Nutritional characterization of patients with oropharyngeal cancers: Impact of human papillomavirus status

doi:10.21203/rs.3.rs-4803916/v1

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Nutritional characterization of patients with oropharyngeal cancers: Impact of human papillomavirus status

https://doi.org/10.21203/rs.3.rs-4803916/v1

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Background

Oropharyngeal squamous cell carcinoma (OPSCC) of human papillomavirus (HPV)-positive status is increasing relative to HPV-negative disease. Nutritional features of OPSCC patients according to HPV status is unclear.

Subjects/Methods:

Canadian and Spanish patients with OPSCC were assessed for body mass index (BMI), weight loss grade (WLG), and computed tomography-defined skeletal muscle index (SMI). Chi-square, t-test, Mann-Whitney-U, Kruskal-Wallis tests were conducted to compare HPV positive and negative groups. Overall survival (OS) was assessed by univariable Kaplan-Meier and Cox proportional hazard methods.

Results

No differences in BMI, WLG, SMI and adipose tissue index between the 308 (Canada) and 134 (Spain) patients according to HPV status; hence cohorts were pooled (n = 442). HPV-positive patients (n = 317) were overweight/obese (72.8%), had WLG of 0/1 (59.6%) and high SMI (83.4%) while HPV-negative patients were normal/underweight (61.5%), had high WLG 3/4 (50.8%), and moderate/severe SMI depletion (46.9%)(p < 0.003). These overall differences notwithstanding, there was crossover i.e. 35% of HPV-positive patients had high WLG and/or moderate/severe muscle depletion and 29% of HPV-negative patients had minimal weight loss and high SMI. HPV-negative patients had a higher risk of mortality (HR 3.78, 95% CI 2.70 to 5.29, P < 0.001) and this difference was retained after multivariable adjustment for WLG, SMI, age, and disease stage (HR 3.19, 95% CI 2.12 to 4.79, P < 0.001).

Conclusion

Nutrition features of patients with OPSCC did not differ between Canada and Spain. Distinctive nutrition features exist in patients according to HPV status. The high heterogeneity of individual nutritional profiles invites an individualized approach to nutrition care.

Biological sciences/Cancer/Head and neck cancer/Oral cancer

Health sciences/Health care/Nutrition

The rise of oropharyngeal squamous cell carcinoma (OPSCC) incidence globally is largely attributed to Human papillomavirus (HPV) [1, 2]. Prevalence of HPV positive (+ ive) OPSCC varies geographically[3] and this subgroup is viewed as histo-pathologically distinct from HPV negative (-ive) OPSCC. The American Joint Committee on Cancer (AJCC)/Union International Cancer Control (UICC) staging systems 8th edition have defined HPV + ive and HPV-ive OPSCC separately, as the former is associated with better prognosis [4–6]. Patients with OPSCC are a recognized high-risk group for cancer-associated malnutrition due to its anatomic location and the toxicity associated with the treatment plan which is usually based on radiotherapy (RT) with/without concomitant chemotherapy [7, 8]. There is some suggestion that HPV + ive patients have a lower nutritional risk in general, based on high body mass index (BMI) and lower incidence and severity of nutrition impact symptoms before treatment [9–11]. However, issues with small sample size and inconsistent methods of nutritional assessment contributes to the uncertainty in the prevalence of cancer-associated malnutrition according to HPV status. Nutrition criteria like BMI do not capture specific skeletal muscle or fat mass depletion. The European Society of Clinical Nutrition and Metabolism and European Society of Medical Oncology guidelines recommend the validated measure of weight-loss grade (WLG)[12] concurrently with body composition to assess nutrition status of patients with cancer. Low muscle mass (i.e. sarcopenia) is associated with increased risk of mortality in patients with OPSCC [13–15]. Despite the increased incidence of HPV + ive OPSCC, studies evaluating depleted skeletal muscle mass (SMM) according to HPV status are scarce. A recent systematic review[16] reported a prevalence of sarcopenia ranging from 19–69% in patients with HPV + ive status, and inconsistencies in the methodology such as different vertebral landmark measurements and cutoff values were deemed responsible for the divergent prevalence values.

