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Reporting summary
Further information on research design is available in the 
PMC10011554
Supplementary information
Supplementary InformationReporting Summary
PMC10011554
Supplementary information
The online version contains supplementary material available at 10.1038/s41467-023-36976-1.
PMC10011554
Acknowledgements
The authors thank the patients and their families who made this study possible and the clinical study teams who participated in the study. The authors also thank Olga Ferrero, the primary research nurse for the study, and Esther Chan for assistance with pharmacodynamic analyses. This study was sponsored by Celgene, a Bristol Myers Squibb Company. The study sponsor was involved in the study design, analysis of data, and writing the manuscript. Medical writing and editorial assistance were provided by Bernard Kerr, PGDipSci, and Agata Shodeke, of Spark, funded by Bristol Myers Squibb.
PMC10011554
Author contributions
RECRUITMENT
R.S., B.A., X.W., Z.N., V.M., and I.B. contributed to the study design. V.M., M.V., J.M.S., V.G., T.H.-G., B.D., O.S., C.C.-S., J.-M.M., A.I., M.M., C.C., A.P., and I.B. contributed to patient recruitment. B.H. contributed to PK data analysis and interpretation. I.A. and E.F. contributed to
PMC10011554
Peer review
PMC10011554
Data availability
Anonymized participant-level data cannot be shared due to an increased risk of patient reidentification. Bristol Myers Squibb will consider requests to share anonymized clinical trial data from interventional trials in patients that have completed on or after January 1, 2008. In addition, primary results from these trials must have been published in peer-reviewed journals and the medicines or indications approved in the United States, EU, and other designated markets. Requests to access clinical trial data will be considered case by case and may be submitted to Celgene, a Bristol Myers Squibb Company, using the inquiry form at
PMC10011554
Competing interests
ONCOLOGY, EMD
V.M. has received consulting fees from Bristol Myers Squibb, Basilea, Bayer, Janssen, Nanobiotix, Pieris Pharmaceuticals, Regeneron/Sanofi, and Roche, and honoraria from Bristol Myers Squibb and Bayer. M.V. has received personal fees from Roche, EMD Serono, and TFS. J.M.S. has received personal fees and non-financial support from Celgene (a Bristol Myers Squibb Company), AbbVie, and Astellas, non-financial support from Ipsen, and research grants from Pfizer and IDP Pharma. J.-M.M. has received research grants from Bristol Myers Squibb, AstraZeneca, Boehringer Ingelheim, GSK, INCA, Janssen Cilag, Merck, Novartis, Pfizer, Roche, and Sanofi, non-financial support from Bristol Myers Squibb, AstraZeneca, Bayer, Boehringer Ingelheim, GSK, MedImmune, Merck, NH TherAguix, Pfizer, and Roche, and other support from Bristol Myers Squibb, AstraZeneca, Boehringer Ingelheim, Eli Lilly Oncology, F. Hoffmann-La Roche Ltd, Merck, Merck Sharp & Dohme, Pfizer, and Regeneron. A.I. has received consulting fees from Epizyme, Lilly, Merck Sharp & Dohme, Novartis, Pharmamar, and Roche, and received research grants from Bristol Myers Squibb, AstraZeneca, Bayer, Chugai, Merck Sharp & Dohme, Novartis, Pharmamar, Pfizer, and Roche. M.M. has received honoraria from AstraZeneca and Sanofi. C.C. has received consulting fees for acting in an advisory role from Bristol Myers Squibb, Regeneron, Novartis, and Takeda. A.P. has received honoraria from Bristol Myers Squibb, F. Hoffmann-La Roche Ltd, Helsinn Healthcare, Janssen, Celgene, Gilead Sciences, Incyte, Servier, Merck Sharp & Dohme, and Takeda. I.B. has received personal fees from Bristol Myers Squibb, AstraZeneca, Merck Serono, Merck Sharp & Dohme, Orion Pharma, Rakuten Aspyrian, Roche, and research funding from Bristol Myers Squibb, AstraZeneca, Merck Serono, Merck Sharp & Dohme, Orion Pharma, Rakuten Aspyrian, Roche, Celgene, GlaxoSmithKline, Incyte, Janssen, Kura, Novartis, Pfizer, Shattuck Labs, and VCN Biosciences. V.G., T.H.-G., B.D., O.S., and C.C.-S. have no conflicts of interest to disclose. R.S., B.A., and Z.N. are employed by the Centre for Innovation and Translational Research Europe, a Bristol Myers Squibb Company. E.F., B.H., and X.W. are employed by Bristol Myers Squibb. B.H., E.F., R.S., X.W., and Z.N. hold Bristol Myers Squibb stock. I.A. was employed by Bristol Myers Squibb at the time of the study.
PMC10011554
References
PMC10011554
Methods
PMC9979657
Study Design
We used a randomized, double-blind, placebo-controlled cross-over design (
PMC9979657
Randomization
We randomly assigned participants to travel in one of two minivans on each study day. One vehicle was randomly selected to employ cabin air filtration using an electrostatic air filter while the other had a placebo air filter (i.e., unfiltered air). Following a 1-week washout period participants “crossed over” to the other air supply condition, traveling along the same driving route. Thus, each participant was exposed once to filtered air and once to unfiltered air over two visits. Drivers and study participants were blinded to air supply conditions (filtered or unfiltered) during all commutes. Participants traveled in the same vehicle and sat in the same seat during each trip. Up to three participants rode in the vehicle, and participants were asked to rest quietly and not to engage in discussion during the exposure route. Vehicle ventilation settings were the same for all trips: medium airflow, recirculation off, dashboard vent, and temperature set to 22 °C. Minivans were used to fit multiple participants comfortably and to accommodate the exposure equipment.
PMC9979657
Air Filter Selection
Commercially available electrostatic cabin air filters designed to fit Chrysler and Dodge branded minivans were used in this study. These filters were selected based on pilot testing conducted in an Environment and Climate Change Canada laboratory prior to starting the field study, as described in a separate publication.
