Characteristics of 218 Recent Reviews on Natural Health Products in Integrative Cancer Care: A Bibliometric Analysis of Trends in the Research Literature

Bibliometric Analysis

The field of integrative oncology is very broad and diverse with an increasing number of human studies being published on a variety of natural health products (NHPs), cancer types, conventional treatment contexts, etc. Bibliometric analyses enable high-level overviews of the research literature landscape on an extensive topic and can be used to identify trends and characteristics of publications. Several types of bibliometric analyses have been conducted on various aspects of natural health products (NHPs) in the past decade or so (Du, & Tang, 2014; Fu, 2010; Hung, & Ernst, 2010; Kim, Kim, Lee, Kim, Wieland, & Shin, 2014; Koo, 2017; Leung, Chan, & Song, 2006; Li, Cui, & Cui, 2009; Li, Tao, Zhou, & Ling, 2011; Wieland, Manheimer, Sampson, Barnabas, Bouter, Cho, & et al., 2013; Zyoud, Al-Jabi, & Sweileh, 2015). To our knowledge, a bibliometric analysis of systematic reviews of human controlled studies on the use of NHPs in integrative cancer care has not been undertaken.

This article utilizes data from a large, exploratory ‘positive-focused’ evidence maps project we conducted with the aim of identifying ‘signals’ to inform our future research agenda to develop best practice guidance documents. Details on the evidence maps methods (including the full search strategy) and results are being published in four related reports. Briefly, a MEDLINE database search was conducted by an experienced information specialist for systematic or comprehensive reviews on NHPs in integrative cancer care. Included reviews had to synthesize human studies that used a control group (experimental or observational), and be published in English from 2010 to July 3, 2017. The search strategy was based on the PubMed Dietary Supplements Subset search filter, which contains over 1300 rows of NHP terms (https://www.nlm.nih.gov/bsd/pubmed_subsets/diet_strategy.html). Over 1950 records were screened for eligibility, and ultimately 218 systematic or comprehensive reviews were included (Figure 1).

A full bibliography of the 218 included reviews is listed in Appendix 1 below. Data were extracted specifically for the bibliometric analysis on country of review conduct, publication date, and the NHP categories covered by each review (i.e., Nutraceuticals, Botanical and Fungi preparations, and Traditional Chinese and Asian Medicine formulations). A digital summarization tool for PubMed search results called Anne O’Tate, which was developed by the Arrowsmith project (and is freely available at http://arrowsmith.psych.uic.edu), was used to analyze all of the review authors and journals.

Figure 1 presents the NHP category results, which were fairly evenly distributed. 87 of the included reviews covered Nutraceutical products, 69 were on Botanical and Fungi preparations, and 75 on Traditional Chinese and Asian Medicine formulations. Note that some reviews covered more than one NHP category so these numbers total more than 218.

Figure 1. Screening Results and Natural Health Product Categories *

* Refer to Portable Document Format for figures and tables

There was an overall trend of increasing numbers of publications by date across the 7.5 years covered by the search date limits of January 1, 2010 to July 3, 2017 (Figure 2). In fact, roughly half of the 218 included reviews were published in just the most recent 2.5 years compared to the other half of the publications across the previous five years.

Figure 2. Publication Dates of the 218 Included Reviews

China was by far the most prolific country of conduct for the included systematic and comprehensive reviews of human controlled studies on the use of NHPs in integrative cancer care, with 38% (83/218) of the reviews (Figure 3). The countries of conduct of the most reviews after China were the USA and Australia, having 28 (13%) and 21 (10%) reviews, respectively. These top three countries were followed by the UK (N=16), Canada (N=15), and Germany (N=14). Eight of our 218 included reviews were conducted in South Korea. The other countries that had more than one review included were: Italy, France, and Brazil (4 each); and the Netherlands, Japan, and Israel (3 each).

