The berries on the top

Abstract

BACKGROUND:

Berries are important sources of crucial dietary components such as vitamins and minerals, as well as various phytonutrients that may be potentially beneficial to human health and could be used against chronic diseases including cancer and cardiovascular disorders.

OBJECTIVE:

The current study aimed to identify and analyze the 100 most cited papers related to berry research.

METHODS:

The Scopus database was searched to extract data. Two of the authors independently evaluated the manuscripts for relevance. Bibliometric data, including citation count, were analyzed together with the words in the titles and abstracts of the 100 most cited berry-related papers.

RESULTS:

Seventy-two of the 100 most cited papers were research articles. Most of them were published during the 2000s, and related to subject areas of agricultural and biological sciences (n = 64), biochemistry, genetics and molecular biology (n = 35), chemistry (n = 29), medicine (n = 24), and nursing (n = 10). Journal of Agricultural and Food Chemistry was the dominating choice of publication outlet (n = 26).

CONCLUSIONS:

Antioxidant and anticancer benefits appeared to be the major subject terms. Berries that were mentioned in at least 10% of the 100 papers were strawberry, blueberry, cranberry, raspberry, blackberry, bilberry, and grape berry. The review could provide a valuable guide for designing future studies based on berries, berry extracts, and bioactive compounds.

Keywords

Antioxidant berry bibliometrics chemistry citation analysis food science highly cited paper Scopus VOSviewer

1 Introduction

Berries contain not only crucial dietary components such as vitamins and minerals, but also a wide range of phytonutrients that may be potentially beneficial to human health [1] and could be used against chronic diseases including cancer and heart disorders [2]. For instance, the consumption of berry may enhance the human liver function in terms of reducing the alanine aminotransferase (ALAT) values [3], increasing high-density lipoprotein (HDL) cholesterol, and reducing blood pressure, all of which could help reduce systemic inflammation and risk of cardiovascular and metabolic diseases [4]. Moreover, it was reported that dietary consumption of strawberry could increase the plasma antioxidant capacity [5, 6] and improve the insulin sensitivity [7]. There have been numerous comprehensive reviews on the phenolic contents of berries, including phenolic acids, tannins, lignans, stilbenes, and flavonoids [8], and their antioxidant, anticancer, anti-inflammatory as well as neuroprotective properties [9, 10].

Research on berries could be traced back as early as in the mid–18th century, according to Scopus literature database (https://www-scopus-com-s.web.bisu.edu.cn). Interestingly, the earliest publications seemed to focus on berry poisoning and associated deaths [11 –13], instead of the current focus on the health benefits of consuming berries as introduced above. Undoubtedly, there have been numerous publications on berry ripening; the berry research field, after over two centuries of development, has literally ripened. It is worthwhile to identify the most impactful publications on berries and give a brief overview of them. Therefore, in the current study, we aimed to identify and analyze the 100 most cited papers on berries. Besides, the aim was to identify also the hot topics, prominent authors and countries contributing to these publications, as well as the most popular berries that were investigated in these publications. Last but not least, as multiple studies have indicated a higher journal impact factor as well as defined journal specialties would lead to an increased citation count [14 –16]. We tested if such association existed within the 100 most cited berry-related papers, and hypothesized the existence of a positive correlation between the journal impact factor and the paper citation count (both total and adjusted counts).

2 Materials and methods

2.1 Data source

Bibliometric data were extracted from Scopus, an online multidisciplinary, bibliographic and citation database launched in 2004 and hosted by Elsevier. Upon a preliminary search, we have found that many of the highly cited papers involving the word “berry” were related to Berry’s phase or Berry’s conjecture which are the concepts used in physics, but certainly not related to the berry fruits. To systematically exclude these irrelevant papers, in September 2018, we searched Scopus to identify papers with the following string: TITLE-ABS-KEY (“berry” OR “berry*” OR “berries” OR “berries*”) AND NOT (“berry’s phase” OR “berry phase” OR “berry’s conjecture” OR “berry conjecture” OR “berry’s curvature” OR “berry curvature”). This string searched for papers that mentioned berry or berries in their titles, abstracts or keywords as fruits, but not Berry as a part of terms used in physics named after a scientist.

