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PATIENTS AND METHODS
PMC10417045
Patient eligibility
NSCLC
ONCOLOGY, DISEASE, RECURRENCE, NSCLC
Patients with histologically or cytologically confirmed non‐squamous NSCLC with measurable disease were enrolled. Other eligibility criteria included: Stage IIIB (without indications for radical chest radiation therapy), Stage IV, or postoperative recurrence; age ≥20 and <75 years; Eastern Cooperative Oncology Group (ECOG) performance status (PS) 0 or 1; no prior chemotherapy, no palliative radiotherapy; epidermal growth factor receptor (EGFR) mutation‐negative; adequate hematopoietic function (leukocyte count ≥4000/μL, neutrophil count ≥2000/μL, hemoglobin ≥9.0 g/dL, platelet count ≥10.0 × 10
PMC10417045
Study design and treatment
toxicities, proteinuria, hemoptysis, Cancer
ONCOLOGY, THORACIC, S; HEMOGLOBIN, CANCER
Patients received induction chemotherapy of cisplatin (75 mg/mThe criteria to start maintenance therapy included: PS 0 or 1; neutrophil count ≥1500/μL; hemoglobin ≥8.0 g/dL; platelet count ≥7.5 × 10Administration of maintenance therapies was suspended if any of the following occurred: neutrophil count <1500/μL; platelet count <75,000/μL; hemoglobin <8.0 g/dL; total serum bilirubin >2.0 mg/dL; AST and ALT >100 IU/L; serum creatinine >1.5 mg/dL; or Grade 3 non‐hematological toxicities. Administration of only bevacizumab was suspended if there was active hemoptysis or proteinuria ≥2+. When these conditions improved, maintenance therapies were resumed.This randomized, Phase II study was registered with the UMIN Clinical Trials Registry (number UMIN000010681). The present study protocol was approved by the ethics committees of Tochigi Cancer Center and all participating centers. The present study was conducted in accordance with the Declaration of Helsinki. All patients provided their written, informed consent according to the protocol before study entry. Patients were recruited at 19 investigational sites of the Thoracic Oncology Research Group (TORG) in Japan.
PMC10417045
Assessment of treatment
tumor, Tumor, SD, Tumors, Toxicity
ADVERSE EVENT, TUMOR, METASTASIS, TUMOR, TUMORS, ADVERSE EVENT
Before commencement of therapy, a complete medical history, physical examination, and resting 12‐lead electrocardiogram were performed. Tumor staging was determined by physical examination, routine chest radiography, computed tomography (CT) of the chest and abdomen, bone scintigraphy, or positron emission tomography (PET), and magnetic resonance imaging (MRI) of the head. Staging was performed according to the 7th edition of the tumor, node, metastasis (TNM) system. A complete blood count including differential leukocyte count, urinalysis, and biochemical analyses were performed two or three times per month during induction therapy and once per course during maintenance therapy. Physical examinations and adverse event assessments according to the Common Toxicity Criteria of Adverse Events, version 4.0 were evaluated for each course of therapy. Tumor efficacy was evaluated radiologically using the Response Evaluation Criteria In Solid Tumors version 1.1. Chest X‐rays were performed at least twice per course during induction therapy and once per course during maintenance therapy.After the second cycle of induction chemotherapy with cisplatin, pemetrexed, and bevacizumab, CT of the chest and abdomen was performed. After the fourth cycle of induction chemotherapy, CT of the chest and abdomen and MRI of the head were performed between Day 15 and Day 29 after the fourth cycle of induction chemotherapy. In induction therapy, tumor response of CR and PR was needed to confirm the four‐week response duration in this study. After the tumor response evaluation of induction therapies, patients with CR, PR, and SD following induction therapy were randomized (1:1) to receive maintenance therapy with pemetrexed plus bevacizumab or pemetrexed alone. The maintenance therapy started between 3 weeks and 8 weeks after the fourth cycle of induction therapy. During maintenance therapy, CT of the chest and abdomen was performed every 6 weeks, and tumor efficacy was evaluated. All CT and MRI examinations were diagnosed by independent radiologists.
PMC10417045
Statistical analysis
NSCLC, SD
ADVERSE EVENTS, ADENOCARCINOMA, NSCLC, EVENTS, PATHOLOGY
The primary endpoint of this study was progression‐free survival (PFS) from randomization. Secondary endpoints were the objective response rate (ORR), overall survival (OS) from randomization, and adverse events. The sample size was calculated with a one‐sided significance level of 0.05 and 80% statistical power using the case number design of Lachin and Foulkes.All data of this study were maintained in the TORG coordinating office, which was independent of the attending physicians and institutions. All data maintained in the TORG coordinating office were not available to attending physicians. The entries of all patients were conducted by physicians and assistants at each institution. The random allocation was stratified by response to induction therapy (SD, PR, and CR), pathology (adenocarcinoma vs. non‐adenocarcinoma), PS (0 vs. 1), and institution. The minimization method was applied to balance the distribution of prognostic factors between the pemetrexed group and the pemetrexed plus bevacizumab group. Zelen's method was used to balance the number of patients allocated to the two groups.Although this study proceeded with the above settings, the combination of immune checkpoint‐inhibitor and chemotherapy has been the standard first‐line therapy for advanced NSCLC since January 2019. It was expected that it would be difficult to collect new cases after 2019 in Japan; therefore, the sample size was re‐calculated with a one‐sided significance level of 0.10 and statistical power of 80% at December 2018. In this setting, a sample size of 54 patients was estimated to achieve the desired statistical power, and events in 52 of 54 patients were needed to estimate the primary endpoint. In addition, 66 patients were randomized at December 2018. Due to these circumstances, case entry was conducted until March 2019 without opening the data. When events occurred in 52 patients, all data were analyzed.