Figure 3. Top Countries of the 218 Included Reviews

Regarding the MEDLINE-indexed journals where these reviews were published, the top 15 are presented in Table 1 along with frequencies. The top journal with the most reviews from our set was Evidence-Based Complementary and Alternative Medicine (9%, or 19/218). The Cochrane Database of Systematic Reviews was the second most prolific source (N=13), followed closely by Integrative Cancer Therapies (N=12), Journal of Cancer Research and Therapeutics (N=11), and PLoS One (N=11). An e-book collection called PDQ Cancer Information Summaries published 10 of the included reviews.

Table 1. Top 15 Journals of the 2018 Included Review

Table 2 lists in order of frequency the top 40 authors of the 218 included reviews obtained from the Anne O’Tate analysis results. The researcher with the most publications among this set was Dr. Dugald Seely with 12/218 (6%) reviews. The next eight individual authors, with between 7-9 reviews each, were: Drs. H. Fritz, Y. Wang, K. Cooley, J. Li, D. Fergusson, D. Kennedy, R. Wong, and Y. Zhang. The PDQ Integrative, Alternative, and Complementary Therapies Editorial Board, an institutional group of authors within the US National Cancer Institute, had nine included review publications.

Table 2. Top 40 Authors of the 2018 Included Review

In summary, the annual rate of review publications in this field is steadily increasing, and the reviews were distributed across all three NHP categorizations. China was the leading country of conduct, primarily due to the large volume of randomized controlled studies that have been conducted on Traditional Chinese Medicine. Furthermore, our included reviews on Traditional Chinese and Asian Medicine formulations provide very valuable syntheses of the extensive research on this topic published in Chinese and other languages that is often difficult for Western audiences to access. The search was limited to English and MEDLINE for feasibility reasons, but this excluded reviews published in European and other languages and in high quality journals that are not indexed in MEDLINE. This bibliometric analysis of our set of 218 systematic or comprehensive reviews provides a high-level overview of the human research literature landscape spanning this very broad topic on the use of natural health products in integrative cancer care.

Competing Interests

The authors declare that they have no competing interests.

Funding

This project was funded by the Patterson Institute for Integrative Cancer Research at the Canadian College of Naturopathic Medicine.

Acknowledgments

We wish to thank Sukriti Bhardwaj for performing data extractions for the evidence maps project, and Dr. Nancy Rawling for her helpful advice on the project.

We also gratefully acknowledge the generous support of John and Thea Patterson as founding donors of the Patterson Institute.

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Appendix 1. Bibliography of 218 Included Reviews

Allegra, A., Innao, V., Russo, S., Gerace, D., Alonci, A., & Musolino, C. (2017). Anticancer Activity of Curcumin and Its Analogues: Preclinical and Clinical Studies. Cancer Invest, 35, 1-22.

Aucoin, M., Cooley, K., Knee, C., Fritz, H., Balneaves, L. G., Breau, R. et al. (2017). Fish-Derived Omega-3 Fatty Acids and Prostate Cancer: A Systematic Review. Integr.Cancer Ther., 16, 32-62.

Bae, K., Park, J. H., Kim, J., Cho, C. K., Oh, B., Costa, D. et al. (2017). Traditional Oriental Herbal Medicine and Natural Killer Cells for Cancer Patients: A Systematic Review and Meta-analysis. Phytother.Res., 31, 519-532.

Bao, Y., Kong, X., Yang, L., Liu, R., Shi, Z., Li, W. et al. (2014). Complementary and alternative medicine for cancer pain: an overview of systematic reviews. Evid.Based Complement Alternat.Med., 2014, 170396.

Ben-Arye, E., Attias, S., Tadmor, T., & Schiff, E. (2010). Herbs in hemato-oncological care: an evidence-based review of data on efficacy, safety, and drug interactions. Leuk.Lymphoma, 51, 1414-1423.

Ben-Arye, E., Polliack, A., Schiff, E., Tadmor, T., & Samuels, N. (2013). Advising patients on the use of non-herbal nutritional supplements during cancer therapy: a need for doctor-patient communication. J Pain Symptom.Manage., 46, 887-896.

