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Bibliometric review of achachairu (Garcinia humilis): a promising agent for health and future food applications

Revisão bibliométrica do achachairu (Garcinia humilis): um agente promissor para a saúde e futuras aplicações em alimentos

Abstract

The achachairu (Garcinia humilis (Vahl) C.D. Adams) is a Bolivian fruit species that adapts well to tropical and sub-tropical climates and may feasibly be disseminated in other parts of the world. Data from the literature has revealed that both the plant and the fruit exhibited promising compounds for both nutritional and pharmacological purposes. This work aimed to review available publications involving the achachairu (G. humilis) through a bibliometric analysis using data from the Web of Science© (WOS) database. For greater precision and completeness in the research, the filters used included both the scientific nomenclature, and the popular name of the fruit, G. humilis and achachairu, respectively. The data-gathering stage yielded only 29 works containing the terms used in the search. Comprising 25 publications, Brazil was the country having the most records in the database, possibly because its climate is favorable for achachairu cultivation. Among the main research focus areas were attributes related to its chemical structure and pharmacological properties, particularly Guttiferone A, the compound responsible for the gastroprotective, antinociceptive and antiproliferative properties of its fruit, which occurs primarily in its seed. The peel also exhibited a bioactive and antioxidant composition. Thus, these two parts of the fruit, which are considered underutilized, due to the exclusive consumption of the fruit pulp, may have the potential for other purposes. Finally, considering the scarce scientific data regarding this matrix, which has a diversity of positive characteristics for the pharmacological and food industries, this bibliometric analysis revealed an opportunity for further research.

Keywords:
Benzophenone; Guttiferone A; Seed; Antioxidants; Bioflavonoids

Resumo

O achachairu (Garcinia humilis) é uma espécie frutífera boliviana, que apresenta boa adaptação em climas tropicais e subtropicais, podendo, portanto, ser cultivada em diferentes partes do mundo. Os dados da literatura revelam que tanto a planta, em especial o fruto, apresentam compostos promissores para fins nutricionais e farmacológicos. Diante do exposto, o objetivo deste trabalho foi verificar as publicações disponíveis envolvendo o achachairu (Garcinia humilis), por meio de uma análise bibliométrica, utilizando informações da base de dados Web of Science© (WOS). Para uma maior precisão e abrangência na pesquisa, os filtros utilizados incluíram a nomenclatura científica e o nome popular da fruta, Garcinia humilis e achachairu, respectivamente. A etapa de coleta de dados resultou em apenas 29 trabalhos contendo os termos utilizados na busca. Com 25 publicações, o Brasil liderou os registros encontrados, possivelmente devido ao clima favorável do país para o cultivo do achachairu. Entre os principais focos de pesquisa, foram identificados atributos relacionados à estrutura química e às propriedades farmacológicas do fruto, em especial a Gutiferona A, um composto responsável por características gastroprotetoras, antinociceptivas e antiproliferativas, cuja ocorrência é principalmente na semente. A casca do fruto exibiu uma composição bioativa e antioxidante. Assim, verificou-se que essas duas partes do fruto, consideradas subutilizadas devido ao consumo exclusivo da polpa do fruto, podem ter potencial para outras finalidades. Por fim, diante dos escassos dados científicos sobre essa matriz, que possui uma diversidade de características positivas para as indústrias farmacêutica e alimentícia, a análise bibliométrica revelou uma oportunidade para novas pesquisas.

Palavras-chave:
Benzofenona; Gutiferona A; Semente; Antioxidantes; Bioflavonóides

HIGHLIGHTS

• Brazil is the leader in publications on the terms: Garcinia humilis and achachairu

• Guttiferone A stands out in the study focuses on Garcinia humilis and achachairu

• Achachairu seed and peel are promising sources as co-products

1 Introduction

Fruit consumption is gradually increasing, mainly as a result of greater awareness of the health benefits of ingesting it. However, the sensory characteristics of these products also contribute to their nutritional and therapeutic appeal (Ayala-Zavala et al., 2011Ayala-Zavala, J. F., Vega-Vega, V., Rosas-Domínguez, C., Palafoxcarlos, H., Villa-Rodriguez, J. A., Siddiqui, M. D., Dávila-Aviña, J. E., & González-Aguilar, G. A. (2011). Agro-industrial potential of exotic fruit byproducts as a source of food additives. Food Research International, 44(7), 1866-1874. http://dx.doi.org/10.1016/j.foodres.2011.02.021
http://dx.doi.org/10.1016/j.foodres.2011...
; Silva et al., 2014Silva, L. M. R., Figueiredo, E. A. T., Ricardo, N. M. P. S., Vieira, I. G. P., Figueiredo, R. W., Brasil, I. M., & Gomes, C. L. (2014). Quantification of bioactive compounds in pulps and by-products of tropical fruits from Brazil. Food Chemistry, 143, 398-404. PMid:24054258. http://dx.doi.org/10.1016/j.foodchem.2013.08.001
http://dx.doi.org/10.1016/j.foodchem.201...
). In view of these benefits, the consumption of fruits and vegetables is widely recommended to prevent non-communicable chronic illnesses such as type 2 diabetes, obesity, some types of cancer, metabolic syndrome, and cardiovascular inflammatory, as well as intestinal diseases, among others (Anderson & Waters, 2013Anderson, J. W., & Waters, A. R. (2013). Raisin consumption by humans: Effects on glycemia and insulinemia and cardiovascular risk factors. Journal of Food Science, 78(Suppl. 1), 11-17. PMid:23789931. http://dx.doi.org/10.1111/1750-3841.12071
http://dx.doi.org/10.1111/1750-3841.1207...
; Habauzit & Morand, 2012Habauzit, V., & Morand, C. (2012). Evidence for a protective effect of polyphenols-containing foods on cardiovascular health: An update for clinicians. Therapeutic Advances in Chronic Disease, 3(2), 87-106. PMid:23251771. http://dx.doi.org/10.1177/2040622311430006
http://dx.doi.org/10.1177/20406223114300...
; Kundu & Surh, 2013Kundu, J. K., & Surh, Y. J. (2013). Cancer chemopreventive effects of selected dried fruits. In C. Alasalvar & F. Shahidi (Eds.), Dried fruits: Phytochemicals and health effects (pp. 19-51). Oxford: Wiley-Blackwell. http://dx.doi.org/10.1002/9781118464663.ch2.
http://dx.doi.org/10.1002/9781118464663....
; Lever et al., 2014Lever, E., Cole, J., Scott, S. M., Emery, P. W., & Whelan, K. (2014). Systematic review: the effect of prunes on gastrointestinal function. Alimentary Pharmacology & Therapeutics, 40(7), 750-758. PMid:25109788. http://dx.doi.org/10.1111/apt.12913
http://dx.doi.org/10.1111/apt.12913...
; Slavin & Lloyd, 2012Slavin, J. L., & Lloyd, B. (2012). Health benefits of fruits and vegetables. Advances in Nutrition, 3(4), 506-516. PMid:22797986. http://dx.doi.org/10.3945/an.112.002154
http://dx.doi.org/10.3945/an.112.002154...
).

