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A systematic review of body temperature variations in older people

Shu-Hua Lu, Angela-Renee Leasure and Yu-Tzu Dai

Aim. The purpose of this systematic review was to determine the extent to which the research literature indicates body temperature norms in the geriatric population.

Objectives. The specific questions addressed were to examine normal body temperature values in persons 60 years of age and older; determine differences in temperature values depending on non-invasive measurement site and measurement device used;

and, examine the degree and extent of temperature variability according to time of day and time of year.

Background. The traditional ‘normal’ temperature of 98Æ6 F/37 C may in fact be lower in older people due to the ageing process. Age-associated changes in vasomotor sweating function, skeletal muscle response, temperature perception and physical behaviours may influence the ability to maintain optimum temperature.

Design. A systematic literature review.

Methods. A search of multiple databases yielded 22 papers which met inclusion criteria. Studies were included which focused on temperature measurement, sampled persons 60 years of age and older, collected data from non-invasive temperature mea- surement sites and which used a prospective study design. Studies were independently appraised using a structured appraisal format.

Results. Temperature normal values by site were rectal 98Æ8 F/37Æ1 C, ear-based 98Æ3 F/36Æ8 C, urine 97Æ6 F/36Æ5 C, oral 97Æ4 F/36Æ3 C and axillary 97Æ1 F/36Æ2 C. Temperature exhibited a 0Æ7 F/0Æ4 C diurnal and 0Æ2 F/0Æ1 C circannual variation.

Conclusions. Synthesis of data indicated that normal body temperature values in older people by sites were rectal 0Æ7 F/0Æ4 C, ear-based 0Æ3 F/0Æ2 C, oral 1Æ2 F/0Æ7 C, axillary 0Æ6 F/0Æ3 C lower than adults’ acceptable value from those traditionally found in nursing textbooks.

Relevance to clinical practice. Given the fact that normal body temperature values were consistently lower than values reported in the literature, clinicians may need to re-evaluate the point at which interventions for abnormal temperatures are initiated.

Key words: axillary temperature, body temperature, ear-based temperature, oral temperature, rectal temperature, urine temperature

Accepted for publication: 6 February 2009

Introduction

To intervene accurately in the care of older people, nurses should be armed with the knowledge of normal temperature range and mean, predictable variations as well as potential

sources of measurement error. An accurate measurement of body temperature depends upon three factors: an accurate thermometer; a valid measurement site; and, the skills of the individual measuring the temperature. Measurement error can arise from any one of the three factors and result in either

Authors: Shu-Hua Lu, PhD, RN, Lecturer, Department of Nursing, Mackay Medicine, Nursing and Management College, Taipei, Taiwan; Angela-Renee Leasure, PhD, RN, CNS, CCRN, Associate Professor, College of Nursing, University of Oklahoma Health Sciences Center and, Research Investigator, Department of Veterans Affairs Medical Center, Oklahoma City, OK, USA; Yu-Tzu Dai, PhD, RN, Professor, Department of Nursing, College of Medicine,

National Taiwan University and, Director, Department of Nursing, National Taiwan University Hospital, Taipei, Taiwan

Correspondence: Yu-Tzu Dai, Professor, No. 1, Jen-AI RD., SEC.1, Taipei, 10051, Taiwan, R.O.C. Telephone: +886 2 2312 3456 (ext.

88437, 62178).

E-mail: yutzu@ntu.edu.tw

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unnecessary or delayed treatment for conditions ranging from infection to hypothermia. As well as external sources of measurement error can result from both systematic and random sources of temperature variability, albeit within a narrow range, within each person.

Wunderlich (1869) is credited with establishing the ranges of normal body temperature in l869. He supervised the collection of axillary temperatures of 25,000 healthy subjects and then defined normal body temperature as being 98Æ6 F/

37 C and the normal temperature range as 97Æ2 F/36Æ2 C to 99Æ4 F/37Æ5 C. Wunderlich found temperature values reached their nadir period in the mornings between two and eight and zenith in the evenings between four and nine. He also reported a 0Æ9 F/0Æ5 C lower reading in older people as compared to adults of a younger age. Wunderlich’s values have been widely adopted since that time although we now know that temperature values differ across measurement sites, modern thermometry has improved accuracy; and we now know that temperature has predictable variability. Also, the thermometer Wunderlich used was later found to read 1Æ4–2Æ2 C higher than the thermometry in use today (Mackowiak & Worden 1994).

Aim

The aims of this systematic review was to evaluate existing evidence to (i) determine a normal body temperature value and range for persons 60 years of age and older; (ii) determine differences in temperature ranges according to non-invasive measurement site and device in older people and (iii) examine the degree and extent of temperature variability according to time of day and time of year.

Background knowledge

Temperature monitoring sites and devices are evaluated against their ability to estimate core body temperature (Cereda & Maccioli 2004). In this section, the literature on the sites and temperature measurement devices will be reviewed to examine their theoretical base, strengths and limitations.

Noninvasive temperature measurement sites

Several non-invasive and more accessible sites including rectum, oral cavity, urinary bladder, axilla and ear canal have been widely used to measure body temperature. A site receiving afferent blood supply and airless space is presumed to be more likely to reflect core body temperature, the temperature of the hypothalamus. The gold standard of core

temperature obtained with a pulmonary artery catheter is not used in daily clinical practice due to the invasiveness of catheterization.

