hospital for SickChildren, Yorkhill, GlasgowG3 8SJ.Accepted 30 January 1996

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Tappin, Ford, Nelson, Price, Macey, Dove, Larkin, Slade

EQUIPMENTEach HomeLog system was based on a 286IBM-PC compatible laptop computer withcustom hardware and software allowing up to16 signals to be recorded simultaneously to thehard disc.3 Temperature probes were based on

a semiconductor and were validated locally.4The probes had a relative accuracy of 0.01 °C4;thus (within record) temperature changes weremeasured very accurately. Regular calibrationwas performed on each set of temperatureprobes to an absolute accuracy of 0*1-C usinga mercury in glass reference thermometer.Temperature measurements were sampled at arate of 1 Hz, digitised, and recorded. Rectaltemperature was recorded from a probe 5 cmfrom the anal margin, sealed in a soft plasticfeeding tube. A second probe in this plastictube 2 cm from the anal margin was alsopresent. If similar recordings were presentfrom both the rectal and anal probes, then therectal probe was positioned correctly and hadnot slipped down. Graseby MR10 respirationmonitors were used to record breathing byabdominal movement. This signal was sam-

pled at 10 Hz. Monitors were calibratedmonthly to reduce troublesome false alarms.Parents were supplied with a clipboard to lognightly details which included: the time thebaby was put down to sleep, sleep times, timeof morning waking, and the start and finish offeeds and nappy changes. A digital clockattached to the computer, used by parents fornoting times, was synchronised with theHomeLog computer clock. After each three orseven night period of recording, data - about20 megabytes - were downloaded from theHomeLog PC to an optical drive, allowingimmediate access for analysis and graphing.

ANALYSISRecords were inspected using BabyLog soft-ware5 and bad segments removed. Bad seg-ments (areas of recording that had data lossof either temperature or respiration) werecommon in the early stages of the study whentemperature probes were prone to failure.Improved design of the wiring of the tempera-ture sensors solved these problems. Grasebymonitors were also prone to false alarms,which sometimes led parents to disconnectthem. This was resolved by monthly calibra-tion. Other bad sectors removed includedperiods when anal temperature was not closelyrelated to rectal temperature, indicating thatthe probe may have been dislodged.

Information from parental logs was trans-ferred onto the computer record. Midday wasdefined as the start of each 'day', so that onewhole night of recording would be in each'day'. Further variables marked were: periods ofsleep ('S' in fig 1; this particular sleep periodwas continuous, although many were inter-rupted by feeds or nappy changes); periods of'regular' breathing ('Q' in fig 1, marked manu-

ally by visual inspection as the low amplitudeareas seen on a complete night of Grasebysignal); feed and nappy changes, taken from theparental logs (no feeds or nappy changes

occurred in this night of recording); and theinitial drop in rectal temperature on falling asleep('O' in fig 1, marked by visual inspection of therectal temperature trace). Figure 2 shows thesame night ofGraseby signal. The arrows pointto expanded 30 s periods of this Grasebysignal. The high amplitude area can be seen as'active' breathing, with highly variable breathlengths, the low amplitude area can be seen as'regular' breathing, with stable breath lengths.BabyLog analysis used peak to peak detec-

tion to calculate the length of each individualbreath.6

For this analysis we chose to cut each recordinto sequential 5 min epochs. Although 1 minepochs have used for sleep staging using res-piratory variables,7 we were also interested intemperature changes. The oscillations in rectaltemperature are of the order of 1 h,2 so a 5 minepoch was considered an adequate period todetect changes in temperature but shortenough for sleep staging to be accurate. In eachepoch there were 300 rectal temperature read-ings from which were derived the medianrectal temperature and the rate of change inrectal temperature in each epoch. The medianrather than the mean was used to minimise theeffect of outlying points in case of artefacts.Also for each epoch, breath lengths (usually150 to 200 breaths for each 5 min epoch) werecalculated and transformed into median breathlength (breath length=60/breath rate), upperquartile breath length, and lower quartilebreath length. The differences between the lat-ter two have been used extensively to describebreath rate variability, an important variableused to define sleep state.7 The data wereimported into the SAS statistical package8 andcomparisons made between multiple variables.Each night record was visibly examined for

the presence of obvious regular oscillations inrectal temperature.2 Oscillations were definedas of at least 0@1GC in amplitude and of about1 h in duration and could be seen and wereobvious to the naked eye throughout at least50% of the night trace (fig 1).

