Dewhirst Mark W, Oleson James R, Kirkpatrick John, Secomb Timothy W
Department of Radiation Oncology, Duke University School of Medicine, Durham, NC 27710, USA.
Department of Physiology, University of Arizona, Tucson, AZ 85724, USA.
Cancers (Basel). 2022 Mar 27;14(7):1701. doi: 10.3390/cancers14071701.
Numerous randomized trials have revealed that hyperthermia (HT) + radiotherapy or chemotherapy improves local tumor control, progression free and overall survival vs. radiotherapy or chemotherapy alone. Despite these successes, however, some individuals fail combination therapy; not every patient will obtain maximal benefit from HT. There are many potential reasons for failure. In this paper, we focus on how HT influences tumor hypoxia, since hypoxia negatively influences radiotherapy and chemotherapy response as well as immune surveillance. Pre-clinically, it is well established that reoxygenation of tumors in response to HT is related to the time and temperature of exposure. In most pre-clinical studies, reoxygenation occurs only during or shortly after a HT treatment. If this were the case clinically, then it would be challenging to take advantage of HT induced reoxygenation. An important question, therefore, is whether HT induced reoxygenation occurs in the clinic that is of radiobiological significance. In this review, we will discuss the influence of thermal history on reoxygenation in both human and canine cancers treated with thermoradiotherapy. Results of several clinical series show that reoxygenation is observed and persists for 24-48 h after HT. Further, reoxygenation is associated with treatment outcome in thermoradiotherapy trials as assessed by: (1) a doubling of pathologic complete response (pCR) in human soft tissue sarcomas, (2) a 14 mmHg increase in pO2 of locally advanced breast cancers achieving a clinical response vs. a 9 mmHg decrease in pO2 of locally advanced breast cancers that did not respond and (3) a significant correlation between extent of reoxygenation (as assessed by pO2 probes and hypoxia marker drug immunohistochemistry) and duration of local tumor control in canine soft tissue sarcomas. The persistence of reoxygenation out to 24-48 h post HT is distinctly different from most reported rodent studies. In these clinical series, comparison of thermal data with physiologic response shows that within the same tumor, temperatures at the higher end of the temperature distribution likely kill cells, resulting in reduced oxygen consumption rate, while lower temperatures in the same tumor improve perfusion. However, reoxygenation does not occur in all subjects, leading to significant uncertainty about the thermal-physiologic relationship. This uncertainty stems from limited knowledge about the spatiotemporal characteristics of temperature and physiologic response. We conclude with recommendations for future research with emphasis on retrieving co-registered thermal and physiologic data before and after HT in order to begin to unravel complex thermophysiologic interactions that appear to occur with thermoradiotherapy.
众多随机试验表明,与单独放疗或化疗相比,热疗(HT)联合放疗或化疗可改善局部肿瘤控制、无进展生存期和总生存期。然而,尽管取得了这些成功,但仍有一些个体对联合治疗无效;并非每个患者都能从热疗中获得最大益处。失败的原因有很多。在本文中,我们重点关注热疗如何影响肿瘤缺氧,因为缺氧会对放疗和化疗反应以及免疫监视产生负面影响。临床前研究已充分证实,肿瘤因热疗而发生的复氧与暴露时间和温度有关。在大多数临床前研究中,复氧仅发生在热疗期间或之后不久。如果临床上也是如此,那么利用热疗诱导的复氧将具有挑战性。因此,一个重要的问题是热疗诱导的复氧在临床上是否具有放射生物学意义。在这篇综述中,我们将讨论热疗史对接受热放疗的人类和犬类癌症复氧的影响。几个临床系列的结果表明,复氧现象在热疗后被观察到并持续24 - 48小时。此外,在热放疗试验中,复氧与治疗结果相关,具体表现为:(1)人类软组织肉瘤的病理完全缓解(pCR)翻倍;(2)达到临床反应的局部晚期乳腺癌的pO2增加14 mmHg,而无反应的局部晚期乳腺癌的pO2下降9 mmHg;(3)犬类软组织肉瘤的复氧程度(通过pO2探针和缺氧标记药物免疫组化评估)与局部肿瘤控制持续时间之间存在显著相关性。热疗后24 - 48小时复氧现象的持续存在与大多数报道的啮齿动物研究明显不同。在这些临床系列中,热数据与生理反应的比较表明,在同一肿瘤内,温度分布较高端的温度可能会杀死细胞,导致氧消耗率降低,而同一肿瘤内较低的温度会改善灌注。然而,并非所有受试者都会发生复氧,这导致了热生理关系的显著不确定性。这种不确定性源于对温度和生理反应的时空特征的了解有限。我们最后提出了未来研究的建议,重点是在热疗前后获取共同注册的热数据和生理数据,以便开始揭示热放疗中似乎发生的复杂热生理相互作用。