Rectal site measurement

Among non-invasive sites, temperatures measured using the rectal site is considered to most closely reflect core body temperature (Smith 2003a). However, rectal temperatures are not commonly used in the home and ambulatory care settings because it is often considered to be intrusive and thus less acceptable to patients. Sources of error can result from excess faecal matter in the rectum, faecal incontinence, as well as inadequate depth of thermometer insertion. Also rectal temperature is thought to lag behind core temperature changes during times of rapid temperature changes.

Oral site measurement

The oral cavity is a popular site for temperature measure- ment, because the thermometer probe is placed in a sublin- gual pocket near deep tongue arteries that are supplied by the carotid artery (Fulbrook 1993). Hot and cold beverages, smoking of cigarettes and chewing gum should be avoided for a minimum of 30 minutes before temperature measurement (Sugarek 1986, Quatrara et al. 2007) to avoid false high or low readings. In older people, dentures may impair the accuracy of readings due to the difficulty keeping the probe in place and the lips sealed (Marion et al. 1991). Also, persons with dementia or experiencing confusion may have inaccu- rate readings due to the inability of the individual to keep the temperature probe in the sublingual pocket and the lips sealed. Neither use of supplemental oxygen therapy being delivered at <6 l/minute nor the presence of an endotracheal tube have been consistently shown to significantly alter oral temperature readings (Hasler & Cohen 1982, Yonkman 1982).

Urine temperature measurement

Urinary bladder temperatures can be measured using an

indwelling urinary bladder thermistor catheter which pro-

vides a continuous digital display of temperature readings

(Lilly et al. 1980). Although considered to be one type of core

temperature measurement, this type of temperature measure-

ment is considered to be intrusive and is used almost

exclusively with critically ill patients. A more popular way

to measure urine temperature is to void urine into a

container through a funnel containing a thermometer. The

resulting urine temperature, an indirect measure of bladder

(3)

temperature, has been shown to be highly correlated with both rectal (Brooke et al. 1973, Ehrenkranz 1986) and vaginal temperatures (Samples & Abrams 1984).

Axillary site measurement

In contrast to oral, urinary bladder and rectal sites; the axillary site does not carry the same exposure to body fluid contact. The axillary site is an area that is protected from radiant heat loss. The asymmetrical location of chest organs may suggest a predictable difference between right and left axilla (Giuffre et al. 1990, Heidenreich & Giuffre 1990);

vasodilatation and vasoconstriction may increase and decrease axillary temperatures respectively; and, during times of rapid temperature changes, axillary temperatures are thought to lag behind core temperatures. Today, axillary temperatures are considered to be less accurate, reflecting skin rather than core temperature.

Ear-based temperature measurement

Ear-based or tympanic membrane temperature measurement is used popularly in the clinical setting, because it is non- invasive and convenient. The blood supply to the tympanic membrane arises from the same branch of the carotid arteries as the hypothalamus (Boulant 1998). However, it is still controversial whether ear-based temperature represents the core body temperature.

Temperature measurement devices

The search for an ideal measurement device which reflects core temperature change accurately, safely, quickly and with easy access continues (Erickson & Yount 1991, Varney et al.

2002). Each of the temperature measurement devices avail- able today has strengths and limitations. An acceptable difference between measurement devices was set a priori at 0Æ4 F/0Æ2 C (Hanneman 2008).

Mercury-in-glass thermometers

Mercury-in-glass thermometers have been considered to be a highly reliable tool for years and as such were used as the temperature measurement device in many of the studies included in this systematic review. However, due to concerns about mercury poisoning and environmental pro- tection, mercury-in-glass thermometers have all but disap- peared from clinical practice although they may still be found in many homes. These bulb thermometers contain mercury which responds to heat by rising in a standardised

manner. Temperatures are read based upon marks on the glass of the thermometer which corresponds to the height of the mercury column. A temperature is taken in a ‘shake and take’ manner where the mercury is ‘shaken down’ into the bulb of the thermometer prior to use. The mercury then rises within the glass thermometer column to the highest temperature and remains there until ‘shaken down’. The National Institute of Standards and Technology (NIST) is responsible for maintenance and dissemination of the International Temperature Scale of l990 (ITS-90) for the United States. Thermometers are evaluated for accuracy using a water bath and comparing at three different temperature points. Thermometer readings are compared against an NIST calibrated and certified thermometer.

Thermometers which differ more than ± 0Æ2 F/0Æ1 C from the calibrated reference thermometer at the three tempera- ture points are not considered to be accurate (Wise 1991, 1994).

Electronic thermometers

Electronic thermometers are comprised of a metal thermo- probe coupled with an electronic display unit. The metal probe is covered with a single use plastic cover. Electronic thermometers use internal circuitry to predict body temper- ature based upon initial heat curves in typically 30–50 sec- onds (Erickson & Meyer 1994, Prentice & Moreland 1999).

Ear-based thermometry

Infrared ear thermometers (IET) include a speculum like probe which when inserted into the aural canal samples radiant heat coming from the tympanic membrane and surrounding structures. Readings can be set to display as actual mode, core equivalent, oral equivalent, or rectal equivalent through use of an internal conversion utility. As different IET use different algorithms, the actual mode was considered to be desirable when using this type of thermo- meter for data collection in the studies (Terndrup & Rajk 1992, Christensen & Boysen 2002). IET was initially derived from the direct contact tympanic membrane thermometer.

Tympanic membrane thermometers consisted of a thin wire which was advanced until making contact with the tympanic membrane and either left at that point or withdrawn a short distance.