Sleep state (awake, rapid eye movement[REM], quiet, or undetermined) was assignedto each epoch using respiratory variablesaccording to the method described by Harper.7'Harper' sleep state classification was made for83-7% (n= 11 420) of 13 646 epochs, with16*3% (n=2226) 'undetermined': awake 1*8%(n=250), REM sleep 55 7% (n=7602), andquiet sleep 26-2% (n=3568). The length ofeach period of quiet and REM sleep (inepochs) was defined by examining sequentialepochs recorded on each infant, the position ofeach epoch within the period ofREM or quietsleep was also defined. The calculated quietsleep state epochs have been entered as 'F' infig 1 (between 'Q' and 'O'). From fig 1,'regular' breathing periods ('Q'), closelyapproximate to quiet sleep ('F').

For this report we have analysed the controlnights only: the three nights ofrecording at twoweeks ofage (n=43), and the three nights priorto vaccination at six weeks (n=44), threemonths (n=55), and five months (n=49).The 95% confidence intervals around the

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Sleep state and temperature oscillations

BABY-LOG

ni_! k=-_l__ !_==. . ... ..Graseby

1I 11111, II

between oscillations in rectal temperature,'regular' breathing observed in overnightrecords (figs 1 and 2), and sleep state in normalinfants at home during the first six months oflife.

ResultsIn 70% of control night records, regular oscil-lations in rectal temperature could clearly be

- seen: 21 of 43 nights (49%) at two weeks, 32 of44 nights (73%) at six weeks, 37 of 55 nights(68%) at three months, and 44 of 49 nights

)C Rectal temperature (90%) at five months. A correlation was seenbetween increasing infant age and the presence

l5 lof visible oscillations in rectal temperature(R2=0.78).On inspection, the oscillations in rectal tem-

°0 perature were temporally associated with achange in respiratory pattern (fig 1). As breath-

.-5 ing patterns are related to sleep state,7 we firstexamined if 'regular' breathing (as identified

.0 on our recordings) was related to sleep state (as0.0 2.0 4.0 6.0 8.0 10.0 12.0 defined by Harper's method). Regular breath-

ing accounted for 28-9% of all epochs, whileTime (h) Harper's 'quiet' sleep accounted for 26-2%.

e 1 An 11 h overnight recording in a 3 month old well infant. The rectal There were 3568 epochs of Harper quiet sleep!rature shows regular oscillations with amplitude of 202°C and period of 1 h. The in all records, and 2495 were marked as regular,by respiration signal shows a pattern 'regular' and 'active' breathing with the same

brahn.Teewe762posofH prlicity of about 1 h. The key to the scale below the title 'BABYLOG' shows S=periods breathing. There were 7602 epochs of Harperp (this child was asleep throughout the record), Q='regular' breathing, determined REM sleep and 7039 were not marked asual inspection, F=the epochs designated by Harpers method as 'quiet' sleep, 0=the regular breathing. Regular breathing had 70%of temperature drop associated with the onset of sleep. sensitivity and 93% specificity when used to

describe quiet sleep defined by Harper'smean drop in rectal temperature were calcu- method. Figure 1 illustrates the close associa-lated by adding and subtracting 1.96Xstan- tion between regular breathing ('Q') anddard error (SE) of the mean. SE=the standard Harper quiet sleep ('F'), which has beendeviation for each mean value divided by the marked on this computer record. Harper sleepsquare root of the number of values which state was used for subsequent analysis, becausemade up that mean. of the close association with breathing state.A total of 13 646 control night epochs (1137 The relation between rectal temperature

hours) which had adequate temperature and changes and sleep state for each epoch is pre-respiratory signals was available for analysis. sented in table 1A. To ensure that these resultsThis dataset was used to describe the relations were not due to spurious findings we sequen-

tially removed epochs which may have maskedthing patterns the close association between sleep state and

temperature change. Firstly, all epochs whichparents had recorded as non-sleep wereremoved, then epochs without visible oscilla-tions in rectal temperature were removed, thenepochs associated with the initial drop in rectaltemperature on falling asleep were removed.Table 1 B shows the temperature changes inthe remaining 7918 epochs. By this progressiveanalysis, portions of data were removed whichmight have influenced the direct association

B. Active breathing

Figure 2 The same night of Graseby recording is shown asfig 1. Arrows point to areaswhere the Graseby recording has been expanded to show two 30 s periods, A and B. A is aperiodmarked as 'regular' breathing on the whole night record: the expanded trace shows alow amplitude waveform, but more importantly breaths of equal length. B is a period'active' breathing, with a higher amplitude waveform, but with breaths of variable length.

