Abstract
Background
During cytoreductive surgery combined with hyperthermic intraperitoneal chemotherapy (HIPEC), precise core temperature monitoring is critical for patient safety. This prospective study evaluated the agreement among three core temperature monitoring modalities: nasopharyngeal temperature (Tnaso), zero-heat flux cutaneous thermometer (TSpotOn), and oesophageal temperature (Teso).
Methods
Temperatures were measured simultaneously; agreement between monitoring sites was assessed using Bland–Altman analysis for repeated measures including mean bias, 95% limits of agreement, and confidence intervals, alongside Lin’s concordance correlation coefficient (LCCC). The proportion of paired differences within the clinically acceptable limit of 0.5 °C was reported.
Results
The mean difference between Tnaso and TSpotOn was −0.04 ± 0.33 °C (95% limits: −0.69 to 0.62), and between Tnaso and Teso was 0.02 ± 0.35 °C (95% limits: −0.66 to 0.71), with LCCC for both comparisons at 0.94 (95% CI: 0.93–0.94), indicating substantial agreement. However, up to 14% of Teso pairs exceeded the 0.5 °C threshold, suggesting potential clinical relevance. Notable rapid temperature decline and subsequent rebound were observed post-HIPEC at Tnaso and TSpotOn sites.
Conclusion
All three monitoring methods correlated strongly overall, but Teso exhibited phase-dependent discrepancies, particularly after HIPEC. These findings support tailoring core temperature measurement site selection with attention to the target organ, especially in laparotomy-based HIPEC procedures.
Trial registration: The study was registered in the clinical trials registry cris.nih.go.kr (Registration Number: KCT0003980).
Keywords: Cytoreductive surgery, Hyperthermic intraperitoneal chemotherapy, Zero-heat flux cutaneous thermometer, Oesophageal temperature, Rebound heating
Background
Hyperthermic intraperitoneal chemotherapy (HIPEC) is a rapidly evolving treatment for peritoneal carcinomatosis offering improved survival compared to traditional palliation [1]. The high-concentration delivery of heated intraperitoneal chemotherapy, with limited systemic absorption [2], has revolutionised patient management.
Under normal conditions, the body temperature is not uniform, often exhibiting a 2–4 °C difference between core and shell temperatures. Vasomotor thermoregulation helps maintain a stable core temperature by redistributing heat in response to environmental temperature changes. However, rapid cooling or rewarming can disrupt this equilibrium [3].
The administration of heated chemotherapeutics intraperitoneally poses unique anaesthetic challenges, including large fluctuations in core temperature that necessitate vigilant thermoregulation [4–6]. Hence, accurate temperature monitoring is crucial for maintaining normothermia throughout the procedure. Although pulmonary artery catheterization remains the gold standard for core temperature, its invasiveness limits routine use, requiring alternative sites such as nasopharyngeal, oesophageal, and zero-heat flux cutaneous sites. The susceptibility of these sites to localized thermal effects during HIPEC mandates comparative evaluation to guide appropriate monitoring [7–9].
In this study, we aimed to compare the effectiveness of nasopharyngeal temperature (Tnaso) monitoring with that of two other core temperature measurement techniques, ZHF (TSpotOn) and oesophageal temperature (Teso), during HIPEC paired with cytoreductive surgery.
Materials and methods
Data collection spanned from July 2019 to December 2022. Sample size calculations, based on prior ZHF thermometry studies [9] determined that 55 participants would provide adequate power to detect temperature differences of ±0.5 °C with a SD within ±0.05 °C and 95% confidence, accounting for a 10% dropout rate. During the study period, 55 patients who had provided written informed consent underwent cytoreductive surgery combined with HIPEC at our hospital. Eligibility was assessed for adult patients scheduled for cytoreductive surgery under general anaesthesia, and all consenting participants were included in the study. Patients were excluded if they had: systemic or local infections of the forehead, contraindications to oesophageal or nasal probe insertion, or altered chemotherapy plans for various reasons.