There are many factors that may result in an inaccurate measurement when taking ear-based temperature including:

cerumen or hair follicles in the auditory canal; the natural

curvature of the aural canal or its size which result in inaccurate

positioning of the thermometer probe; and a chipped or dirty

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infrared detector may each impede unobstructed access to the tympanic membrane. Ear-based temperature readings in these situations tend to be inaccurate and show a falsely low body temperature. Some sources recommend tugging the ear down and back to straighten the external auditory canal. As use of an ear tug is not universal included studies were reviewed regarding inclusion of this measurement method. Stability of measurement can be negatively impacted by errors introduced when the opposite, rather than near ear, is used. Also, values can be falsely elevated if the ear used has been occluded by a pillow (Erickson & Meyer 1994, Hasel & Erickson 1995, Petersen & Hauge 1997, Braun et al. 1998, Heusch &

McCarthy 2005).

Urine thermometry

Urine temperatures are collected using a device which has a thermometer placed below a funnel. Although designs vary depending on the specific device used, urine is voided into a collecting jar through a funnel which contains a thermome- ter. The thermometer tip partially occludes the funnel mouth which allows a longer immersion time with the urine.

Accuracy of urine temperatures is decreased when <100 ml of urine is collected, in cold ambient environments and in situations where the urine stream is passed from a great height (Ellenbogen & Nord 1972, Brooke et al. 1973, Judson et al. 1979, Samples & Abrams 1984).

Galinstan-in-glass thermometers

Galinstan-in-glass thermometers an alloy of gallium, indium and tin, are being used as nontoxic replacements for mercury- in-glass thermometers. These devices have not yet been widely used in temperature research but have garnered interest among clinicians in an effort to reduce possible cross-contamination of patients with communicable illnesses. Evidence to date has indicated clinical agreement between mercury-in-glass and Galinstan-in-glass thermometers (oral Æ203 F; axillary Æ253 F and rectal Æ05 F bias across site). Both mercury-in-glass and Galinstan-in-glass thermometers are checked for accuracy using a swirling water bath and checking against a NIST calibrated thermometer (Smith 2003b).

Methods

Study inclusion criteria

Original studies were included in this review if they focused on normal body temperature of older people and

met the following inclusion criteria: (i) study samples which included human subjects ages 60 and older; (ii) measured body temperature at least one time and used at least one non-invasive method of temperature measurement and (iii) used a prospective design.

Search strategy

A systematic literature review was performed, using both Chinese and Western scientific databases including: MED- LINE (1966–2008), CINAHL (1982–2008), Ageline (1978–

2008), EMBASE (1988–2008), Current Contents, Cochrane and the Electronic Theses and Dissertations System. Terms searched were: axillary temperature, basal body tempera- ture, body temperature, body temperature measurement, core temperature, mouth temperature, normal body temper- ature, oral temperature, rectal temperature, skin temperature, temperature, temperature measurement, ear temperature, tympanic temperature, temperature measurement, tempera- ture monitoring, temperature recording, elderly, aged, age- ing and geriatric. The results were then merged and cross-searched. Studies were limited to human and to adults (middle-aged and aged) when these limits were available. Additionally, the references of retrieved studies were examined for additional studies which met inclusion criteria.

From this search 290 studies were retrieved. From this initial number, abstracts were reviewed for inclusion. From the abstracts reviewed 23 full text articles were evaluated for inclusion. Studies were excluded which: grouped afebrile and febrile subjects: reported correlations and measures of agree- ment rather than group means; collected data through chart review; and combined those 60 and over with other age groups. Twenty-two articles were selected for inclusion in this systematic review.

Definitions

Older people were defined as persons 60 years of age and

older to be as inclusive of as many studies as possible. Studies

were included in this systematic review which sampled a

larger age range if those 60 years or older could be identified

for subgroup analysis. Definitions of non-invasive tempera-

ture vary widely. For the purposes of this review non-invasive

sites of temperature were considered to be oral, rectal, ear-

based, urine and axillary. Hand, groyne and cutaneous sites

were excluded due to the infrequent use of these sites

for temperature measurement in the clinical practice

environment.

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Results

Summary of papers selected for inclusion in the review

Studies included in the review were independently appraised by two different reviewers using a structured appraisal sheet.

Discrepancies in ratings were resolved through discussion and when necessary consultation with a third person. Some studies only indicated mean temperatures, making it impos- sible to identify the distribution of temperature highs, lows and extremes. If the primary data did not specifically include range values, the temperature range was indicated with the mean (v) value ± 2 standard deviations (SD) provided in the study report and the results were labelled with an asterisk (*).

If the primary data did not include body temperature means and SD, they were indicated by a dash (–).

Among the 22 sampled studies, ten of the studies reviewed sampled community dwelling elders, five sampled nursing home residents and eight recruited older subjects from hospital inpatients. Two studies (Fox et al. 1973b, Primrose

& Smith 1982) used a systematic random sampling procedure while the other studies used non-random sampling proce- dures. Sample size for the included studies ranged from 18–1020 subjects. The measurement site and device most frequently reported was the oral temperature using a mercury thermometer. Few studies reported information assuring inter-rater reliability testing and training of data collectors, number of data collectors used and methods of assuring stability and consistency of measurement. Finally, in studies which compared values obtained from different temperature measurement sites, statistical analyses were primarily corre- lational rather than graphed as Bland and Altman plots (Bland & Altman 1995). Table 1 provides a synthesis of study findings.

The methods described by Sund-Levander et al. (2002) guided the meta-analysis of temperature data across studies.

When data was reported by differing age groups, time of day, time of year, sites, devices, or setting; new mean values were calculated by using the formula [(v

1

n

1

+ v

2

n

2

…)/n

1

+ n

2

…].