PMC9979657
Study Population
cardiac or cognitive conditions on the study
ASTHMA
Study participants (Healthy young participants were recruited to minimize impacts of pre-existing cardiac or cognitive conditions on the study results. Our interest was in acute subclinical impacts. Pregnant women, subjects with self-reported respiratory (other than asthma) or cardiovascular illnesses, and people with pacemakers were excluded from the study. Our sample size was limited by the breadth of health measurements collected, and the laboratory’s resources to carry out the measurements. This may have impacted our statistical power. The study was approved by the Health Canada Research Ethics Board and is registered with
PMC9979657
Health Outcomes
PMC9979657
Heart Rate Variability
HEART
Heart rate variability (HRV) was monitored before, during, and after the commute using an ambulatory ECG (Holter) monitor (GE Seer Light or SEER Light Extend recorders). Measures of HRV were calculated as outlined by the Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, and both time (standard deviation of normal-to-normal intervals [SDNN]; root mean square of the successive differences [RMSSD]); and frequency domain measures of HRV (low-frequency spectral power [LF]; high-frequency spectral power [HF]).
PMC9979657
Saliva Cortisol
Salivary cortisol was measured before, during, and after the commute on each study day (10 min prior to the commute; 45 min into the commute; 10 min postcommute; and 80 min postcommute). The timing of measurements was consistent across days for each participant to control for diurnal patterns. Participants could not eat, drink, or chew gum for 30 min before giving a saliva sample or ingesting a large meal less than 1 h before the saliva sample. Samples were collected using Salivette swabs (Nümbrecht, Germany). Participants rolled the swab in their mouths for 60 s and returned the swab to the Salivette tube. Samples were kept on ice during transport and stored at −20 °C. The saliva was analyzed with a high-sensitivity enzyme-linked immunosorbent assay kit from Salimetrics (State College, PA), and all samples were analyzed in duplicate, with the average of the duplicates used for statistical analyses.
PMC9979657
Cognitive Function
RTI
The CANTAB testing battery is a cognitive assessment system administered by touch screen. Participants were introduced to the CANTAB tasks during an introductory visit before the study commenced to minimize any learning effects. The CANTAB battery was administered on each study day before and after the commute and included four “tasks” focusing on different cognitive domains and functional areas.The Attention Switching Task (AST) indicates the costs of multitasking, showing cognitive flexibility, and is indicative of executive function. For this test, an arrow is shown pointing left or right and is displayed on the left or right side of the screen. Participants are asked to indicate either the side of the screen on which the arrow appears or its direction. Sometimes, the arrow’s side and direction are incongruent, whereas sometimes they agree. Longer reaction times for incongruent stimuli are an indication of a Stroop effect (automatic processing being faster than conscious visual control) or The Reaction Time (RTI) task measures reaction and moving times under simple and 5-choice scenarios. For this task, the subject holds down a button until a spot is shown on the monitor, at which point they move their finger to touch the spot with the same finger. The spot can appear either in a single location (Simple) or in one of five locations (5-choice).The Rapid Visual Processing (RVP) task measures continuous performance as well as visual sustained attention. For this task, 100 single digits per minute appear in the center of a screen, and the subject must indicate when they see specific number sequences by pressing a button. The outcome measure The Spatial Working Memory (SWM) task measures subjects’ capacity to retain and process spatial information. For this, subjects search for blue squares by touching larger squares covering them, without revisiting boxes where a blue square was previously uncovered.
PMC9979657
Exposure Assessment
The following air pollutants were simultaneously monitored inside the vehicle and outside the vehicle using instruments mounted on the roof-top: UFPs, PM
PMC9979657
Statistical Analysis
REGRESSION
Linear regression models were used to estimate the impact of air filter use (as a dichotomous variable) on in-vehicle pollutant concentrations, adjusting for concurrent rooftop concentrations. Linear mixed models with random intercepts for subject were used for all health analyses to account for repeated measurements within subjects; pollutant coefficients were scaled to reflect interquartile range (IQR) increases in pollutant levels (BC = 1818 ng/m
PMC9979657
Results
PMC9979657
Impact of Cabin Air Filter on In-Vehicle Exposures
In-vehicle and rooftop pollutant concentrations were measured during 48 vehicle commutes over 24 weekdays in October and November 2015 (mean duration 94 [SD 10] min) (
PMC9979657
Mean In-Vehicle Environmental Conditions with and without a Cabin Air Filter
Adjusted for outdoor-rooftop measurement, except CORegardless of the presence of a cabin air filter, concentrations of UFPs, PMParticulate concentrations increased considerably when passing through vehicle tunnels.
PMC9979657
Study Population
Mean BMI and baseline systolic and diastolic blood pressure measurements in our participants (53% female; mean age 26 (range 29–49) years) are indicative of a population in good health (
PMC9979657
Saliva Cortisol
After 45 min in-vehicle, IQR increases in UFPs associated with 18% increases to cortisol levels in women, whereas in men, PM
PMC9979657
Percent Change in Saliva Cortisol per IQR Increase in Pollutant or Filter Presence
In-vehicle exposures preceding saliva collection used for PM2.5, UFP, and BC analyses.Adjusted for baseline cortisol measurement, sickness reported in the past week, and indoor temperature. Percent changes in saliva cortisol are per IQR change in pollutant: PM
PMC9979657
Cognitive Function
decrements to neurocognitive function
In-vehicle exposures were associated with decrements to neurocognitive function, most frequently for BC (
PMC9979657
Percentage Change in Neurocognitive Outcome Score per IQR Increase in Pollutants or by Filter Presence
RTI
AST = attention switching task; RTI = reaction time; RVP = rapid visual processing; SWM = spatial working memory. Adjusted for sickness reported in the past week and indoor temperature. Statistically significant results in bold (On the rapid visual processing task, BC was associated with small decreases in A’ prime, indicating lower sensitivity to the target sequences. Similarly, spatial working memory was diminished, as evidenced by increased In general, filter presence itself was not associated with changes to neurocognitive outcomes. We did not examine sex-related differences in cognitive function outcomes due to ethical considerations.