PMC10417045
Analysis of circulating immunocytes of peripheral blood
Circulating immunocytes, such as MDSCs, cluster of differentiation (CD) 4 T‐cells, CD8 T‐cells, and Tregs, were analyzed. To analyze circulating immunocytes, peripheral blood samples of patients were collected at four points (before and after induction chemotherapy, 4–8 weeks after the start of maintenance treatment, and after maintenance treatment). The peripheral blood samples of patients were centrifuged at 3000 rpm, and peripheral blood mononuclear cells (PBMCs) were separated by density gradient centrifugation within 6 hours of blood collection. The collected PBMCs were stained by antibodies for surface markers.The percentage of each subset of PBMCs was counted by flow cytometry. The number of each subset of PBMCs was calculated by multiplying the percentage of each subset of PBMCs by the total number of granulocytes. MDSCs are commonly defined as a CD11b
PMC10417045
RESULTS
PMC10417045
Patients' characteristics and treatment administration
NSCLC
LUNG CANCER, DISEASE, NSCLC
A total of 108 patients were entered into this study between June 2013 and March 2019. Patients were recruited at 19 investigational sites of TORG in Japan. The patients' characteristics are listed in Table Patients' background characteristics.Abbreviations: NSCLC, non‐small cell lung cancer; NOS, not otherwise specified; PR, partial response; SD, stable disease.Trial profile.The range of maintenance treatment cycles was 1–24 cycles in the Pgroup and 1–42 cycles in the PBgroup. The median number of treatment cycles of maintenance therapy was 7 in the Pgroup and 8 in the PBgroup. The median and mean relative dose intensities of pemetrexed were 85.7% and 87.3% in the PBgroup and 98.1% and 95% in the Pgroup. The median and mean relative dose intensities of bevacizumab were 85.7% and 84.6% in the PBgroup, respectively.
PMC10417045
Antitumor activity
PD
ADVERSE EVENTS, DISEASE
Of the 108 eligible patients who received induction chemotherapy, 101 were assessable for response to chemotherapy. Seven patients could not be assessed for response because of discontinuation during induction therapy. The reasons for discontinuation during induction therapy were: patients' refusal, four patients; adverse events, three patients; and ineligible, one patient. None of the patients showed CR, 43 (40.2%) showed PR, 48 (44.9%) showed SD, and nine (8.4%) showed PD. CR and PR were needed to confirm 4 week response duration. All patients who had experienced PR after two cycles of induction therapy maintained the response until the end of the induction therapy. Finally, the overall response rate and disease control rate to chemotherapy were 40.2% (95% confidence interval, 30.8%–50.1%) and 85.0% (95% confidence interval, 76.9%–91.2%), respectively.PFS of the two groups is shown in Figure (A) Progression‐free survival from randomization. (B) Overall survival from randomization in an intent to treat analysis. (C) Overall survival from randomization excluded for seven ALK‐positive patients.OS of the two groups is shown in Figure The OS of the two groups, except for patients who were ALK rearrangement‐positive, separated by their response to induction therapy, such as PR or SD, are shown in Figure Overall survival from randomization: response to induction chemotherapy.
PMC10417045
Adverse events
hemorrhage, Proteinuria, hypertension
PROTEINURIA, ADVERSE EVENTS, ADVERSE EVENT, HEMORRHAGE, HYPERTENSION
Grade 3 and 4 hematological adverse events in all cycles of maintenance therapy of all 70 patients are listed in Table Adverse events (Grade 3 or 4) during maintenance therapy.Abbreviation: AST, aspartate aminotransferase; ALT, alanine aminotransferase.Proteinuria, hemorrhage from some organs, and hypertension are generally observed in patients who undergo bevacizumab. The number of patients who experienced Grade 3 hypertension was shown in Table 
PMC10417045
Analysis of circulating immunocytes of peripheral blood
PD
Circulating immunocytes, such as MDSCs, CD 4 T‐cells, CD8 T‐cells, and Tregs, were analyzed. To analyze circulating immunocytes, peripheral blood samples were collected in ten patients. Eight of the ten patients were from the PBgroup and two of the ten patients were from the Pgroup. The eight patients in the PBgroup were divided into two groups of four each. One group was the poor PFS group, and the other group was the good PFS group. In the poor PFS group, two patients had received induction therapy only, and two patients had received less than two cycles of maintenance therapy consisting of pemetrexed and bevacizumab. The reason for discontinuation of therapy in these four patients was PD. In the good PFS group, all four patients had received induction therapy and more than eight cycles of maintenance therapy, also consisting of pemetrexed and bevacizumab. Pretreatment M‐MDSC counts of peripheral blood of the patients are shown in Figure Pretreatment monocytic‐myeloid derived suppressor cell (M‐MDSC) counts of patients in the pemetrexed plus bevacizumab group by progression‐free survival (PFS). Counts tend to be greater in patients with poor PFS than in those with good PFS (
PMC10417045
DISCUSSION
NSCLC, toxicities, human venous blood samples, tumor
TUMOR, NSCLC
A randomized, Phase II study of pemetrexed plus bevacizumab versus pemetrexed alone after treatment with cisplatin, pemetrexed, and bevacizumab in untreated advanced non‐squamous, NSCLC was conducted. To the best of our knowledge, this is the first study to demonstrate the significant progression free survival benefit of adding bevacizumab in maintenance therapy after induction therapy with cisplatin, pemetrexed, and bevacizumab for non‐squamous NSCLC. In addition, although this was a small‐sample analysis, this is the first study to have assessed immune‐suppressive cells of human venous blood samples in advanced NSCLC patients treated with chemotherapy including a VEGF inhibitor.This study showed that the addition of bevacizumab to pemetrexed in maintenance therapy prolonged PFS significantly. In the PARAMOUNT study, which was a Phase III, randomized study comparing pemetrexed with placebo in maintenance therapy, the median PFS of maintenance therapy with pemetrexed alone was 4.1 months.Recently, the addition of immune checkpoint‐inhibitors to platinum‐based chemotherapy showed significant survival benefits over chemotherapy alone in advanced, non‐squamous NSCLC.Some previous studies could not show sufficient data to support the OS benefit of the addition of bevacizumab to platinum‐based chemotherapy in the treatment of advanced, non‐squamous NSCLC. However, we have often experienced cases in which platinum‐based chemotherapy with bevacizumab is highly effective. The present study has limitations in assessing OS. This is because OS is not included in the primary endpoint and the number of cases is small to assess OS. In the present study, OS tended to be similar in the Pgroup and the PBgroup. However, when the response to induction therapy was PR, the median OS tended to be longer in the PBgroup than in the Pgroup. When the response to induction therapy was SD, the median OS tended to be similar in the PBgroup and the Pgroup. In the present study, the evaluation of PR to induction therapy needed to confirm a response duration of 4 weeks. Therefore, the tumor reduced clearly within two cycles of induction therapy in patients with PR. Many previous studies of advanced NSCLC have not shown that the addition of bevacizumab could prolong OS significantly.Recently, VEGF has been found to increase and activate immunosuppressor cells, such as MDSCs and Tregs, and their effects.In conclusion, a randomized, Phase II study comparing maintenance therapies of pemetrexed plus bevacizumab versus pemetrexed alone after treatment with cisplatin, pemetrexed, and bevacizumab was conducted. The addition of bevacizumab to pemetrexed in maintenance therapy after treatment with cisplatin, pemetrexed, and bevacizumab is effective with tolerable toxicities in untreated, advanced, non‐squamous NSCLC. The potential effects of bevacizumab on immune function were also suggested. Therefore, bevacizumab should be considered in combination with cisplatin, pemetrexed, and immune checkpoint‐inhibitors. In addition, early PR to induction therapy and pretreatment M‐MDSC counts in peripheral blood may be related to the survival benefit of the addition of bevacizumab to the combination of cisplatin and pemetrexed.
