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Psidium sartorianum (O. Berg) Nied., AnIndigenous Plant to Mexico, from Biology

to Biological Activity

F. DELGADO-VARGAS,1,2,3 S.P. DÍAZ-CAMACHO, 4,3 G. SALAZAR-ZAMORA,1

M.J. URIBE-BELTRAN 4,3 AND R. VEGA-AVIÑA 5, 3

Abstract

Psidium ssp. are of the family Myrtaceae that have been traditionally used asa source of therapeutic agents. Psidium guajava is the most studied species,biological activities have been scientifically demonstrated and chemicalcomponents characterized. Psidium sartorianum produces a high range ofsecondary metabolites. In Sinaloa, Mexico, P. sartorianum has been used forthe treatment of diarrhoea, cough, ulcers, among other diseases. The physico-chemical and nutritional characteristics of P. sartorianum fruit are reported;the edible portion is an excellent source of vitamin C (53 mg / 100 g); it has ahigh content of tannins and phytic acid, 11 and 0.82 g / 100 g dry weight,respectively. Seed components are also reported. Methanol and aqueous extractsof fruit showed antifungal (vs. Candida ssp. and Trichophyton ssp.),antibacterial (vs. some strains of Streptococcus, Staphylococcus, Enterococcus,Salmonella, Shigella and Escherichia) and antiparasitic properties (vs.Giardia lamblia and Hymenolepis nana). P. sartorianum has a multipurposepotential to be used in a rational exploitation scheme.

Key words : Taxonomy, Fruit, Proximate composition, Antinutritional,Antibacterial, Antiparasitic

1. Maestría en Ciencia y Tecnología de Alimentos2. To whom it may correspond. Mexico 68 # 1697, Colonia Sinaloa, Culiacan, Sinaloa

80260, Mexico. Phone/Fax +52-667-7136615; E-mail: [email protected]. This paper was written based on a multidisciplinary approach. Authors are in

alphabetical order and each one collaborates in his/her area of expertise.4. Unidad en Investigaciones en Salud Publica Louis Pasteur of the Facultad de

Ciencias Químico Biológicas5. Facultad de Agronomia, Universidad Autonoma de Sinaloa, Culiacan, Sinaloa 80010,

Mexico.

D: Salasar/Vol.-13/ art-04/Proof-3/Date : September’ 2005

Francisco

Comment on Text

1.Delgado-Vargas, F, Díaz-Camacho, S.P., Salazar-Zamora, G., Uribe-Beltrán, M.J. and Vega-Aviña, R. 2005. Psidium sartorianum (O. Berg) Nied., an Indigenous Plant to Mexico, from Biology to Biological Activity. In Search for Natural Drugs. Vol. 13, Recent Progress in Medicinal Plants, eds. Govil JN, Singh VK & Arunachalam C, pp. 81-114. Houston, TX: Studium Press LLC.

82 Recent Progress in Medicinal Plants Vol.13–Search for Natural Drugs


Biological description and characteristics ofP. sartorianum (O. Berg) Nied

Taxonomy

As classified by Cronquist (1981):

Kingdom Plantae

Division Magnoliophyta

Class Magnoliopsida

Subclass Rosidae

Order Myrtales

Family Myrtaceae

Genus Psidium

Species P. sartorianum

The Myrtaceae family

Myrtaceae A. L. de Jussieu 1789 nom. conserv.

The Myrtle (mirto, arrayan, murta) Family

Description

The Myrtaceae family is represented by trees and shrubs. Leaves are simple,opposite, although sometimes they are alternate or verticillate; commonlycoriaceous, always entires, glandular with gland-dotted; pinnately veinedor parallel veined, or one veined; stipules are vestigial or absent. Flowersare rarely solitary or usually aggregated in ‘inflorescences’; in cymes, inspikes, in corymbs and in panicles or in heads. The terminal inflorescenceunit is usually cymose. Inflorescences are terminal or axillary, or oftenintercalary; spikes, cymes, corymbs, panicles, even heads; with or withoutinvolucral bracts. Flowers are often bibracteolate; bisexual or rarelyunisexual and cyclic. Free hypanthium is present. Hypogynous disk ispresent (lining the hypanthium, when perigynous). Flowers are mainlynectariferous being important for the attraction of animals (birds and bats)involved in pollinization. Perianth usually shows distinct calyx and corollaor adnate to one another sometimes forming an operculum; or petaline, orsepaline; 1 or 2 whorled. Sepals (3) 4-5 (6) are either free of one another,imbricated; polysepalous or gamosepalous (then sometimes splittingirregularly at anthesis, or shed entire); regular and calyptrate or notcalyptrate. Petals (3)4-5(6) are imbricated and sometimes conniventsforming a calyptrate or not; regular; white, or yellow, or red, or pink, orpurple (not blue). Stamens are commonly in high number and free one ofanother or grouped forming fascicles (4-5), alternating with petals. Anthers