PMC9979657
Discussion
PMC9979657
Exposure
Although Canadians and Americans only spend an average of five to six percent of their time in vehicles,Because of considerable daily variability in TRAP concentrations during the study, filter presence itself was not a perfect indicator of in-vehicle pollutant exposure; indeed, some participants were exposed to higher in-vehicle pollutant concentrations during the filtered exposure because of substantially higher outdoor pollutant concentrations on the “filtered” study day. As a result, the in-vehicle pollutant measurements were more appropriate for use in health analyses, owing to less exposure misclassification.While this study only looked at the benefit of cabin air filtration when using “outdoor air” mode, using “recirculation” mode can also reduce in-vehicle exposures to pollutants from outside the vehicle, particularly when a cabin air filter is in place. However, using the recirculation mode for extended periods of time may lead to elevated concentrations of other contaminants, including COIn-vehicle TRAP exposures may affect commuters’ cardiovascular and stress responses and affect cognitive function. We demonstrated the effectiveness of cabin air filtration at reducing in-vehicle pollution exposures. Cabin air filtration using regularly maintained, best-available technologies may reduce in-vehicle exposures and protect health.
PMC9979657
Heart Rate Variability
HEART
Heart rate variability is used to evaluate the health and balance of the autonomic nervous system, with both increased and decreased HRV identified as risk factors for cardiac mortality.
PMC9979657
Saliva Cortisol
Saliva cortisol is a noninvasive indicator of active free cortisol, a glucocorticoid used as a biomarker of stress, and HPA axis activation.Our study found that common TRAP pollutant exposures were associated with marked changes to saliva cortisol, indicating that commuter exposures may impact acute stress responses, particularly during the period of exposure, with effects subsiding shortly after the exposure is reduced. In the present study, cortisol increased in women in relation to some TRAP constituents, while men showed a significant decline for several other TRAP constituents. Given the time of the commute (morning), we would expect to see either constant or declining cortisol levels in all participants across the period of the commute, due to the decline following the cortisol awakening response (CAR),
PMC9979657
Cognitive Function
Alzheimer’s disease, dementia, cognitive impairment
Air pollution exposure may reduce cognitive function, with associated effects ranging from mild cognitive impairment to Alzheimer’s disease and dementia.
PMC9979657
Strengths and Limitations
Strengths of this study include the use of a double-blind cross-over design where neither the study participants nor the study staff (apart from the lead investigator responsible for installing filters in the vehicles) were aware of which vehicle had the cabin air filter in place on a given day. As a cross-over study, participants acted as their own control in the two filter conditions, reducing variability and confounding from time in-varying factors. As with all interventional studies in humans, the sample size was limited by what was feasible, reducing the power of the study, although this was offset by the statistically efficient cross-over design. We did not adjust for multiple comparisons in our analysis but focused on the size and direction of the effect, along with the 95% confidence intervals. This may have increased the type I error rate.
PMC9979657
Supporting Information Available
The Supporting Information is available free of charge at Cross-over study design; driving route in Montreal, QC; in-vehicle, rooftop, and ambient environmental conditions during filtered and unfiltered periods; effect of air filtration on indoor–outdoor ratios of measured air pollutants and descriptive statistics; time series of in-vehicle PM2.5, black carbon, and UFPs for a typical daily drive; population characteristics; percent change in frequency domain HRV per IQR change in pollutant at the end of the ride, 45′ post, and 90′ postexposure; percent change in time domain HRV per IQR change in pollutants at the end of the ride, 45′ post, and 90′ post exposure per IQR change in in-vehicle pollutant exposure; percent changes in HRV associated with the cabin air filter; baseline scores on the CANTAB neurocognitive test battery; and schedule of participant activities during the day of study visit (
PMC9979657
Supplementary Material
es2c06556_si_001.pdfThe authors declare no competing financial interest.
PMC9979657
Acknowledgments
This study was funded by Health Canada.
PMC9979657
References
PMC9979657
Introduction
xerostomia, HNC, head and neck cancer
ADVERSE EFFECTS, SECONDARY, XEROSTOMIA, HEAD AND NECK CANCER
Radiotherapy-induced xerostomia (RIX) is one of the most common adverse effects of radiotherapy (RT) in head and neck cancer patients (HNC) and a major determinant of survivors’ quality of life. The primary objective was to evaluate the reduction of patients’ xerostomia symptoms after the utilisation of a sodium-hyaluronate mouthwash compared to a placebo solution. The secondary objectives were to evaluate the improvement of quality of life and to evaluate the patients’ satisfaction.
PMC10584731
Methods
The protocol was approved by the ethical committee (Ref. 50,053/19) and registered at ClinicalTrials.gov (ID: NCT05103124). The study was a double-blind randomised clinical trial (RCT) with a crossover design and was conducted at the Fondazione Policlinico Universitario A. Gemelli, Rome.
PMC10584731
Results
Xerostomia
XEROSTOMIA
Thirty-two patients completed the study protocol. Lower values of the modified Xerostomia Questionnaire (XQ) were retrieved when comparing the baseline scores to the ones after the treatment, when compared with placebo (Mann–Whitney
PMC10584731
Conclusions
ADVERSE EVENTS
This RCT highlights the advantages of treating RIX with the sodium-hyaluronate mouthwash since it seems to be clinically effective in reducing its symptoms, without any reported adverse events.ClinicalTrials.gov: NCT05103124 in 17/10/2021.
PMC10584731
Supplementary Information
The online version contains supplementary material available at 10.1007/s00520-023-08090-x.
PMC10584731
Keywords
DEL
Open access funding provided by Università Cattolica del Sacro Cuore within the CRUI-CARE Agreement.