PMC10417045
AUTHOR CONTRIBUTIONS
PMC10417045
FUNDING INFORMATION
This research did not receive any specific grant from funding agencies in the public, commercial, or not‐for‐profit sectors.
PMC10417045
CONFLICT OF INTEREST STATEMENT
The authors have declared no conflicts of interest.
PMC10417045
ACKNOWLEDGMENTS
The authors would like to thank the patients and their families for consenting to participate in the study.
PMC10417045
DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created or analyzed in this study.
PMC10417045
REFERENCES
PMC10417045
Subject terms
psychotic symptoms, impaired delayed verbal recall
SYNDROME, POSITIVE
As countries adopt more permissive cannabis policies, it is increasingly important to identify strategies that can reduce the harmful effects of cannabis use. This study aimed to determine if increasing the CBD content of cannabis can reduce its harmful effects. Forty-six healthy, infrequent cannabis users participated in a double-blind, within-subject, randomised trial of cannabis preparations varying in CBD content. There was an initial baseline visit followed by four drug administration visits, in which participants inhaled vaporised cannabis containing 10 mg THC and either 0 mg (0:1 CBD:THC), 10 mg (1:1), 20 mg (2:1), or 30 mg (3:1) CBD, in a randomised, counter-balanced order. The primary outcome was change in delayed verbal recall on the Hopkins Verbal Learning Task. Secondary outcomes included change in severity of psychotic symptoms (e.g., Positive and Negative Syndrome Scale [PANSS] positive subscale), plus further cognitive, subjective, pleasurable, pharmacological and physiological effects. Serial plasma concentrations of THC and CBD were measured. THC (0:1) was associated with impaired delayed verbal recall (t(45) = 3.399,
PMC10156730
Introduction
psychotic symptoms
ADVERSE EFFECTS
Several countries and US states have decriminalised or legalised cannabis use, and many permit the use of cannabis preparations for medicinal purposes. Over a similar period, the potency of cannabis, as indexed by its ∆9-tetrahydrocannabinol (THC) content, has been progressively increasing [As well as THC, cannabis also contains cannabidiol (CBD), which has very different effects. CBD does not impair cognitive performance, and has antipsychotic properties [These findings suggest that cannabis with a relatively high CBD:THC ratio may be less likely to have adverse effects than cannabis with a low CBD:THC ratio. The present study sought to investigate this by examining the acute effects of cannabis containing four different CBD:THC ratios (0:1, 1:1, 2:1 and 3:1) on cognitive performance and psychotic symptoms in healthy volunteers. These ratios were selected to reflect the CBD:THC ratios typically found in recreational cannabis, and in medicinal cannabis products [
PMC10156730
Methods
The study was approved by the King’s College London Research Ethics Committee (RESCMR-16/17-4163). All participants provided written informed consent and the study was conducted in compliance with the principles of Good Clinical Practice, the Declaration of Helsinki (1996). The study was registered on Open Science Framework (
PMC10156730
Design
CRF
CRF, APPENDIX
This randomised, double-blind, four-arm, within-subjects study was conducted at the NIHR Wellcome Trust Clinical Research Facility (CRF) at King’s College Hospital, London, UK (randomisation and masking described in Appendix 
PMC10156730
Participants
DISORDER, APPENDIX
Forty-six healthy volunteers (age 21–50 years), who had used cannabis at least once in the past, but had not used cannabis >1/week over the last 12 months, had never used synthetic cannabinoids, and did not have a substance use disorder were recruited. Additional inclusion/exclusion criteria are listed in Appendix 
PMC10156730
Procedure (Fig. 