In this study we aimed to assess and compare nutritional and body composition features according to HPV status in patients with OPSCC in Canada and Spain.

Study Design and Participants

Our pooled cohort (see Statistical Analysis section for pooling criteria) included data from Canadian and Spanish cohorts. The Canadian cohort was selected from a population-based sample of patients diagnosed with head and neck cancer who were seen in new patient clinic for treatment planning at the Cross Cancer Institute serving in northern Alberta, Canada (population ~ 2.0 million). Included were consecutive patients (1/2011 to 11/2018) with an OPSCC diagnosis, known p16 immunohistochemistry status ^(INK4a) using immunohistochemistry protocol [17] (histology detection kit by Ventana Medical System, Inc. Tucson, Arizona) and abdominal computed tomography (CT) imaging prior to treatment initiation. The electronic health records were reviewed for height, weight, and planned treatments and dates of death and last follow-up.

The Spanish cohort included patients who were eligible to participate in a prospective multicenter observational cohort study (Protocol PR 138/19) who attended Head & Neck Cancer Functional Unit at the Catalan Institute of Oncology, L’Hospitalet del Llobregat (Barcelona) (serving ~ 2.0 million in Catalonia region, Spain) between 09/2016 to 04/2022. The inclusion criteria for the study were primary OPSCC diagnosis, planned treatment with curative intent and known HPV status determined by double positivity for HPV DNA and p16^INK4a from formalin-fixed paraffin-embedded tumor samples prior to treatment initiation. Exclusion criteria: refusing to participate in study, metastatic tumor stages, tumor recurrence in the previous 5 years and patients without baseline weight and height. Excluded from the body composition analysis were those patients without an abdominal CT.

This study was in accordance with the Declaration of Helsinki and the Spanish cohort received approval from the Hospital Universitari de Bellvitge Ethics Committee for Clinical Research, Protocol PR138/19) and Canadian cohort received approval from the Health Research Ethics Board of Alberta - Cancer, Protocol CC_17–0433.

Clinical data

Both study cohort’s demographic and clinical data were prospectively collected. The Canadian cohort demographics, cancer stage and dates of death and last follow-up were obtained from the Alberta Cancer Registry, certified by the North American Association for Central Cancer Registries. These data elements for the Spanish cohort were drawn from the prospective observational cohort study (Protocol PR 138/19) (see above). For uniformity both the Canadian and Spanish cohorts applied American Joint Committee on Cancer (AJCC) (7th ed.) staging of head and neck cancer [18]. Percent (%) weight loss was calculated as follows: [(current weight in kg- previous 6-month weight in kg) / previous 6-month weight in kg)] x 100. BMI was calculated as weight (kilograms) / height² (meters²). Weight Loss Grade (WLG), 0–4 calculated as previously described [19][20]. Eastern Cooperative Oncology Group (ECOG) Performance Status (ECOG-PS) was used[21] .The SMI (cm²/m²) groups were defined as:Normal (males: ≥ 45.3; females: ≥ 41.0), Class I SMI depletion (males: 45.2 to 37.5; females: 40.9 to 34.2) and Class II SMI depletion (males: <37.5; females: <34.2) [20]. Presence of Nutrition Impact Symptoms (NIS) were collected qualitatively from physician and dietitian clinical progress notes (Spain) or Patient-Generated Subjective Global Assessment-Short Form© [22](Canada).