PMC10584731
Introduction
xerostomia, Head and neck cancers, Xerostomia, HNC, Cancer
XEROSTOMIA, XEROSTOMIA, ADVERSE EFFECTS, SECONDARY, HEAD AND NECK CANCER, CANCER
Head and neck cancers (HNC) have a reported incidence of more than 900,000 new cases per year [RT-induced xerostomia (RIX) is one of the most common adverse effects of RT in patients with HNC and a major determinant of survivors’ quality of life (QoL) [The above-mentioned agent has already been tested in retrospective and prospective clinical trials [The primary objective of this RCT was to evaluate the reduction of patients’ xerostomia symptoms due to RT through a modified version of the Xerostomia Questionnaire (XQ) [The secondary objectives of this study were (1) to evaluate the improvement in QoL, evaluated through the European Organisation for Research and Treatment of Cancer (EORTC) QLQ-C30 and QLQ-H&N35 questionnaires [
PMC10584731
Materials and methods
DEL
The protocol was approved by the ethics committee of the ‘Università Cattolica del Sacro Cuore’ (Ref. 50,053/19) and is registered at ClinicalTrials.gov (ID: NCT05103124). This study has been reported according to the CONSORT guidelines (Supplementary files,
PMC10584731
Trial design
The present study was conducted as a double-blind RCT with a crossover design; thus, the whole population received both the sodium-hyaluronate mouthwash and placebo.
PMC10584731
Participants
xerostomia, Tumour, HNC, psychiatric, Sjogren’s syndrome
XEROSTOMIA, TUMOUR
Patients with HNC who visited the Oral Medicine, Head and Neck Department – Fondazione Policlinico Universitario A. Gemelli—IRCSS between October 2020 and March 2022 were screened for inclusion. Patients were assessed during their routine follow-up within the context of the multidisciplinary Tumour Board.The following inclusion criteria were applied:Patients older than 18 years.Patients diagnosed with HNC who had received local RT involving the salivary glands at least 3 months before the beginning of the study both for curative and palliative purposes, with or without chemotherapy, reporting xerostomia symptoms.Patients diagnosed with HNC who had received local RT as an adjuvant to surgical resection at least 3 months before the beginning of the study, with or without chemotherapy, reporting xerostomia symptoms.The exclusion criteria were as follows:Patients with documented contraindications to any of the components of sodium-hyaluronate mouthwash (including excipients).Patients with neurological and psychiatric conditions influencing their ability to self-apply the treatment.Patients unwilling to complete the request diary card.Patients unable to attend the ambulatory visits scheduled by the protocol.Patients participating in other clinical studies.Patients who had received antitumour treatment during the previous 3 months.Patients with concomitant Sjogren’s syndrome.Other causes of xerostomia (i.e. pharmacological treatment).
PMC10584731
Interventions
xerostomia
XEROSTOMIA
A baseline visit (T0) was conducted 3 months after the end of RT. Demographic data and a thorough medical history were recorded with particular attention to oncologic history (i.e. chemotherapy, oncologic surgery, and RT dose) and smoking habits.The basal and stimulated salivary flow rates were measured, and patients were asked to complete the questionnaires to assess their xerostomia grade. The unstimulated salivary flow rate was assessed using the spitting method. Patients were instructed to collect their saliva for 5 min in a graded tube. The stimulated salivary flow was determined in a similar manner. Salivary secretion was stimulated by applying a solution of 2% citric acid to the sides of the tongue at intervals of 30 s [The investigational product sodium-hyaluronate mouthwash (HydralThe patients were divided into two groups: on day 1 (baseline—T0), after the questionnaires were answered, group A received the treatment product and group B received the placebo. On day 30, the administration of the products was stopped, and the questionnaires were administered together with the Likert scale. Following this, a 30-day washout phase was conducted, followed by Phase 2 of the study. On day 61, patients completed the questionnaires again, and each group was treated with the alternative product. On day 90, the final questionnaires were administered, and all endpoints were investigated. Each visit is described in the study flowchart (Fig. Consort flow diagram of the trial
PMC10584731
Outcome measures
xerostomia
HYPOSALIVATION, XEROSTOMIA
The primary objective of this RCT was to evaluate the reduction in patients’ xerostomia symptoms due to RT in contrast to hyposalivation, which can be objectively evaluated using sialometry. The measurement of xerostomia is problematic because it comprises a set of symptoms, and therefore can be assessed only by directly questioning individuals. The following questionnaires were used in this RCT: a modified version of the XQ [
PMC10584731
Randomisation sequence, allocation concealment, and blinding
The statistician and principal investigator (C.L.) generated the allocation sequence using a simple computer-generated random list. Allocation concealment was performed using sequentially numbered opaque sealed envelopes (SNOSE) [
PMC10584731
Sample size and statistical methods
cancer, xerostomia
REGRESSION, CANCER, XEROSTOMIA
Assuming that sodium-hyaluronate mouthwash can cause a 20% reduction in the XQ scores when compared with the placebo, setting a bilateral 95% confidence interval and a study power of 80% in a crossover design, a minimum sample of 32 is required. Assuming a dropout rate of 20%, a sample size of 40 patients was required. The calculation was carried out using PASS2021 software. Such a high dropout rate was decided because of the particularly fragile nature of HNC patients and difficulty in predicting the course of cancer therapy in these patients.The clinical and demographic characteristics of the sample were described by applying descriptive statistical techniques. Qualitative variables are described using absolute and percentage frequencies, while quantitative variables are summarised either as mean and standard deviation (SD) when normally distributed or as median and interquartile range (IQR) when non-normally distributed. The intraclass correlation coefficient (ICC) test was used to determine the reliability between patients for each questionnaire at each time point. The ICC test was based on each question and the overall score. A coefficient major of 0.7 was considered reliable.The normality of quantitative variables was assessed using the Shapiro–Wilk test. Differences between groups for quantitative variables were assessed by the Mann–Whitney If any of the variables were associated with a reduction in xerostomia in univariate analysis, it was entered into a multivariate logistic regression model by inserting the therapy as a covariate and the XQ scores as outcome variables.Statistical significance was set at
PMC10584731
Results
PMC10584731
Participant flow and recruitment
GROUP B
The patients participating in this study were recruited between October 2020 and March 2022; the last follow-up consultation was conducted 3 months later, in June 2022. Thirty-nine patients were recruited. Of these, seven patients dropped out during the treatment because of cancer recurrence and the need for chemotherapy (four from Group A and three from Group B). The results of the remaining 32 patients were used for statistical analysis. Further details regarding the study course are shown in Fig. 