The identified papers were sorted out by citation count in descending order. Two of the authors (AWKY and AGA) independently evaluated the manuscripts for relevance and compiled the list of 100 most cited papers. We did not place any additional restrictions on the search, such as year of publication and other parameters.

2.2 Data extraction

The 100 most cited papers were evaluated and recorded for: (1) publication year; (2) journal title; (3) 2017 journal impact factor (released by Clarivate Analytics in InCites Journal Citation Reports 2018); (4) total citation count; (5) adjusted citation count (i.e., citation count per year since publication); (6) authorship; and (7) manuscript type.

Meanwhile, Pearson’s correlation tests were conducted in SPSS 25.0 (IBM, New York, USA) to evaluate if there existed a correlation between the citation counts (total / adjusted) of the 100 most cited papers and journal impact factor or number of authors. Test results with p < 0.05 were considered significant.

2.3 Term map

The software VOSviewer was utilized to extract and analyze words that appeared in the titles and abstracts of these 100 most cited papers [17], and visualize them with a bubble map. Each bubble represents a term or phrase. The bubble size indicates how often the word appeared among the 100 manuscripts (binary counting was used, which implied that multiple appearances in a single paper counted as one). The bubble color indicates the averaged citation count received by manuscripts involving the term. Two bubbles are nearer to each other if the two terms co-occurred in manuscripts more often. The term map visualizes terms that appeared in at least two of the 100 papers.

3 Results and discussion

The search resulted in 21,508 papers. The 100 most cited berry-related papers are listed in Table 1. They were mainly research articles (n = 72) and reviews (n = 21), with a few conference papers (n = 6) and a short survey (n = 1). All 100 papers were written in English, most of which published during the 2000s (Fig. 1), and were related to subject areas of agricultural and biological sciences (n = 64), biochemistry, genetics and molecular biology (n = 35), chemistry (n = 29), medicine (n = 24), and nursing (n = 10). These 100 papers listed 1 to 17 authors (mean±SD: 4.4±3.2), and were published in journals with impact factor ranging from no impact factor value to 79.258 (mean±SD: 4.882±7.860).

Fig.1

Distribution of the 100 most cited berry-related papers across the publication years. Year 2007 was the most influential year when 16 out of the 100 most cited berry-related papers were published.