At baseline, participants were assessed for study eligibility, and practiced the inhalation procedure. At baseline and all experimental visits, urine drug and pregnancy screen as well as alcohol and carbon monoxide breath tests (<10 ppm CO to verify 12 h tobacco abstinence) were completed. Participants were asked to avoid using cannabis and all other illicit drugs during the entire course of the study, including the periods between sessions.Timeline of baseline and experimental sessions (baseline did not include bloods or return to sobriety).Prior to each experimental visit participants had their usual breakfast and amount of caffeine – caffeine was not allowed again until completion of cognitive tests. An intravenous cannula was inserted before participants were administered vaporised cannabis (detailed below). Fifteen minutes after the completion of cannabis inhalation, participants completed a battery of cognitive tasks (30–35 min). This was followed by assessments of pleasurable responses to cannabis as well as a ‘hospital walk’ (15 min), a task previously been found to increase paranoia following THC [
PMC10156730
Study drug and administration
The study drug was provided in the form of granulated cannabis inflorescence by Bedrocan BV (Netherlands) produced in accordance with Good Manufacturing Practice and confirms to the European Medicines Agency’s contaminant levels for products used in the respiratory tract. Each cannabis dose consisted of 10 mg of THC (two standard THC units [Cannabis preparations were administered using a Volcano® Medic Vaporiser (Storz-Bickel GmbH, Tüttlingen, Germany). Each preparation was vaporised at 210 °C into a transparent polythene bag. This temperature has been found to maximise cannabinoid delivery [
PMC10156730
Blood collection and analysis
Venous blood samples were taken before drug administration, and at 0, 5, 15, and 90 min following the final exhalation, alongside blood pressure, heart rate and temperature. The concentration of Δ9-THC, 11-OH-Δ9-THC (OH-THC), 11-COOH-Δ9-THC (COOH-THC), CBD and 7-OH-CBD were determined using high performance LC/MS at the Mass Spectrometry Facility, KCL [
PMC10156730
Cognitive tasks
PMC10156730
Hopkins verbal learning task—Revised (HVLT-R) [
A researcher read out a list of 12 words to the participant, who then repeated the list back. This was repeated over three trials, with the total number of words recalled indexing immediate recall. 20–25 min later participants were asked to recall the words again, indexing delayed recall. The percentage of correctly recalled words indexed retention. Recalled words that were related to the words in the original list, but not part of it, were defined as intrusions. Repetitions referred to the number of times a correctly recalled word was repeated. A different word list was used on each study visit and the order was randomised.
PMC10156730
Forward and reverse digit span
Digit span is a measure of verbal working memory and attention, involving the recall of sequences of numbers with increasing length (WAIS-III). Beginning with three digits on forward and two digits on reverse, the task ceased when the participant failed two consecutive attempts at a number sequence.
PMC10156730
Spatial N-back [
Participants responded to a visual stimulus appearing in one of eight locations, with task demand varied across 0-back, 1-back, and 2-back conditions. Participants were required to indicate (by pressing a Yes or No button) whether the stimulus appeared at the 12 o’clock position (0-back), the same position as the previous visual stimulus (1-back), or the same position as the visual stimulus two previous (2-back).
PMC10156730
Psychological measures
PMC10156730
Positive and negative syndrome scale—positive subscale (PANSS-P) [
hyperactivity, grandiosity, hallucinations, delusions, suspiciousness, psychotic symptoms, hostility
The PANSS-P is an investigator-rated semi-structured interview, which assesses positive psychotic symptoms (delusions, conceptual disorganisation, hallucinations, hyperactivity, grandiosity, suspiciousness, and hostility). Information from this assessment was supplemented by the researcher’s observations of, and interactions with the participant, while they were intoxicated.
PMC10156730
State social paranoia scale (SSPS) [
The SSPS was used to assess persecutory thoughts.
PMC10156730
Community assessment of Psychic Experiences—state (CAPE-state) [
The CAPE-state is a self-rated scale and was used to assess psychotic-like experiences.
PMC10156730
Psychotomimetic states inventory (PSI) [
The PSI questionnaire was used to assess psychotic-like experiences following the use of cannabis use.
PMC10156730
Visual analogue scales (VAS)
VAS were used to measure subjective effects along a continuum. Participants marked on a 100 mm horizontal line to indicate the level of a given feeling at that moment (0 mm ‘Not at all’ to 100 mm ‘Extremely’). The feeling states included:
PMC10156730
Pleasurable responses
Pleasurable effects of cannabis were assessed by the participant rating their enjoyment of a piece of either milk (Marabou) or dark (Lindt 70%) chocolate, and a self-selected piece of music, on a visual analogue scale (VAS), ranging from −5 to +5 on a 100 mm line. The centre of the line (indicated by 0) indicates that the chocolate and music is enjoyed as much as it was at baseline. A negative score indicates that they were enjoyed less compared to baseline, while a positive score indicates that they were more enjoyable.
PMC10156730
Statistical analysis
psychotic-like reactions
According to our power calculation, at 80% power and Bonferroni adjusted alpha <0.008, a sample size of The effect of THC was determined by comparing outcome scores from the baseline visit with those following administration with THC alone (0:1) using paired t-tests. For the primary analysis, we used linear mixed models to assess the effect of varying the CBD:THC ratio on delayed recall on the HVLT-R. The four CBD:THC ratios (0:1, 1:1, 2:1, 3:1) were included as a fixed effect, with participant as a random effect to account for the dependency between repeated measures. All 6 contrasts were of interest (0:1 vs 1:1, 0:1 vs 2:1, 0:1 vs 3:1, 1:1 vs 2:1, 1:1 vs 3:1, 2:1 vs 3:1) and alpha was set according to the results of our power calculation at For pharmacokinetics, VAS scores and physiological outcomes, both peak effects (0 min for pharmacokinetic and physiological outcomes) and area under the curve (AUC) were investigated. For the AUC analyses, values were baseline corrected before using the spline method using the bayestestR package (version 0.7.5.1) [The relationships between both inhalation time and coughing with peak plasma THC and CBD, in addition with their respective AUCs, were assessed using Pearson’s correlation coefficients.We additionally categorised clinically significant psychotic-like reactions as increases in PANSS scores from baseline of ≥3 points, as in previous studies due to floor effects [Multiple imputation chain equations (MICE) were used to impute missing values in pharmacokinetic, cognitive, pleasurable, and physiological outcomes using the mice package (version 3.13.0) [All analyses were conducted using R version 3.5.3. lme4 (version 1.1-26) [
PMC10156730
Results
PMC10156730
Participants and demographics
80 potential participants were screened from which 64 were randomised and 46 completed the study (Fig. Study flow diagram.Demographics and cannabis use at baseline.