Beuth, J. (2010). Evidence-based complementary oncology: innovative approaches to optimise standard therapy strategies. Anticancer Res., 30, 1767-1771.

Braga, M., Wischmeyer, P. E., Drover, J., & Heyland, D. K. (2013). Clinical evidence for pharmaconutrition in major elective surgery. JPEN J Parenter.Enteral Nutr., 37, 66S-72S.

Brami, C., Bao, T., & Deng, G. (2016). Natural products and complementary therapies for chemotherapy-induced peripheral neuropathy: A systematic review. Crit Rev.Oncol.Hematol., 98, 325-334.

Burden, S., Todd, C., Hill, J., & Lal, S. (2012). Pre-operative nutrition support in patients undergoing gastrointestinal surgery. Cochrane Database Syst.Rev., 11, CD008879.

Bussing, A., Raak, C., & Ostermann, T. (2012). Quality of life and related dimensions in cancer patients treated with mistletoe extract (iscador): a meta-analysis. Evid.Based Complement Alternat.Med., 2012, 219402.

Buttigliero, C., Monagheddu, C., Petroni, P., Saini, A., Dogliotti, L., Ciccone, G. et al. (2011). Prognostic role of vitamin d status and efficacy of vitamin D supplementation in cancer patients: a systematic review. Oncologist., 16, 1215-1227.

Cao, H., Mu, Y., Li, X., Wang, Y., Chen, S., & Liu, J. P. (2016). A Systematic Review of Randomized Controlled Trials on Oral Chinese Herbal Medicine for Prostate Cancer. PLoS One, 11, e0160253.

Chakraborty, R., Savani, B. N., Litzow, M., Mohty, M., & Hashmi, S. (2015). A perspective on complementary/alternative medicine use among survivors of hematopoietic stem cell transplant: Benefits and uncertainties. Cancer, 121, 2303-2313.

Chan, R. J., McCarthy, A. L., Devenish, J., Sullivan, K. A., & Chan, A. (2015). Systematic review of pharmacologic and non-pharmacologic interventions to manage cognitive alterations after chemotherapy for breast cancer. Eur.J Cancer, 51, 437-450.

Chaudhary, T., Chahar, A., Sharma, J. K., Kaur, K., & Dang, A. (2015). Phytomedicine in the Treatment of Cancer: A Health Technology Assessment. J Clin.Diagn.Res., 9, XC04-XC09.

Chen, J., Song, Y., & Zhang, L. (2013). Effect of lycopene supplementation on oxidative stress: an exploratory systematic review and meta-analysis of randomized controlled trials. J Med.Food, 16, 361-374.

Chen, J., Chen, Y. J., & Wu, M. D. (2014). Herbal extract elemene intrathoracic injection in the treatment of lung cancer patients with malignant pleural effusion: a meta-anaylsis. J Cancer Res.Ther., 10 Suppl 1, 56-59.

Chen, L., Chen, Y., Wang, X., Li, H., Zhang, H., Gong, J. et al. (2015). Efficacy and safety of oral branched-chain amino acid supplementation in patients undergoing interventions for hepatocellular carcinoma: a meta-analysis. Nutr.J, 14, 67.

Chen, M., May, B. H., Zhou, I. W., Xue, C. C., & Zhang, A. L. (2014). FOLFOX 4 combined with herbal medicine for advanced colorectal cancer: a systematic review. Phytother.Res., 28, 976-991.

Chen, M., May, B. H., Zhou, I. W., Xue, C. C., & Zhang, A. L. (2016). Meta-Analysis of Oxaliplatin-Based Chemotherapy Combined With Traditional Medicines for Colorectal Cancer: Contributions of Specific Plants to Tumor Response. Integr.Cancer Ther., 15, 40-59.

Chen, M., May, B. H., Zhou, I. W., Sze, D. M., Xue, C. C., & Zhang, A. L. (2016). Oxaliplatin-based chemotherapy combined with traditional medicines for neutropenia in colorectal cancer: A meta-analysis of the contributions of specific plants. Crit Rev.Oncol.Hematol., 105, 18-34.