Patients underwent standardized balanced anaesthesia. Temperature probes were inserted as follows: nasopharyngeal probe (E-temp, Ewha Biomedics, Seoul, South Korea) to depth approximating the nares-to-earlobe distance; oesophageal probe (E-temp, Ewha Biomedics) to 30 cm from the nostrils or 20 cm from the lips after intubation using the Mekjavic and Rempel formula; and the SpotOn ZHF sensor (3MBair Hugger™ Temperature Monitoring System, 3 M, St Paul, MN, USA) was applied to the forehead [10].
All HIPEC procedures utilized an open technique lasting 90 min, with perfusate temperature maintained at 41.5–41.8 °C using a hyperthermic lavage system. (Hyperthermia pump, Belmont Instrument Corporation, Billerica, MA, USA).
The paclitaxel or mitomycin was administered depending on the cancer origin. Continuous temperature monitoring was performed at the inlet and outlet of the perfusate system during HIPEC.
Normothermia was maintained by a Barkey S-line fluid warmer (Barkey GmbH, Germany), an upper-body convective thermal blanket (Bair Hugger Upper Body Convective Warming Blanket, 3M, UK), and a circulating water mattress (Blanketrol Ⅱ, Cincinnati Sub-Zero, Cincinnati, OH, USA).
Temperature measurements were recorded concurrently at 5-min intervals throughout the perioperative period. Temperature differences were then calculated for each measurement pair.
Statistical analysis
Agreement between measurement sites was evaluated using Bland–Altman analysis for repeated measures [11], including calculation of mean bias, 95% limits of agreement, and corresponding confidence intervals. The clinically significant threshold was specified as differences within ±0.5 °C based on existing guidelines [12]. Lin’s concordance correlation coefficient (LCCC) was applied to assess reproducibility and strength of agreement based on McBride’s strength-of-agreement criteria for continuous variables (almost perfect: 0.99; substantial: 0.95–0.99; moderate: 0.90–0.95; poor: 0.90) [13] and all estimates included 95% confidence intervals. Results are presented as mean ± SD or mean SD (95% limits of agreement). Analyses were performed with IBM SPSS Statistics 26 (IBM Corp., Armonk, NY, USA) and MedCalc 17.7.2 (Medcalc software, Ostend, Belgium).
Results
A total of 55 patients were initially enrolled; however, 14 were excluded due to changes in chemotherapy protocol or failure to undergo HIPEC following cytoreductive surgery. Accordingly, 41 patients were included in the final analysis (Fig. 1).
Fig. 1.
Flow chart
Demographic and surgical details are shown in Table 1. Categorical data are expressed as numbers and percentages (n, %), whereas quantitative data are reported as median values with interquartile ranges (25th–75th percentiles).
Table 1.
Demographic and surgical characteristics
| Characteristic | Value (median [interquartile range] or number (percentage)) |
|---|---|
| Age (years) | 59 [50–63] |
| Sex (Male) | 13 (32%) |
| Body mass index (kg/m2) | 24 [22–25] |
| ASA physical status | |
| ASA 1 | 8 (19%) |
| ASA 2 | 27 (66%) |
| ASA 3 | 6 (15%) |
| Type of surgery | |
| Ovary cancer | 13 (32%) |
| Colon cancer | 17 (41%) |
| Pseudomyxoma | 8 (20%) |
| Primary peritoneal carcinoma | 3 (7%) |
| Anaesthesia time (min) | 545 [465–635] |
| Operation time (min) | 495 [405–595] |
| Blood loss (mL) | 600 [320–1150] |
Post hoc power analysis, based on the observed sample size and effect estimates, demonstrated over 80% power to detect a clinically meaningful temperature difference (δ = 0.5 °C), validating the robustness of this cohort for the primary endpoint.
Temperature agreements between Tnaso and other monitoring sites (TSpotOn and Teso) were also analysed separately for pre-, during, and post-HIPEC periods (Table 2; Figs. 4a, b, 5a, b).
Table 2.
