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Accuracy of Peripheral Thermometers for Estimating Temperature: A Systematic Review and Meta-analysisAccuracy of Peripheral Thermometers

Daniel J. Niven, MD, MSc; Jonathan E. Gaudet, MD, MSc; Kevin B. Laupland, MD, MSc; Kelly J. Mrklas, MSc; Derek J. Roberts, MD, PhD; and Henry Thomas Stelfox, MD, PhD
[+] Article, Author, and Disclosure Information

From Peter Lougheed Centre, Foothills Medical Centre, and University of Calgary, Calgary, Alberta; and Royal Inland Hospital, Kamloops, British Columbia, Canada.

Acknowledgment: The authors thank Drs. Juan Posadas, Wataru Inoue, Byoungchun Lee, and Ebba Kurz for their help in translating, screening, and extracting data from relevant non–English-language articles; Dr. Sharon Straus for her comments on an earlier version of this manuscript; and the editors and reviewers for their suggestions that strengthened this manuscript.

Financial Support: This study did not receive any specific funding from any organization. Drs. Niven and Roberts are funded through Clinician Fellowship Awards from Alberta Innovates–Health Solutions and Knowledge Translation Canada Student Fellowship and Training Program grants. Dr. Stelfox is supported by a New Investigator Award from the Canadian Institutes of Health Research and a Population Health Investigator Award from Alberta Innovates–Health Solutions.

Disclosures: Authors have disclosed no conflicts of interest. Forms can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M15-1150.

Editors' Disclosures: Christine Laine, MD, MPH, Editor in Chief, reports that she has no financial relationships or interests to disclose. Darren B. Taichman, MD, PhD, Executive Deputy Editor, reports that he has no financial relationships or interests to disclose. Cynthia D. Mulrow, MD, MSc, Senior Deputy Editor, reports that she has no relationships or interests to disclose. Deborah Cotton, MD, MPH, Deputy Editor, reports that she has no financial relationships or interest to disclose. Jaya K. Rao, MD, MHS, Deputy Editor, reports that she has stock holdings/options in Eli Lilly and Pfizer. Sankey V. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose. Catharine B. Stack, PhD, MS, Deputy Editor for Statistics, reports that she has stock holdings in Pfizer.

Reproducible Research Statement:Study protocol, statistical code, and data set: Available to approved persons by written agreements (Dr. Niven; e-mail, Daniel.niven@alberta healthservices.ca).

Requests for Single Reprints: Daniel J. Niven, MD, Department of Critical Care Medicine, Peter Lougheed Centre, 3500 26th Avenue Northeast, Calgary, Alberta T1Y 6J4, Canada; e-mail, Daniel.niven@albertahealthservices.ca.

Current Author Addresses: Drs. Niven and Gaudet: Department of Critical Care Medicine, Peter Lougheed Centre, 3500 26th Avenue Northeast, Calgary, Alberta T1Y 6J4, Canada.

Dr. Laupland: Department of Medicine, Royal Inland Hospital, 311 Columbia Street, Kamloops, British Columbia V2C 2T1, Canada.

Ms. Mrklas: Foothills Medical Centre, South Tower, 1403 29th Street Northwest, Calgary, Alberta T2N 2T9, Canada.

Dr. Roberts: Department of Critical Care Medicine, Foothills Medical Centre, 3134 Hospital Drive Northwest, Calgary, Alberta T2N 5A1, Canada.

Dr. Stelfox: Teaching, Research, and Wellness Building, University of Calgary, 3280 Hospital Drive Northwest, Calgary, Alberta T2N 4Z6, Canada.

Author Contributions: Conception and design: D.J. Niven, K.B. Laupland, D.J. Roberts, H.T. Stelfox.

Analysis and interpretation of the data: D.J. Niven, K.B. Laupland, K.J. Mrklas, D.J. Roberts.

Drafting of the article: D.J. Niven, D.J. Roberts, H.T. Stelfox.

