Efficacy and safety of dexamethasone sparing for the prevention of nausea and vomiting associated with moderately emetogenic chemotherapy: A systematic review and meta-analysis of Clinical Practice Guidelines for Antiemesis 2023 from Japan Society of Clinical Oncology

doi:10.21203/rs.3.rs-4845344/v1

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Efficacy and safety of dexamethasone sparing for the prevention of nausea and vomiting associated with moderately emetogenic chemotherapy: A systematic review and meta-analysis of Clinical Practice Guidelines for Antiemesis 2023 from Japan Society of Clinical Oncology

https://doi.org/10.21203/rs.3.rs-4845344/v1

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published 17 Oct, 2024

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Background

Palonosetron, a second-generation 5-HT₃ receptor antagonist (5-HT₃RA), is more effective than first-generation 5-HT₃RA. Several studies have investigated whether dexamethasone (DEX), when combined with palonosetron as a 5-HT₃RA, can be spared in the delayed phase after moderately emetogenic chemotherapy (MEC). In this systematic review, we aimed to determine which between 1- and 3-day DEX administration, when combined with palonosetron, is more useful in patients receiving MEC.

Methods

The PubMed, Cochrane Library, and Ichushi-Web databases were searched for relevant studies published between 1990 and 2020. We included studies that compared the efficacy of 1- and 3-day DEX administration in preventing nausea and vomiting associated with MEC. Outcomes were “prevention of vomiting (complete response rate and no vomiting rate),” “prevention of nausea” (complete control rate, total control rate, no nausea rate, and no clinically significant nausea rate)” in the delayed phase, “prevention of blood glucose level elevation,” and “prevention of osteoporosis.”

Results

Eight studies were included in this systematic review. The no vomiting rate was significantly higher in the 3-day DEX group than in the 1-day DEX group. However, the other efficacy items did not significantly differ between the two groups. Meanwhile, insufficient evidence was obtained for “prevention of blood glucose level elevation” and “prevention of osteoporosis.”

Conclusions

No significant differences in most antiemetic effects were found between 1- and 3-day DEX administration. Thus, DEX administration could be shortened from 3 days to 1 day when used in combination with palonosetron.

Systematic review

Meta-analysis

Palonosetron

Dexamethasone

Moderately emetogenic chemotherapy

Chemotherapy-induced nausea and vomiting

Chemotherapy-induced nausea and vomiting (CINV) is a distressing symptom that reduces the quality of life of patients with cancer [1]. Most patients hope to avoid CINV [2]. Furthermore, CINV can lead to treatment discontinuation and worsen patient prognosis [3]. Thus, controlling CINV is important.

Anticancer drugs are classified into four categories based on their antiemetic risk: highly emetogenic chemotherapy (HEC), moderately emetogenic chemotherapy (MEC), low emetogenic chemotherapy (LEC), and minimal emetogenic chemotherapy [4]. MEC is defined as chemotherapy with an emetic frequency of 30–90%. Carboplatin is a MEC drug that is emetic. Antiemetic therapy is important in HEC and MEC.

Various guidelines recommend a two-drug antiemetic regimen comprising a 5-HT₃ receptor antagonist (5-HT₃RA) and the steroid dexamethasone (DEX) for MEC [4–6]. For regimens containing carboplatin with an area under the curve greater than or equal to 4 mg/mL/min, these guidelines recommend including a neurokinin-1 receptor antagonist (NK1RA).

Steroids are widely used drugs for various diseases, and DEX has long been used to treat CINV [7]. However, steroids have various adverse events (AEs), including insomnia, gastrointestinal disorders, decreased bone density, and diabetes [8, 9]. Although DEX for CINV is administered within only a few days, the cumulative dose often increases with repeated chemotherapy. The amount of steroids used should be reduced as much as possible to avoid their AEs.

5-HT₃RA has been proven effective and used as an antiemetic therapy since the 1990s [10]. Palonosetron, a second-generation 5-HT₃RA, is more effective than first-generation 5-HT₃RA [11]. Several studies have examined whether DEX, when combined with palonosetron as a 5-HT₃RA, can be spared in the delayed phase after MEC [12–18].

In this systematic review, we aimed to determine which between 1- and 3-day DEX administration, when combined with palonosetron, is more useful in patients receiving MEC.