PMC10156730
Pharmacokinetics
There were no significant differences in either peak plasma THC, OH-THC or COOH-THC, or their respective AUCs between the CBD:THC ratios (
PMC10156730
Blood plasma THC and CBD concentrations over time and across CBD:THC ratio.
Plasma concentrations of
PMC10156730
Cognitive effects
PMC10156730
Hopkins verbal learning task
When the 0:1 condition (THC only) was compared to baseline, there were impairments in both immediate (t(45) = 5.580,
PMC10156730
Digit span
There was significant impairment in the 0:1 condition compared to baseline in forward digit span (t(45) = 3.309,
PMC10156730
Spatial N-Back
There were no significant differences between baseline and 0:1, or between CBD:THC ratios (
PMC10156730
Psychological effects
PMC10156730
PANSS positive subscale
There was a significant increase in PANSS positive score between baseline and 0:1 (t(45) = −4.709,
PMC10156730
SSPS
There were no significant differences in SSPS scores between baseline and 0:1, between CBD:THC ratios (t(45) = −1.096,
PMC10156730
CAPE
There was a significant increase in total CAPE score between baseline and 0:1 (t(45) = −4.088,
PMC10156730
PSI
There was a significant increase in total PSI score between baseline and 0:1 (t(39) = −7.461,
PMC10156730
VAS
There were no significant differences in subjective effects between CBD:THC ratios in terms of either VAS AUC or peak VAS ratings (
PMC10156730
Pleasurable responses
All CBD:THC ratios increased scores for both chocolate and music compared to baseline, but there were no significant differences between the CBD:THC ratios (
PMC10156730
Physiological effects
PMC10156730
Blood pressure
There were no significant differences in systolic (t(44) = −1.19,
PMC10156730
Heart rate
There was a significant increase in heart rate in the 0:1 condition compared to baseline (t(44) = −9.35,
PMC10156730
Body temperature
APPENDIX
There were no significant differences in body temperature between any of the conditions (Appendix 
PMC10156730
Inhalation and coughing
APPENDIX
There was evidence of greater CBD:THC ratios increasing inhalation time and coughing in a dose responsive manner (Appendix 
PMC10156730
Order and sex effects
fatigue
APPENDIX
Adding order to the models did not have any impact on the significance or direction of pharmacokinetic, cognitive, psychological, subjective, pleasurable, or physiological effects. Restricting the analysis of the primary outcome to visit 1 found no differences across conditions, suggesting no evidence for significant practice or fatigue effects (Appendix 
PMC10156730
Discussion
psychotic symptoms, cognitive impairments
Our main finding is that the co-administration of CBD with THC had no effect on the induction of either cognitive impairments or psychotic symptoms following cannabis use. Similarly, CBD did not influence the subjective (as measured by VAS) or the pleasurable effects (music and chocolate) of THC. This was true across the range of CBD:THC dose ratios that are typically present in both recreational and medicinal cannabis [Using a within-subjects design minimised the potentially confounding effects of inter-individual differences in responses to THC and CBD [Including an additional placebo arm might have made it easier to establish the effects of THC. However, the focus of the study was to compare cannabis with different CBD:THC ratios, rather than to examine the effects of THC alone. The latter have been described in previous studies, and the cognitive and psychological effects of THC that we observed relative to baseline were in line with those reported relative to placebo in infrequent users [Our findings are consistent with previous reports that co-administration of CBD with THC did not alter the effects of THC on memory, psychotic symptoms [There are other mechanisms by which cannabis with higher CBD:THC ratios may be less harmful to users. The cannabis plant produces both THC and CBD (in their acid forms) from a precursor named cannabigerolic acid [
PMC10156730
Conclusions
ADVERSE EFFECTS
At the doses typically present in recreational and medicinal cannabis, we found no evidence of CBD reducing the acute adverse effects of THC on cognition and mental health. Similarly, there was no evidence that it altered the subjective or pleasurable effects of THC. These results suggest that the CBD content in cannabis may not be a critical consideration in decisions about its regulation or the definition of a standard THC unit [
PMC10156730
Supplementary information
The online version contains supplementary material available at 10.1038/s41386-022-01478-z.
PMC10156730
Acknowledgements
BROWN
We would like to wholeheartedly thank all the participants who took part in this study, both the ones who completed as well as the ones who withdrew. We thank George Brown, John Villajin, Louisa Green, Asha Mathews, Chifundo Stubbs, Olabisi Awogbemila, Noah Yogo, Elka Giemza, Stephanie David, Adebukola Shopade, and Herman Rocha of the NIHR Wellcome Trust Clinical Research Facility for supporting this study. We also thank Storz-Bickel GmbH for generously providing us with the cannabis vaporisers and related equipment for this study. We would like to thank Bedrocan BV for their support and advice in supplying the study drug, as well as the Maudsley Pharmacy for their support in receiving, storing, preparing, and dispensing of the study drug. We thank GW Pharmaceuticals for kindly providing us with reference standards for plasma analysis of cannabinoid metabolites, and thanks as well to the Mass Spectrometry Facility at King’s for analysing the samples. We would like to thank the following physicians who assisted us with medical screening of participants: Giulia Spada, Victoria Rodriguez, Graham Blackman, Robert McCutcheon, Matthew Nour, and Marco Colizzi. As well as a special thanks to Cathy Davies for helping in the early stages of the study.
PMC10156730
Author contributions
AE, TF, RM and PMG conceptualised and designed the study, as well as provided continuous review and oversight of the running of the study along with PFP and JS. AE, DO, EC, LC, JW, SS and ADM recruited participants, collected, and interpreted data. JH set up the randomisation algorithm and contributed to the power analysis and statistical analysis plan. All authors participated in the writing and editing of this manuscript and approved the final submitted version. The corresponding authors had final responsibility for the decision to submit for publication.