Critical revision of the article for important intellectual content: D.J. Niven, J.E. Gaudet, K.B. Laupland, K.J. Mrklas, D.J. Roberts, H.T. Stelfox.

Final approval of the article: D.J. Niven, J.E. Gaudet, K.B. Laupland, K.J. Mrklas, D.J. Roberts, H.T. Stelfox.

Statistical expertise: D.J. Niven, D.J. Roberts, H.T. Stelfox.

Administrative, technical, or logistic support: H.T. Stelfox.

Collection and assembly of data: D.J. Niven, J.E. Gaudet, K.J. Mrklas.


Ann Intern Med. 2015;163(10):768-777. doi:10.7326/M15-1150
Text Size: A A A

Background: Body temperature is commonly used to screen patients for infectious diseases, establish diagnoses, monitor therapy, and guide management decisions.

Purpose: To determine the accuracy of peripheral thermometers for estimating core body temperature in adults and children.

Data Sources: MEDLINE, EMBASE, Cochrane Central Register of Controlled Trials, and CINAHL Plus from inception to July 2015.

Study Selection: Prospective studies comparing the accuracy of peripheral (tympanic membrane, temporal artery, axillary, or oral) thermometers with central (pulmonary artery catheter, urinary bladder, esophageal, or rectal) thermometers.

Data Extraction: 2 reviewers extracted data on study characteristics, methods, and outcomes and assessed the quality of individual studies.

Data Synthesis: 75 studies (8682 patients) were included. Most studies were at high or unclear risk of patient selection bias (74%) or index test bias (67%). Compared with central thermometers, peripheral thermometers had pooled 95% limits of agreement (random-effects meta-analysis) outside the predefined clinically acceptable range (± 0.5 °C), especially among patients with fever (−1.44 °C to 1.46 °C for adults; −1.49 °C to 0.43 °C for children) and hypothermia (−2.07 °C to 1.90 °C for adults; no data for children). For detection of fever (bivariate random-effects meta-analysis), sensitivity was low (64% [95% CI, 55% to 72%]; I2 = 95.7%; P < 0.001) but specificity was high (96% [CI, 93% to 97%]; I2 = 96.3%; P < 0.001). Only 1 study reported sensitivity and specificity for the detection of hypothermia.

Limitations: High-quality data for some temperature measurement techniques are limited. Pooled data are associated with interstudy heterogeneity that is not fully explained by stratified and metaregression analyses.

Conclusion: Peripheral thermometers do not have clinically acceptable accuracy and should not be used when accurate measurement of body temperature will influence clinical decisions.

Primary Funding Source: None.

Figures

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Appendix Figure 1.

Summary of evidence search and selection.

* Consisted of healthy volunteers excluded because of the absence of any medical illness.

† Survey (n = 3), case report or series (n = 2), and retrospective cohort (n = 1).

‡ Retrospective cohort (n = 2) and case series (n = 1).

§ 69 of 75 studies estimated the mean difference between index and reference thermometer using methods appropriate for repeated measures data.

|| 20 of 75 studies provided data required to determine pooled estimates of sensitivity and specificity for detecting fever or hypothermia.

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Appendix Figure 2.

Mean temperature difference between nonvascular central thermometers and the pulmonary artery catheter.

Weights are from random-effects analysis.

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Appendix Figure 3.

Summary of the QUADAS-2 risk-of-bias assessment for included studies.

Detailed quality assessment for individual studies available from Dr. Niven (e-mail, Daniel.niven@albertahealthservices.ca) on request. QUADAS = Quality Assessment of Diagnostic Accuracy Studies.

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Figure.

Pooled sensitivity and specificity for detecting fever by using peripheral thermometers.

* Pooled estimates obtained by a bivariate random-effects model (50).

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Appendix Figure 4.

Hierarchical SROC curve for detecting fever.