Table 1

The list of 100 most cited berry-related papers

Rank	Reference	Impact factor 2017 (IF)	Total citation count	Adjusted citation count
1	Kähkönen MP, Hopia AI, Vuorela HJ, Rauha J, Pihlaja K, Kujala TS, Heinonen M. Antioxidant activity of plant extracts containing phenolic compounds. J Agric Food Chem 1999;47(10):3954–62.	3.412	2190	115.3
2	Aggarwal BB, Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol 2006;71(10):1397–421.	4.235	1196	99.7
3	Frémont L. Minireview: Biological effects of resveratrol. Life Sci 2000;66(8):663–73.	3.234	1119	62.2
4	Adlercreutz H, Mazur W. Phyto-oestrogens and western diseases. Ann Med 1997;29(2):95–120.	3.007	1029	49.0
5	Aggarwal BB, Bhardwaj A, Aggarwal RS, Seeram NP, Shishodia S, Takada Y. Role of resveratrol in prevention and therapy of cancer: Preclinical and clinical studies. Anticancer Res 2004;24(5 A):2783–840.	1.865	985	70.4
6	Clifford MN. Chlorogenic acids and other cinnamates - nature, occurrence and dietary burden. J Sci Food Agric 1999;79(3):362–72.	2.379	896	47.2
7	Leuning R. A critical appraisal of a combined stomatal-photosynthesis model for C₃ plants. Plant Cell Environ 1995;18(4):339–55.	5.415	896	39.0
8	Pellegrini N, Serafini M, Colombi B, Del Rio D, Salvatore S, Bianchi M, Brighenti F. Total antioxidant capacity of plant foods, beverages and oils consumed in Italy assessed by three different in vitro assays. J Nutr 2003;133(9):2812–9.	4.398	873	58.2
9	Prior RL, Cao G, Martin A, Sofic E, McEwen J, O’Brien C, Lischner N, Ehlenfeldt M, Kalt W, Krewer G, Mainland CM. Antioxidant capacity as influenced by total phenolic and anthocyanin content, maturity, and variety of Vaccinium species. J Agric Food Chem 1998;46(7):2686–93.	3.412	867	43.4
10	Lindström J, Tuomilehto J. The diabetes risk score: A practical tool to predict type 2 diabetes risk. Diabetes Care 2003;26(3):725–31.	13.397	847	56.5
11	Wang SY, Lin H-. Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage. J Agric Food Chem 2000;48(2):140–6.	3.412	812	45.1
12	Fukumoto LR, Mazza G. Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem 2000;48(8):3597–604.	3.412	798	44.3
13	Del Rio D, Rodriguez-Mateos A, Spencer JPE, Tognolini M, Borges G, Crozier A. Dietary (poly)phenolics in human health: Structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal 2013;18(14):1818–92.	6.530	777	155.4
14	Halvorsen BL, Holte K, Myhrstad MCW, Barikmo I, Hvattum E, Remberg SF, Wold A-, Haffner K, Baugerød H, Andersen LF, Moskaug O, Jacobs Jr. DR, Blomhoff R. A systematic screening of total antioxidants in dietary plants. J Nutr 2002;132(3):461–71.	4.398	740	46.3
15	Kähkönen MP, Hopia AI, Heinonen M. Berry phenolics and their antioxidant activity. J Agric Food Chem 2001;49(8):4076–82.	3.412	678	39.9
16	Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: A growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Protection 2004;67(10):2342–53.	1.510	663	47.4
17	Adlercreutz H. Western diet and western diseases: Some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Invest 1990;50(s201):3–23.	1.498	627	22.4
18	Moyer RA, Hummer KE, Finn CE, Frei B, Wrolstad RE. Anthocyanins, phenolics, and antioxidant capacity in diverse small fruits: Vaccinium, Rubus, and Ribes. J Agric Food Chem 2002;50(3):519–25.	3.412	625	39.1
19	Rauha J-, Remes S, Heinonen M, Hopia A, Kähkönen M, Kujala T, Pihlaja K, Vuorela H, Vuorela P. Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int J Food Microbiol 2000;56(1):3–12.	3.451	619	34.4
20	Kumar S, Pandey AK. Chemistry and biological activities of flavonoids: An overview. Sci World J 2013;2013 : 162750.	No IF	618	123.6
21	Herman C, Adlercreutz T, Goldin BR, Gorbach SL, Hockerstedt KAV, Watanabe S, Hamalainen EK, Markkanen MH, Makela TH, Wahala KT, Hase TA, Fotsis T. Soybean phytoestrogen intake and cancer risk. J Nutr 1995;125(3 SUPPL.):757S–70 S.	4.398	578	25.1
22	Spayd SE, Tarara JM, Mee DL, Ferguson JC. Separation of sunlight and temperature effects on the composition of Vitis vinifera cv. merlot berries. Am J Enol Vitic 2002;53(3):171–82.	1.765	535	33.4