Table 1 Percentage ofepochs with temperature changes ineach 'Harper' sleep state category

Rectal temperature changes (%o)Harper sleep state Fall Static Rise

A (n= 13 646)Quiet (n=3568) 66 14 20REM (n=7602) 35 11 54Awake (n=250) 35 8 57Undetermined (n=2226) 52 14 34B (n= 7918)Quiet (n=2604) 66 14 20REM (n=3857) 24 12 64Awake (n=81) 10 12 78Undetermined (n= 1376) 64 12 24

REM=rapid eye movement.

as0

38.00

37

37

36

36

Figur6tempeGraseperiodof sleeby visregion

Brea

A. Regular breathing

30s

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Table 2 Length ofperiods of 'quiet' and rapid eye movement (REM) sleep and infant age

Mean length ofHarper sleep state periods (minutes) by ageHarper sleepstate 2 Weeks 6 Weeks 3 Months S Months Overall

Quiet (SD) 10-3 (6-4) 17-6 (8 5) 22-1 (10-7) 20-0 (11 0) 18-9 (10-6)% Time 9 26 34 30 26REM (SD) 54-4 (39 5) 31-4 (21-4) 23-0 (15-5) 20-2 (13-0) 29-1 (24 7)% Time 80 61 46 43 56

0.20.15

2-o) 0.1

c 0.05

X O-7.5 -2.5

0): <0i-0a)

E -0.2a,- -2

between quiet sleep and a fall in rectaltemperature, which is demonstrated in fig 1.The association between sleep state andchange in rectal temperature was remarkablystable.The length of sleep state periods is illus-

trated in table 2. The length of quiet sleepperiods increased, and REM sleep periodsdecreased, as infants got older. The overallproportion of time spent in the two sleep stateschanged in a similar way. At two weeks of ageonly 9% of the epochs were spent in Harperquiet sleep, whereas 80% were spent in REMsleep; at six weeks, 26% were spent in quietsleep and 61% in REM sleep; at three months,34% were spent in quiet sleep and 46% inREM sleep; and at five months, 30% were

spent in quiet sleep and 43% in REM sleep.The mean temperature change in epochs of

quiet and REM sleep are illustrated in fig 3,with 95% confidence intervals. Each period ofREM or quiet sleep was made up of a numberof sequential epochs. These epochs were num-bered from '1', the first epoch in a period ofsleep, to 'n', the total number of epochs whichmade up the period of sleep. It can be seen thatthe rate of fall of temperature within quietsleep was on average higher than the rate of risein REM sleep. The fall in temperature hadusually started before the first epoch of quietsleep, and was maximal during it. The rise intemperature during REM sleep was on averagemaximal during the third epoch ofREM sleep.

DiscussionThe aim of this study was to look at the res-

piratory and temperature patterns of infants atlow risk of cot death. Many studies have

RE MI' sleep

I . 7 5 12 17 2 2 31 7 5 12 5 17 5 22-5 27-5 32-5 37 5- -0-05 /i-,- -0.1 'quiet' sleep

- -0.15

Time from the start of the sleep period (min)Figure 3 All periods of rapid eye movement (REM) and 'quiet' sleep are illustratedtogether in this figure. The total temperature change over all the first epochs within periodsofREM sleep were added and then divided by the number offirst REM epochs to give amean change of + 0 01°C per hour. This value was marked at 2 5 min after the start ofREM sleep periods (halfway through the first 5 min epoch). Similarly for 'quiet' sleep thetemperature change over allfirst epochs was divided by the number of epochs to give amean change of -0-21°C per hour. Similar calkulations were made for all second epochsand so on. The error bars indicate that we are 95% confident that the mean value oftemperature change was within this range, and was calculated as: the mean + or-1 *96XSEM. The length of the error bars largely inversely reflected the number of epochscontributing towards the mean value. ForREM sleep, there were 1249 'first' epochs and253 'eighth' epochs. For 'quiet' sleep there were 939 'first' epochs and 27 'eighth' epochs.

looked at high risk infants; data on such infantsin Christchurch have shown the relationsbetween respiratory patterns and rectal tem-perature oscillations.2 The present reportdescribes this association for low risk infants inmore detail on a large dataset of 1 137 hours ofrecording from 21 normal, well infants duringtheir first six months of life. We have clearlyshown that there is a strong relation betweenrectal temperature and breathing and sleepstate. During epochs of quiet sleep (or 'regular'breathing) the rectal temperature fell.Conversely during REM sleep there was anassociated rise in rectal temperature.A random sample of normal babies was not

possible to enrol because the ethics committeewould not allow the parents to be approacheddirectly. Data collection was only logisticallypossible on 20 babies at each age so it wasimportant to look at a homogeneous sample ofinfants. We looked at healthy babies at low riskof cot death over a full six month period so thatcomparison could be made with data alreadycollected on high risk infants.The BabyLog methods allowed physio-