The SROC, estimates of sensitivity and specificity for the individual comparisons of index to reference thermometer, the summary operating point, and the 95% confidence contour for the summary point are shown. Numbered data points correspond to individual study estimates as follows: tympanic membrane thermometers: 1. Akinyinka, 2001 (58); 2. Allegaert, 2014 (57); 3. Duru, 2012 (59); 4. Edelu, 2011 (74); 5. Jean-Mary, 2002 (66); 6. Muma, 1991 (65); 7. Nimah, 2006 (61); 8. Paes, 2010 (73); 9. Petersen, 1997 (72); 10. Schmitz, 1995 (63); 11. Smitz, 2000 (71); 12. Teller, 2014 (70); 13. Yaron, 1995 (69); temporal artery thermometers: 14. Allegaert, 2014 (57); 15. Hebbar, 2005 (60); 16. Kimberger, 2007 (45); 17. Nimah, 2006 (61); 18. Odinaka, 2014 (68); 19. Schuh, 2004 (62); 20. Stelfox, 2010 (47); 21. Teran, 2012 (67); axillary thermometers: 22. Jean-Mary, 2002 (66); 23. Muma, 1991 (65); 24. Nimah, 2006 (61); 25. Schmitz, 1995 (63); 26. Zengeya (chemical dot), 1996 (64); 27. Zengeya (electronic), 1996 (64); 28. Zengeya (mercury), 1996 (64); and oral thermometers: 29. Schmitz, 1995 (63). Detailed 2 × 2 contingency tables for each included study available from Dr. Niven (e-mail, Daniel.niven@albertahealthservices.ca) on request. AUC = area under the curve; SROC = summary receiver-operating characteristic.

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Appendix Figure 5.

Pooled positive and negative likelihood ratios for detecting fever by using peripheral thermometers.

Pooled estimates obtained by using a bivariate random-effects model (50).

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Tables

References

Letters

NOTE:
Citing articles are presented as examples only. In non-demo SCM6 implementation, integration with CrossRef’s "Cited By" API will populate this tab (http://www.crossref.org/citedby.html).

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Comment
Posted on December 16, 2015
Mattia Bonzi, Fiorelli EM, Solbiati M, Montano N
Università degli Studi di Milano
Conflict of Interest: None Declared
We read with great interest the systematic review by Niven et al. (1) regarding the accuracy of peripheral thermometers for estimating core body temperature. They found that both the 95% limits of agreement between peripheral and central thermometers were outside the predefined clinically acceptable range (± 0.5 °C) and that the most commonly used peripheral thermometers have a poor diagnostic accuracy for detecting fever and hypothermia. The authors concluded that peripheral thermometers do not have clinically acceptable accuracy.
Although the question is very interesting we wonder if the authors’ findings should change clinical practice.
Indeed, before recommending the routine use of central thermometers in order to estimate body temperature, the evidence that a difference of at most 1.4 °C of temperature is clinically significant is warranted. It should be proved that a precise temperature assessment is able to improve clinical outcomes. If the most accurate evaluation of body temperature wouldn’t change clinical practice, the use of an invasive method to assess it could be inappropriate. On the same line of reasoning, since the non invasive evaluation of blood pressure has been proven not to be as accurate as the invasive one (2), one might say that an arterial line should be placed in order to measure blood pressure.
Finally, the studies included in the meta-analysis are very heterogeneous in terms of patients’ selection (adult and pediatric patients, patients in the intensive care unit, emergency department or surgical and medical wards), design of the studies, index tests and reference standards considered. This might affects per se the accuracy of the results, leading to questionable clinical application (3).