Fruits generally exhibit large quantities of vitamins, mineral salts, and fibers. These components are responsible for providing health benefits related to a greater life expectancy, improved disposition, the prevention of pathologies and increased vitality. In fact, exotic fruits are an alternative for diversifying people’s diet (Lorenzi & Lacerda, 2006Lorenzi, H., & Lacerda, M. (2006). Frutas brasileiras e exóticas cultivadas (de consumo in natura) (1. ed.). São Paulo: Instituto Plantarum.).

Exotic fruit cultivation presents itself as an option for small producers to complement their family income, as well as a potential opportunity for research whose goal is to identify new business opportunities. However, to achieve popularity on the market, the fruit must exhibit properties that satisfy the palate of the general population, as well as quality characteristics related to the physicochemical parameters of the product (Lima et al., 2012Lima, C. S. M., Galarça, S. P., Betemps, D. L., Rufato, A. R., & Rufato, L. (2012). Avaliação física, química e fitoquímica de frutos de Physalis, ao longo do período de colheita. Revista Brasileira de Fruticultura, 34(4), 1004-1012. http://dx.doi.org/10.1590/S0100-29452012000400006
http://dx.doi.org/10.1590/S0100-29452012...
). Against this backdrop, the achachairu, a fruit belonging to the Garcinia genus, humilis species, originally from Bolivia, stands out as a promising alternative due to its sensory characteristics (Nunes, 2004Nunes, J. S. (2004). Propagación del achachairú (Rheedia achachairu Rusby) por estacas (Monografia). Carrera de Ciencia y Producción Agropecuária, Zamorano. ). Although it is native to Bolivia, the achachairu is widely cultivated in Brazil since it adapts easily to both tropical and sub-tropical climates, and records show that it has been cultivated in diverse regions of Brazil. However, details regarding the availability of its characteristics and properties are still scarce in the literature (Barbosa & Artioli, 2007Barbosa, W., & Artioli, F. A. (2007). A fruta achachairú. Retrieved in 2021, December 18, from <http://www.infobibos.com/Artigos/2007_1/achachairu/index.htm.
http://www.infobibos.com/Artigos/2007_1/...
; Soprano & Koller, 2008Soprano, E., & Koller, O. L. (2008). Avaliação de frutos de espécies frutíferas tropicais com potencial para cultivo em Santa Catarina. In XX Congresso Brasileiro de Fruticultura, 53th Annual Meeting of the Interamerican Society for Tropical Horticulture. Vitória: Sociedade Brasileira de Fruticultura.).

In its country of origin, the achachairu is greatly prized for its sensory characteristics; however, it is a seasonal product with a short harvest period, being available on the market only between the months of February and April. Despite its limited demand, plans currently exist to boost production in order to disseminate its applications for food industries. The goal of industrializing and exporting the fruit is to preserve the nutritional and antioxidant benefits of the in natura product, the form in which it is currently widely commercialized (Nunes, 2004Nunes, J. S. (2004). Propagación del achachairú (Rheedia achachairu Rusby) por estacas (Monografia). Carrera de Ciencia y Producción Agropecuária, Zamorano. ; Instituto Boliviano de Comércio Exterior, 2010Instituto Boliviano de Comércio Exterior - IBCE. (2010). Perfil de mercado: Copoazú y Achachairú. Retrieved in 2021, December 16, from www.ibce.org.bo.
www.ibce.org.bo...
).

Scarce records appear in the literature regarding either the plant or the fruit. Among those studies that were found, Bagattoli et al. (2016)Bagattoli, P. C. D., Cipriani, D. C., Mariano, L. N. B., Correa, M., Wagner, T. M., Noldin, V. F., Cechinel Filho, V., & Niero, R. (2016). Phytochemical, antioxidant and anticancer activities of extracts of seven fruits found in the southern Brazilian flora. Indian Journal of Pharmaceutical Sciences, 78(1), 34-40. PMid:27168679. http://dx.doi.org/10.4103/0250-474X.180239
http://dx.doi.org/10.4103/0250-474X.1802...
and Tomé et al. (2019)Tomé, A. C., Mársico, E. T., Silva, F. A., Kato, L., Nascimento, T. P., & Monteiro, M. L. G. (2019). Achachairú (Garcinia humilis): Chemical characterization, antioxidant activity and mineral profile. Journal of Food Measurement and Characterization, 13(1), 213-221. http://dx.doi.org/10.1007/s11694-018-9934-x
http://dx.doi.org/10.1007/s11694-018-993...
highlighted its nutritional and antioxidant potential, as well as the mineral load present in the fruit. Barros et al. (2017)Barros, R. G. C., Andrade, J. K. S., Denadai, M., Nunes, M. L., & Narain, N. (2017). Evaluation of bioactive compounds potential and antioxidant activity in some Brazilian exotic fruit residues. Food Research International, 102, 84-92. PMid:29196016. http://dx.doi.org/10.1016/j.foodres.2017.09.082
http://dx.doi.org/10.1016/j.foodres.2017...
identified bioactive compounds, whereas Terrazas et al. (2013)Terrazas, P. M., Marques, E. S., Mariano, L. N. B., Cechinel-Filho, V., Niero, R., Andrade, S. F., & Maistro, E. L. (2013). Benzophenone guttiferone A from Garcinia achachairu Rusby (Clusiaceae) presents genotoxic effects in different cells of mice. PLoS One, 8(11), e76485. PMid:24250785. http://dx.doi.org/10.1371/journal.pone.0076485
http://dx.doi.org/10.1371/journal.pone.0...
suggested that the fruit may perform diverse functions in the human body, such as healing, digestive and laxative activities, and may also fight rheumatism, gastric ulcers, and inflammation. In addition, both leaves and fruits exhibit several biflavonoid and benzene compounds with potential for immunotoxic, anti-inflammatory and anticancer activities (Cury et al., 2016Cury, G. C., Gisbert, M. C. A., & Porcel, W. J. R. (2016). Um estudo da fruta comestível de Garcinia gardeneriano. Revista Boliviana de Química, 33(4), 158-163. ).