This systematic review was conducted based on “Minds Clinical Practice Guideline Development Guide 2017” [19].

Search strategy

The PubMed, Cochrane Library, and Ichushi-Web databases were searched for relevant studies published between January 1990 and December 2020. The search terms were “moderately emetogenic chemotherapy,” “chemotherapy-induced nausea and vomiting,” “nausea,” “vomiting,” “dexamethasone,” “corticosteroid,” “sparing,” “side effect,” “CINV,” “MEC,” “carboplatin,” and “oxaliplatin.” We added literature obtained by manual search to the retrieved literature.

We conducted two rounds of screening (primary and secondary) and selected the literature for evaluation in the systematic review. Each screening was conducted by two reviewers (K.N. and A.Y.). If the two members disagreed, a third reviewer made the decision (M.M.). The primary screening was performed based on the titles and abstracts of all articles, whereas the secondary screening was performed based on the full texts.

Selection criteria

We selected randomized controlled trials (RCTs) using the population, intervention, comparator, and outcome (PICO) approach with the highest priority. When no or few RCTs were available, we selected non-RCTs, single-group trials, case-control studies, and observational studies from which data could be extracted. We excluded guidelines, reviews, letters, abstracts without articles, laboratory studies, and case reports.

We set the PICO for this clinical question as follows: “Population” was defined as adult patients with cancer treated with MEC, “Intervention” was defined as DEX administration for 1 day, and “Comparator” was defined as DEX administration for 3–4 days.

The outcomes were “prevention of vomiting” in the delayed phase (24–120 h post-chemotherapy), “prevention of nausea” in the delayed phase, “prevention of blood glucose level elevation,” and “prevention of osteoporosis.”

“Prevention of vomiting” was evaluated based on complete response (CR: no vomiting and no use of rescue therapy) and no vomiting (NV) rates. “Prevention of nausea” was evaluated based on complete control (CC; no vomiting, no rescue, no significant nausea) rate, total control (TC: no vomiting, no rescue, no nausea) rate, no nausea (NN) rate, and no significant nausea (NSN) rate. NSN was defined as < 25 mm on the visual analog scale, 2 or less on the numerical rating scale, and none or mild on the categorical rating scale.

Data extraction and quality assessment

After the second screening, the author (K.N.) of the systematic review team reassessed the articles and extracted data using standardized data abstraction forms. The evidence indicated by individual studies related to critical outcomes included within the clinical questions posed by the guideline creation team was divided into groups based on study design and quality. The leader (M.A.) of the guideline creation team resolved conflicts and questions. The level of evidence was evaluated not for individual references but for each outcome for studies grouped by study design. The certainty of the evidence was assessed based on the risk of bias, inconsistency, imprecision, indirectness, and publication bias. The literature quality and body of evidence were evaluated using the Grading of Recommendations, Assessment, Development, and Evaluation approach and then classified into four levels: “strong,” “medium,” “weak,” and “very weak” [20].

Statistical analysis

Review Manager version 5.3 was used for statistical analyses. The risk difference (RD) for each endpoint was calculated, and the effect size was described as a 95% confidence interval (CI). They were calculated using random-effects models depending on the level of heterogeneity. Results of the meta-analysis were presented as forest plots. The degree of heterogeneity was assessed using I² and chi-squared-based Q tests. Z test results were considered statistically significant at p < 0.05. The potential for publication bias was demonstrated using a funnel plot.

Literature search

A flowchart of the search strategy and study selection process is shown in Fig. 1. Based on the literature search for this CQ, 13 PubMed, 252 Cochrane, and 46 Ichushi-Web articles were identified. In addition to six hand-searched articles, primary screening was conducted on 317 articles. Thirteen articles were assessed during secondary screening. Nine articles were included in this study. One reference [21] was a post hoc analysis of an RCT [13] that was also extracted. This was treated as preliminary material and was excluded from the systematic review. Finally, eight articles were included in the systematic review.

The seven studies that conducted an efficacy evaluation are listed in Table 1 [12-18]. All were RCTs that compared 1- and 3-day DEX administration. Doxorubicin plus cyclophosphamide combination (AC) therapy for breast cancer is currently classified as HEC, but it was previously classified as MEC. Two studies included AC therapy for breast cancer [12, 13]. Some studies were limited to cancer type or chemotherapy regimen [12, 15-17].