PMC10584731
Baseline data and numbers analysed
GROUP B
The final sample included 32 patients (13 women and 19 men), with a mean age of 54.6 years (SD: 10.7; range: 24–72). The general patient characteristics are shown in Table General characteristics of the included sample. No statistically significant differences were found between the groupsThe main results, as well as the scores recorded after the 1-month washout, were as follows: in Group A, the modified XQ score was 70.1 (SD: 25.7; range: 15.4–100) at baseline and 63.2 (SD: 24.3; range: 15.4–96.8) after the washout phase; for Group B patients, the modified XQ score was 58 (SD: 21.2; range:20.9–81.4) at baseline and 59.9 (SD: 21; range: 16.5–90.2) after the washout phase.No statistically significant difference was found between any of the analysed variables (total and divided according to the different categories) or between the groups at different time points. Consequently, the baseline scores were grouped together with the scores after the washout phase, and then the statistical analyses were stratified according to the administered product.To establish the reliability of patients’ answers to the questionnaires, an ICC analysis was performed between baseline questionnaires (before the beginning of Phase 1) and the questionnaires at the beginning of Phase 2, matching the answers for each patient to the same questions: ICC measured at baseline was 0.834, while that measured after the washout period was 0.866.
PMC10584731
Discussion
dysphagia, xerostomia, caries, hyposalivation, dysgeusia, trismus
DYSPHAGIA, XEROSTOMIA, ADVERSE EVENTS, FUNGAL INFECTIONS, CARIES, HYPOSALIVATION, OSTEORADIONECROSIS, CAVITY, TRISMUS
RT may cause significant adverse events in the oral cavity of patients with HNC (i.e. osteoradionecrosis, dysphagia, dysgeusia, caries, and trismus) [No differences were found in the other variables. Probably, RT has a significant damaging effect on the salivary glands, making the effect of smoking negligible. The same explanation could be provided regarding previous oncologic therapies (chemotherapy and surgery), which did not show any influence on xerostomia symptoms, confirming how RIX is mainly or totally due to RT damage to the salivary glands. Finally, this study did not highlight any differences in patient age. The incidence of xerostomia is usually higher in older patients because they show several comorbidities and undergo pharmacological therapies, which usually lead to hyposalivation and xerostomia [Another limitation of this study is that we only enrolled 32 patients. Although the crossover design has virtually allowed for doubling the sample size, further trials, with more patients, are needed to increase the generalisability of our results.In conclusion, the product has shown a promising effect in reducing the discomfort associated with RIX, but other potential effects, such as its role in preventing caries and modifying the oral microbiota by reducing the risk of fungal infections, are yet to be determined in further trials.
PMC10584731
Conclusions
ADVERSE EVENTS
The results of this double-blind RCT highlight the advantages of treating RIX with sodium-hyaluronate mouthwash, as it seems to be clinically effective in offering relief of RIX symptoms in the majority of the patients, without any reported adverse events.
PMC10584731
Author contribution
Conceptualisation, C.R. and C.L.; methodology, C.L.; software, C.R.; validation, R.P., A.L., F.M., and M.M.; formal analysis, C.L.; investigation, A.B., C.R., and G.G.; resources, C.L.; data curation, C.L.; writing—original draft preparation, C.R.; writing—review and editing, C.L.; visualization, R.P.; supervision, A.L.; project administration, C.L.; funding acquisition, C.L. All authors have read and agreed to the published version of the manuscript.
PMC10584731
Funding
DEL
Open access funding provided by Università Cattolica del Sacro Cuore within the CRUI-CARE Agreement. This research was funded by Sunstar Europe S.A., Route de Pallatex 11, P.O. Box 32, 1163 Etoy, Switzerland (prot. CA-19–0888).
PMC10584731
Data Availability
Data are available upon request to the authors.
PMC10584731
Declarations
PMC10584731
Conflict of interest
This research was funded by Sunstar Europe S.A., Route de Pallatex 11, P.O. Box 32, 1163 Etoy, Switzerland. (prot. CA-19-0888). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
PMC10584731
Ethics approval and consent to participate
DEL
The protocol was approved by the ethics committee of the ‘Università Cattolica del Sacro Cuore’ (Ref. 50053/19) and is registered at ClinicalTrials.gov (ID: NCT05103124). The informed consent was carried out in line with the Declaration of Helsinki and was obtained from all subjects involved in the study. Written informed consent approved by the ethics committee (Ref. 50053/19) has been obtained from the patients to publish this paper.
PMC10584731
References
PMC10584731
Introduction
anxiety, coronavirus infectious disease, infection, depression, humor
INFECTION
The emergence of the novel coronavirus infectious disease (COVID-19) has put the health and life quality of the global populace at risk. The fear of infection, coupled with prolonged isolation because of quarantine restrictions and social distancing mandates led to a range of detrimental outcomes, including financial instability [In these challenging times, the female gender has been identified as more susceptible to mental health issues, as many COVID-19 stressors were related with their reproductive functioning [In South Korea, the burden of child-care caused by school closures and a reduction in child-care services increased significantly during the pandemic; however, while paternal responsibility increased from 3.6% to 7.5%, maternal responsibility increased more substantially, from 29.2% to 36.8% [However, delivering interventions to alleviate psychological stress during the pandemic proved challenging because of the strict social distancing measures implemented in most countries. Nevertheless, owing to the pressing need for strategies to address mental health emergencies, several web-based psychotherapeutic interventions were developed for vulnerable populations to use while maintaining social distancing. This population included COVID-19 patients [Laughter is believed to be more than a mere response to humor; it holds potential benefits for both physiological and psychological functions. These benefits include decreased stress hormones; enhanced immune system function; reduced perceived stress, anxiety, and depression; and improved self-esteem, cognitive functions, and quality of life [Traditionally, LT has been conducted through face-to-face interactions. However, the current pandemic has prompted the introduction of non-face-to-face LT, facilitated via online platforms. Given its advantages of being non-pharmacological and more readily acceptable to various populations compared to other psychotherapies [However, during the pandemic, the application of LT has been primarily limited to specific populations, particularly nursing students [In this study, we developed and implemented a distance laughter therapy (DLT) program targeting mothers with young children during the pandemic, facilitated via Zoom (H1-1: DLT will decrease depression levels in the experimental group post-intervention.H1-2: Compared to those in the control group, the depression levels in the experimental group will decrease post-intervention.H2-1: DLT will decrease the anxiety levels in the experimental group post-intervention.H2-2: Compared to those in the control group, the anxiety levels in the experimental group will decrease post-intervention.H3-1: DLT will decrease parenting stress levels in the experimental group post-intervention.H3-2: Compared to those in the control group, the parenting stress levels in the experimental group will decrease post-intervention.