Although the composition of the achachairu (G. humilis) exhibits favorable characteristics, studies involving the fruit are still scarce. The small amount of scientific research that has been conducted on the achachairu made possible a quantitative assessment of the records regarding the fruit. For this purpose, one of the approaches that makes it possible to track publication data, as well as information regarding the fields, regions and dates of studies that have already been conducted, is the bibliometric review based on a statistical analysis. According to Rodríguez-Rojas et al. (2019)Rodríguez-Rojas, A., Arango Ospina, A., Rodríguez-V’elez, P., & Arana-Florez, R. (2019). ¿What is the new about food packaging material? A bibliometric review during 1996-2016. Trends in Food Science & Technology, 85, 252-261. http://dx.doi.org/10.1016/j.tifs.2019.01.016
http://dx.doi.org/10.1016/j.tifs.2019.01...
, the purpose of applying the method of bibliometric review is to extract results, identify authors, institutions, and journals in their respective areas of knowledge, for the purpose of serving as a guide or focus for subsequent publications, as well as to show tendencies for keywords submitted as part of the investigation.

In line with these purposes, this study aimed to conduct a bibliometric analysis to ascertain the information on the achachairu (G. humilis) currently available in the literature by tracing the data that has been published on this species, since there is not yet any collection of studies regarding this fruit, which is considered underexplored, despite the fact that promising studies have been published regarding its composition.

2 Characteristics and properties of the achachairu (Garcinia humilis)

The achachairu, known also by the names mangosteen, tapacuarai, cachicheruqui, chachairu, tatairu, Bolivian bacupari, shashairú, ibaguazú, cachicheruqui and apacuarai, belongs to the Clusiaceae family, Garcinia genus; however, its previous designation was Rheedia, and its species is humilis. The plant is originally from western Bolivia, a region containing a great variety of fruit species (Barbosa & Artioli, 2007Barbosa, W., & Artioli, F. A. (2007). A fruta achachairú. Retrieved in 2021, December 18, from <http://www.infobibos.com/Artigos/2007_1/achachairu/index.htm.
http://www.infobibos.com/Artigos/2007_1/...
; Instituto Boliviano de Comércio Exterior, 2010Instituto Boliviano de Comércio Exterior - IBCE. (2010). Perfil de mercado: Copoazú y Achachairú. Retrieved in 2021, December 16, from www.ibce.org.bo.
www.ibce.org.bo...
). The Garcinia genus includes approximately 600 species, both trees and bushes, of which the best known is the mangosteen (G. mangostana L.) (Duarte, 2011Duarte, O. (2011). Achachairú (Garcinia humilis) (Vhal) C. D. Adam. Postharvest Biology and Technology of Tropical and Subtropical Fruits, 54, 48-53. http://dx.doi.org/10.1533/9780857092762.48
http://dx.doi.org/10.1533/9780857092762....
; Janick & Paull, 2008Janick, J., & Paull, R. E. (2008). Rheedia laterifolia - Achachairú. In J. Janick & R. E. Paull (Eds.), The encyclopedia of fruit & nuts (pp. 272-273). Cambridge: CABI. http://dx.doi.org/10.1079/9780851996387.0000.
http://dx.doi.org/10.1079/9780851996387....
; Lorenzi & Lacerda, 2006Lorenzi, H., & Lacerda, M. (2006). Frutas brasileiras e exóticas cultivadas (de consumo in natura) (1. ed.). São Paulo: Instituto Plantarum.).

Although the G. humilis is originally from Bolivia, the plant also grows in diverse regions of Brazil. The tree is non-deciduous, meaning that it retains its leaves throughout all seasons of the year; its height varies between 10 and 15 meters, and yellow latex is extracted from the trunk. It has coriaceous leaves that are glabrous and lustrous on the upper surface and whose length varies between 10 and 18 cm. Its flowers may occur alone or in groups, in both axillary fascicles, may be androgynous or hermaphroditic, and form between the months of July and September.

The term achachairu is a Guarani word meaning “honey kiss”. In Bolivia, although the fruit is quite popular and there is a significant commercial market for it, no records exist regarding industrialized production, since its consumption is being limited to its in natura state (Instituto Boliviano de Comércio Exterior, 2010Instituto Boliviano de Comércio Exterior - IBCE. (2010). Perfil de mercado: Copoazú y Achachairú. Retrieved in 2021, December 16, from www.ibce.org.bo.
www.ibce.org.bo...
).

The achachairu can grow in a variety of soils, thus making possible its cultivation in all types of regions, and easily adapts to mainly the tropical and sub-tropical climates. As a result, one of the countries that has most broadly disseminated the fruit is Brazil, where the plant was introduced in the twentieth century and is currently found in the states of Minas Gerais, São Paulo, Pernambuco, Pará, Goiás and Santa Catarina. Despite the wide distribution of cultivation, the achahairu is not popular in the country and is sometimes confused with fruits of other species (Barbosa et al., 2008Barbosa, W., Chagas, E. A., Martins, L., Pio, R., Tucci, M. L. S., & Artioli, F. A. (2008). Germinação de sementes e desenvolvimento inicial de plântulas de achachairu. Revista Brasileira de Fruticultura, 30(1), 263-266. http://dx.doi.org/10.1590/S0100-29452008000100049
http://dx.doi.org/10.1590/S0100-29452008...
).