Comparison between Tnaso and reference methods
| Period/method | Mean (SD) temperature (°C) | 95% limits of agreement (95% CI) | Proportion of differences within 0.5 °C (95% CI) | LCCC (95% CI) |
|---|---|---|---|---|
| Overall | ||||
| Teso | 0.02 (0.35) | −0.66 to 0.71 | −0.06 (−0.08 to−0.05) | 0.94 (0.93–0.94) |
| TSpotOn | −0.04 (0.33) | −0.69 to 0.62 | 0.03 (0.01–0.04) | 0.94 (0.93–0.94) |
| Pre-HIPEC period | ||||
| Teso | 0.09 (0.26) | −0.42 to 0.60 | 0.00 (−0.04 to 0.03) | 0.85 (0.84–0.87) |
| TSpotOn | −0.07 (0.27) | −0.59 to 0.46 | −0.01 (−0.04 to 0.03) | 0.85 (0.83–0.87) |
| HIPEC period | ||||
| Teso | −0.12 (0.39) | −0.89 to 0.65 | −0.03 (−0.06 to 0.00) | 0.90 (0.89–0.91) |
| TSpotOn | −0.03 (0.41) | −0.84 to 0.77 | 0.01 (−0.02 to 0.05) | 0.90 (0.88–0.91) |
| Post-HIPEC period | ||||
| Teso | 0.15 (0.37) | −0.58 to 0.87 | −0.01 (−0.07 to 0.04) | 0.88 (0.85–0.90) |
| TSpotOn | 0.04 (0.30) | −0.55 to 0.63 | 0.03 (−0.01 to 0.07) | 0.93 (0.91–0.94) |
Tnaso nasopharyngeal temperature, TSpotOn® temperatures measured at the forehead using a SpotOn® sensor, Teso oesophageal temperature, CI confidence interval, SD standard deviation, LCCC Lin’s concordance correlation coefficient
Fig. 4.
Bland–Altman plots of core temperature measurements during the HIPEC period comparing Tnaso was compared to temperatures measured using: a a ZHF thermometer and b an oesophageal probe. Dotted lines indicate the 95% limits of agreement
Fig. 5.
Bland–Altman plots of core temperature measurements after the HIPEC period. Tnaso was compared to temperatures measured using: a a ZHF thermometer and b an oesophageal probe. Dotted lines indicate the 95% limits of agreement
Pre-HIPEC phase
At induction and during initial surgical preparation, core temperatures measured at the nasopharyngeal (Tnaso), forehead (zero-heat flux; TSpotOn), and oesophageal (Teso) sites were stable and normothermic. The mean Tnaso was 35.9 ± 0.1 °C. Temperature differences among modalities were minimal during this phase, with mean bias values of 0.09 °C (Tnaso vs. Teso) and −0.07 °C (Tnaso vs. TSpotOn). Limits of agreement remained tight (see Table 2), and over 94% of paired measurements were within the clinically accepted ±0.5 °C threshold. Lin’s concordance correlation coefficients (LCCC) indicated moderate to substantial agreement (0.85 for both comparisons).
HIPEC phase
During the pre-HIPEC phase, baseline core temperatures were consistent across nasopharyngeal (Tnaso), forehead zero-heat flux (TSpotOn), and oesophageal (Teso) measurements. The mean Tnaso was 35.9 ± 0.1 °C (range: 35.7–36.3 °C), establishing stable and normothermic conditions.
Table 2 reports the statistical agreement for this phase: the mean difference (bias) between Tnaso and Teso was 0.09 °C (SD 0.26 °C; 95% limits: −0.42 to 0.60 °C), while that between Tnaso and TSpotOn was −0.07 °C (SD 0.27 °C; 95% limits: −0.59 to 0.46 °C). Lin’s concordance correlation coefficient (LCCC) was 0.85 for both comparisons. Notably, more than 94% of paired measurements for all modalities fell within the clinically relevant range (±0.5 °C). These results confirm high reliability among monitoring sites in stable peri-induction conditions.
Post-HIPEC phase
Following cessation of hyperthermic perfusate, rapid temperature decline was observed at all measurement sites, with mean Tnaso decreasing to 36.8 ± 0.4 °C (range: 36.2–37.7 °C). Table 2 provides comparative statistical results for the post-HIPEC phase: mean difference between Tnaso and TSpotOn was 0.04 °C (SD 0.30 °C; 95% limits: −0.55 to 0.63 °C), and between Tnaso and Teso was 0.15 °C (SD 0.37 °C; 95% limits: −0.58 to 0.87 °C). The agreement remained high, with LCCC values of 0.93 and 0.88, respectively.