Psidium sartorianum (O. Berg) Nied., An Indigenous Plant To Mexico 83

are versatile; mostly tetrasporangiate with two thecas; connective has anapical secretory cavity. Ovary is inferior 2-5 (16), of joined carpels and withone or more lobes; style is usually terminal, long, capitated or sessile andlobed; placenta is axillar with two or many ovules in each lobe. Fruit is aberry with one to many seeds, with a loculicidal capsule, or sometimes is anut or a drupe (Cronquist, 1981; Hora, 1978; McVaugh, 1963).

In Myrtaceae plants, leaves and youth parts and, in general,parenchymatous tissue have translucent glands that are observed asbrilliant dots. They contain essential oils, proanthocyanidins, gallic andellagic acids, saponins and calcium oxalate crystals. By these characteristics,this family grouped plants considered as allelopathic. They suppress thedevelopment of organisms which compete with them for nutrients and light(Cronquist, 1981; Hora, 1978).

Distribution and economic importance

Myrtaceae family grouped plants of around 140 genera and 3900 species.These plants are distributed in tropical sub-tropical regions of the world,mostly of South America and Australia, including the temperate area ofAustralia (Cronquist, 1981; Parra-O., 2002).

The myrtle (Myrtus communis L.) and eucaliptus (Eucaliptus ssp.)are cropped as ornaments. Moreover, Eucaliptus is an important genus forforestry uses in Australia where it grows in the humid-temperate regionsand it shows a high of more than 100 m. Floral buds of Syzygium aromaticum(L.) Cerril & Perry are used as condiments and they are known as flavorcloves. The fruits of Pimenta dioica (L.) Merrill are used as condiment andknown as pepper or black pepper. Fruits of P. guajava L. are edible andknown as guava. Moreover, several species are used as adorn by their beautyflowers (Cronquist, 1981). The whole plant of P. sartorianum is used fordifferent purposes as described below.

P. sartorianum

Description of the genus

Psidium plants are trees or shrubs. Flowers are generally big with axillarypeduncles and 1 to 3 flowers. Calyx is formed by a campanulate or urceolatetube; limbus is 4-5 dentate, or lobed, or completely joined before the anthesis.Petals are sometimes eye-catching, 4-5, extended and white. Ovary is 2-7locular. Fruit is a fleshy berry, globose, of pear like form, with multipleseeds and generally big and edible. Seeds show forms like horseshoe orkidney and they have a hard seed coat. Embryo is uncinated or curved(McVaugh, 1963; Standley, 1924).

This genus is endemic of America and it includes more than 100 species.The type species of this genus is P. guajava L. and it is widely distributedin all the tropical zones around the world (McVaugh, 1963).



Synonimies

The scientific name of the plant object of our study is

Psidium sartorianum (O. Berg) Nied. in Engl. & Prantl, Nat.Pflanzenfam. 3, Abt. 7: 69. 1893.

Basionym:

Mitranthes sartoriana O. Berg

Linnaea 29(2): 248. 1958

However, the following synonymy has been used through time(McVaugh, 1963):

Mitranthes sartoriana Berg. Linnaea 29: 248. 1858.

Calycorectes protractus Grises. Cat. Pl. Cub. 284. 1866.

Calyptropsidium sartorianum (Berg.) Drug & Urban ex Urban, Bot.Jahrb. 19: 571. 1895.

Calyptranthes tonduzii Donn. Sm. Bot. Gaz. 23: 245. 1897.

Psidium microphyllum Britton, Sci. Surv. P. R. & Virgen Is. 6: 555.1930.

Mitropsidium sartorianum (Berg.) Burret, Notizbl. Bot. Gart. Berlin15: 487. 1941.

Psidium yucatanense Lundell, Contr. Univ. Mich. Herb. 7: 35. 1942.

Psidium solisii Standl. Field Mus. Bot. 23: 133. 1944.

Psidium molinae Amshoff. Act. Bot. Néerl. 5: 277. 1956.

Psidium sartorianum var. yucatanense McVaugh, Fieldiana, Bot. 29:527. 1963.