Association between the prevention of vomiting and DEX sparing

Two outcomes were evaluated in the delayed phase: “CR rate” (7 RCTs [12-18]) and “NV rate” (3 RCTs [12, 13, 18]). In individual studies, many showed slightly favorable trends in the 3-day DEX group.

Figure 2a shows the results of a meta-analysis of the CR rate in the delayed phase (n=1305). The CR rate was higher in the 3-day DEX group than in the 1-day DEX group, but the difference was not statistically significant (RD -0.04 (95% CI: -0.10, 0.02; p=0.18)). The funnel plots did not show any distribution, suggesting a publication bias (Fig. 2b).

Figure 3 shows the results of a meta-analysis of the NV rate in the delayed phase (n=747). The NV rate was significantly higher in the 3-day DEX group than in the 1-day DEX group (RD -0.06 (95% CI: -0.11, -0.01; p=0.02)).

The evidence for this outcome was determined to be “strong.”

Association between the prevention of nausea and DEX sparing

Four outcomes were evaluated in the delayed phase: “CC rate ” (6 RCTs [13-18]), “TC rate ” (5 RCTs [14-18]), “NN rate ” (4 RCTs [13, 15, 17, 18]), and “NSN rate ” (three RCTs [15, 17, 18]).

Figure 4 shows the results of a meta-analysis of the CC rate in the delayed phase (n=997). The CC rate was higher in the 3-day DEX group than in the 1-day DEX group, but the difference was not statistically significant (RD -0.04 (95% CI: -0.10, 0.02; p=0.17)).

Figure 5 shows the results of a meta-analysis of the TC rate in the delayed phase (n=673). No significant difference in TC rate was found between the two groups (RD -0.01 (95% CI: -0.08, 0.07); p=0.81)).

Figure 6 shows the results of a meta-analysis of the NN rate in the delayed phase (n=583). No significant difference in NN rate was observed between the two groups (RD -0.04 (95% CI: -0.12, 0.04; p=0.38)).

Figure 7 shows the results of a meta-analysis of the NSN rate in the delayed phase (n=259). The NSN rate was higher in the 3-day DEX group than in the 1-day DEX group, but the difference was not statistically significant (RD -0.08 (95% CI: -0.18, 0.03; p=0.15)).

The evidence for this outcome was determined to be “strong.”

Association between the prevention of blood glucose level elevation and DEX sparing

No studies have evaluated the suppression of blood glucose level elevation. Hence, this outcome could not be evaluated.

Association between the prevention of osteoporosis and DEX sparing

Only one cohort study was included in this evaluation [22]. It was a single-arm observational study on patients with gastrointestinal cancer treated using steroids to prevent nausea/vomiting and allergies (n=74), and the endpoints were bone mineral density and changes in bone metabolism markers after 16 weeks. A sub-analysis of this study revealed no significant difference in the incidence of bone mineral density loss between the 1-day and multiple-day steroid administration groups (95% CI: -0.24, 0.28; p=0.90). Therefore, the evidence was determined to be “very weak.”

In this systematic review, we determined which between 1- and 3-day DEX administration, when combined with palonosetron, is more useful in patients receiving MEC.

Regarding “prevention of vomiting” and “prevention of nausea,” the control group had significantly better results only in terms of NV rate. However, for the other items, no significant differences in the other items were found between the 1- and 3-day DEX groups. Celio and Okada conducted a meta-analysis to assess the effect of palonosetron plus one-day DEX compared with palonosetron plus 3-day DEX for controlling CINV in patients receiving HEC and MEC, respectively [23, 24]. Their meta-analysis demonstrated that DEX-sparing regimens do not cause any significant loss in protection against CINV caused by MEC or AC. Based on the results of our systematic review and these previous reports, shortening the administration period of DEX is useful.

No studies could be evaluated regarding “prevention of blood glucose level elevation.” Only one cohort study was included in the evaluation regarding “prevention of osteoporosis.” However, it was a small single-arm study, and single-day versus multi-day steroid administration was evaluated in the subgroup analysis. Furthermore, this study focused on gastrointestinal cancers; included MEC, LEC, and HEC; used varied doses of steroids; and did not indicate the duration of steroid administration. Sufficient evidence about AEs was not obtained in this systematic review. Although many of the individual RCTs included in this study found no differences in the incidence or severity of all AEs [13–15, 17], further research regarding AEs is needed.