Its fruits (Figure 1) are drupes, have an average mass of 30 g and a rounded oblong shape, whose transverse and longitudinal dimensions are approximately 35.8 mm and 45.2 mm, respectively. Its peel is thick (average thickness of 3.53 mm), smooth, firm, and resistant, with an external coloration that may vary between yellow and orange, and an internal cream-straw color. The pulp, which does not adhere to the peel, is white and succulent, exhibiting a mucilaginous texture that oxidizes quickly and a sweet flavor of approximately 15 degrees Brix and a pH of 4.1. Each fruit usually has on average 3 seeds, two of which frequently remain underdeveloped and are unfit for germination; these are referred to as chochas (Janick & Paull, 2008Janick, J., & Paull, R. E. (2008). Rheedia laterifolia - Achachairú. In J. Janick & R. E. Paull (Eds.), The encyclopedia of fruit & nuts (pp. 272-273). Cambridge: CABI. http://dx.doi.org/10.1079/9780851996387.0000.
http://dx.doi.org/10.1079/9780851996387....
). In relation to the total mass of the fruit, the peel represents around 52%, the pulp corresponds to ⅓, that is, 33% of the pulp, and the seed represents approximately 15% of the fruit.

Figure 1
(A) Ripe achachairu on the tree; (B) Peel and pulp of achachairu; (C) Seeds of achachairu; (D) Achachairu at three ripening stages.

The development related to the maturation of the achachairu occurs between December and April, with the most significant transformations beginning in February. When they begin their development, the fruits are smaller, and their peels exhibit a green color. During the maturation process, the external color changes until it becomes reddish orange (Figure 1). During this period, natural reactions occur that cause the fruit to develop, the most important of which are a reduction in acidity, a gradual increase in sweetness and a softening of its structure. Its size also changes as a result of its growth. It is recommended that the mature fruit be harvested at the end of April, the time at which it reaches its maximum size and orange color. After being harvested, the fruits prove to be resistant upon being transported and conserve well under refrigeration (Barbosa et al., 2008Barbosa, W., Chagas, E. A., Martins, L., Pio, R., Tucci, M. L. S., & Artioli, F. A. (2008). Germinação de sementes e desenvolvimento inicial de plântulas de achachairu. Revista Brasileira de Fruticultura, 30(1), 263-266. http://dx.doi.org/10.1590/S0100-29452008000100049
http://dx.doi.org/10.1590/S0100-29452008...
). However, the achachairu is considered a non-climacteric fruit, that is, it exhibits low respiratory activity and a slight deterioration after harvesting, meaning that it is incapable of completing the maturation process after being harvested. Therefore, fruits must be harvested at their optimal point to be fit for consumption (Chitarra & Chitarra, 2005Chitarra, M. I. F., & Chitarra, A. B. (2005). Pós-colheita de frutos e hortaliças: Fisiologia e manuseio (2. ed.). Lavras: UFLA.).

The achachairu is an easily cultivated fruit that shows great market potential due to its resilience upon being handled and transported, thus providing it with competitive advantages, in addition to exhibiting properties that are beneficial for health (Soprano & Koller, 2008Soprano, E., & Koller, O. L. (2008). Avaliação de frutos de espécies frutíferas tropicais com potencial para cultivo em Santa Catarina. In XX Congresso Brasileiro de Fruticultura, 53th Annual Meeting of the Interamerican Society for Tropical Horticulture. Vitória: Sociedade Brasileira de Fruticultura.).

3 Bibliometric review methodology

The bibliometric analysis was conducted during the month of February of 2022 according to the method described by Araújo et al. (2020)Araújo, A. G., Carneiro, A. M. P., & Palha, R. P. (2020). Sustainable construction management: A systematic review of the literature with meta-analysis. Journal of Cleaner Production, 256, 120350. http://dx.doi.org/10.1016/j.jclepro.2020.120350
http://dx.doi.org/10.1016/j.jclepro.2020...
; data were collected from the Main Collection of the Web of Science© (WOS) database. The filters used terms that describe both scientific nomenclature (Garcinia humilis) and the popular name of the fruit (achachairu). The purpose for including both search terms was to study all works related to the fruit with greater precision. Both searches were conducted in the section with the heading “topic,” the category that includes data for titles, abstracts, keywords, and keywords plus. The data extracted included type of publication, geographical distribution, date and field of the studies, journals and institutions involved in the execution of the studies.

After collecting the information from the database, the data were correlated using the VOSviewer (Java version 1.8.0_261) software with the keywords of all identified studies involving Garcinia humilis and achachairu. To rank the results, the co-occurrence of keywords was established without regard to the strength of the link as described by the program.

4 Bibliometric analysis

The search of the database produced only 29 works related to the search terms, 24 of which were for the name achachairu, and 15 of which for the term Garcinia humilis, thus resulting in 10 works in which both terms were used.

Upon evaluating the publication categories, it was observed that 27 of the 29 documents obtained from the search were complete articles, while the remaining two publications were meeting abstracts.

4.1 Chronological and geographical information

The data collection observed that the first publications involving G. humilis and achachairu appeared in 2005, for which only one journal article was found, and remained scarce until the year 2008, for which another publication record was found. In 2011 and 2020 there were only two recorded publications each year, and the frequency of studies involving the fruit remained low, with three works being recorded annually for the years 2012, 2013, 2016, 2018 and 2019. The greatest number of publications occurred in the years 2017 and 2021, each of which it could be found four works published (Figure 2).

Figure 2
Number of publications per year related to the terms Garcinia humilis and achachairu.

Although records exist of studies involving the achachairu conducted on consecutive years, their volume remained low throughout the entire period under consideration, reaching a maximum of four publications per year that deal with the species.

The limited number of studies involving the achachairu may be a result of its being a seasonal product, as well as its lack of popularity in the scientific community. However, this lack of information represents opportunities for research on a little-known matrix that may have promising characteristics.

Although the achachairu is native to Bolivia, 27 of the 29 works identified were published in English, and the remaining two in Portuguese. According to the bibliometric analysis, Brazil had the greatest number of recorded studies, with a total of 25 works. The United States of America (USA) was the second, with a total of three publications, and the remaining countries listed had only one publication each (Table 1).