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Method
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Participants
This study was a mixed method, parallel, pilot randomized controlled trial (RCT) aiming to examine the feasibility and effectiveness of DLT among women with young children aged under 6 years. Participants’ inclusion criteria were as follows: women who 1) had at least one child under 6 years; 2) had no acute mental health crisis that needed emergency intervention and had not taken psychotropic medications within the past 3 months; 3) could use Zoom at home; and 4) faced difficulties while caring for their children at home during the pandemic. To recruit the participants, web-flyers advertising this study were uploaded on online platforms, including the researchers’ social network services and boards of regional community networks.Each group had approximately 10 to 11 participants. This number was not optimized for between-group comparisons, as achieving 80% power (effect size = .5, α = .05) to detect differences between two independent groups requires a minimum sample size of 51 per group. However, because of the logistical challenges in managing larger groups in a Zoom-based intervention and considering the importance of participant interaction within our program, we opted for a smaller sample size. Eventually, 22 participants were recruited. Participants voluntarily provided written informed consent via email; thereafter, the online baseline survey was conducted.
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Contents of the distance laughter therapy.
HuLA
Opening (Self introduction and greetings)Facial stretching and raising mouth cornerExpressing oneself with laughter “This is me” (1Reinforcing the positivity with laughter “I thank to…” (2Increasing self-esteem with laughter “I like me because…” (3Complimenting each other with laughter “Yes, I hear that a lot” (4Relaxing and sharing the emotionSaying good-byeThe DLT employed in this study had several distinct features. First, we instructed all participants to adjust their Zoom settings to display all attendees, including the therapist, on a single screen. They were also required to keep their cameras on and show their faces throughout the session, enabling them to see their own and others’ faces during the program.Second, we employed a simulated laughter approach. Literature on laughter therapy frequently differentiates between “simulated” and “spontaneous” laughter [Finally, in our study, the DLT specifically targeted positive, humor-free laughter, in line with the Humour-Laughter-Affect (HuLA) model [The DLT in this study comprised four sessions; it was performed twice per week for two weeks. It was based on previous meta-analysis [
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Conditions for control group
The control group was asked to watch a popular South Korean 50-minute entertainment TV show titled “Infinite Challenge” via their personal computers, while the experimental group participated in four sessions of group-based laughter therapy. The treatment provided to the control group was the same in length and frequency as the one provided to the experimental group; further, the treatment was delivered in the same condition: at home.
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Study procedure
RA
One research assistant (RA), who was not involved in this study, randomly divided the 22 participants into two groups: an experimental group (n = 11) and a control group (n = 11), using a research randomizer site (Before the intervention, the RA sent a URL to participants as well as the participation schedule (date and time). Using the URL sent, the experimental group accessed a Zoom classroom for LT and the control group accessed the TV show. After completing two-weeks of intervention, a post-test of the two groups was conducted online. Among the 22 participants, five were excluded: one participant had registered for this study but did not show up for the baseline survey, and four participants in the experimental group had withdrawn because of their busy schedules. No participant from the control group was excluded.After the intervention, the researchers asked participants in the experimental group to participate in an exit phone interview, and five participants volunteered. Using a semi-structured questionnaire, four questions were asked: 1) what was your participation experience in the four DLT sessions conducted through a virtual meeting?; 2) what did you feel about DLT, whether good or bad?; 3) what do you think about the program’s effects, if any, and why?; 4) do you perceive any changes after participating in this program, compared to before? Each interview lasted between 30 and 40 minutes. All interviews were audio-recorded and had verbatim transcription. The participants who completed the study were compensated with 17.33 USD (20,000 KRW), and those who participated in the exit interview were offered an additional 8.67 USD (10,000 KRW). The specific procedure is illustrated in
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Flow diagram of study procedure.
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Measurement
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Depression
depression, Depression
To assess the depression, the Korean version of the CES-D (Center of Epidemiologic Studies Depression Scale) was used [
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State/Trait anxiety
Anxiety, anxiety
State and trait anxiety was measured based on the Korean-version of the State-Trait Anxiety Inventory [
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Parental stress
Parental stress was assessed using Korean Parenting Stress Scale, a Korean cultural-specific tool developed by Kim and Kang [
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Data analysis
Quantitative data were analyzed using SPSS version 26. A Shapiro-Wilk test, which is recognized for its power in detecting non-normality in continuous data with a small sample size (n < 50), was performed [Qualitative data were analyzed using a conventional content analysis [
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Ethical consideration
The current research was conducted and reported by following the CONSORT 2010 [
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Results
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Demographic characteristics of participants
The mean age of the participants was 35.41 years old (SD: 4.67), and the average number of children was 1.64 (SD: .58). All participants were married, and the majority of them identified as non-religious (72.7%). Moreover, 54.5% were housewives and 31.8% reported that they were taking time off from their work at the time of the survey. Two participants had part-time jobs and one had a full-time job. Their perceived socioeconomic status (SES) varied from high to middle-low: more than half of the participants (59.1%) identified their SES as a middle, and none of them had low SES. On average, they spent 13.16 hours per day on childcare (SD: 5.19).