Importantly, up to 14% of Teso comparisons again exceeded ±0.5 °C, as shown graphically in Fig. 5a and b. Rebound hyperthermia was prominent at nasopharyngeal and forehead sites, with some patients experiencing transient temperatures above 39 °C (Fig. 2). This phenomenon poses potential risks for hemodynamic instability and may impact postoperative cognitive and neurological outcomes, as well as increase metabolic demand and influence drug pharmacokinetics—elements requiring further clinical vigilance.
Fig. 2.
Mean temperatures during the operation
Bland–Altman analysis revealed minimal bias and tight limits of agreement between Tnaso and TSpotOn, and Tnaso and Teso, consistent across pre-HIPEC, intra-HIPEC, and post-HIPEC phases (Figs. 2, 3; Table 2). Lin’s concordance correlation coefficients exceeded 0.90 at all intervals, confirming substantial agreement.
Fig. 3.
Bland–Altman plot of core temperature measurements comparing nasopharyngeal temperature (Tnaso) to different measurements. a The ZHF thermometer (TSpotOn) and b with an oesophageal probe (Teso). Dotted lines indicate the 95% limits of agreement
Discussion
This study primarily evaluated the reliability of the ZHF method during the HIPEC period. The findings underscore a strong correlation between Tnaso, TSpotOn, and Teso temperatures during cytoreductive surgery with HIPEC. The oesophageal temperature, however, exhibited notable phase-dependent variability, especially post-HIPEC, likely reflecting influences from exposure of the abdominal cavity, local tissue conduction, and hemodynamics.
Notably, during the post-HIPEC period, rebound heating was observed at all monitoring sites, especially in the nasopharyngeal and forehead (ZHF) areas.
During the initial phase of surgery prior to HIPEC, temperatures across all monitoring sites were consistent and within the normothermic range, exhibiting minimal measurement discrepancies. This reflects a stable physiological state, wherein the redistribution of heat is well maintained by the body’s thermoregulatory mechanisms, resulting in tight agreement among sites [14] (Figs. 4, 5).
However, during active HIPEC administration, when rapid core temperature changes occur, discrepancies increased, particularly involving the oesophageal probe. The reliability of zero-heat flux devices under dynamic temperature conditions has been questioned, with studies reporting site-dependent error margins of up to 1 °C, particularly during rapid rewarming or cooling phases [9, 15]. Our study demonstrated strong correlations during phases of rapid core temperature change. The mean difference between Teso and Tnaso of −0.09 ± 0.46 °C, and between Tnaso and TSpotOn was 0.03 ± 0.41 °C. However, site-to-site discrepancies became increasingly pronounced, with up to 14% of paired comparisons surpassing a 0.5 °C threshold and absolute differences reaching as high as 1.5 °C. Absolute differences exceeding 0.5 °C occurred in fewer than 6% of cases, though 14% of pairs showed discrepancies greater than 0.5 °C between Tnaso and Teso.
These discrepancies are of clinical relevance: even a 1 °C elevation in core temperature can trigger a cascade of management interventions, including initiation of forced-air or intravenous fluid cooling, or adjustment of perfusate temperature.
Interestingly, after the HIPEC phase, temperatures rapidly decreased, followed by a noticeable rebound, particularly Tnaso and TSpotOn (Fig. 1). The maximum difference between Teso and other temperatures was 1.5 °C (Tnaso) and 1.5 °C (TSpotOn). Rebound hyperthermia observed post-HIPEC aligns with documented phenomena in cardiac surgery, where rewarming can increase the cardiovascular load and cause collapse due to peripheral vasodilation, resulting in a reduction in the core temperature as cold blood returns from the extremities [16]. Although no prior studies have explicitly documented post-HIPEC rebound hyperthermia, a similar phenomenon was reported in HIPEC patients undergoing secondary cytoreductive surgery [17].
Central nervous system vulnerability to hyperthermia may exacerbate postoperative delirium and cognitive dysfunction, particularly as memory impairment has been documented at core temperatures exceeding 38.8 °C [18, 19].
It may also influence pharmacokinetic profiles of anesthetic and chemotherapeutic agents through enhanced enzymatic activity and altered tissue perfusion. The redistribution of heat and peripheral vasodilation during rewarming may further obscure the accuracy of core monitoring, particularly when measurement sites are discordant in response to dynamic shifts in thermal gradients [20, 21].