Several studies have reported the efficacy of olanzapine against CINV [25–30]. Olanzapine has also been proven effective in patients receiving MEC [27–30]. Furthermore, the efficacy of fosnetupitant as a new NK1RA in preventing emesis caused by HEC has been recently demonstrated [31]. The combination of olanzapine and fosnetupitant may provide sufficient antiemetic effects in DEX sparing for MEC. Treatment with these agents may completely remove the need for DEX.

Our study has several limitations. First, the studies analyzed in our systematic review included various chemotherapy regimens. Some studies included AC, which is currently classified as HEC [12, 13]. Some studies have reported a mixture of carboplatin-based regimens, which are emetic, and non-carboplatin regimens. Whether these patients can be treated as having the same emetic risks is unclear. Second, among the studies included in this review, none used a NK1RA, although some included AC and carboplatin-based regimens. Watanabe et al. performed a meta-analysis to assess the effect of 1-day DEX versus 3-day DEX with a NK1RA on preventing CINV in patients receiving MEC [32]. Their report showed that 3-day DEX with a NK1RA exerts a greater antiemetic benefit than 1-day DEX with a NK1RA. When using a carboplatin-based regimen, administering DEX for 3 days may be better. Therefore, the duration of DEX administration may need to be adjusted depending on the MEC regimen.

No significant differences in CR, CC, TC, NN, and NSN rates were found between the 1- and 3-day DEX groups. Thus, DEX administration could be shortened from 3 days to 1 day when used in combination with palonosetron to help prevent nausea and vomiting associated with MEC.

Acknowledgments

We thank Ms. Natsuki Fukuda and Ms. Kyoko Hamada for their valuable comments and suggestions, and invaluable supports. We thank Mr. Naohiko Yamaguchi and Ms. Yuko Mitsuoka for their contributions to the literature search. We thank Editage (www.editage.jp) for the English language editing.

Funding

This study was supported by Japan Society of Clinical Oncology.

Author contributions

All authors contributed to the conception and design of this study. Kazuhisa Nakashima wrote the original draft of the manuscript. All other authors reviewed and edited the manuscript.

Data availability

Data associated with this systematic review can be accessed from the corresponding author upon request.

Conflicts of interest

Kazuhisa Nakashima received honoraria from Taiho Pharmaceutical Co., Ltd., Chugai Pharmaceutical Co., Ltd., AstraZeneca K.K., and Eli Lilly Japan K.K. Michiyasu Murakami received honoraria from Taiho Pharmaceutical Co., Ltd. Eriko Satomi received honoraria from Shionogi & Co., Ltd. Masayuki Takeda received honoraria from Chugai Pharmaceutical Co., Ltd., AstraZeneca K.K., Novartis Pharma K.K., Ono Pharmaceutical Co., Ltd., and Bayer. Takako Eguchi Nakajima received research funding from KBBM, Inc. and Takeda Pharmaceutical Co., Ltd. Junichi Nishimura received honoraria from Taiho Pharmaceutical Co., Ltd. Narikazu Boku received honoraria from Ono Pharmaceutical Co., Ltd., Bristol Myers Squibb, Daiichi Sankyo Co., Ltd., Taiho Pharmaceutical Co., Ltd., and Eli Lilly Japan K.K. Koji Matsumoto received honoraria from MSD K.K., Kyowa Kirin Co., Ltd., and Chugai Pharmaceutical Co., Ltd. as well as research funding from Daiichi Sankyo Co., Ltd., MSD K.K., Gilead Sciences, Inc., and Eli Lilly Japan K.K. Nobuyuki Yamamoto received honoraria from MSD K.K., Accuray Japan K.K., AstraZeneca K.K., Abbvie Inc., Amgen Inc., Ono Pharmaceutical Co., Ltd., Guardant Health Japan Corp., Daiichi Sankyo Co., Ltd., Taiho Pharmaceutical Co., Ltd., Takeda Pharmaceutical Co., Ltd., Chugai Pharmaceutical Co., Ltd., Chugai Foundation for Innovative Drug Discovery Science, Lao Tsumura Co., Ltd., Terumo Corporation, Eli Lilly Japan K.K., Nippon Kayaku Co., Ltd., Novartis AG, Pfzer Global Supply Japan Inc., Merck Biopharma Co., Ltd, Pfzer Global Supply Japan Inc., Merck Biopharma Co., Ltd., Janssen Pharmaceutical K.K., and USACO Corporation, as well as legal fees in case of lawsuit from Taiho Pharmaceutical Co., Ltd., Boehringer Ingelheim Japan, Chugai Pharmaceutical Co., Ltd., Kyowa Kirin Co., Ltd., Nippon Kayaku Co., Ltd., Prime Research Institute for Medical RWD, Inc., AstraZeneca K.K., and A2 Healthcare Corporation. Other authors declare that they have no conflict of interest.