23	Reid KE, Olsson N, Schlosser J, Peng F, Lund ST. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 2006;6 : 27.	3.930	530	44.2
24	Puupponen-Pimiä R, Nohynek L, Meier C. Antimicrobial properties of phenolic compounds from berries. J Appl Microbiol 2001;90(4):494–507.	2.160	520	30.6
25	Adlercreutz H. Phytoestrogens: Epidemiology and a possible role in cancer protection. Environ Health Perspect 1995;103(SUPPL. 7):103–12.	8.309	504	21.9
26	Zafra-Stone S, Yasmin T, Bagchi M, Chatterjee A, Vinson JA, Bagchi D. Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol Nutr Food Res 2007;51(6):675–83.	5.151	497	45.2
27	Häkkinen SH, Kärenlampi SO, Heinonen IM, Mykkänen HM, Törronen AR. Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries. J Agric Food Chem 1999;47(6):2274–9.	3.412	488	25.7
28	Zheng W, Wang SY. Oxygen radical absorbing capacity of phenolics in blueberries, cranberries, chokeberries, and lingonberries. J Agric Food Chem 2003;51(2):502–9.	3.412	471	31.4
29	Boss PK, Davies C, Robinson SP. Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv shiraz grape berries and the implications for pathway regulation. Plant Physiol 1996;111(4):1059–66.	5.949	458	20.8
30	Heinonen IM, Meyer AS, Frankel EN. Antioxidant activity of berry phenolics on human low-density lipoprotein and liposome oxidation. J Agric Food Chem 1998;46(10):4107–12.	3.412	456	22.8
31	Ozgen M, Reese RN, Tulio Jr. AZ, Scheerens JC, Miller AR. Modified 2,2– azino-bis– 3– ethylbenzothiazoline– 6– sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2^′– diphenyl– 1– picrylhydrazyl (DPPH) methods. J Agric Food Chem 2006;54(4):1151–7.	3.412	446	37.2
32	Seeram NP, Adams LS, Zhang Y, Lee R, Sand D, Scheuller HS, Heber D. Blackberry, black raspberry, blueberry, cranberry, red raspberry, and strawberry extracts inhibit growth and stimulate apoptosis of human cancer cells in vitro. J Agric Food Chem 2006;54(25):9329–39.	3.412	440	36.7
33	Wu X, Gu L, Prior RL, McKay S. Characterization of anthocyanins and proanthocyanidins in some cultivars of Ribes, Aronia, and Sambucus and their antioxidant capacity. J Agric Food Chem 2004;52(26):7846–56.	3.412	435	31.1
34	Kennedy JA, Jones GP. Analysis of proanthocyanidin cleavage products following acid-catalysis in the presence of excess phloroglucinol. J Agric Food Chem 2001;49(4):1740–6.	3.412	429	25.2
35	De La Lastra CA, Villegas I. Resveratrol as an anti-inflammatory and anti-aging agent: Mechanisms and clinical implications. Mol Nutr Food Res 2005;49(5):405–30.	5.151	416	32.0
36	Häkkinen S, Heinonen M, Kärenlampi S, Mykkänen H, Ruuskanen J, Törrönen R. Screening of selected flavonoids and phenolic acids in 19 berries. Food Res Int 1999;32(5):345–53.	3.520	400	21.1
37	Wu X, Prior RL. Systematic identification and characterization of anthocyanins by HPLC-ESI-MS/MS in common foods in the United States: Fruits and berries. J Agric Food Chem 2005;53(7):2589–99.	3.412	396	30.5
38	Hanhineva K, Törrönen R, Bondia-Pons I, Pekkinen J, Kolehmainen M, Mykkänen H, Poutanen K. Impact of dietary polyphenols on carbohydrate metabolism. Int J Mol Sci 2010;11(4):1365–402.	3.687	395	49.4
39	Attele AS, Zhou Y-, Xie J-, Wu JA, Zhang L, Dey L, Pugh W, Rue PA, Polonsky KS, Yuan C-. Antidiabetic effects of Panax ginseng berry extract and the identification of an effective component. Diabetes 2002;51(6):1851–8.	7.273	391	24.4
40	Gautier-Hion A, Duplantier J-, Quris R, Feer F, Sourd C, Decoux J-, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay J-. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 1985;65(3):324–37.	3.127	389	11.8
41	Gamfeldt L, Snäll T, Bagchi R, Jonsson M, Gustafsson L, Kjellander P, Ruiz-Jaen MC, Fröberg M, Stendahl J, Philipson CD, Mikusiński G, Andersson E, Westerlund B, Andrén H, Moberg F, Moen J, Bengtsson J. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 2013;4 : 1340.	12.353	383	76.6
42	Downey MO, Dokoozlian NK, Krstic MP. Cultural practice and environmental impacts on the flavonoid composition of grapes and wine: A review of recent research. Am J Enol Vitic 2006;57(3):257–68.	1.765	377	31.4