Common names

P. sartorianum is present in several countries and different common namesare given, e.g. guayabilla in Cuba and El Salvador. In Mexico, P. sartorianumis known as: Guayabillo (Chihuahua, Guerrero, Oaxaca, Chiapas andYucatan); choqui (Sonora); arrayan (Sinaloa, Veracruz, Oaxaca andDurango); pichiche (Mayan name from Yucatan); rayana (Oaxaca); choquey(word of a guarigia tongue from Chihuahua); guayabito (Tabasco); cho´ca,guayavillo and rowili (Tarahumara) (CIDE, 2005; Pennington and Sarukhan,1968; Rebollar et al., 1994; Standley, 1924).

Description

Form

The tree is perennial or deciduous within April and May. It reaches up to15 m high and a diameter up to 60 cm. Stem is straight with ascending andthick branches. The top of the tree is narrow and dense (Figure 1A) (CIDE,



2005; McVaugh, 1963; Pennington and Sarukhan, 1968; Rebollar et al., 1994;Standley, 1924).

Bark

External bark is scaly and it is detached in smooth pieces, thin and long; itscolor is brown with yellow tones and gray spots. External bark measuresaround 1 mm (Fig. 1B). The internal bark color is within the range frombrown with pink tones to clear brown with red tones; it reaches up to 5 mmthickness and it is brittle and astringent (Pennington and Sarukhan, 1968;Rebollar et al., 1994).

Wood

The color of sapwood is from cream with yellow tones to clear chestnut withyellow tones. The color of heartwood shows from dark gray to chestnuthues. Its odor is not characteristic and it shows a bitter flavor. It shows anintermediate brilliancy and a stressed veined. The wood texture is delicateand fibers are straight. Pores, axial parenchyma and rays are only visiblewith a magnifying glass. The growth zones are not clearly observed(Pennington and Sarukhan, 1968; Rebollar et al., 1994).

Fig. 1. P. sartorianum. The tree has a straight stem with ascending and thick branches(A) Stem is characterized by a scaly external bark (B) Leaf is decussated, simpleand its margin is entire (C).



Youth branches

They are scaly, from dark gray to brown gray, without lenticels, pubescentwhen young but glabrous as aged (Pennington and Sarukhan, 1968).

Leaves

Buds are up to 0.5 mm, rounded, covered with scales, tanned glabrous.Stipules are absent. Leaves are decussated, simple. Blades are 1.5-6.5 cmlength and 0.7-2.3 cm width; they are ovate and occasionally obovate,lanceolate or elliptic. Margin is entire, acute apex and a long or obtuseacumen. Leaf base is acute, rounded or cuneate, sometimes decurrent overthe petiole. The upper side of a leaf is green with yellow tones and brilliantand the lower side is pale green; both surfaces are glabrous (Fig. 1C). Petiolesare 1-4 mm high and glabrous. A high number of transparent glands coverall the surface of the blade. Leaves are completely renovated during Apriland May (McVaugh, 1963; Pennington and Sarukhan, 1968; Rebollar et al.,1994; Standley, 1924).

Flowers

They are rarely solitary or form trifloral cymes usually being the centralflower sessile and the laterals having peduncles of 7 - 8 mm length. Solitaryflowers have peduncles of 10-15 mm length and are pubescent (Fig. 2A and2B). Flowers are aromatic, actinomorphic and of 12-15 mm diameter. Calyxhas a cupule-like base of 3 mm length, closed as a button; it has four recurvedlobes of 1.5 mm length, they open irregularly and both surfaces are denselycovered by glands. Petals 1-5 are 2-4 mm long; sometimes one or morepetals are smaller; they are orbicular, inserted in the neck of the calyxtube, below the petals. Anthers are 0.4-0.5 mm length; style is thick of 4-5mm length, it is as taller as stamens; near the base, style is pilose andcapitated. Ovary is inferior, 2-3 loculed, with a high number of ovules (around20 per lobe) (McVaugh, 1963; Pennington and Sarukhan, 1968; Rebollar etal., 1994; Standley, 1924).

Fruits

They are globulous pear-like berries, of 1.0-2.5 cm diameter and yellowwhen ripe. Flavor is similar to guava (P. guajava), sweet to acid-sweet,mesocarp is fleshy and of 1-2 cm width and it has a calyx frequentlypersistent (Fig. 2C). Seeds are angular (1-2 per lobe, 1-5 per fruit), of 5-8mm length, hard and of yellow color (Fig. 2D). The season of fruit maturationis mainly from September to March; however, P. sartorianum may flowermore than once and it may produce fruits in other months of the year(McVaugh, 1963; Pennington and Sarukhan, 1968; Rebollar et al., 1994;Standley, 1924).