Computed tomography (CT) Analysis

Skeletal muscle was measured as previously described, using Slice-O-Matic-V5.0 (Tomovision, Magog, Canada)[23, 24]. The cross-sectional area of all muscles in a single axial image landmarked at the 3rd lumbar vertebra was determined on unenhanced or contrast-enhanced CT studies, within a prespecified Hounsfield unit (HU) range (-29 to + 150 HU). Scanning parameters were as follows: CT scanners, (Canada: Phillips Gemini TF TOF16, Siemens Biograph 40, General Electric Discovery MI) (Spain: GE Healthcare Lightspeed 16 Pro, 366044CN6; Canon Medical Systems Aquilion Primer BCB17Z2468 and Aquilion One Prism, 1KA20X2061); slice thickness range, 1.5–6.5 mm; tube voltage 120 kV; dose modulation (mA) range, 100–500. A single expert observer at each institution was blinded to patients’ survival status and finalized all segmentations. The Canadian and Spanish expert’s precision test for Skeletal muscle area (SMA) was ± 0.84 cm² and ± 0.92 cm² respectively. Visceral and subcutaneous adipose tissue (-50 to – 150 HU and − 30 to -190 HU, respectively) were summed up in total adipose tissue (TAT). Both SMA and TAT were normalized by patient height (m²) and expressed as skeletal muscle index (SMI) (cm²/m²) and total adipose tissue index (TATI) (cm²/m²).

Statistical Analysis

Analyses completed using IBM SPSS Statistics for Windows V25.0 (SPSS, Chicago, IL). Variables tested for normality using the Shapiro-Wilk test. Differences between groups were assessed by Pearson’s Χ²-tests (categorical variables), 2-tailed t-test (continuous variables), or Fisher’s exact tests [post hoc Bonferroni corrections] or non-parametric (Mann-Whitney, Kruskal-Walli’s test) when appropriate. Data presented as means (and standard deviation, SD), medians (and interquartile range, IQR) or frequency (%). For overall survival (OS) analysis Kaplan-Meier with log-rank tests and hazard ratios (HR) compared survival between HPV groups. Univariable and multivariable analyses for OS were performed using the Cox proportional hazards model. Results were considered statistically significant when P-value was < 0.05.

The criterion for pooling cohorts was the absence of significant differences (using z-tests) in age and sex-specific regression coefficients for SMI between linear regression models for individual cohorts and the Pooled cohort [25]. There was a lack of statistically significant of all nutritional features between the two data sets, in addition to the z-tests.

Baseline Characteristics from Canadian and Spanish cohorts

The flow diagrams (Fig. 1A and 1B) depict the patients population cohorts from Canada and Spain of patients with OPSCC and known HPV status. A total of 308 and 134 patients respectively were included in the final analysis. Demographic and clinical characteristics of the Canadian and Spanish cohorts are shown in Supplemental Table 1. The Canadian cohort had a higher proportion of HPV + ive patients compared to HPV-ive patients (83.4% vs 16.5%, p < 0.001). Both cohorts showed a high proportion of males (84.7 and 73.9%) and Stage IVa/b disease (71.4 and 69.4%). Treatment plans differed between Canada and Spain. Patients in the Spanish cohort were more likely to be offered radiation-based treatment in contrast to patients in the Canadian cohort who equally offered radiation or surgical based treatments (p < 0.001).

The Canadian and Spanish cohorts did not show any statistically significant differences when their nutritional characteristics (World Health Organization BMI categories, WLG, skeletal muscle depletion) were compared within HPV status categories (Supplemental Table 2). Additionally, the age and sex-specific regression coefficients for SMI in linear regression models between the Canadian and Spanish cohorts did not differ (Supplementary Table 3). Based on this high degree of similarity between the patients from Canada and Spain in regard of BMI, weight loss and body composition, the cohorts were pooled for further analyses.

Baseline characteristics from pooled data

Demographic and clinical characteristics of the pooled sample (n = 442) are summarized in Table 1. Compared with patients HPV-ive status, those with HPV + ive were younger (mean age = 62.0 (SD = 9.6) vs 58.7 (SD = 8.3) (p < 0.001) and had better ECOG-PS 0–1 (86.1% vs 79.2%, p = 0.042)).

Comparison of baseline nutritional and body composition features according to HPV status.

Nutrition and body composition features of the pooled cohort and by HPV status is shown in Table 2. Compared to patients with HPV-ive status, HPV + ive patients were more likely to have BMI > 25kg/m² (38.4% vs 72.8%, p < .001), WLG 0–1 (40.8% vs. 58.3%, p < .001) and no skeletal muscle depletion (Normal SMI) (50.5% vs 83.4%, p < .001). The sex-specific body composition features of SMI and TATI show that both sexes of patients HPV + ive have significantly higher muscularity and higher adiposity than HPV-ive sub-group (Table 2). Figure 3 illustrates the cross-tabulation of WLG and SMI by HPV status. This illustration underscores the low prevalence of SMI depletion across all grades of weight loss, as well as the high prevalence of low WLG in the HPV + ive group. While these constituted the overall main differences, it is worthy of note that some HPV + ive patients had low SMI and/or high-grade weight loss and that some HPV-ive patients had high SMI and low WLG.