For comparison C was converted to F using the for- mula



C 

95



þ 32 ¼



F.

Normal body temperature values across measurement sites

The data of body temperature from five measurement sites in 22 studies were examined. Three studies measured a total of 547 rectal temperatures for v = 98Æ76 (SD 0Æ08). Using these values the normal rectal temperature would be 98Æ8 F/

37Æ1 C and the normal temperature range would be 98Æ6 to

99Æ0 F/37Æ0 to 37Æ2 C. Five studies collected 1118 ear-based temperatures v = 98Æ3 (SD 0Æ81). Using these values the normal ear-based temperature would be 98Æ3 F/36Æ8 C with a normal temperature range of 97Æ5 to 99Æ1 F/36Æ4 to 37Æ3 C. Four studies collected 1282 urine temperatures with a v = 97Æ59 (SD 0Æ28). Thus, the normal urine temperature would be 97Æ6 F/36Æ5 C with a urine temperature range of 97Æ3 to 97Æ9 F/36Æ3 to 36Æ7 C.

Among the 16 studies which sampled oral temperatures, the overall lowest value registered was 85Æ99 F/30 C which was considered to be an outlying data point (Howell 1975).

The primary study author calculated temperature midpoints with and without the next lowest value, 95 F/32Æ6 C. Thus the study mean based upon the second lowest temperature value of temperature of 95 F/32Æ6 C, rather than 85Æ99 F/

30 C, was used in calculations. Also, temperature values from two publications (Marion et al. 1991, McGann et al.

1993) which described findings from the same group of subjects were included only once in the analysis. Across 2265 oral temperature measurements a v = 97Æ41 (SD 0Æ17) was obtained. The mean temperature difference between elec- tronic and mercury thermometry was compared to determine differences based upon type of thermometry used. The mercury to electronic thermometer difference was 0Æ16 F/

0Æ1 C which falls within an acceptable range of difference.

Thus a normal oral temperature would be 97Æ4 F/36Æ3 C and the oral temperature range would be 97Æ0 to 97Æ8 F/36Æ1 to 36Æ6 C. Across 395 axillary temperatures measurements from four studies the mean was v = 97Æ06 (SD 0Æ87) with a resulting normal axillary temperature would be 97Æ10 F/

36Æ2 C and the axillary temperature range would be 96Æ2 to 97Æ9 F/35Æ7 to 36Æ6 C. Figure 1 is a schematic representa- tion of temperature ranges across studies grouped by site of temperature measurement. In summary, when rectal temper- atures were used as the standard of comparison, the rectal site yielded body temperatures 0Æ5 F/0Æ3 C higher than the ear- based site; 1Æ2 F/0Æ6 C higher than urine temperatures;

1Æ4 F/0Æ7 C higher than the oral site; and 1Æ7 F/0Æ9 C higher than the axillary site (Table 2).

Temperature variability

Diurnal variation was examined comparing 1344 oral tem-

perature readings. Morning mean temperatures were v = 96Æ9

(SD 0Æ20) and afternoon v = 97Æ6 (SD 0Æ17) resulting in a

0Æ7 F/0Æ4 C diurnal variation. Circannual variation was

based upon 237 oral temperature measurements. Mean body

temperatures in the summer were v = 97Æ53 (SD 0Æ44) and in

the winter were slightly lower at v = 97Æ3 (SD 0Æ60) which

resulted in a 0Æ2 F/0Æ1 C variation.

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Table 1 Sum mary and review of included studies No. Auth ors C ase Numbe r/setting Age Seaso n/time of day Site (Devi ce) Mean ( F/ C) Range/mea n ± 2S D ( F/ C) Notes 1 Colli ns et al. (19 81) 17 Elderly 70 –80 N o t specified Oral (E) 98 Æ1/ 36 Æ79 6 Æ4–99 Æ7/35 Æ8–37 Æ6

*

No exclusi on criteri on was speci fied 13 Young 18 –39 97 Æ9/ 36 Æ69 6 Æ8–99 Æ0/36 Æ0–37 Æ2

*

R esearch centre 2 Cham berlai n et al. (19 95) 49 7 Hosp ital 66 –75 N o t specified Ear (IE T) 97 Æ6/ 36 Æ59 6 Æ1–99 Æ2/35 Æ6–37 Æ3 Exclu sion criteria were re ported. Infrared ear thermo meter (Therm oscan



Pro-1) wa s used. Mode wa s reporte d in the actua l mode and were collecte d fr o m the right ea r

76 –85 97 Æ5/ 36 Æ49 5 Æ8–99 Æ3/35 Æ5–37 Æ4 > 85 97 Æ5/ 36 Æ49 5 Æ9–99 Æ2/35 Æ5–37 Æ3 3 Darowsk i et al. (1991) 50 Hospi tal ‡ 70 10 a.m. R ectal (M) 98 Æ9/ 37 Æ29 8 Æ2–99 Æ7/36 Æ8–37 Æ6 Recta l the rmome ters were inse rted a dept h o f 5 cm from the anus. Audito ry canal thermo meter was used

6 p.m. Oral (E) 97 Æ9/ 36 Æ69 6 Æ7–99 Æ0/36 Æ1–37 Æ2 A xillary (M) 97 Æ3/ 36 Æ39 5 Æ9–98 Æ6/35 Æ5–37 Æ0 Ear (ACT) £ 9 8 Æ2/ 36 Æ89 7 Æ7–98 Æ8/36 Æ5–37 Æ1 4 Fox et al. (1973a) 72 Commu nity 65 –91 Wi nter Oral (M) 97 Æ0/ 36 Æ19 4 Æ8–99 Æ1/34 Æ9–37 Æ3