Distribution

In America, the presence of P. sartorianum has been registered in thefollowing countries: Mexico, Belize, Guatemala, Nicaragua, Cuba, CostaRica, Panama, Honduras, El Salvador, Colombia, Venezuela, Ecuador, Peruand Bolivia (McVaugh, 1963; W3T, 2005).

In Mexico, P. sartorianum is found in the following States along theGulf of Mexico: Veracruz, Tabasco, Campeche, Yucatan and Quintana Rooand in the States of the Pacific Ocean strip, Sonora, Sinaloa, Chihuahua,Durango, Nayarit, Jalisco, Colima, Queretaro, Michoacan, Guerrero, Oaxacay Chiapas (McVaugh, 1963; Pennington and Sarukhan, 1968; Rebollar etal., 1994; Standley, 1924).

In the State of Sinaloa, P. sartorianum is distributed along and acrossthe State. Its presence has been reported in the Municipalities ofBadiraguato, Mocorito, Culiacan, San Ignacio and Escuinapa (Aguilar-Hernandez H. 116, 223; Gutierrez-Garcia J.A. 99, 121, 212, 622, 811;Hernandez-Alvarez F. 1175, 1382; Hernandez-Vizcarra J.A. 359 y Vega-Aviña R. 851, 2636, 5400, 7340, 7636, 8008, 8164). These materials were

Fig. 2. P. sartorianum flowers are actinomorphic, in trifloral cymes and they have acupule-like calyx (A and B). Fruits are globulous berries (C) and seeds are angu-lar and hard (D).



consulted in the ‘Jesus Gonzalez Ortega’ (UAS) herbarium of the Faculty ofAgronomy, Autonomous University of Sinaloa.

Ecology

P. sartonianum grows in deciduous tropical forests and in sub-deciduousforests (sub-perennis median forests and subdeciduous); it is also foundwithin the secondary vegetation. The soil types where P. sartorianumgrows are so varied from clayish to sandier. In Chihuahua, Durango,Guerrero, Jalisco and Oaxaca, States of Mexico, P. sartorianum has ariparian habitat, it grows in oak forests and in pine-oak forests, as well aswith other coniferous trees, in lands in the range of 700 m to 2450 mabove the sea level. In Sinaloa, Mexico, P. sartorianum plants have beenfound from the sea level up to 800 m above. They appear either as smallforests or individual plants. Fishbein et al. (1998) have registered ‘it isnot a dominant species in the forests but it shows a irregular dispersionin ravines and canyons’ (CIDE, 2005; McVaugh, 1963; Pennington andSarukhan, 1968).

Management. P. sartorianum is propagated by seed and by airlayering. It is cultivated in family orchards for ornament or by its ediblefruit (CIDE, 2005).

The Importance of Psidium genus as a source ofbioactive components

Phytochemicals and health

Around the world, undernutrition and malnutrition are related with themain causes of morbidity and mortality. These nutritional deficienciesaltogether with poverty and poor sanitary conditions are strongly correlatedwith infectious diseases in which parasitic diseases are included (WHO,2003).

During the 40´s, with the success of the treatment of infections withantibiotics, it was believed that the era of infectious diseases was near toan end. However, these diseases are still a public health concern and theircontrol and prevention are a priority for governments and for internationalhealth organizations. In 2002, the World Health Organization registeredmore than 10 million deaths by infectious diseases (WHO, 2003). Consideringbacterial diseases, one of the most important factors that contribute to theirpersistence is the appearance of the resistance phenomenon (WHO, 2002).The selection pressure has favored the emergence of resistant strains;nowadays, the overuse and misuse of antimicrobial agents by human beingis an important component of this pressure and resistance is sometimesdeveloped in very short periods of time (Tabla 1) (Hancock and Strohl, 2001;Walch, 2003).



Usually, the treatment of human and animal parasitary diseases hasbeen focused in the use of antiparasitary agents with multiple activitiessuch as nitroimidazols, benzimidazols, macrocyclic lactones, imidathiazolesand tetrahydropyrimidines. Most of these antiparasitary agents weredeveloped during the 50´s with the exception of nitazoxanide, which is anitroimidazol that were developed 20 years ago for the treatment ofhelmintiosis and protozoosis (Watkins, 2003). Most of these drugs are stillin use in spite of their toxicity and the inefficiency of most them,characteristic mainly associated with the appearance of resistant parasites(Geerts and Gryseels, 2001; Land and Johnson, 1999; Sundar, 2001). Aswith other microbial diseases, resistance phenomenon is one of the maintroubles associated with chemotherapy of a range of parasitary diseases;and drug exposition and parasite biology are both involved in suchphenomenon. The mechanisms involved in the development of resistanceare various and within them are included increment in the efflux rate ofdrugs by changes in membrane transporting channels and increment of adiverse range of enzymes, among others (Hopkins and Hunt, 2003).