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Findings from the exit interview data
The themes and categories from the exit interview are listed in
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Themes and categories from the exit interview data.
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Perceived changes
depressive emotions
MUSCLE RELAXATION
After participating in DLT, participants reported numerous changes, encompassing physical, emotional, social, self-perception, and stress-coping domains. Under the physical changes category, two sub-categories, “feeling relaxed and energized” and “transition from awkward to natural smile,” emerged. Participants reported that the experiences from the program fostered a sense of bodily comfort and energy, and they observed muscle relaxation. Participant R2 described her experience, stating, Regarding emotional changes, two sub-categories, “simulated laughter evolving into genuine happiness” and “alleviation of depressive emotions through laughter,” emerged. Participants initially believed that laughter was solely a result of feeling happy, but they discovered that the act of laughing itself lifted their moods. Participant R3 shared, Regarding the social aspect, a single sub-category, “improved social relations,” emerged. Participants reported enhancements in their relationships, particularly with family members, after participating in DLT. For instance, participant R3 shared a joyful experience with her family using what she learned from the therapy: Numerous participants also reported shifts in their self-perception, falling into two sub-categories: “rediscovering lost smiles” and “boosting self-esteem through self-focus.” As they had primarily identified as mothers and wives for an extended period, the program enabled them to reconnect with their individual identities. Observing their smiles on screen, participants realized they had rediscovered their lost smiles. Participant R4 reflected, “Lastly, participants discussed their improved stress-coping abilities, encapsulated by two sub-categories: “managing stress through laughter” and “commitment to change and continued efforts.” When feeling overwhelmed, they applied the laughing techniques learned from the DLT, finding it effective in mitigating their stress. Participant R5 noted,
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Program feedbacks
Participants provided feedback on their experiences with DLT. One key aspect they discussed involved the advantages and drawbacks of the web-based distance approach. All participants expressed high satisfaction with this method because of its convenience and comfort—they appreciated not needing to dress up, arrange childcare, or commute. They particularly noted its appropriateness during the pandemic, when social gatherings were restricted. Participant R2 commented, The second feedback theme involved gratitude for the opportunity to interact with other mothers with young children. Given their shared experiences and challenges while caring for young children during the COVID-19 pandemic within Korean society, participants noted that they could easily establish rapport with like-minded individuals through shared understanding and empathy. Participant R3 remarked,
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Discussion
depression, ’ parental stress, anxiety, self-induced
DER, MUSCLE RELAXATION
We developed and applied DLT using a virtual meeting technology for mothers caring for their young children during the pandemic. We evaluated its impact on reducing levels of depression, anxiety, and parental stress and assessed its application feasibility. We found that parental stress levels during the pandemic were notably more severe compared to those in previous years. The mean score for mothers’ parental stress in this study was 3.30 and were higher than the scores reported by Korean mothers with young children in 2002 and 2007, which were 2.51 and 2.73 respectively, using the same scale [In this study, participants in the experimental group demonstrated a significant decrease in their depression and anxiety levels after completing the DLT. These findings align with Van der Wal and Kok [However, the degree of decrease in depression and anxiety levels did not differ significantly from that observed in the control group, who were exposed to an entertainment TV show. Therefore, hypotheses H1-2 and H2-2 were not supported. This might be attributed to the positive effects that the general TV entertainment show had on the participants’ depression and anxiety levels.Parental stress was significantly reduced in the experimental group post-intervention, contrasting with the control group where it remained relatively unchanged. As such, Hypothesis H3-1 is supported. This suggests that, unlike solitary TV viewing, simulated laughter and group interaction may help alleviate parenting-induced stress. However, since the degree of between-group difference did not reach statistical significance, our interpretation requires caution, and thus Hypothesis H3-2 is not supported.Considering our quantitative results, we cannot definitively claim that DLT is the superior choice for mothers, particularly given the effort and resources required for participation compared to simply watching TV. Indeed, a substantial number of participants (n = 5) withdrew from the experimental group because they were “busy,” while none withdrew from the control group. Nevertheless, owing to our small sample size, the quantitative findings should be interpreted with caution and require confirmation through future studies. Additionally, as we did not measure or compare the amount of laughter between the experimental and control groups, we could not ascertain the frequency of laughter in the control group or how effective the amount of laughter was in reducing depression, anxiety, and parental stress.Despite the limited effects of DLT, as indicated by the quantitative data, the study participants reported positive experiences and changes from multiple perspectives, including physical transformations. Specifically, they mentioned muscle relaxation and feeling energized, which aligns with Yim’s findings [A noteworthy observation was the effectiveness of simulated laughter as a self-care strategy, given its ease of self-implementation and repetition. In contrast, spontaneous laughter, which is not as easily self-induced or repetitively invoked, may not be an effective self-care strategy. This contrast might explain why simulated laughter has consistently shown more positive outcomes compared to spontaneous laughter in previous meta-analyses [This study’s participants reported an increase in feelings of happiness and joy, which they attributed to observing their own and others’ laughter-filled faces. Furthermore, participants noted positive changes in their children and spouses who observed their bouts of laughter and merriment. This phenomenon may reflect the “contagion effect of laughter” noted in previous studies, which assert that witnessing or hearing another person’s laughter can trigger one’s laughter [The ongoing pandemic has significantly curtailed social interaction, leaving health professionals struggling to adapt existing interventions for isolated individuals. Even though the DLT program in this study did not outperform entertainment TV shows in terms of impact, we still advocate for its use as an intervention for isolated mothers. Using virtual meeting technology, the DLT has showed a significant effect in alleviating levels of depression, anxiety, and parental stress among mothers, and it has garnered positive feedback. Participants voiced high satisfaction levels, appreciating the opportunity to participate comfortably in an enjoyable environment. They also expressed appreciation for the chance to meet and interact with like-minded people through the DLT during the pandemic. Moreover, according to the Balance between Risks and Resources theory, parental burnout can occur when the demands of parenting surpass available resources [However, it is important to note that the findings of this study may not be readily applicable to diverse populations with varying ethnic backgrounds in different geographic locations because of the limited sample of women from a single ethnicity. Moreover, the small sample size utilized in this study necessitates cautious interpretation of the results obtained from quantitative data analysis. It is also worth mentioning that the effectiveness of the program on unmarried or divorced women remains unexplored, as our study did not include this demographic. Additionally, as we did not conduct a quantitative follow-up to assess the duration of the program’s effects beyond completion, we cannot determine how long these effects persist. Another factor to consider is that the humorous content of the TV show exposed to the control group may have had an impact, as it is known to have its own benefits, including solitary laughter [Therefore, it is imperative that further research is conducted to address these limitations. Specifically, future studies should aim to test the efficacy of DLT using a larger sample size to ensure sufficient statistical power. Additionally, it is crucial to explore the effects of DLT while considering participant characteristics such as parents’ gender, age, relationship with their children, and existing social support systems. Finally, it is necessary to investigate the impact of DLT on diverse populations residing in various geographical regions, as well as its long-term effects.