*

Exclu sion criteria no t speci fied. Reliability of data collection instrum ents not reporte d U rine 97 Æ5/ 36 Æ49 4 Æ3-1 00 Æ7/34 Æ6-38 Æ2

*

5 Fox et al. (1973b) 10 20 Commu nity ‡ 65 Wi nter Oral (M) 96 Æ8/ 36 Æ09 4 Æ3–99 Æ4/34 Æ6–37 Æ4

*

Exclu sion criteria were speci fied. The inve stigators did not report how reliabil ity was establ ished U rine 97 Æ3/ 36 Æ39 5 Æ5–99 Æ1/35 Æ3–37 Æ3

*

8–10 a.m. Oral (M) 97 Æ6/ 36 Æ59 5 Æ8–99 Æ5/35 Æ4–37 Æ5

*

4–6 p.m. U rine 98 Æ0/ 36 Æ69 5 Æ8–10 0 Æ1/35 Æ5–37 Æ8

*

6 Gian tin et al. (2008 ) 1 0 7 Hosp ital 65–104 Jun e–August A xillary (G) 98 Æ4/ 36 Æ99 6 Æ2–10 0 Æ6/35 Æ7–38 Æ1

*

Room temperature wa s constan tly maintai ned at 23 C. Infrared ear thermo meter (First Temp



Genius



Model 3000A) was used and the m ode was not report ed. Re liability of the temperature m easurem ent device s was repo rted

A xillary (E) 98 Æ4/ 36 Æ99 6 Æ2–10 0 Æ6/35 Æ7-38 Æ1

*

A xillary £ 9 7 Æ7/ 36 Æ59 5 Æ5–99 Æ8/35 Æ3–37 Æ7

*

Ear (IE T) 98 Æ8/ 37 Æ19 6 Æ2-1 01 Æ3/35 Æ7-38 Æ5

*

7 Gomo lin et al. (2005) 10 0 Nurs ing Home 65 –98 6 a.m. Oral (E) 97 Æ3/ 36 Æ39 4 Æ0–98 Æ8/34 Æ4–37 Æ1 Calib ration of thermo meter s was not report ed 4 p.m. 97 Æ4/ 36 Æ39 5 Æ5–99 Æ6/35 Æ2–37 Æ6 50 Commu nity 10 p.m. 97 Æ8/ 36 Æ69 6 Æ1–99 Æ6/35 Æ6–37 Æ6 Mi dday 97 Æ7/ 36 Æ59 5 Æ7–99 Æ1/35 Æ4–37 Æ3 8 Gomo lin et al. (2007) 16 7 Nurs ing hom e 65–102 6–8 a.m. Oral (E) 97 Æ3/ 36 Æ39 4 Æ0–99 Æ0/34 Æ4–37 Æ2 There was no descri ption of verificati on of thermo meter accuracy 21 Teenagers 4–5 p.m. 97 Æ4/ 36 Æ39 5 Æ1-9 9 Æ6/35 Æ1–37 Æ6 6–8 a.m. 97 Æ1/ 36 Æ29 5 Æ5-9 8 Æ7/35 Æ3–37 Æ1 14 –17 Æ8 4–5 p.m. 97 Æ8/ 36 Æ69 6 Æ0–99 Æ2/35 Æ6–37 Æ3 9 Gun es and Z aybak (2008) 13 3 Nurs ing hom e 6 5 –90 8 a.m. A xillary (M) 96 Æ2/ 35 Æ69 5 Æ0–97 Æ7/35 Æ0-36 Æ5 The m ethod of establ ishing accuracy of thermo meters was report ed 2 p.m. 96 Æ3/ 35 Æ79 4 Æ1–97 Æ7/34 Æ5–36 Æ5 6 p.m. 96 Æ8/ 36 Æ09 5 Æ5-9 7 Æ7/35 Æ3–36 Æ5 10 Higg ins (1983 ) 6 0 Commu nity 65 –90 9–12 a.m. Oral (M) 97 Æ9/ 36 Æ6 – Exclu sion criteria were speci fied. The thermo meter used for data collect ion was cali brated

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Tabl e 1 (Co ntinued) No. Auth ors Case Number/ setting Age Seaso n/time of day Site (Device ) Mean ( F/ C) Rang e/mean ± 2S D ( F/ C ) Notes 11 Howel l (1972) 105 Hosp ital 60–1 00 11 a.m. Axillary (E) 96 Æ4/ 35 Æ89 3 Æ2–99 Æ3/34 Æ0–3 7 Æ4 E x clusion criteri a were not speci fied. The elec tric thermo meter wa s calibrat ed 12 Howel l (1975) 105 Hosp ital 61–1 00 11 a.m. Oral (E ) – 85 Æ9–99 Æ0/30 Æ0–3 7 Æ2 Inclusi on and exclusion criteri a were not specified 13 Keilson et al. (1985) 97 Elderly 65–90 Nov ember– Apri l Oral (E ) 9 7 Æ2/ 36 Æ29 5 Æ7–98 Æ7/35 Æ4–3 7 Æ0

*

The only exclusion criteria specified wa s n o known acute il lness 20 Adult Commu nity 22–43 Urine 97 Æ5/ 36 Æ49 6 Æ3–98 Æ8/35 Æ7–3 7 Æ1