43	Pantelidis GE, Vasilakakis M, Manganaris GA, Diamantidis G. Antioxidant capacity, phenol, anthocyanin and ascorbic acid contents in raspberries, blackberries, red currants, gooseberries and cornelian cherries. Food Chem 2007;102(3):777–83.	4.946	370	33.6
44	Wang SY, Jiao H. Scavenging capacity of berry crops on superoxide radicals, hydrogen peroxide, hydroxyl radical’s, and singlet oxygen. J Agric Food Chem 2000;48(11):5677–84.	3.412	367	20.4
45	Mikkilä V, Räsänen L, Raitakari OT, Pietinen P, Viikari J. Consistent dietary patterns identified from childhood to adulthood: The cardiovascular risk in young finns study. Br J Nutr 2005;93(6):923–31.	3.657	361	27.8
46	Häkkinen SH, Törrönen AR. Content of flavonols and selected phenolic acids in strawberries and Vaccinium species: Influence of cultivar, cultivation site and technique. Food Res Int 2000;33(6):517–24.	3.520	361	20.1
47	Harikumar KB, Aggarwal BB. Resveratrol: A multitargeted agent for age-associated chronic diseases. Cell Cycle 2008;7(8):1020–37.	3.304	356	35.6
48	Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K. Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 2007;58(8):1935–45.	5.354	356	32.4
49	Alarcón De La Lastra C, Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: Mechanisms and clinical implications. Biochem Soc Trans 2007;35(5):1156–60.	3.394	355	32.3
50	Montonen J, Knekt P, Järvinen R, Aromaa A, Reunanen A. Whole-grain and fiber intake and the incidence of type 2 diabetes. Am J Clin Nutr 2003;77(3):622–9.	6.549	353	23.5
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52	Bell S-, Henschke PA. Implications of nitrogen nutrition for grapes, fermentation and wine. Austr J Grape Wine Res 2005;11(3):242–95.	1.913	347	26.7
53	Dimitrios B. Sources of natural phenolic antioxidants. Trends Food Sci Technol 2006;17(9):505–12.	6.609	342	28.5
54	Bergqvist J, Dokoozlian N, Ebisuda N. Sunlight exposure and temperature effects on berry growth and composition of cabernet sauvignon and grenache in the central San Joaquin valley of California. Am J Enol Vitic 2001;52(1):1–7.	1.765	333	19.6
55	Rimando AM, Kalt W, Magee JB, Dewey J, Ballington JR. Resveratrol, pterostilbene, and piceatannol in vaccinium berries. J Agric Food Chem 2004;52(15):4713–9.	3.412	327	23.4
56	McGhie TK, Walton MC. The bioavailability and absorption of anthocyanins: Towards a better understanding. Mol Nutr Food Res 2007;51(6):702–13.	5.151	325	29.5
57	Mattivi F, Guzzon R, Vrhovsek U, Stefanini M, Velasco R. Metabolite profiling of grape: Flavonols and anthocyanins. J Agric Food Chem 2006;54(20):7692–702.	3.412	323	26.9
58	Walker AR, Lee E, Bogs J, McDavid DAJ, Thomas MR, Robinson SP. White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J 2007;49(5):772–85.	5.775	319	29.0
59	She Q, Bode AM, Ma W, Chen N, Dong Z. Resveratrol-induced activation of p53 and apoptosis is mediated by extracellular-signal-regulated protein kinases and p38 kinase. Cancer Res 2001;61(4):1604–10.	9.130	317	18.6
60	Määttä-Riihinen KR, Kamal-Eldin A, Törrönen AR. Identification and quantification of phenolic compounds in berries of Fragaria and Rubus species (family Rosaceae). J Agric Food Chem 2004;52(20):6178–87.	3.412	312	22.3
61	Bishayee A. Cancer prevention and treatment with resveratrol: From rodent studies to clinical trials. Cancer Prev Res 2009;2(5):409–18.	4.021	311	34.6
62	Downey MO, Harvey JS, Robinson SP. The effect of bunch shading on berry development and flavonoid accumulation in shiraz grapes. Austr J Grape Wine Res 2004;10(1):55–73.	1.913	310	22.1
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66	Jones GV, Davis RE. Climate influences on grapevine phenology, grape composition, and wine production and quality for bordeaux, france. Am J Enol Vitic 2000;51(3):249–61.	1.765	303	16.8
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70	Seeram NP, Momin RA, Nair MG, Bourquin LD. Cyclooxygenase inhibitory and antioxidant cyanidin glycosides in cherries and berries. Phytomedicine 2001;8(5):362–9.	3.610	299	17.6
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73	Katsube N, Iwashita K, Tsushida T, Yamaki K, Kobori M. Induction of apoptosis in cancer cells by bilberry (Vaccinium myrtillus) and the anthocyanins. J Agric Food Chem 2003;51(1):68–75.	3.412	294	19.6