Systematic reviews by Boisson et al. and Conway et al. confirm that, despite strong overall agreement, ZHF thermometry may diverge from core temperature measurements by as much as 1 °C during rapid thermal changes characteristic of HIPEC [9, 14]. Our findings demonstrate narrower limits of agreement between zero-heat flux (ZHF) and oesophageal temperature measurements compared to those reported by Boisson et al., who observed wider limits during rapid core temperature changes associated with HIPEC and other surgical settings. This may be attributed to larger sample size, standardized anesthetic and warming protocols, uniform probe placement guided by validated formulas, and controlled timing of measurements, all of which contributed to reduced variability. Our data reinforce that while ZHF thermometry is reliable during stable temperature phases, caution is warranted during rapid temperature fluctuations common in HIPEC.
These findings underscore the need for precise, site-appropriate temperature monitoring during HIPEC, as reliance on a single measurement site may not reliably reflect true core temperature throughout all procedural phases.
The oesophageal temperature tended to reflect abdominal cavity temperature during cytoreductive surgery. Overall, Teso readings were lower than Tnaso and TSpotOn; however, during HIPEC, Teso was higher than TSpotOn. This inconsistency may be explained by adjunctive tissue conduction, blood flow, and heat dissipation via the open abdominal cavity. Temperature discrepancies between Teso and other measurement sites were inconsistent, being positive during pre- and post-HIPEC periods but negative during HIPEC itself.
These discrepancies in Teso warrant clinical attention during intraoperative management. An overestimation or underestimation of true core temperature at a selected measurement site may provoke either unnecessary interventions or missed opportunities for timely management, with corresponding effects on intraoperative metabolic acidosis, hemodynamic stability, and neurological status. Notably, core hyperthermia accelerates enzymatic drug metabolism and elevates cardiovascular demand, necessitating vigilant intraoperative monitoring and nuanced anaesthetic management [22].
The primary limitation of this investigation is the absence of pulmonary artery temperature monitoring, precluding direct comparison with the gold-standard core temperature. Furthermore, the exclusive focus on open cytoreductive surgery with HIPEC may constrain generalizability to minimally invasive or alternative perfusion techniques. The potential impact of environmental factors, device placement, and patient-specific variables warrants further exploration in future multi-center, randomized studies.
Conclusions
All examined core temperature monitoring methods demonstrate close agreement during HIPEC; however, clinically significant discrepancies—especially with oesophageal measurements—necessitate careful, phase-specific selection and interpretation of monitoring sites to optimize intraoperative temperature management. These results reinforce the imperative for anaesthesiologists and surgical teams to interpret temperature measurements judiciously, considering the inherent limitations and phase-specific behaviors of each monitoring modality.
Acknowledgements
We would like to thank Dongwook Kim for assisting with the statistical analysis for this study.
Abbreviations
- CI
Confidence interval
- HIPEC
Hyperthermic intraperitoneal chemotherapy
- LCCC
Lin’s concordance correlation coefficient
- SD
Standard deviation
- Tnaso
Nasopharyngeal temperature
- TSpotOn
Temperatures measured at the forehead using a SpotOn sensor
- Teso
Oesophageal temperature
- ZHF
Zero-heat flux cutaneous thermometer
Author contributions
SWA: Study design, patient recruitment, data collection, data analysis, drawing up the first draft of the paper and correspondence; JWK: statistical analysis and manuscript drafting; JHK: patient recruitment, data collection, statistical management; SO: patient recruitment and data collection. All authors have read and approved the final manuscript.
Funding
None of the authors has any personal financial interests related to this research.
Availability of data and materials
Additional supporting files whenever possible.
Declarations
Ethics approval and consent to participate
This study was approved by the Ethics Committee for Research with Medicine of CHA Bundang Medical Centre, CHA University Hospital, Gyeonggi-do, Korea, on 15 August 2019 (Approval Number: CHAMC-04-050-007). The study was conducted according to institutional and Good Clinical Practice guidelines. Written informed consent was obtained from all participating patients.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Data Availability Statement
Additional supporting files whenever possible.