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Supporting information
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CONSORT 2010 checklist of information to include when reporting a randomised trial*.
(DOC)Click here for additional data file.(PDF)Click here for additional data file.(PDF)Click here for additional data file.
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References
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2. Methods
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2.1. Study Design
RECRUITMENT
This study was a randomized, prospective study assessing the effect of an exercise-based injury-prevention program on MSI incidence, motor performance and psychosocial status. The recruitment period was 15 December 2019 to 1 March 2020. The study period was 6 months (2 March 2020 to 16 August 2020). Outcome variables were measured and recorded at the baseline and after the 6-month study period. This study received ethical approval from the University of Tartu Research Ethics Committee (No. 298/T-10, 18.11.2019). This study was registered at
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2.2. Participants
injuries
The participants in this study were Estonian Military Academy cadets. Potential participants were briefed on the study objectives. All participants provided written informed consent prior to enrollment. Participants were included in the study if they had no current injuries causing limited duty days or inability to participate in the proposed injury-prevention program. Participant health status, in accordance with set criteria, was assessed by an orthopedic surgeon. All participants were randomly assigned to one of two groups: an intervention (INT) group that followed the injury-prevention program and a control (CON) group that continued their usual physical training without the additional injury-prevention program. The participant flow through the study is presented in
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2.3. Injury Incidence
musculoskeletal injury, injuries
The primary outcome of interest in our study was incidence of musculoskeletal injury during the 6-month study period. Injury tracking was performed through the Estonian Defence Forces medical database. Since participants receive health care through the military health care system, any musculoskeletal condition severe enough to seek treatment from a medical provider is registered. Additionally, participants were asked to recall any musculoskeletal conditions at 3 and 6 months from the beginning of the study in order to catch potential injuries not reported to a military medical provider, or for which they might have obtained treatment from a nonmilitary medical care provider.
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2.4. Motor Performance Testing
Prior to motor performance testing, baseline body mass (kg) and height (cm) were measured. Based on these, body mass index (BMI) was calculated (BMI = weight (kg)/height (m)
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2.5. Isokinetic Muscle Strength Testing
Strength parameters of the knee flexor and extensor muscles were recorded using a computerized dynamometer (CON-TREX
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2.6. Postural Sway Measurement
A force platform (Kistler 9286A, Switzerland, dimensions 40 × 60 cm) and biomechanical movement analysis system Elite Clinic with Sway software
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2.7. Physical Fitness Test
EVENT
Participant physical fitness was assessed with a test consisting of a 2-min maximal-effort push-up event, a 2-min maximal-effort sit-up event and a 3.2 km timed run.
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2.8. Psychosocial Status
pain
To assess participant psychosocial status, the RAND 36-item Health Survey 1.0 was used. All items in this survey are scored on a scale from 0 to 100, with a high score defining a more favorable health state. For analysis, the following subscales were used: physical functioning, role limitations due to physical health problems, role limitations due to personal or emotional problems, energy/fatigue, emotional well-being, social functioning, bodily pain and general health perception.
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2.9. Exercise Intervention
Participants in the INT group were asked to follow a prescribed injury-prevention program (PP) during warm-up before physical training for 6 months, 4 times per week. The PP was a structured warm-up routine, taking 20 min to finish. It was divided into 3 sequential parts: (1) whole-body range of motion and bodyweight strength exercises, (2) aerobic load—jogging, and (3) jump, balance and running exercises with a change of direction. A written PP description is provided in
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2.10. Statistical Analysis
Descriptive statistics (mean, SD) in both groups were calculated. Differences between INT and CON groups were analyzed using an independent sample Student’s
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3. Results
musculoskeletal injury
There were no significant group differences between the INT and CON groups at baseline. During the 6-month study period, the musculoskeletal injury incidence was lower in the INT group compared with the CON group. The noted 20% risk reduction was not statistically significant (
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4. Discussion
Based on the results in our study, we were unable to detect any effect of an exercise-based injury-prevention program on MSI incidence in the military cadet population. One of the reasons why significant differences in injury incidence were not detected might be related to the prevention program specifics. This study, in contrast to some previous studies, did not have any progression (e.g., increase in number of repetitions) built into the program [An additional purpose of the study was to investigate whether the prevention program had any influence on motor performance or psychosocial status of study participants. Motor performance assessment was included because our MSI-prevention program was designed to correct potential deficits in biomechanics and physical fitness. Psychosocial assessment was included because it has been reported that emotional problems and stress contribute to MSI risk and should be considered when planning preventive measures [The strength of our study is that we assessed the effect of an exercise-based injury-prevention program simultaneously on injury incidence, motor performance and psychosocial status. Previous research has focused on just a single outcome area, making it somewhat difficult to understand which element has resulted in a reduced injury risk. Furthermore, the 6-month study period should be considered a strength of the current study. This study also has several limitations. Although not an exclusion criterion, due to the small female sample size, female participants were not included in the analysis, which prevents generalizability of our findings to females. Furthermore, the statistical power of this study was low due to the small sample size.
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