logical variables to be displayed and analysedand information from parental logs could bemarked on the computer record. So that rectaltemperature and respiratory patterns could becompared, all records were cut into sequentialfive minute segments or epochs. By the use ofrespiratory variables, Harper7 was able toassign sleep state to infants from one week tosix months with 80% accuracy. This comparedvery favourably with trained observers usingEEG, EOG, and other somatic variables, whoonly achieved 85% accuracy.7 We used theHarper method to assign sleep state usingbreath rate and breath rate variability for eachepoch in the SAS dataset. Harper was able toassign sleep state to 95% of one minuteepochs. We were able to assign sleep state to83-7% of five minute epochs. This differencemay be explained by the epoch length. As onecomplete period of oscillation in breathing andsleep takes about an hour, two epochs per hourwill be likely to span from quiet to REM sleepor vice versa. With one minute epochs, onlytwo minutes will be affected out of each hour,which is 3 3% of epochs. But if epochs are fiveminutes in length, then up to 10 minutes ofeach hour will be affected (up to 17% ofepochs). The five minute epoch time waschosen to allow detectable changes in temper-ature and breathing to occur but to be shortenough to allow accurate sleep staging.There was a close association between quiet

sleep and regular breathing. Regular breathingwas only marked when it was definite, andperiods of possible regular breathing wereexcluded; therefore the 700/o sensitivity ofregular breathing at picking up all quiet sleepperiods is reasonable. The 93% specificity ofregular breathing at correctly describing quietsleep is good. Regular breathing, defined bylooking at a full night of Graseby signal andpicking those areas with an even, low ampli-tude breathing signal, can therefore be used asa good approximation of quiet sleep state.When we further examined the relation

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Sleep state and temperature oscillations 431

between sleep state and temperature oscilla-tions (which is well shown in fig 1) by remov-ing other causes of a fall in temperature,non-sleep periods, and nights without appar-ent oscillations, the proportion of quiet sleepepochs with falls in rectal temperature did notchange (table 1). This can be explained by thepresence of a phase difference (or time lag)between the onset of quiet sleep and the fall inrectal temperature. In these 21 normal infants,the temperature drop had on average started10 minutes before the onset of quiet sleep andthe fall was maximal (fig 3) during the firstepoch of quiet sleep. This contrasted with therise in temperature associated with REM sleepwhich on average began at the start of theREM sleep period but did not reach its peakfor 10-15 minutes.

This dataset shows an increase in length ofquiet sleep periods and an increase in the pro-portion of epochs spent in quiet sleep from theage of 2 weeks (9%) to the age of 3 months(34%). Temperature fall occurs during quietsleep. We therefore hypothesise that thematuration of infant temperature patterndescribed by Wailoo and Petersen9 is closelyassociated with as similar maturation of sleepstate involving an increase in the proportion oftime spent in quiet sleep.We have now clearly established that rectal

temperature rise and fall is associated withchanges in breathing and sleep state. The oscil-lations in rectal temperature must now be

considered to involve changes in sleep stateand breathing pattern. The presence orabsence of temperature oscillations under vari-ous circumstances such as infant age, illness,stress, and overwrapping, may be a significantdevelopmental marker for the maturation ofrespiration/sleep/temperature control mech-anisms, and thus play a part in explaining theenigma of cot death.The Canterbury Cot Death Fellowship supported DMT; theScottish Cot Death Trust supported BS (research nurse),NCHRF (The Cot Death Association) supported KN (bio-statistician). We wish to thank the parents who participated.

1 Fleming PJ, Levine MR, Azaz Y, Wigfield R, Stewart AJ.Interactions between thermoregulation and the control ofrespiration in infants: possible relationship to sudden infantdeath. Acta Paediatr Suppl 1993; 389; 57-9.

2 Brown PJ, Dove RA, Tuffnell CS, Ford RP. Oscillations ofbody temperature at night. Arch Dis Child 1992; 67:1255-8.

3 Ford RP, Brown PJ, Dove RA, Tuffnell CS, Macey PM.HomeLog: long-term recording of infant temperature,respiratory and cardiac signals in the home environment.J Paediatr Child Health 1992; 28 (suppl 1): S26-32.

4 Brown J, Dove R, Price B, Fong S, Ford R. Continuousmultiple location body temperature measurement oninfants. Aust Phys Eng Sci Med 1990; 13: 85-7.

5 Dove R, Brown J, Fright R, Tuffnell C, Ford R. Computerpolygraphic system for infants at risk for sudden infant deathsyndrome (SIDS). Aust Phys Eng SciMed 1990; 13: 188-91.

6 Macey PM, Ford RPK, Brown PJ, Larkin J, Fright WR,Garden KL. Apnoea detection: human performance andreliability of a computer algorithm. Acta Paediatr 1995; 84:1103-7.

7 Harper RM, Schechtman VL, Kluge KA. Machine classifi-cation of infant sleep state using cardiorespiratorymeasures. Electroencephalogr Clin Neurophysiol 1987; 67:379-87.

8 SAS Institute Inc, Cary, NC.9 Lodemore M, Petersen SA, Wailoo MP. Development of

night time temperature rhythms over the first six months oflife. Arch Dis Child 1991; 66: 521-4.

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