74	Miller HE, Rigelhof F, Marquart L, Prakash A, Kanter M. Antioxidant content of whole grain breakfast cereals, fruits and vegetables. J Am Coll Nutr 2000;19 : 312S– 9 S.	2.175	294	16.3
75	Mazza G, Kay CD, Cottrell T, Holub BJ. Absorption of anthocyanins from blueberries and serum antioxidant status in human subjects. J Agric Food Chem 2002;50(26):7731–7.	3.412	293	18.3
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79	Heinonen IM, Lehtonen PJ, Hopia AI. Antioxidant activity of berry and fruit wines and liquors. J Agric Food Chem 1998;46(1):25–31.	3.412	289	14.5
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82	Aziz MH, Kumar R, Ahmad N. Cancer chemoprevention by resveratrol: In vitro and in vivo studies and the underlying mechanisms (review). Int J Oncol 2003;23(1):17–28.	3.333	283	18.9
83	Herwaldt BL, Ackers M-. An outbreak in 1996 of cyclosporiasis associated with imported raspberries. New Engl J Med 1997;336(22):1548–56.	79.258	283	13.5
84	Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP. The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 2007;143(3):1347–61.	5.949	282	25.6
85	Bhardwaj A, Sethi G, Vadhan-Raj S, Bueso-Ramos C, Takada Y, Gaur U, Nair AS, Shishodia S, Aggarwal BB. Resveratrol inhibits proliferation, induces apoptosis, and overcomes chemoresistance through down-regulation of STAT3 and nuclear factor-κB-regulated antiapoptotic and cell survival gene products in human multiple myeloma cells. Blood 2007;109(6):2293–302.	15.132	281	25.5
86	Cacace JE, Mazza G. Mass transfer process during extraction of phenolic compounds from milled berries. J Food Eng 2003;59(4):379–89.	3.197	278	18.5
87	Dragland S, Senoo H, Wake K, Holte K, Blomhoff R. Several culinary and medicinal herbs are important sources of dietary antioxidants. J Nutr 2003;133(5):1286–90.	4.398	278	18.5
88	Wolfe KL, Kang X, He X, Dong M, Zhang Q, Liu RH. Cellular antioxidant activity of common fruits. J Agric Food Chem 2008;56(18):8418–26.	3.412	276	27.6
89	Bogs J, Downey MO, Harvey JS, Ashton AR, Tanner GJ, Robinson SP. Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiol 2005;139(2):652–63.	5.949	276	21.2
90	Castellarin SD, Matthews MA, Di Gaspero G, Gambetta GA. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 2007;227(1):101–12.	3.249	275	25.0
91	Seeram NP. Berry fruits: Compositional elements, biochemical activities, and the impact of their intake on human health, performance, and disease. J Agric Food Chem 2008;56(3):627–9.	3.412	272	27.2
92	Singh M, Arseneault M, Sanderson T, Murthy V, Ramassamy C. Challenges for research on polyphenols from foods in Alzheimer’s disease: Bioavailability, metabolism, and cellular and molecular mechanisms. J Agric Food Chem 2008;56(13):4855–73.	3.412	270	27.0
93	Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G. Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 2007;30(11):1381–99.	5.415	270	24.5
94	Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR. Transcriptomic and metabolite analyses of cabernet sauvignon grape berry development. BMC Genomics 2007;8 : 429.	3.730	269	24.5
95	Park EJ, Pezzuto JM. Botanicals in cancer chemoprevention. Cancer Metastasis Rev 2002;21(3–4):231–55.	6.081	269	16.8
96	Ojeda H, Andary C, Kraeva E, Carbonneau A, Deloire A. Influence of pre- and postveraison water deficit on synthesis and concentration of skin phenolic compounds during berry growth of Vitis vinifera cv. shiraz. Am J Enol Vitic 2002;53(4):261–7.	1.765	269	16.8
97	Mazur W. Phytoestrogen content in foods. Bailliere’s Clin Endocrinol Metab 1998;12(4):729–42.	No IF	266	13.3
98	Adlercreutz H. Lignans and human health. Crit Rev Clin Lab Sci 2007;44(5–6):483–525.	6.481	265	24.1
99	Neto CC. Cranberry and blueberry: Evidence for protective effects against cancer and vascular diseases. Mol Nutr Food Res 2007;51(6):652–64.	5.151	264	24.0
100	Hannum SM. Potential impact of strawberries on human health: A review of the science. Crit Rev Food Sci Nutr 2004;44(1):1–17.	6.015	264	18.9