Ethical approval

Not applicable.

Informed consent

Formal consent was not required for this type of study.

Consent to participate

Not applicable.

Consent for publication

All authors consented to the publication of this study.

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Table 1

Study	Antiemetics	Chemotherapy	Cancer type	N
Aapro 2010 [12]	PALO 0.25 mg iv day 1 DEX 8 mg iv day1, Placebo day 2, 3	Cyclophosphamide AC	Breast cancer	151
	PALO 0.25 mg iv day 1 DEX 8 mg iv day1, DEX 4 mg po bid day 2, 3			149
Celio 2011 [13]	PALO 0.25 mg iv day 1 DEX 8 mg iv day 1	AC Oxaliplatin-based Carboplatin-based Irinotecan-based etc.	Solid cancer	166
	PALO 0.25 mg iv day 1 DEX 8 mg iv day 1–3			166
Komatsu 2015 [14]	PALO 0.75 mg iv day 1 DEX 9.9 mg iv day 1	Oxaliplatin-based Irinotecan-based Carboplatin-based etc.	Malignant tumor	151
	PALO 0.75 mg iv day 1 DEX 9.9 mg iv day 1 DEX 8 mg po or 6.6 mg iv day 2, 3			154
Furukawa 2015 [15]	PALO 0.75 mg iv day 1 DEX 20 mg iv day 1	TC	Gynecological cancer	43
	PALO 0.75 mg iv day 1 DEX 20 mg iv day 1, DEX 8 mg po day 2, 3			39
Matsuura 2015 [16]	PALO 0.75 mg iv day 1 DEX (20 mg iv: TC, 9.9 mg iv: ddTC day 1)	TC	Gynecological cancer	56
	PALO 0.75 mg iv day 1 DEX (20 mg iv: TC, 9.9 mg iv: ddTC day 1) DEX 8 mg po day 2, 3			53
Celio 2019 [17]	PALO 0.25 mg iv day 1 Histamine blocker OLZ 10 mg po day 1–3 DEX 16 mg iv day 1	TC	Gynecological cancer	27
	PALO 0.25 mg iv day 1 Histamine blocker OLZ 10 mg po day 1–3 DEX 16 mg iv day 1, DEX 4 mg po bid day 2, 3			27
van der Vorst PAL 2020 [18]	PALO 0.25 mg iv day 1 DEX 8 mg iv on day 1	Oxaliplatin-based Carboplatin-based Irinotecan-based Anthracycline-based etc.	Solid cancer	63
	Ondansetron 8 mg iv DEX 8 mg iv day 1 DEX 4 mg po bid days 2, 3			60

CR: complete response, PALO: palonosetron, iv: intravenous injection, DEX: dexamethasone, po: per os, bid: bis in die, AC: doxorubicin plus cyclophosphamide combination therapy, TC: carboplatin plus paclitaxel combination therapy, ddTC: dose-dense TC, OLZ: olanzapine

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Editorial decision: Minor revisions
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Efficacy and safety of dexamethasone sparing for the prevention of nausea and vomiting associated with moderately emetogenic chemotherapy: A systematic review and meta-analysis of Clinical Practice Guidelines for Antiemesis 2023 from Japan Society of Clinical Oncology

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Abstract

Background

Methods

Results

Conclusions

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Introduction

Materials and methods

Search strategy

Selection criteria

Data extraction and quality assessment

Statistical analysis

Results

Discussion

Conclusion

Declarations

References

Table 1

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