A comparison of nutrition impact symptoms by HPV status from Canada and Spain shown in Table 3. These data are only comparable within country, because of different methods of symptom data collection. HPV + ive patients had lower incidence of most nutrition impact symptoms.

Survival analysis

Consistent with the literature HPV + ive patients were more likely to be alive at time of censoring (79.2%, n = 251). Kaplan Meier analysis of overall survival (OS) (Fig. 2) illustrates the large difference in survival according to HPV status, with HPV + ive having a median survival of 90.0 months, 95% CI, 84.2 to 96.8 months while HPV-ive survived a median of 22 months, 95% CI, 4.9 to 39.1 months (p < .001). HPV-ive patients had a higher risk of mortality (HR 3.78, 95% CI 2.70 to 5.29, P < 0.001) in univariable Cox proportional hazard model. After multivariable adjustment for WLG, SMI, age, and disease stage, the HPV-ive patients still had a higher risk or mortality (HR 3.19, 95% CI 2.12 to 4.79, P < 0.001) (Table 4), suggesting that nutritional features do not explain the well-known survival difference attributed to HPV status.

Historically the detrimental effects of cancer-associated malnutrition and sarcopenia have been well-documented in patients with OPSCC[13, 14], but most of the available data are in patients with OPSCC associated with tobacco and alcohol consumption (i.e. HPV-ive). We studied nutrition status and body composition in OPSCC to determine if these features are distinctly different between HPV + ive and -ive subsets. Patients from two different geographical areas (Canada and Spain) showed no significant regional differences in BMI, % of weight loss, WLG, SMI and TATI or in the prevalence of Class I and Class II skeletal muscle depletion. These similarities justified pooling the data, allowing us to confirm a distinctive nutritional profile of HPV + ive and -ive patients with OPSCC at time of diagnosis. Overall, HPV + ive patients had little nutritional risk with low-grade weight loss, high BMI and total fat index and had SMI values in the normal range, whereas HPV-ive patients had high nutritional risk characterized by high grade weight loss, normal-underweight BMI and moderate-severe SMI depletion. Despite these considerable differences according to HPV status, a discrete subset of HPV + ive patients exhibited characteristics that were more akin to those in the HPV-ive group (Grade 3/4 weight loss and Class I/II muscle depletion). Likewise, a subset of HPV-ive patients had a weight loss of Grade 0 and normal SMI. These findings point out the high heterogeneity within HPV + ive and HPV-ive groups, despite the polarity of the overall differences between the groups. Distinctive nutritional features exist in patients according to HPV status, but heterogeneity of individual nutritional profiles invites an individualized approach to nutrition care.

Our data align with previous suggestions that BMI was 3 to 5 kg/m² higher in HPV + ive patients [10, 11, 26]]. We additionally provide values for WLG, which considers weight loss in conjunction with BMI [12, 20]patients with HPV + ive OPSCC who had low-grade weight loss, if any. CT-based body composition measures in our study add depth to the nutritional assessment. With this approach, we confirm that HPV + ive patients have a higher fat index and are more muscular than those with HPV-ive status. We ranked the patients’ SMI values using the recently derived categorical scale for normal muscle mass, Class I SMI depletion and Class II SMI depletion in patients with cancers of the head and neck [20]. By these criteria, 85% of HPV + ive patients had SMI in the normal range, whereas HPV-ive status was associated with higher prevalence of Class I/II SMI depletion. Skeletal muscle depletion should be investigated due to well-established impact on clinical outcomes in patients with OPSCC [14]. Evaluation of skeletal muscle depletion at diagnosis offers clinicians the opportunity to consider the best course of nutritional management. Class I or Class II muscle depletion could be lurking in some individuals.