Chen, M. H., May, B. H., Zhou, I. W., Zhang, A. L., & Xue, C. C. (2016). Integrative Medicine for Relief of Nausea and Vomiting in the Treatment of Colorectal Cancer Using Oxaliplatin-Based Chemotherapy: A Systematic Review and Meta-Analysis. Phytother.Res., 30, 741-753.

Chen, S., Flower, A., Ritchie, A., Liu, J., Molassiotis, A., Yu, H. et al. (2010). Oral Chinese herbal medicine (CHM) as an adjuvant treatment during chemotherapy for non-small cell lung cancer: A systematic review. Lung Cancer, 68, 137-145.

Chen, S., Wang, Z., Huang, Y., O’Barr, S. A., Wong, R. A., Yeung, S. et al. (2014). Ginseng and anticancer drug combination to improve cancer chemotherapy: a critical review. Evid.Based Complement Alternat.Med., 2014, 168940.

Chen, X., Deng, L., Jiang, X., & Wu, T. (2016). Chinese herbal medicine for oesophageal cancer. Cochrane Database Syst.Rev., CD004520.

Cheon, S., Zhang, X., Lee, I. S., Cho, S. H., Chae, Y., & Lee, H. (2014). Pharmacopuncture for cancer care: a systematic review. Evid.Based Complement Alternat.Med., 2014, 804746.

Cho, H. K., Jeong, Y. M., Lee, H. S., Lee, Y. J., & Hwang, S. H. (2015). Effects of honey on oral mucositis in patients with head and neck cancer: A meta-analysis. Laryngoscope, 125, 2085-2092.

Choi, J., Kim, T. H., Choi, T. Y., & Lee, M. S. (2013). Ginseng for health care: a systematic review of randomized controlled trials in Korean literature. PLoS One, 8, e59978.

Chu, K. J., Lai, E. C., Yao, X. P., Zhang, H. W., Lau, W. Y., Fu, X. H. et al. (2010). Vitamin analogues in chemoprevention of hepatocellular carcinoma after resection or ablation–a systematic review and meta-analysis. Asian J Surg., 33, 120-126.

Chung, V. C., Wu, X., Hui, E. P., Ziea, E. T., Ng, B. F., Ho, R. S. et al. (2015). Effectiveness of Chinese herbal medicine for cancer palliative care: overview of systematic reviews with meta-analyses. Sci.Rep., 5, 18111.

Chung, V. C., Wu, X., Lu, P., Hui, E. P., Zhang, Y., Zhang, A. L. et al. (2016). Chinese Herbal Medicine for Symptom Management in Cancer Palliative Care: Systematic Review And Meta-analysis. Medicine (Baltimore), 95, e2793.

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Dasari, S., Kathera, C., Janardhan, A., Praveen, K. A., & Viswanath, B. (2017). Surfacing role of probiotics in cancer prophylaxis and therapy: A systematic review. Clin.Nutr., 36, 1465-1472.

Datta, M. & Schwartz, G. G. (2013). Calcium and vitamin D supplementation and loss of bone mineral density in women undergoing breast cancer therapy. Crit Rev.Oncol.Hematol., 88, 613-624.

de Aguiar Pastore, S. J., Emilia de Souza, F. M., & Waitzberg, D. L. (2015). Omega-3 supplements for patients in chemotherapy and/or radiotherapy: A systematic review. Clin.Nutr., 34, 359-366.

Dedong, C., Huilin, X., Anbing, H., Ximing, X., & Wei, G. (2016). The Effect of ShenQi FuZheng Injection in Combination with Chemotherapy versus Chemotherapy Alone on the Improvement of Efficacy and Immune Function in Patients with Advanced Non-Small Cell Lung Cancer: A Meta-Analysis. PLoS One, 11, e0152270.

Deng, B., Jia, L., & Cheng, Z. (2016). Radix Astragali-Based Chinese Herbal Medicine for Oxaliplatin-Induced Peripheral Neuropathy: A Systematic Review and Meta-Analysis. Evid.Based Complement Alternat.Med., 2016, 2421876.