*

Oral (E ) 9 7 Æ5/ 36 Æ49 6 Æ0–99 Æ1/35 Æ6–3 7 Æ2

*

Urine 97 Æ7/ 36 Æ59 6 Æ4–99 Æ1/35 Æ8–3 7 Æ3

*

14 Mar ion et al. (1991) 93 Hospita l & Commun ity 62–96 Nov ember Oral (M ) 9 8 Æ3/ 36 Æ89 7 Æ5–99 Æ1/36 Æ4–3 7 Æ3

*

Ex clusion criteri a were clearly ide ntified. Therm ometers were calibr ated in a w ater bath befo re and af ter each me asurem ent

Oral (E ) 9 8 Æ5/ 36 Æ99 7 Æ5–99 Æ4/36 Æ4–3 7 Æ5

*

Urine 98 Æ6/ 37 Æ09 7 Æ7–99 Æ4/36 Æ5–3 7 Æ5

*

15 McGan n et al. (1993) 92 Commun ity 64–96 Nov ember Oral (M ) 9 8 Æ4/ 36 Æ99 7 Æ5–99 Æ2/36 Æ4–3 7 Æ3

*

Ex clusion criteri a clearly speci fied. Mercu ry in gla ss thermo meters were calibr ated 16 Nak amura et al. (1997) 57 Nursing home 75 Æ7( SD 6 Æ3) Mo rning Oral (E ) Inclusi on cr iteria were speci fied. The procedure for establishing and m onitoring the accuracy of thermo meter s was no t speci fied

Sum mer 97 Æ5/ 36 Æ49 6 Æ2-98 Æ7/35 Æ7-37 Æ1

*

Wi nter 98 Æ4/ 36 Æ19 4 Æ8–99 Æ2/34 Æ9–3 7 Æ3

*

A fterno on Sum mer 98 Æ3/ 36 Æ99 7 Æ0–99 Æ7/36 Æ1–3 7 Æ6

*

Wi nter 98 Æ0/ 36 Æ69 6 Æ1–99 Æ7/35 Æ6–3 7 Æ6

*

17 Prent ice and Morela nd (19 99) 18 Hospita l Not speci fied Not speci fied Oral (M ) 9 9 Æ7/ 36 Æ5 – Ex clusion criteri a were not speci fied. Infrared ear thermo meter (Th ermoscan



Pro-1) was used and the mode wa s not reported. Intra-ra ter and int er-rater dif ferences were clearl y described Oral (E ) 9 7 Æ8/ 36 Æ5– Ear (IET) 97 Æ5/ 36 Æ4– 18 Primro se and Smith (1982) 220 Commu nity 65–9 4 Nov ember– Decem ber 9 a.m. & 1 p.m .

Oral (E ) 9 7 Æ0/ 36 Æ09 5 Æ9–99 Æ1/35 Æ5–3 7 Æ3 E x clusion criteri a were not speci fied. The procedure for establishing int ra- and int er-rater reliabil ity amo ng data col lector s described 19 Salvo sa et al. (1971) 40 Commun ity 69–93 Wi nter Oral (M ) A m bient room temperatures were repo rted for each group of subject s. Meas ures of body mass index and skin fol d thi ckness bo dy fat were reporte d

Mo rning 96 Æ4/ 35 Æ89 4 Æ0–98 Æ7/34 Æ5–3 7 Æ1

*

Aftern oon 97 Æ0/ 36 Æ19 4 Æ8–99 Æ2/35 Æ0–3 7 Æ4

*

Sum mer Mo rning 96 Æ7/ 35 Æ99 5 Æ1–98 Æ3/35 Æ1–3 6 Æ9

*

Aftern oon 97 Æ3/ 36 Æ39 5 Æ3–99 Æ4/35 Æ2–3 7 Æ4

*

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Discussion

Normal body temperature values in older people

This systematic review demonstrated a mean rectal temper- ature of 98Æ8 F/37Æ1 C, range 98Æ6 to 99Æ0 F/37Æ0 to 37Æ2 C; ear-based temperature of 98Æ3 F/36Æ8 C, range 97Æ5 to 99Æ1 F/36Æ4 to 37Æ3 C, urine temperature of 97Æ6 F/

36Æ5 C, range 97Æ3 to 97Æ9 F/36Æ3 to 36Æ7 C; oral temper- ature of 97Æ4 F/36Æ3 C, range 97Æ0 to 97Æ8 F/36Æ1 to 36Æ6 C; and axillary temperature of 97Æ1F/36Æ2 C, range 96Æ2 to 97Æ9 F/35Æ7 to 36Æ6 C. The commonly reported temperatures in adults (Potter & Perry 2009) were compared to the values obtained in this review (Table 3). Body temperatures from all sites demonstrated lower values in older people group than in the adult group, suggesting the findings of this study confirm the theory of ‘the older are colder.’

Temperature variation by measurement site

The literature adds evidence to the generally held belief that rectal temperatures are usually 1Æ0 F/0Æ5 C higher than oral and ear-based temperature and axillary temperatures are usually 1Æ0 F/0Æ5 C lower than oral temperatures (Potter &

Perry 2009). In this study rectal temperatures, the noninva- sive gold standard, were 0Æ5 F/0Æ3 C higher than ear-based;

1Æ2 F/0Æ6 C higher than urine; 1Æ4 F/0Æ8 C higher than oral; and 1Æ7 F/0Æ9 C higher than axillary temperatures.

The results of temperature variations across sites must be interpreted with caution. Due to the small numbers of comparisons across several sites these findings represent a preliminary estimate. Many of the oral temperatures were collected with mercury thermometers which are no longer widely used. Also, no studies made comprehensive compar- isons of body temperature across each of the measurements sites. Studies using thermometry found in today’s health care setting and comparing body temperature across measurement sites are needed to validate these findings.