Table 1
Regions and main institutions with record of publications on the terms Garcinia humilis and achachairu.

Regarding geographical distribution, the records included authors and co-authors from various places, thus involving different research institutions. From the data collected, 32 organizations were identified that made publications with the terms Garcinia humilis and achachairu. Of these organizations, four had more than two publications (12, 5, 4 and 3), which were made by researchers from institutions located in several regions of Brazil, including the South (Santa Catarina), the Southwest (São Paulo) and the Center-East (Goiás and Mato Grosso do Sul) (Table 1). This observation confirmed the association of the fruit with a tropical climate, typical of Brazil, and the facility with which it may be cultivated.

4.2 Categories of publication and review of the main results

Concerning the field of study, the database search revealed 12 fields of publication involving the terms studied. The most prominent was the field of pharmacology pharmacy, which accounted for 10 publication records involving the terms Garcinia humilis and achachairu, followed by food science technology, for which 9 studies were recorded.

Among the other fields that were identified, agriculture represented a total of six works. Chemistry, integrative complementary medicine, plant sciences and toxicology had three publications each, while biochemistry molecular biology had two records each. In addition, four other fields, corresponding to immunology, medical laboratory technology, nutrition dietetics and science and technology - other topics, each have only one record in the database about the terms that were studied. Representing these fields of publication, 24 journals were identified. Of this total, only four journals (Abstracts of Papers of The American Chemical Society, Chemico Biological Interactions, LWT Food Science and Technology and Revista de Agricultura Neotropical) had more than one publication, each of which had two published works. However, the records from the Abstracts of Papers of The American Chemical Society had only meeting abstracts, unlike the remaining journals, which had complete articles. The remaining 20 journals identified in the database for the terms Garcinia humilis and achachairu had one publication each. By means of a study of the journals, it was possible to identify data regarding authorship, date, impact factor, focus of the study, the portion of the plant studied, and the number of quotations (Table 2).

Table 2
Authorship, impact factor, focus of the study, part of the fruit studied and number of citations of journals with publication records on Garcinia humilis and achachairu.

Although the publications have a significant impact factor, the number of quotations of the works is still low, with a maximum of 49 article references published in 2005 in the Journal of Natural Products. This detail reveals how little research has been conducted on the fruit and its species, since the total number of quotations was less than 50 over a period of 16 years.

Regarding the main research focus areas, a wide range of topics was observed (Table 2), including chemical characterization, bioactive and antioxidant composition, identification of antiparasitic agents, determination of phytochemicals, antimicrobial activity, enzymatic activity and protection against oxidation, germination properties, and genotoxic and clastogenic effects, among others. However, all studies highlighted the gastroprotective properties related to the benzophenone Guttiferone A.

Guttiferones are defined as polyprenylated benzophenones and are associated with various biological activities. They may exhibit free-radical scavenging activity, anti-ulcer effects, cytotoxicity, nitric oxide synthesis inhibition, chemoprevention of cancer, induction of apoptosis, anti-HIV activity and trypanocidal effects (Naldoni et al., 2009Naldoni, F. J., Claudino, A. L. R., Cruz-Junior, J. W., Chavasco, J. K., Faria-Silva, P. M., Veloso, M. P., & dos Santos, M. H. (2009). Antimicrobial activity of benzophenones and extracts from the fruits of Garcinia brasiliensis. Journal of Medicinal Food, 12(2), 403-407. PMid:19459744. http://dx.doi.org/10.1089/jmf.2007.0622
http://dx.doi.org/10.1089/jmf.2007.0622...
).

Various studies have shown that Guttiferona A in particular exhibits properties related to antioxidant capacity, confirmed by DPPH and ABTS tests (Acuña et al., 2010Acuña, U. M., Figueroa, M., Kavalier, A., Jancovski, N., Basile, M. J., & Kennelly, E. J. (2010). Benzophenones and Biflavonoids from Rheedia edulis. Journal of Natural Products, 73(11), 1775-1779. PMid:21028890. http://dx.doi.org/10.1021/np100322d
http://dx.doi.org/10.1021/np100322d...
), a protective effect upon cells that have been damaged by iron sulfate, inhibition of lipid peroxidation, oxidative degradation of 2-deoxyribose (Figueredo et al., 2011Figueredo, Y. N., Garcia-Pupo, L., Cuesta Rubio, O., Delgado Hernández, R., Naal, Z., Curti, C., & Pardo Andreu, G. L. (2011). A strong protective action of guttiferone A, a naturally occurring prenylated benzophenone, against iron-induced neuronal cell damage. Journal of Pharmacological Sciences, 36(116), 36-46. PMid:21512303. http://dx.doi.org/10.1254/jphs.10273FP
http://dx.doi.org/10.1254/jphs.10273FP...
), antioxidant activity and moderate antiplasmodial activity by means of P. falciparum (Ngouela et al., 2006Ngouela, S., Lenta, B. N., Noungoue, D. T., Ngoupayo, J., Boyom, F. F., Tsamo, E., Gut, J., Rosenthal, P. J., & Connolly, J. D. (2006). Antiplasmodial and antioxidant activities of constituents of the seed shells of Symphonia globulifera Linn f. Phytochemistry, 67(3), 302-306. PMid:16368120. http://dx.doi.org/10.1016/j.phytochem.2005.11.004
http://dx.doi.org/10.1016/j.phytochem.20...
), antimicrobial activity in fungi (Trichophyton rubrum and Candida albicans), bacteria (Staphylococcus aureus and Escherichia coli) and parasites (Trypanosoma cruzi, T. brucei, Plasmodium falciparum, Leishmania infantum and L. amazonenses), in addition to cytotoxicity in MRC-5 cells, belonging to the lineage present in lung cells (Monzote et al., 2011Monzote, L., Cuesta-Rubio, O., Matheeussen, A., Van Assche, T., Maes, L., & Cos, P. (2011). Antimicrobial evaluation of the polyisoprenylated benzophenones nemorosome and guttiferone A. Phytotherapy Research, 25(3), 458-462. PMid:21259352. http://dx.doi.org/10.1002/ptr.3401
http://dx.doi.org/10.1002/ptr.3401...
).