Deng, B., Deng, C., & Cheng, Z. (2017). Chinese Herbal Extractions for Relieving Radiation Induced Lung Injury: A Systematic Review and Meta-Analysis. Evid.Based Complement Alternat.Med., 2017, 2141645.

Deng, G. E., Rausch, S. M., Jones, L. W., Gulati, A., Kumar, N. B., Greenlee, H. et al. (2013). Complementary therapies and integrative medicine in lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 143, e420S-e436S.

Derksen, T. M., Bours, M. J., Mols, F., & Weijenberg, M. P. (2017). Lifestyle-Related Factors in the Self-Management of Chemotherapy-Induced Peripheral Neuropathy in Colorectal Cancer: A Systematic Review. Evid.Based Complement Alternat.Med., 2017, 7916031.

Diorio, C., Salena, K., Ladas, E. J., Lam, C. G., Afungcwhi, G. M., Njuguna, F. et al. (2017). Traditional and complementary medicine used with curative intent in childhood cancer: A systematic review. Pediatr Blood Cancer, 64.

Dong, J., Su, S. Y., Wang, M. Y., & Zhan, Z. (2010). Shenqi fuzheng, an injection concocted from Chinese medicinal herbs, combined with platinum-based chemotherapy for advanced non-small cell lung cancer: a systematic review. J Exp.Clin.Cancer Res., 29, 137.

Dong, J. Y. & Qin, L. Q. (2011). Soy isoflavones consumption and risk of breast cancer incidence or recurrence: a meta-analysis of prospective studies. Breast Cancer Res.Treat., 125, 315-323.

Drewe, J., Bucher, K. A., & Zahner, C. (2015). A systematic review of non-hormonal treatments of vasomotor symptoms in climacteric and cancer patients. Springerplus, 4, 65.

Dugoua, J. J., Wu, P., Seely, D., Eyawo, O., & Mills, E. (2010). Astragalus-containing Chinese herbal combinations for advanced non-small-cell lung cancer: a meta-analysis of 65 clinical trials enrolling 4751 patients. Lung Cancer (Auckl.), 1, 85-100.

Dulai, P. S., Singh, S., Marquez, E., Khera, R., Prokop, L. J., Limburg, P. J. et al. (2016). Chemoprevention of colorectal cancer in individuals with previous colorectal neoplasia: systematic review and network meta-analysis. BMJ, 355, i6188.

Eliza, W. L., Fai, C. K., & Chung, L. P. (2012). Efficacy of Yun Zhi (Coriolus versicolor) on survival in cancer patients: systematic review and meta-analysis. Recent Pat Inflamm.Allergy Drug Discov., 6, 78-87.

Eltweri, A. M., Thomas, A. L., Metcalfe, M., Calder, P. C., Dennison, A. R., & Bowrey, D. J. (2017). Potential applications of fish oils rich in omega-3 polyunsaturated fatty acids in the management of gastrointestinal cancer. Clin.Nutr., 36, 65-78.

Ferreira, E. B., Vasques, C. I., Gadia, R., Chan, R. J., Guerra, E. N., Mezzomo, L. A. et al. (2017). Topical interventions to prevent acute radiation dermatitis in head and neck cancer patients: a systematic review. Support.Care Cancer, 25, 1001-1011.

Finnegan-John, J., Molassiotis, A., Richardson, A., & Ream, E. (2013). A systematic review of complementary and alternative medicine interventions for the management of cancer-related fatigue. Integr.Cancer Ther., 12, 276-290.

Flower, G., Fritz, H., Balneaves, L. G., Verma, S., Skidmore, B., Fernandes, R. et al. (2014). Flax and Breast Cancer: A Systematic Review. Integr.Cancer Ther., 13, 181-192.