Diurnal and circannual temperature variation

Body temperature exhibited a 0Æ7 F/0Æ4 C diurnal variation which is less than half of the 1Æ8 F/1Æ0 C diurnal variation reported in adults (Kelly 2006). This finding is congruent with the report of other investigators who have found that circadian rhythms of older people are different from those of young adults (Campbell & Murphy 1998, Gubin et al. 2006).

A circannual oral temperature variation of 0Æ2 F/0Æ1 C lower in the winter season than summer was demonstrated Table 1 (Con tinued ) No. Authors Case Number/ setting Age Season/ time of day Site (Devi ce) Mean ( F/ C) Range/mea n ± 2S D ( F/ C) N otes 20 Sund-Le vander and Wahren (20 02)

237 Nurs ing hom e 71–9 8 7–9 a.m. Re ctal (E) 98 Æ2/36 Æ89 6 Æ8–99 Æ7/36 Æ0–37 Æ6

*

Ex clusion criteri a were speci fied. Accuracy of the temp eratur e measu rement devi ces wa s established and reported. Infrared ear thermo meter (First Temp



Gen ius



Model 3000A) and the unad juste d mod e were used . T h e author did not report dep th of insert ion of re ctal therm ometers

99 Æ1/37 Æ39 7 Æ7–10 0 Æ6/36 Æ5–38 Æ1

*

6–8 p.m. Ear (IET) 98 Æ4/36 Æ99 6 Æ2–10 0 Æ6/35 Æ7–38 Æ1

*

7–9 a.m. 99 Æ1/37 Æ39 7 Æ3–10 0 Æ9/36 Æ3–38 Æ3

*

6–8 p.m. 21 Thatch er (1983 ) 100 Commu nity 60–9 4 Summ er Oral (E) 98 Æ3/36 Æ99 7 Æ4–99 Æ2/36 Æ3–37 Æ4 E x clusion criteri a were report ed. The accuracy of the thermom eter wa s verified Winter 97 Æ4/36 Æ49 6 Æ3-9 8 Æ7/35 Æ7-3 7 Æ1 22 Vaux et al. (2000 ) 260 Hosp ital ‡ 75 Winter Re ctal (M) 98 Æ8/37 Æ19 7 Æ7–99 Æ7/36 Æ5–37 Æ6 Inf rared ear thermom eter (Fi rst Temp



Genius



Model 30 00A) wa s used and mode wa s not reported. Recta l therm ometers were inse rted 3 cm from the anal margin and read af ter three minutes.

Ear (IET) 98 Æ8/37 Æ19 7 Æ5–10 0 Æ2/36 Æ4–37 Æ9 Note: 1. ‘* ’ indic ates that range was calcu lated with/ mean ± 2 S D ; ‘–’ indicat es that pri mary data do not inc lude Mean or/mean ± 2 SD; £, Tempe rature site/ device excl uded from analy sis. 2. Dev ice of therm ometer used : M , Merc ury-in-g lass; E, Electronic thermo meter ; U , Urine temperature devi ce; G, Ga linsta n-in-glass; IET, Infrared ear thermo meter ; ACT, auditory cana l thermo meter .

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across comparisons. However, the small circannual temper- ature variation may have been influenced by the ambient temperatures of the rooms where temperatures were collected

as well as the small number of comparisons. So although the studies included in this review do show a decrease in body temperature during the winter as compared to summer

88 90 92 94 96 98 100 102

3 20 22 2 3 6 17 20 22 4 5 13 14 1 3 4 5 7 8 10 12 13 14 15 16 17 18 19 21 3 6 9 11

Different studies and various measurement site

Temperature (degree F) Max

Min Mean

Urine Axillary

Ear Oral

Rectal

Figure 1 The specific mean and range of body temperatures in the elderly arranged by measurement sites represented from 22 studies. Note: ‘1,2,3….’ corresponds to study numbers listed in Table 1.

Table 2 Comparison of overall statistics of body temperature in the elderly collected from different measurement sites and times 22 studies

Mean Range Difference

Sites

Rectal 98Æ8 F/37Æ1 C 98Æ6–99Æ0 F/37Æ0–37Æ2 C

Ear-based 98Æ3 F/36Æ8 C 97Æ5–99Æ1 F/36Æ4–37Æ3 C 0Æ5 F/0Æ3 C lower than the rectal site Urine 97Æ6 F/36Æ5 C 97Æ3–97Æ9 F/36Æ3–36Æ7 C 1Æ2 F/0Æ6 C lower than the rectal site Oral 97Æ4 F/36Æ3 C 97Æ0–97Æ8 F/36Æ1–36Æ6 C 1Æ4 F/0Æ7 C lower than the rectal site Axillary 97Æ1 F/36Æ2 C 96Æ2–97Æ9 F/35Æ7–36Æ6 C 1Æ7 F/0Æ9 C lower than the rectal site Diurnal variations

Morning 96Æ9 F/36Æ0 C 0Æ7 F/0Æ4 C

Afternoon 97Æ6 F/36Æ4 C

Circannual variations

Summer 97Æ5 F/36Æ4 C 0Æ2 F/0Æ1 C

Winter 97Æ3 F/36Æ3 C

Table 3 Comparison of mean temperature value of adult group and older group by measurement sites

Sites Mean body temperature in adult* Mean body temperature in the elderly



Difference

Rectal 99Æ5 F/37Æ5 C 98Æ8 F/37Æ1 C 0Æ7 F/0Æ4 C lower than adult

Ear-based 98Æ6 F/37Æ0 C 98Æ3 F/36Æ8 C 0Æ3 F/0Æ2 C lower than adult

Oral 98Æ6 F/37Æ0 C 97Æ4 F/36Æ3 C 1Æ2 F/0Æ7 C lower than adult

Axillary 97Æ7 F/36Æ5 C 97Æ1 F/36Æ2 C 0Æ6 F/0Æ3 C lower than adult

*Source from: Potter and Perry (2009). Vital signs. In Potter PA & Perry AG (eds.), Fundamentals of nursing (7th edn, pp. 503). St. Louis:

Mosby Elsevier.