An examination of the group of studies identified using the search terms Garcinia humilis and achachairu revealed that Guttiferone A was the predominant compound identified in the seed of the fruit (Niero et al., 2012Niero, R., Dal Molin, M. M., Silva, S., Damian, N. S., Maia, L. O., Delle Monache, F. D., Cechinel-Filho, V., & de Andrade, S. F. (2012). Gastroprotective effects of extracts and guttiferone A isolated from Garcinia achachairu Rusby (Clusiaceae) against experimentally induced gastric lesions in mice. Naunyn-Schmiedeberg’s Archives of Pharmacologist, 385(11), 1103-1109. PMid:22926730. http://dx.doi.org/10.1007/s00210-012-0788-1
http://dx.doi.org/10.1007/s00210-012-078...
). The studies highlighted that the raw methanolic extract and the pure compound (Guttiferone A) exhibit a rich medicinal profile, showing antinociceptive and gastroprotective properties with antileishmanial and antimicrobial activities (Dal Molin et al., 2012Dal Molin, M. M., Silva, S., Alves, D. R., Quintão, N. L. M., Delle Monache, F., Cechinel-Filho, V., & Niero, R. (2012). Phytochemical analysis and antinociceptive properties of the seeds of Garcinia achachairu. Archives of Pharmacal Research, 35(4), 623-631. PMid:22553054. http://dx.doi.org/10.1007/s12272-012-0405-3
http://dx.doi.org/10.1007/s12272-012-040...
; Cechinel-Filho et al., 2013Cechinel-Filho, V., Meyre-Silva, C., Niero, R., Mariano, L. N. B., Nascimento, F. G., Farias, I. V., Gazoni, V. F., Silva, B. S., Giménez, A., Gutierrez-Yapu, D., Salamanca, E., & Malheiros, A. (2013). Evaluation of antileishmanial activity of selected Brazilian plants and identification of the active principles. Evidence-Based Complementary and Alternative Medicine, 2013, 265025. PMid:23840252. ; Melim et al., 2013Melim, C., Guimarães, K., Martin-Quintal, Z., Alves, A. D., Martins, D. T. O., Monache, F. D., Cechinel-Filho, V., Cruz, A. B., & Niero, R. (2013). Antimicrobial activity of extracts and fractions from aerial parts of selected plants (Garcinia achachairu, Macrosiphonia velame, Rubus niveus and Pilea microphylla) against some pathogenic microorganisms. Natural Product Communications, 8(11), 1567-1569. PMid:24427943. http://dx.doi.org/10.1177/1934578X1300801117
http://dx.doi.org/10.1177/1934578X130080...
), low genotoxicity (Marques et al., 2012Marques, E. S., Silva, S., Niero, R., Andrade, S. F., Rosa, P. C. P., Perazzo, F. F., & Maistro, E. L. (2012). Genotoxicity assessment of Garcinia achachairu Rusby (Clusiaceae) extract in mammalian cells in vivo. Journal of Ethnopharmacology, 142(2), 362-366. PMid:22609977. http://dx.doi.org/10.1016/j.jep.2012.04.045
http://dx.doi.org/10.1016/j.jep.2012.04....
), analgesic properties (Terrazas et al., 2013Terrazas, P. M., Marques, E. S., Mariano, L. N. B., Cechinel-Filho, V., Niero, R., Andrade, S. F., & Maistro, E. L. (2013). Benzophenone guttiferone A from Garcinia achachairu Rusby (Clusiaceae) presents genotoxic effects in different cells of mice. PLoS One, 8(11), e76485. PMid:24250785. http://dx.doi.org/10.1371/journal.pone.0076485
http://dx.doi.org/10.1371/journal.pone.0...
), effects against certain models of induced ulcers and reduction of gastric secretion (Niero et al., 2012Niero, R., Dal Molin, M. M., Silva, S., Damian, N. S., Maia, L. O., Delle Monache, F. D., Cechinel-Filho, V., & de Andrade, S. F. (2012). Gastroprotective effects of extracts and guttiferone A isolated from Garcinia achachairu Rusby (Clusiaceae) against experimentally induced gastric lesions in mice. Naunyn-Schmiedeberg’s Archives of Pharmacologist, 385(11), 1103-1109. PMid:22926730. http://dx.doi.org/10.1007/s00210-012-0788-1
http://dx.doi.org/10.1007/s00210-012-078...
), in addition to pronounced antiproliferative activity against cell lines, revealing potential anticancer activity (Mariano et al., 2015Mariano, L. N. B., Vendramini-Costa, D. B., Ruiz, A. L. T. G., Carvalho, J. E., Corrêa, R., Cechinel-Filho, V., Delle Monache, F. D., & Niero, R. (2015). In vitro antiproliferative activity of uncommon xanthones from branches of Garcinia achachairu. Pharmaceutical Biology, 54(9), 1697-1704. PMid:26704644. http://dx.doi.org/10.3109/13880209.2015.1123279
http://dx.doi.org/10.3109/13880209.2015....
).

The data gathered from the published articles also revealed that 11 studies focused on the seed, six on the peel and six on the fruit as a whole.

John et al. (2018)John, O. D., Wanyonyi, S., Mouatt, P., Panchal, S. K., & Brown, L. (2018). Achacha (Garcinia humilis) rind improves cardiovascular function in rats with diet-induced metabolic syndrome. Nutrients, 10(10), 1425. PMid:30287733. http://dx.doi.org/10.3390/nu10101425
http://dx.doi.org/10.3390/nu10101425...
reported in their studies that the peel of the achachairu, which is considered a food subproduct, exhibits potent cardioprotective properties in rats with metabolic syndromes induced by their diet. The peel also exhibited other favorable properties with nutritional applications, such as antioxidant activity, the presence of minerals (Tomé et al., 2019Tomé, A. C., Mársico, E. T., Silva, F. A., Kato, L., Nascimento, T. P., & Monteiro, M. L. G. (2019). Achachairú (Garcinia humilis): Chemical characterization, antioxidant activity and mineral profile. Journal of Food Measurement and Characterization, 13(1), 213-221. http://dx.doi.org/10.1007/s11694-018-9934-x
http://dx.doi.org/10.1007/s11694-018-993...
) and oxidative stability in meat products (Tomé et al., 2021Tomé, A. C., da Silva, F. A., Monteiro, M. L., & Mársico, E. T. (2021). Effect of achachairu skin on the oxidative stability of mechanically separated tilapia meat and a sensory evaluation of its use in a restructured product. Journal of Aquatic Food Product Technology, 30(1), 2-15. http://dx.doi.org/10.1080/10498850.2020.1850587
http://dx.doi.org/10.1080/10498850.2020....
).