French Speaking Society of Clinical Nutrition and Metabolism (SFNEP) (2014). Clinical nutrition guidelines of the French Speaking Society of Clinical Nutrition and Metabolism (SFNEP): Summary of recommendations for adults undergoing non-surgical anticancer treatment. Dig.Liver Dis., 46, 667-674.

Fritz, H., Kennedy, D., Fergusson, D., Fernandes, R., Doucette, S., Cooley, K. et al. (2011). Vitamin A and retinoid derivatives for lung cancer: a systematic review and meta analysis. PLoS One, 6, e21107.

Fritz, H., Kennedy, D., Fergusson, D., Fernandes, R., Cooley, K., Seely, A. et al. (2011). Selenium and lung cancer: a systematic review and meta analysis. PLoS One, 6, e26259.

Fritz, H., Seely, D., Flower, G., Skidmore, B., Fernandes, R., Vadeboncoeur, S. et al. (2013). Soy, red clover, and isoflavones and breast cancer: a systematic review. PLoS One, 8, e81968.

Fritz, H., Seely, D., McGowan, J., Skidmore, B., Fernandes, R., Kennedy, D. A. et al. (2014). Black cohosh and breast cancer: a systematic review. Integr.Cancer Ther., 13, 12-29.

Fritz, H., Flower, G., Weeks, L., Cooley, K., Callachan, M., McGowan, J. et al. (2014). Intravenous Vitamin C and Cancer: A Systematic Review. Integr.Cancer Ther., 13, 280-300.

Fritz, H., Kennedy, D. A., Ishii, M., Fergusson, D., Fernandes, R., Cooley, K. et al. (2015). Polysaccharide K and Coriolus versicolor extracts for lung cancer: a systematic review. Integr.Cancer Ther., 14, 201-211.

Fu, F., Wan, Y., & Wu, T. (2014). Kanglaite injection combined with hepatic arterial intervention for unresectable hepatocellular carcinoma: a meta-analysis. J Cancer Res.Ther., 10 Suppl 1, 38-41.

Gao, J. J., Song, P. P., Qi, F. H., Kokudo, N., Qu, X. J., & Tang, W. (2012). Evidence-based research on traditional Japanese medicine, Kampo, in treatment of gastrointestinal cancer in Japan. Drug Discov.Ther., 6, 1-8.

Ge, L., Wang, Y. F., Tian, J. H., Mao, L., Zhang, J., Zhang, J. H. et al. (2016). Network meta-analysis of Chinese herb injections combined with FOLFOX chemotherapy in the treatment of advanced colorectal cancer. J Clin.Pharm.Ther., 41, 383-391.

Gerber, M. (2012). Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies. Br.J Nutr., 107 Suppl 2, S228-S239.

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Jia, Y., Du, H., Yao, M., Cui, X., Shi, Q., Wang, Y. et al. (2015). Chinese herbal medicine for myelosuppression induced by chemotherapy or radiotherapy: a systematic review of randomized controlled trials. Evid.Based Complement Alternat.Med., 2015, 690976.

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Jiang, H., Zhang, H., Hu, X., & Ma, J. (2015). A meta-analysis of Shenqi Fuzheng combined with radiation in the treatment of nonsmall cell lung cancer. J Cancer Res.Ther., 11 Suppl 1, C101-C103.

Jiang, X., Hidru, T. H., Zhang, Z., Bai, Y., Kong, L., & Li, X. (2017). Evidence of elemene injection combined radiotherapy in lung cancer treatment among patients with brain metastases: A systematic review and meta-analysis. Medicine (Baltimore), 96, e6963.

Jin, X., Ruiz, B. J., Sze, D. M., & Chan, G. C. (2016). Ganoderma lucidum (Reishi mushroom) for cancer treatment. Cochrane Database Syst.Rev., 4, CD007731.

Jo, S. J., Shin, H., Jo, S., Kwon, O., & Myung, S. K. (2015). Prophylactic and therapeutic efficacy of pyridoxine supplements in the management of hand-foot syndrome during chemotherapy: a meta-analysis. Clin.Exp.Dermatol., 40, 260-270.

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