References
1. Niven DJ, Gaudet JE, Laupland KB, Mrklas KJ, Roberts DJ, Stelfox HT. Ann Intern Med. 2015 Nov 17;163(10):768-77. doi: 10.7326/M15-1150
2. Bur A, Herkner H, Vlcek M, Woisetschläger C, Derhaschnig U, Delle Karth G et al. Factors influencing the accuracy of oscillometric blood pressure measurement in critically ill patients. Crit Care Med. 2003 Mar;31(3):793-9
3. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org
Author's Response
Posted on January 20, 2016
Daniel J. Niven, MD, MSc, PhD, Kevin B. Laupland, Henry Thomas Stelfox, MD, PhD
University of Calgary, Royal Inland Hospital
Conflict of Interest: None Declared
Bonzi et al raise two questions regarding our meta-analysis examining the accuracy of peripheral thermometers (1). A concern of fundamental importance is the effect of inter-study heterogeneity on the clinical applicability of our pooled analyses. Although inter-study heterogeneity was the main limitation of our meta-analysis, we believe our pooled analyses remain clinically applicable. First, data were pooled across all studies, as our main objective was to describe peripheral thermometer accuracy. Second, we recognize that clinicians caring for different populations of patients benefit from data specific to a population or thermometer, and therefore we conducted pre-specified subgroup analyses to examine the effects of numerous factors on thermometer accuracy. These analyses demonstrated that peripheral thermometer accuracy was mostly dependent on thermometer factors, with the most accurate thermometers being electronic oral and tympanic membrane devices that are properly calibrated, and the least accurate being axillary thermometers. Third, in contrast to meta-analyses of randomized trials of therapeutic interventions, inter-study heterogeneity is a common finding in meta-analyses of diagnostic tests, and does not invalidate the pooled data (2).

Bonzi et al also question the importance of accurate temperature measurement in the context of outcomes of patient care. Few diagnostic tools have been shown to be associated with important clinical outcomes (e.g., mortality) and to the best of our knowledge, no studies have examined the association between temperature measurement accuracy and clinical outcomes. However, we believe that accurate temperate measurement may be important in guiding the care of certain patient populations. First, there is strong data that links fever, and/or hypothermia to increased morbidity and mortality in surgical patients (3), critically ill patients (4), and those with brain injury (5). Moreover, among surgical patients, maintenance of perioperative normothermia reduces surgical wound infections and shortens hospital length of stay (3), thus failure to detect hypothermia could expose these patients to potentially preventable adverse events. Although optimal temperature management strategies remain unclear for critically ill patients, and those with brain injury, accumulating further clinical and research experience in these populations is dependent on accurate temperature data. Second, among immunosuppressed patients (e.g. neutropenia) fever is a common sign of severe infections and inaccurate temperature data may delay diagnosis and management of potentially life-threatening infections. For these reasons, we feel that until data show that accurate temperature measurements are not associated with clinical outcomes, clinicians should attempt to monitor temperature using a thermometer that balances accuracy with safety and practicality.

Contributors
DJN: Drafted the manuscript.
KBL: Provided key revisions to the manuscript.
HTS: Provided key revisions to the manuscript.

Funding: This study did not receive any specific funding from any organization. HTS is supported by a Population Health Investigator Award from Alberta Innovates – Health Solutions. DJN and KBL do not have any relevant funding to declare. The funding agencies did not contribute to preparation, review, or approval of the final manuscript.

Declaration of interests: All authors declare no personal, professional, or financial relationships that could have influenced this work.
REFERENCES

1. Niven DJ, Gaudet JE, Laupland KB, Mrklas KJ, Roberts DJ, Stelfox HT. Accuracy of Peripheral Thermometers for Estimating Temperature: A Systematic Review and Meta-analysis. Ann Intern Med. 2015;163:768-77.
2. Leeflang MM, Deeks JJ, Gatsonis C, Bossuyt PM, Cochrane Diagnostic Test Accuracy Working G. Systematic reviews of diagnostic test accuracy. Ann Intern Med. 2008;149:889-97.
3. Kurz A, Sessler DI, Lenhardt R. Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N Engl J Med. 1996;334:1209-15.
4. Young PJ, Saxena M, Beasley R, Bellomo R, Bailey M, Pilcher D, et al. Early peak temperature and mortality in critically ill patients with or without infection. Intensive Care Med. 2012;38:437-44.
5. Saxena M, Young P, Pilcher D, Bailey M, Harrison D, Bellomo R, et al. Early temperature and mortality in critically ill patients with acute neurological diseases: trauma and stroke differ from infection. Intensive Care Med. 2015;41:823-32.

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