In view of the above, it may be seen that the peel and seed of the achachairu, which are treated as waste products from the commercialization of the in natura fruit, in addition to exhibiting pharmacological properties that are beneficial to human health, also appear as potential co-products that should be investigated in order determine their nutrient content and functional capacity in the food industry.

Finally, among the studies that have been conducted on the fruit as a whole, Melo et al. (2017)Melo, M. S., Benett, C. G. S., Melo, B. S., Lourenço, S. L. O., & Barboza, F. S. (2017). Physical-chemical analysis of achachairu fruits collected in different plant parts. Revista de Agricultura Neotropical, 4, 17-21. http://dx.doi.org/10.32404/rean.v4i5.2189
http://dx.doi.org/10.32404/rean.v4i5.218...
related the parts of the plant to the chemical and physical conditions that are most adequate for harvesting the achachairu and indicated that the upper part of the calyx is the most ideal in terms of quality. The parameters used in the evaluation included the mass and diameter of the fruit, the mass of the seed, pH, total soluble solids (ºBrix), total titratable acidity and pulp yield.

Barros et al. (2019)Barros, R. G. C., de Oliveira, C. S., Oliveira, L. T. S., Pereira, U. C., Silva, T. O. M., Denadai, M., & Narain, N. (2019). Enhancement of phenolic antioxidants production in submerged cultures of endophytic microorganisms isolated from achachairu (Garcinia humilis), araca-boi (Eugenia stipitata) and bacaba (Oenocarpus bacaba) fruits. Lebensmittel-Wissenschaft + Technologie, 111, 370-377. http://dx.doi.org/10.1016/j.lwt.2019.05.046
http://dx.doi.org/10.1016/j.lwt.2019.05....
detected endophytic strains of the genus Candida, which were responsible for the high quantities of phenolic compounds present in the achachairu, an observation that corroborated Bagattoli et al. (2016)Bagattoli, P. C. D., Cipriani, D. C., Mariano, L. N. B., Correa, M., Wagner, T. M., Noldin, V. F., Cechinel Filho, V., & Niero, R. (2016). Phytochemical, antioxidant and anticancer activities of extracts of seven fruits found in the southern Brazilian flora. Indian Journal of Pharmaceutical Sciences, 78(1), 34-40. PMid:27168679. http://dx.doi.org/10.4103/0250-474X.180239
http://dx.doi.org/10.4103/0250-474X.1802...
, whose study was promising in terms of the high total phenolic content in the fruit. These authors also highlighted the cytotoxic effect of the methanolic extracted from the seed, as well as the Guttiferona A presented in this extract, both of which inhibited the growth of tumor cells.

The available data points toward the need for more research regarding the composition of the achachairu in the search for technological innovations that may take advantage of the fruit’s potential.

4.3 Correlation of keywords

Based on the co-occurrence of the keywords present in the bibliometric review, the authors were able to identify the tendency of the focus areas in the studies (Figure 3). To obtain these results, the option “all keywords” was selected in the Web of Science database. Upon analysis, the results were seen to cover the widest range of terms, including all keywords cited in the individual studies; the other options were “author keywords” and “keywords plus”, whose search results yielded a smaller range of terms. According to Li (2018)Li, M. (2018). Classifying and ranking topic terms based on a novel approach: Role differentiation of author keywords. Scientometrics, 116(1), 77-100. http://dx.doi.org/10.1007/s11192-018-2741-7
http://dx.doi.org/10.1007/s11192-018-274...
and Rodríguez-Rojas et al. (2019)Rodríguez-Rojas, A., Arango Ospina, A., Rodríguez-V’elez, P., & Arana-Florez, R. (2019). ¿What is the new about food packaging material? A bibliometric review during 1996-2016. Trends in Food Science & Technology, 85, 252-261. http://dx.doi.org/10.1016/j.tifs.2019.01.016
http://dx.doi.org/10.1016/j.tifs.2019.01...
, investigating keywords is an important bibliometric method due to the reference in the archive search, thus facilitating the consultation of the fields of study.

Figure 3
Co-occurrence analysis of keywords present in publications on the terms Garcinia humilis and achachairu.

The filter applied in this analysis included keywords that were present a minimum of two times among the journals, yielding 29 combinations among the 205 keywords that were identified. The number of occurrences is shown in Figure 3 by means of circles that represent each keyword, whose size is proportional to its quantification, that is, a larger circle represents a greater number of occurrences of the keyword. The analysis revealed that the most prominent keyword was “seeds”, which exhibited a close relationship to the words “biflavonoids”, “extracts”, “cytotoxicity” and “benzophenones”, thus affirming the medicinal properties of this part of the fruit and confirming the data resulting from the analysis conducted for the publication categories. However, the terms that were observed to be directly related to “garcinia achachairu” and “achachairu” (“phenolic-compounds”, “antioxidant”, “bioactive compounds” and “natural antioxidant”) referred to the antioxidant properties present in the species, maximizing the bioactive characteristics of the achachairu in publications that are focused primarily on applications in pharmacology.