Source from: the findings of this study.

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months, the magnitude of difference cannot be estimated at this time due to the small number of studies and several potentially confounding variables. To increase confidence in synthesising results across studies, it would be helpful if as well as reporting season of the year; future studies consis- tently report ambient temperatures. This would allow com- parison of results of studies which originate from different parts of the globe and which have different seasonal climates.

Conclusion

Body temperature in older people

Present evidence indicates a lower temperature mean in persons 60 years of age and older than the widely accepted normal value of 98Æ6 F/37 C. Tal et al. (2002) stated that normal physiologic changes associated with the ageing process may result in a lower body temperature which coupled with less temperature variability may result in a ‘blunted fever response’.

It has been suggested that a temperature above 100 F/37Æ8 C and two or more readings above 99 F/37Æ2 C or an increase of 2 F/1Æ1 C represents an index of suspicion for infection (Castle et al. 1991, Bentley et al. 2000).

Temperature findings may in fact be high or low secondary to cognitive impairment which may result in loss of the behavioural response to body signals (Culp & Cacchione 2008). Preliminary evidence indicates a modest increase in core body temperature in patients with Alzheimer’s disease (Klegeris et al. 2007). Alternately, differences in readings may be due to age related physiologic changes such as alterations in cutaneous blood flow (Grassi et al. 2003, Thompson- Torgerson et al. 2008).

Differences in temperature ranges in older people according to measurement site

The temperature difference across sites was greater than the 1 F/0Æ5 C degree difference traditionally discussed in the literature (Potter & Perry 2009). The evidence at this time does not support a conversion factor for comparison of temperature values across sites. Rather the evidence supports the importance of following and treating temperature abnor- malities based upon the readings from one consistent site and using one consistent form of thermometry (Sund-Levander et al. 2004).

Temperature variability in older people

Temperature did reflect a diurnal variation with temperature peaking in the evening. Due to concerns regarding hypother-

mia in older people, perhaps it is time to question the traditional nursing practice of giving baths in the morning when body temperatures are at their nadir rather than considering evening baths when temperatures are at their zenith. Circannual variation was very modest. However this finding may have been influenced by ambient conditions during data collection.

Relevance to clinical practice

The findings of this systematic review show that the normal body temperature values of older people from all sites were consistently lower than values reported in the literature, clinicians may need to re-evaluate the point at which interventions for abnormal temperatures are initiated.

Limitations

Many of the studies included in this review were published 10 years ago or longer; had relatively small samples (<100);

did not measure temperatures at a consistent time of day;

only measured temperatures one time; and, only used one method of temperature measurement. Mercury-in-glass ther- mometers, which are no longer available in many countries, were most frequently used to measure body temperature.

Also, few studies reported the method by which reliability of the measuring thermometer was monitored throughout the study. Although intra-rater and inter-rater reliability of the data collectors may have been established and monitored, it was not routinely reported in the studies reviewed. Partici- pants who were taking medications such as medication that causes vasodilatation which may promote heat loss or thyroid replacement which may increase heat production were not routinely excluded from participation.

Recommendations for future research

Studies which employ a longitudinal study design are needed to examine diurnal and circannual variation in older people.

A cross sectional study design could be used to determine accurate sites for temperature measurement, in addition to the reliable methods of thermometry in those ages 60 and older. Internal validity of future studies could be enhanced through controlling for the consistency of measurement procedures and also through evaluation and reporting of the accuracy and sensitivity of the thermometer used in the study.

To control for potentially confounding variables such as

nutrition, activity and cognitive impairment (Ferro-Luzzi

2005, Culp & Cacchione 2008) a metabolic cart could be

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used to determine basal metabolic rate. A metabolic cart measures heat production and hence energy expenditure.

Thus, the impact of basal metabolic rate on temperature in older people could be examined. There is evidence that basal metabolic rate may in fact increase in some individuals as they age (Henry 2000). Use of a metabolic cart would also address the role of nutritional status as a potentially confounding variable in the young-old as compared to the old-old. It may well be that basal metabolic rate is a more sensitive measure of temperature variation than is age.

Because temperature has nonlinear variability, techniques similar to those being used to measure heart rate variability could be employed to examine temperature variability in older people (Kelly 2006). Differences in variability, as well as baseline ranges may differ between the old and oldest-old age groups.

Acknowledgement

The authors express their appreciation to Deborah Booton- Hiser PhD, RN, FNP Professor and Director of the Nurse Practitioner Program and Mary Ann Pascucci PhD, RN, APRN-BC (Gerontology) at the University of Oklahoma Health Sciences Center for their careful review of several versions of this manuscript. We also thank Mr Mitchell B.

Leasure for his translation from French into English the article by Vaux and colleagues.

Contributions

Study design: SHL, ARL, YTD, data collection and analysis:

SHL, ARL, YTD and manuscript preparation: SHL, ARL, YTD.

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數據

Table 2 Comparison of overall statistics of body temperature in the elderly collected from different measurement sites and times 22 studies

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