PMC10156730
Funding
Maudsley
This study was fully funded by a Research Grant from the Medical Research Council UK (MR/P006841/1). The funder had no involvement in the design, data collection, analysis, interpretation, write up or the decision of where to publish. AE, LC, JH, RMM, and JS are part-funded or supported by the National Institute for Health Research (NIHR) Maudsley Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care.
PMC10156730
Competing interests
AE has received speakers’ honoraria from GW Pharmaceuticals. RMM has received speakers’ honoraria from Lundbeck, Sunovian, Otsuka, and Janssen. JS has undertaken research supported financially by various pharmaceutical companies, but this has not involved studies of cannabis or cannabis-related products. All remaining authors report no conflicting interests.
PMC10156730
References
PMC10156730
Key Points
PMC10369925
Question
lung cancer, tumor
LUNG CANCER, TUMOR
Can we improve time to treatment using circulating tumor DNA (ctDNA) genotyping before tissue diagnosis among patients with suspected advanced lung cancer?
PMC10369925
Findings
lung cancer, nonsquamous
LUNG CANCER, SMALL CELL LUNG CANCER
In this nonrandomized clinical trial, 150 patients with suspected advanced lung cancer underwent ctDNA testing during initial diagnostic workup; 90 patients had tissue confirmation of advanced nonsquamous non–small cell lung cancer. Median time to treatment was 39 days vs 62 days for a reference cohort, with faster turnaround time for genotyping results.
PMC10369925
Meaning
lung cancer
LUNG CANCER
The use of plasma ctDNA testing before tissue diagnosis among patients with suspected advanced lung cancer may expedite biomarker testing and accelerate time to treatment.
PMC10369925
Importance
NSCLC, tumor
SMALL CELL LUNG CANCER, TUMOR, NSCLC
Liquid biopsy has emerged as a complement to tumor tissue profiling for advanced non–small cell lung cancer (NSCLC). The optimal way to integrate liquid biopsy into the diagnostic algorithm for patients with newly diagnosed advanced NSCLC remains unclear.
PMC10369925
Objective
NSCLC, tumor
TUMOR, NSCLC
To evaluate the use of circulating tumor DNA (ctDNA) genotyping before tissue diagnosis among patients with suspected advanced NSCLC and its association with time to treatment.
PMC10369925
Design, Setting, and Participants
lung cancer, Cancer
LUNG CANCER, CANCER
This single-group nonrandomized clinical trial was conducted among 150 patients at the Princess Margaret Cancer Centre–University Health Network (Toronto, Ontario, Canada) between July 1, 2021, and November 30, 2022. Patients referred for investigation and diagnosis of lung cancer were eligible if they had radiologic evidence of advanced lung cancer prior to a tissue diagnosis.
PMC10369925
Interventions
lung cancer
LUNG CANCER
Patients underwent plasma ctDNA testing with a next-generation sequencing (NGS) assay before lung cancer diagnosis. Diagnostic biopsy and tissue NGS were performed per standard of care.
PMC10369925
Main Outcome and Measures
Accelerating Lung Cancer, nonsquamous NSCLC
The primary end point was time from referral to treatment initiation among patients with advanced nonsquamous NSCLC using ctDNA testing before diagnosis (ACCELERATE [Accelerating Lung Cancer Diagnosis Through Liquid Biopsy] cohort). This cohort was compared with a reference cohort using standard tissue genotyping after tissue diagnosis.
PMC10369925
Results
nonsquamous NSCLC
Of the 150 patients (median age at diagnosis, 68 years [range, 33-91 years]; 80 men [53%]) enrolled, 90 (60%) had advanced nonsquamous NSCLC. The median time to treatment was 39 days (IQR, 27-52 days) for the ACCELERATE cohort vs 62 days (IQR, 44-82 days) for the reference cohort (
PMC10369925
Conclusions and Relevance
NSCLC
NSCLC
This nonrandomized clinical trial found that the use of plasma ctDNA genotyping before tissue diagnosis among patients with suspected advanced NSCLC was associated with accelerated time to treatment compared with a reference cohort undergoing standard tissue testing.
PMC10369925
Trial Registration
tumor
SMALL CELL LUNG CANCER, TUMOR
ClinicalTrials.gov Identifier: This nonrandomized clinical trial evaluates the use of circulating tumor DNA genotyping before tissue diagnosis among patients with suspected advanced non–small cell lung cancer and its association with time to treatment.
PMC10369925
Introduction
NSCLC, tumor
SMALL CELL LUNG CANCER, TUMOR, NSCLC
Clinical management of newly diagnosed non–small cell lung cancer (NSCLC) requires knowledge of tumor molecular alterations to guide treatment decisions.Liquid biopsies are minimally invasive blood tests that identify circulating tumor DNA (ctDNA) in patients’ plasma.
PMC10369925
Methods
Cancer, Lung Cancer
CANCER, LUNG CANCER
The ACCELERATE (Accelerating Lung Cancer Diagnosis Through Liquid Biopsy) study is a prospective, single-group, minimally invasive nonrandomized clinical trial conducted at the Princess Margaret Cancer Centre–University Health Network (UHN), Toronto, Ontario, Canada. Conduct of this study was approved by the institutional research ethics board (UHN Board C) and was carried out in accordance with the principles of the Declaration of Helsinki.