3.1 Citation count

The citation count of these 100 papers ranged from 264 to 2,190 (mean±SD: 454.1±276.7). The adjusted citation count (i.e., citation count per year since publication) ranged from 10.7 to 155.4 (mean±SD: 33.0±22.6). In terms of total citation count, Kähkönen et al. published a top-ranked article that reported the antioxidant activity of plant extracts, containing phenolic compounds, which were particularly abundant in aronia and crowberry [18]. In terms of adjusted citation count, the top-ranked paper was a review, published by Del Rio et al. on availability and evidence of benefits of dietary polyphenolics such as anthocyanins from blueberries, blackberries and strawberries against chronic diseases [19].

3.2 Major contributors

The papers were contributed by 160 authors, affiliated with 149 institutions distributed among 25 countries / territories. The five most prolific authors for the most cited papers were Simon P. Robinson from Commonwealth Scientific and Industrial Research Organisation (CSIRO) Plant Industry in Australia (n = 5); Herman Adlercreutz, Marina Heinonen from the University of Helsinki in Finland, Rune Blomhoff and Kari Holte from the University of Oslo in Norway, Navindra P. Seeram from the University of Rhode Island in the United States, and Bharat B. Aggarwal currently affiliated with the Inflammation Research Center in the United States of America (each n = 4, equally ranked second).

The five most prolific institutions were the University of Helsinki (n = 15), the United States Department of Agriculture (USDA, n = 6), the University of Eastern Finland (n = 6), Cooperative Research Centre for Viticulture (Australia, n = 5), and Agriculture and Agri-Food Canada (n = 5). The United States of America has contributed to 38 of these 100 papers, followed by Finland (n = 20), Australia (n = 9), Canada (n = 8), and Japan (n = 6). Perhaps unsurprisingly, the dominance of the United States of America was similar to other research fields such as neuroimaging [20], public health [21], general neuroscience [22 –24], and nutritional neuroscience [25]. This could be potentially explained by the large amount of money invested by private sector into research and development, as well as the large number of PhD students and full-time researchers in the nation [26]. Here in berry research, however, the contribution by Finland was significantly higher than its contribution to the highly cited manuscripts dealing with related fields such as ethnopharmacology [27], phytochemistry concerning cancer [28], and nutraceuticals and functional foods [29]. In fact, berries were identified as important sources of flavonoid intake for Finnish people [30]. This might have hinted an ethnobotanical reason, which is worth to be further investigated. Regarding journals, Journal of Agricultural and Food Chemistry was the dominating choice of publication outlet (n = 26), followed by American Journal of Enology and Viticulture (n = 6). The rest of the journals have each contributed to less than 5% of the 100 most cited berry-related papers. Such dominance by a single most prolific journal is similar to the situation of the 100 most cited papers in ethnopharmacology (Journal of Ethnopharmacology, 17%) [27] but not in nutraceuticals and functional foods field [29].