Nutritional features are strongly associated with overall survival in patients with multiples cancers including those of the head and neck, with survival benefit associated with higher BMI, lower weight loss grade, and normal SMI values [19, 20]. However, OPSCC specifically, studies evaluating depleted skeletal muscle mass (SMM) according to HPV status have been scarce. Our combined cohort allowed us to begin to understand the intersection between the prognostic value of nutritional features, and the fact that positive HPV status is associated with survival benefit, compared to HPV-ive status [6]. Our survival analysis was used to test the possibility that the survival benefit of HPV + ive status might in part be attributable to the superior nutritional status of this patient subgroup. This was not confirmed, as in multivariable analysis adjusted for weight loss and SMI did not significantly modify the association between HPV status and mortality.

A strength of this study is the data aggregation across 2 cohorts. A homogenous approach was applied when assessing weight loss grading and body composition analysis to better characterize these patients and to increase the generalizability of the obtained results. Comparing and combining international datasets has proven a useful paradigm for a better understanding of nutritional features of patients, and further development of international OPSCC datasets would be merited. This study has some limitations. Patients of female sex are limited in number, as OPSCC typically affects more males. Several assessments differed between the Spanish and Canadian cohorts. HPV status in the Canadian cohort was based on p16 immunohistochemistry, whereas in the Spanish cohort double positivity for p16 and HPV DNA was used to confirm the cases. While uniform assessments were sought, the symptom assessments applied across the two cohorts were not comparable; as such, we could only compare the symptoms within each cohort. Other factors, such as smoking and alcohol use may impact the nutritional status of patients, but this information was not available for all patients.

Our results suggest that OPSCC patients in Canada and Spain can be comparable from a nutritional perspective despite variations in their histopathological, clinical, and regional differences, confirming the trends suggested in previous research. Moreover, the study underscores the need of individualized nutrition assessment including WLG, muscle mass and symptoms of patients regardless of HPV status to understand their specific risk of nutritional depletion prior to treatment start. To gain deeper insights into the dynamics of nutritional features according to HPV status in OPSCC patients during cancer treatment and follow-up, prospective studies with large representative samples and standardized nutritional assessments should be designed.

Data availability statement

The data that support the findings of this study are available on request from both corresponding authors, LA and VB. The data are not publicly available due to restrictions related to the participant’s privacy.

Acknowledgements

We would like to express our sincere gratitude to all the patients for their participation in this project. We wish to thank all the members of the research team who contributed to the successful completion of this study. Their technical assistance, critical advice and dedication have been instrumental in the accomplishment of our research objectives.

Author contribution statement

The authors confirm contribution to the paper as follows: study conception and design: VB, RM, LA, MC, CK; data collection: MC, CK, LA, VB; analysis and interpretation of results: MC, CK, VB.; draft manuscript preparation: MC, CK, VB, LA. All authors reviewed the results and approved the final version of the manuscript.

Funding

The authors did not receive financial support from any organization for the present work.

Ethical approval

The present study was developed according to the Declaration of Helsinki and have the ethical approval from the institutional research ethics boards from both countries. For Spain was the Hospital Universitari de Bellvitge Ethics Committee for Clinical Research with the protocol number PR138/19. And for Canada, the Health Research Ethics Board of Alberta – Cancer with the protocol number CC_17-0433. An informed consent was obtained from all patients included in the analysis.

Competing interests

The authors declare that they have no conflict of interest.

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Tables 1 to 4 are available in the Supplementary Files section

There is NO conflict of interest to disclose.

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You are reading this latest preprint version

Nutritional characterization of patients with oropharyngeal cancers: Impact of human papillomavirus status

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Version 1

Abstract

Figures

Introduction

Subjects and Methods

Study Design and Participants

Clinical data

Computed tomography (CT) Analysis

Statistical Analysis

Results

Baseline Characteristics from Canadian and Spanish cohorts

Baseline characteristics from pooled data

Survival analysis

Discussion

Conclusions

Declarations

References

Table

Additional Declarations

Supplementary Files

Status:

Version 1