PMC10369925
Patients
NSCLC, cancer, lung cancer, unresectable stage III or IV lung cancer, pleural effusions, MCC, malignant disease
LUNG, CANCER, DISEASE, MCC, LUNG CANCER, PLEURAL EFFUSIONS, NSCLC, MALIGNANT DISEASE
Between July 1, 2021, and November 30, 2022, 150 patients were enrolled in the ACCELERATE cohort. Patients referred to the UHN Lung Rapid Assessment and Management Program (LungRAMP) were eligible to participate if they had (1) radiologic evidence of unresectable stage III or IV lung cancer; (2) measurable disease with 1 cm or more of disease detected by computed tomography; or (3) a diagnostic tissue biopsy planned or performed without a diagnosis of NSCLC yet. Eligibility was confirmed by the weekly Lung RAMP multidisciplinary case conference (MCC; including interventional respirologists, thoracic surgeons, radiologists, and medical and radiation oncologists). Patients with pleural effusions but no measurable disease were eligible if the MCC favored a diagnosis of malignant disease based on imaging. Patients were excluded if they had concurrent cancer, had a cancer diagnosis other than lung cancer in the past 2 years, or were pregnant due to potentially confounding ctDNA results. Patient self-reported race and/or ethnicity were obtained from the electronic medical record to further characterize the study population, as the frequency of molecular alterations in lung cancer can vary across different ancestral populations.
PMC10369925
Study Procedures
After eligibility confirmation, patients were invited to participate in the study (
PMC10369925
Plasma ctDNA Testing
Plasma ctDNA testing was performed using InVisionFirst-Lung, a highly sensitive and specific NGS assay targeting 37 genes that has been prospectively validated and demonstrates high concordance with tissue results and high sensitivity and specificity for variants, single-nucleotide variants, fusions, and copy number alterations (eFigure 1 in
PMC10369925
Tumor Tissue Molecular Testing
tumor, Trusight Tumor
TUMOR
Reflex molecular testing of tumor tissue was performed per institutional standard of care, including comprehensive NGS (Oncomine Comprehensive Assay, version 3; Thermo Fisher Scientific) (eFigure 1 in For patients in the reference cohort, reflex testing using an NGS assay targeting 15 genes (Trusight Tumor 15 Panel, Illumina Inc) (eFigure 1 in
PMC10369925
Study End Points
nonsquamous NSCLC, tumor
ONCOLOGY, TUMOR
The primary end point was time to treatment, defined as the time from diagnostic program referral to systemic treatment initiation for patients with advanced nonsquamous NSCLC enrolled in the ACCELERATE cohort using ctDNA genotyping prior to pathologic diagnosis compared with a reference cohort of consecutive patients referred to the program in 2018 to 2019, prior to the COVID-19 pandemic. Secondary end points included the frequency of actionable targets identified using plasma ctDNA testing, time to sample collection, and turnaround time of plasma vs tumor tissue profiling for all patients with advanced nonsquamous NSCLC. Actionable alterations were classified according to the European Society for Medical Oncology Scale for Clinical Actionability of Molecular Targets (ESCAT).
PMC10369925
Reference Cohort
lung cancer, NSCLC, Cancer
LUNG CANCER, NSCLC, CANCER
The LungRAMP program maintains a prospective database of all patients referred for investigation of suspected lung cancer. A reference cohort of 89 patients with advanced NSCLC diagnosed through LungRAMP and treated at the Princess Margaret Cancer Centre prior to the COVID-19 pandemic (2018-2019) was identified. Demographic characteristics, molecular data, result turnaround time, and time to treatment were abstracted.
PMC10369925
Statistical Analysis
nonsquamous NSCLC
Patient characteristics and molecular data are summarized using median, IQR, frequency, and percentage. The nonparametric Wilcoxon-Mann-Whitney test was used to compare time to treatment for patients with advanced nonsquamous NSCLC enrolled in the ACCELERATE cohort and the reference cohort. The Wilcoxon signed rank test was used to compare the turnaround time of plasma ctDNA testing vs tissue testing in the ACCELERATE cohort. All analyses were performed using SAS, version 9.4 (SAS Institute Inc). All
PMC10369925
Results
Between July 1, 2021, and November 30, 2022, 150 patients (median age at diagnosis, 68 years [range, 33-91 years]; 80 men [53%] and 70 women [47%]; and 61 patients [41%] were never smokers) were enrolled in the ACCELERATE cohort (
PMC10369925
Baseline Characteristics and Histologic Diagnoses and Stage in the ACCELERATE and Reference Groups
NSCLC, pleural effusion, death, melanoma, liver lesion, plasmacytoma, lung cancer, Hodgkin lymphoma, Lung Cancer
PLEURAL EFFUSION, MELANOMA, UTERINE LEIOMYOSARCOMA, PROSTATE, MESOTHELIOMA, ONCOLOGY, ENDOMETRIAL ADENOCARCINOMA, PLASMACYTOMA, SMALL CELL LUNG CANCER, HODGKIN LYMPHOMA, BONE LESION, LUNG, CARCINOMA OF UNKNOWN PRIMARY, LUNG CANCER, BONE ISLAND, METASTASES, LUNG CANCER, GASTROINTESTINAL NEUROENDOCRINE CARCINOMA, NSCLC, BENIGN CYSTS, DIFFUSE LARGE B-CELL LYMPHOMA
ACCELERATE, Accelerating Lung Cancer Diagnosis Through Liquid Biopsy; ECOG, Eastern Cooperative Oncology Group; NA, not applicable; NOS, not otherwise specified; NSCLC, non–small cell lung cancer.Not documented in the ACCELERATE cohort: ethnicity (n = 24). ECOG performance status and ethnicity were not systematically collected in the historical Lung Rapid Assessment and Management Program cohort.A total of 5 patients did not undergo tissue biopsy: 3 declined, 1 did not tolerate procedure, and 1 underwent rapid deterioration and death before tissue biopsy was done.A total of 18 patients with non–lung cancer diagnoses including diffuse large B-cell lymphoma (n = 4); thoracic metastases from breast, prostate, and gastrointestinal neuroendocrine carcinoma (2 each); gastrointestinal stromal tumor; Hodgkin lymphoma; carcinoma of unknown primary; melanoma; mesothelioma; plasmacytoma; endometrial adenocarcinoma; and uterine leiomyosarcoma (1 each).A total of 3 patients with stage IA NSCLC in the ACCELERATE cohort: 1 with pleural effusion (later determined to be nonmalignant), 1 with suspicious liver lesion (later determined to be benign cysts), and 1 with suspicious bone lesion (benign bone island).