5 Trends for future research on the achachairu

Studies suggest that the Garcinia species may perform diverse functions in the human body, such as healing, digestive and laxative activities, and may also fight rheumatism, gastric ulcers, and inflammation. In addition, both leaves and fruits exhibit several biflavonoid and benzene compounds with potential for immunotoxic, anti-inflammatory and anticancer activity (Cury et al., 2016Cury, G. C., Gisbert, M. C. A., & Porcel, W. J. R. (2016). Um estudo da fruta comestível de Garcinia gardeneriano. Revista Boliviana de Química, 33(4), 158-163. ). As has been shown, the presence of such benefits in the Garcinia genus, particularly in the achachairu, has awakened the interest of the pharmaceutical industry in research involving its main active compounds and potential to cure diseases. Their focus on the achachairu is mainly due to the compound known as Guttiferone A, which is present primarily in the extract from the seed of the fruit (Terrazas et al., 2013Terrazas, P. M., Marques, E. S., Mariano, L. N. B., Cechinel-Filho, V., Niero, R., Andrade, S. F., & Maistro, E. L. (2013). Benzophenone guttiferone A from Garcinia achachairu Rusby (Clusiaceae) presents genotoxic effects in different cells of mice. PLoS One, 8(11), e76485. PMid:24250785. http://dx.doi.org/10.1371/journal.pone.0076485
http://dx.doi.org/10.1371/journal.pone.0...
).

Guttifrerone A, which is obtained from achachairu seed extracts, has been shown to be a compound responsible for benefits such as gastroprotective effects (Niero et al., 2012Niero, R., Dal Molin, M. M., Silva, S., Damian, N. S., Maia, L. O., Delle Monache, F. D., Cechinel-Filho, V., & de Andrade, S. F. (2012). Gastroprotective effects of extracts and guttiferone A isolated from Garcinia achachairu Rusby (Clusiaceae) against experimentally induced gastric lesions in mice. Naunyn-Schmiedeberg’s Archives of Pharmacologist, 385(11), 1103-1109. PMid:22926730. http://dx.doi.org/10.1007/s00210-012-0788-1
http://dx.doi.org/10.1007/s00210-012-078...
), reduction in the ability to feel pain (Dal Molin et al., 2012Dal Molin, M. M., Silva, S., Alves, D. R., Quintão, N. L. M., Delle Monache, F., Cechinel-Filho, V., & Niero, R. (2012). Phytochemical analysis and antinociceptive properties of the seeds of Garcinia achachairu. Archives of Pharmacal Research, 35(4), 623-631. PMid:22553054. http://dx.doi.org/10.1007/s12272-012-0405-3
http://dx.doi.org/10.1007/s12272-012-040...
) and clear antiproliferative activity (Mariano et al., 2015Mariano, L. N. B., Vendramini-Costa, D. B., Ruiz, A. L. T. G., Carvalho, J. E., Corrêa, R., Cechinel-Filho, V., Delle Monache, F. D., & Niero, R. (2015). In vitro antiproliferative activity of uncommon xanthones from branches of Garcinia achachairu. Pharmaceutical Biology, 54(9), 1697-1704. PMid:26704644. http://dx.doi.org/10.3109/13880209.2015.1123279
http://dx.doi.org/10.3109/13880209.2015....
), among other properties. In this sense, there is a future opportunity for research on the potentiation of extraction, as well as the development of techniques for the purification of this compound. Another gap that can be explored in this context is the improvement of cultivars of the humilis species, focusing on the selection of Guttifrerone A.

The studies compiled in this review suggest that the achachairu (G. humilis) represents a promising prototype for obtaining agents with antinociceptive properties and a gastroprotective profile, in addition to anticancer activity. In this context, it was also verified that the use of the seed and peel of this fruit exhibits significant potential in the sector of new product development and applicability as new ingredients for the food industry. An example could be bioactive flour, with the ability to provide the food matrix with the benefits identified in these portions of the fruit.

5.1 Critical argument about the review

One of the deficiencies identified was the fact that the consumption of achachairu was limited to its in natura form. The lack of knowledge about the processes necessary for the conservation and transformation of the fruit limits its use in periods outside its seasonal availability. Therefore, we emphasize the need to implement technologies that allow the use of this fruit at times inverse to its production, such as simple freezing, allowing, in addition to the conservation of the whole fruit, the production of frozen pulp, providing opportunities for the development of technologies in production of flour from residues, as the peels and seeds of the achachairu are currently treated.

The conservation and application of technologies aimed at the pulp of this fruit can also contribute to a greater visibility of this portion, whose scientific records are minimal.

Finally, aiming to provide a healthy diet, rich in nutrients and medicinal agents, we reinforced the investment in the use of the peel and especially the seed in industrial processes in the food sector, especially in the application as a bioactive ingredient, enriching flour or even in the development of biodegradable films due to identified properties.

6 Conclusion

Upon conducting this bibliometric analysis based on the term achachairu and its respective scientific nomenclature, Garcinia humilis, 29 publications were found. This result revealed the low scientific visibility of the species, even though the fruit includes properties that are beneficial for the human organism in both a nutritional and medicinal sense. Therefore, this bibliometric review identified a remarkable opportunity for research involving the achachairu (G. humilis), since the use of this fruit is currently limited to consumption in natura.

In addition to providing an incentive for further research into the promising profile of the fruit regarding its antinociceptive, antiproliferative and gastroprotective properties, which are mainly observed in the seed, the resulting data also suggest that possible applications focus primarily on the field of food science, concerning the reutilization of waste products (peel and seeds) in order to promote the bioactive and antioxidant properties of the achachairu.

  • Cite as: Ikeda, M., Melo, A. M., Costa, B. P., Pazzini, I. A. E., & Ribani, R. H. (2022). Bibliometric review of achachairu (Garcinia humilis): a promising agent for health and future food applications. Brazilian Journal of Food Technology, 25, e2022060. https://doi.org/10.1590/1981-6723.06022
  • Funding: Ministério da Ciência, Tecnologia e Inovação/Conselho Nacional de Desenvolvimento Científico e Tecnológico (314184/2020-1) e Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (88882.381643/2019-01).

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Edited by

Associate Editor: Charles Windson Isidoro Haminiuk.

Publication Dates

  • Publication in this collection
    08 Nov 2022
  • Date of issue
    2022

History

  • Received
    24 May 2022
  • Accepted
    23 Sept 2022
Instituto de Tecnologia de Alimentos - ITAL Av. Brasil, 2880, 13070-178 Campinas - SP / Brasil, Tel 55 19 3743-1762 - Campinas - SP - Brazil
E-mail: bjftsec@ital.sp.gov.br