3.3 Relationship between citation count and author number or journal impact factor

Total citation count and adjusted citation count did not have significant correlation with author number (r = 0.031, p = 0.760; r = 0.135, p = 0.181) or journal impact factor (r = –0.073, p = 0.469; r = –0.065, p = 0.522). Meanwhile, total citation count was positively correlated with adjusted citation count (r = 0.695, p < 0.001).

3.4 Term map

A term map was generated to visualize the words in the titles and abstracts of the 100 papers. There were 731 terms that appeared in two or more of the 100 papers, covering various basic science aspects such as antioxidant and angiogenesis, which in turn might influence carcinogenesis and some chronic diseases (Fig. 2). These foci seemed to have formed the cornerstones of the most cited berry research. Several molecules have 500 + citations per manuscript (Fig. 3), namely trihydroxystilbene (n = 2, citations per paper = 737), isoflavonoid glycoside (n = 3, citations per paper = 704), carotene (n = 3, citations per paper = 637), ferulic acid (n = 2, citations per paper = 629) and caffeic acid (n = 3, citations per paper = 604), isoflavonoid (n = 4, citations per paper = 594), catechin (n = 3, citations per paper = 584), cinnamic acid (n = 2, citations per paper = 580), procyanidin (n = 2, citations per paper = 557), lignin (n = 6, citations per paper = 545), and ellagic acid (n = 4, citations per paper = 543).

Fig.2

Term map of words from the titles and abstracts of the 100 most cited berry-related papers. There were 731 words or phrases that appeared in at least two papers and hence included in the visualization. Each bubble represents a term or phrase. The bubble size indicates its number of appearance. The bubble color indicates the averaged citation count received by papers containing the term or phrase. Two bubbles are closer to each other if the two terms co-appeared in more papers. It seemed that antioxidant capacity and angiogenesis effect were the two major aspects under investigation that may lead to potential health benefits against cancer and chronic diseases.

Fig.3

Notable representative molecules mentioned by berry-related papers. The respective search name and citation per manuscript are in parenthesis.

Meanwhile, the most frequently mentioned berries were strawberry (n = 18, citations per paper = 423), blueberry (n = 16, citations per paper = 456), cranberry (n = 13, citations per paper = 395), raspberry (n = 12, citations per paper = 485), blackberry (n = 12, citations per paper = 463), bilberry (n = 10, citations per paper = 441), and grape berry (n = 10, citations per paper = 351). However, it should be noted that the studies usually investigated multiple berries species [31 –33], instead of focusing on a single one.

3.5 Study limitations

One potential limitation was that the list is compiled by extracting data from Scopus database only, meaning that manuscripts not listed in Scopus were not included in the current report. Scopus in particular was chosen due to its broader coverage of biomedical literature relative to Web of Science Core Collection, another well-known database that keeps track of citation data [34]. On the other hand, Google Scholar, for example, counts citations from non-academic sources such as websites, and hence was not selected by us for performing the current analysis.

4 Conclusions

A bibliometric analysis was performed to identify the 100 most cited berry-related papers. The Journal of Agricultural and Food Chemistry was the preferred choice of publication outlet. The total citation count and adjusted citation count did not appear to have a significant correlation with the number of authors or the journal impact factor. Antioxidant and anti-cancer benefits seemed to be the major topics. Berries species that were mentioned in at least 10% of the 100 papers were strawberry, blueberry, cranberry, raspberry, blackberry, bilberry, and grape berry.

Conflict of interest

The authors have no conflict of interest to report.

Footnotes

Acknowledgments

Atanas G. Atanasov and Dongdong Wang acknowledge the support by the Polish KNOW (Leading National Research Centre) Scientific Consortium “Healthy Animal—Safe Food,” decision of Ministry of Science and Higher Education No. 05–1/KNOW2/2015 and the HOMING programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund. Milen I. Georgiev gratefully acknowledges the support obtained through the project SusMAPWaste, SMIS 104323, Contract No. 89/09.09.2016, from the Operational Program Competitiveness 2014–2020, project co-financed from the European Regional Development Fund.

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