PMC10369925
Tissue Diagnosis
NSCLC, pleural effusion, nonsquamous, squamous carcinoma
PLEURAL EFFUSION, ATYPICAL CARCINOID TUMOR, DISEASE, NSCLC, SQUAMOUS CARCINOMA
Biopsy-proven NSCLC was demonstrated in 107 patients (71%), although 3 patients were later found to have early-stage disease and underwent surgical resection (benign pleural effusion and bone and liver lesions). Of 104 patients with advanced NSCLC, 90 patients had nonsquamous histologic characteristics, 2 had atypical carcinoid tumors, and 12 had squamous carcinoma (
PMC10369925
NGS Testing in Plasma and Tissue
cancer
CANCER
All participants underwent plasma testing; 115 (77%) had tumor-associated variants detected (Among the 18 patients with other cancer diagnoses, 7 did not have detectable cfDNA in plasma, but 3 had potentially informative results based on cancer type (eTable 3 in Combining plasma and tissue results, 53 of 90 patients (59%) had actionable alterations identified by either method: 35 of 53 (66%) in both, 11 of 53 (21%) in plasma only, and 7 of 53 (13%) in tissue only (eFigure 2 in
PMC10369925
Time to Treatment
nonsquamous NSCLC
Most patients (72 of 90 [80%]) started systemic therapy for advanced nonsquamous NSCLC. Median time to treatment was 39 days (IQR, 27-52 days) for the ACCELERATE cohort compared with 62 days (IQR, 44-82 days) for the reference cohort (
PMC10369925
NGS Turnaround Time and Wait Times
In the ACCELERATE cohort, the median turnaround time for plasma testing from blood draw to result reporting was 7 days (IQR, 6-9 days) vs 23 days (IQR, 18-28 days) for tissue NGS, measured from tissue biopsy to reporting (In the reference cohort, referred before the COVID-19 pandemic (
PMC10369925
Discussion
NSCLC, cancer, nonsquamous NSCLC, lung cancer
LUNG CANCER, CANCER, NSCLC
In our study, plasma ctDNA testing before diagnosis in the initial diagnostic workup of patients with suspected advanced NSCLC was associated with shorter time to molecular results than tissue testing and shorter median time to treatment compared with a reference cohort using tissue molecular testing only (39 vs 62 days). Plasma testing was associated with greater detection of ESCAT tier 1 actionable alterations compared with tissue testing alone. Nearly one-fourth of patients started treatment based on plasma results after tissue diagnosis and before tissue NGS results were available, with a median time to treatment of 27 days. These results suggest the clinical utility of adding plasma ctDNA testing before tissue biopsy or confirmed cancer diagnosis to the standard diagnostic workup of patients with suspected advanced lung cancer. Compared with a reference cohort using tissue molecular testing only, the use of liquid biopsy was associated with faster return of molecular results and accelerated time to treatment for all patients, both with and without targetable alterations identified.Preliminary evidence suggests that concurrent plasma ctDNA and tissue NGS testing after lung cancer diagnosis increases the proportion of patients receiving comprehensive molecular testing vs a tissue-only approach.To our knowledge, this is the largest study exploring this prediagnostic approach for suspected advanced lung cancer. Our study demonstrated that plasma ctDNA testing before lung cancer diagnosis was associated with faster time to molecular results, more frequent identification of actionable targets than tissue testing alone, and accelerated time to treatment for all patients with nonsquamous NSCLC participating in the study. Nearly one-fourth of patients (23%) started treatment before tissue molecular testing was available, similar to the pilot study by Cui et al,
PMC10369925
Limitations
lung cancer, cancers, NSCLC
LUNG CANCER, CANCERS, MALIGNANT NEOPLASMS, NSCLC
Our study has limitations, including its single-group prospective design and the fact that it was conducted at a single institution. Despite expert selection of patients with radiologic evidence of advanced lung cancer by a multidisciplinary team, only 70% of patients had biopsy-proven advanced NSCLC, while 30% had other diagnoses or no malignant neoplasms. These results reinforce the need for tissue biopsy for lung cancer diagnosis and pathologic subtyping: plasma first does not mean plasma only.Finally, despite the known benefits of liquid biopsy, cost is a potential barrier limiting its implementation. Although 71% of patients in our study had advanced NSCLC, this percentage will vary across geographic regions. Justifying the cost of liquid biopsy for patients without NSCLC may be challenging, although results were potentially informative for some patients with a diagnosis of other cancers. In a cost-effectiveness analysis by Ezeife et al,
PMC10369925
Conclusions
lung cancer, NSCLC
LUNG CANCER, NSCLC
In this nonrandomized clinical trial, the use of liquid biopsy before lung cancer diagnosis in the initial diagnostic workup of patients with suspected advanced NSCLC was associated with shortened time to treatment and molecular results and yielded a higher rate of detection of actionable alterations. Complementing standard tissue testing with plasma testing before diagnosis could increase access to precision medicine and may improve patient outcomes. Although we believe this is a promising strategy to improve the diagnostic journey and treatment decision-making for patients with advanced NSCLC, the effect of this approach on clinically meaningful outcomes, such as quality of life, survival, and cost-effectiveness, still needs to be demonstrated.
PMC10369925
Subject terms
proarrhythmia
ADVERSE EFFECTS, ATRIAL FIBRILLATION (AF)
Existing antiarrhythmic drugs to treat atrial fibrillation (AF) have incomplete efficacy, contraindications and adverse effects, including proarrhythmia. AP30663, an inhibitor of the KIn a phase 2 clinical trial, an inhibitor of the K
PMC10803288
Main
stroke, heart failure, cardiac arrhythmia
STROKE, HEART FAILURE, ATRIAL FIBRILLATION (AF), CARDIAC ARRHYTHMIA
Atrial fibrillation (AF) is the most common cardiac arrhythmia and is associated with reduced quality of life and increased risk of stroke, heart failure and deathThe KThe AF efficacy of K
PMC10803288
Results
PMC10803288