The control of parasitic diseases based on a good diagnostic and in theuse of effective drugs is a priority. However, if effective antiparasitic drugsare not available, helmintiosis as well as other parasitosis could be includedas new members of the nowadays known ‘neglected diseases’ (Horton, 2003).

Up to date, huge efforts have been carried out to solve the antimicrobialresistance problem and the strategy of scientists has been focused in twoaspects: to find new targets for antimicrobial agents and to develop newantibiotics and antiparasitary drugs with improved activity (Alkane andProjan, 2000; Donadio et al., 2001; Pauli, 2003; Schmidt, 2004; Walch, 2003).

Tabla 1. Evolution of resistance to antibiotics*

Antibiotic Year deployed Resistanceobserved

Sulfonamides 1930s 1940s

Penicillin 1943 1946

Streptomycin 1943 1959

Chloramphenicol 1946 1959

Tetracycline 1948 1953

Eritromycin 1952 1988

Vancomycin 1956 1988

Methicillin 1960 1961

Ampicillin 1961 1973

Cephalosporins 1960s Late 1960s

*Adapted from Walch (2003).



On the other hand, in countries with high income, a major public healthconcern is represented by chronic diseases such as cardiovascular diseases(CVD), diabetes, cancer and obesity. A range of human diseases are causedby mutations and during the XX century around 1000 diseases wereassociated with such changes. Indeed, 97 % of the diseases appear bymonogenic mutations. However, chronic diseases have been correlated withchanges in multiple genes, e.g. 75 loci were correlated with obesity in mice.In addition, food overconsumption is associated with the appearance ofchronic diseases and a relationship has been established with geneexpression, although such studies are hard to replicate. Plantphytochemicals may affect the expression of multiple genes; e.g., thephytosterol genistein shows inhibition of certain protein kinases and inanother reaction bind sterol receptors; these two reactions affect theexpression of different genes (Kaput, 2004).

Historically, plants have been the main source of bioactive compounds.They have been used by different cultures around the world. However, theproduction of scientific evidence of such properties started in the XIX centurywith the discovery of quinine, morphine and codeine. In addition, theimportance of natural products is still remarkable. Approximately 40 % ofthe new drugs developed in North America during the period 1983-1994were of natural origin (Phillipson, 2001; Simmonds, 2003).

Plants are also important components of foods. In fact, the term‘functional foods’ has been introduced to describe foods whose componentsprovide health benefits, prevention or treatment of diseases, in addition totheir nutritive value. The ‘functional’ characteristics are mostly associatedwith phytochemicals derived from dietary or medicinal plants (e.g. soybean,garlic, tea, curcumin) (Table 2). As a matter of fact, the fruit of guava (P.guajava) is considered a functional food (Pennington, 2002).

Epidemiological and animal model studies suggest the ability offunctional foods to prevent or treat several diseases such as cancer. It hasbeen observed a good correlation between dietary intake of tomato andreduced risk of cancer and CVD. The same correlation was observed betweentea polyphenols and cancer, CVD and inflammatory diseases. Pureflavonoids (genistein, quercetin and rutin) inhibit carcinogenesis in animalmodels. Cafeic acid and curcumin are other compounds with potent activitiesagainst skin carcinogenesis in mice (Gosslau and Chen, 2004). Cannabinoidsand curcumin have shown activities against autoimmune diseases (Bright,2004).

Interestingly, a prospective cohort study with Finnish men of theEastern part of Finland showed that fruit and vegetable consumptionreduces the mortality by cardiovascular and non-cardiovascular diseases.This part of the world is characterized by mortality rates 10 times higherthan the observed in the Mediterranean area and a low consumption offruit and vegetables. In decreasing order, vitamin C, folate, lycopene andvitamin E were the nutrients with the highest negative correlations with



all-cause mortality. The benefits of the consumption of fruits and vegetablesare correlated with a range of phytochemicals, with a higher consumptionof fiber, potassium and magnesium, as well as with a low eating of fat,energy and sodium (Rissanen et al., 2003).

A negative correlation between cancer cell proliferation and the intakeof some plant compounds from fruits and berries (rosehips, blueberries,black currant, black chokeberries, apple, sea buckthorn, plum, lingonberries,

Table 2. Classification of plant bioactive components.*

Group Compund(s) Source

Carotenoids a -Carotene Carrot, sweet potatob -Carotene Grapefruit, tomatob -Cryptoxanthin Apple, cantaloupe, mangoLycopene Guava, grapefruitLutein Kiwifruit, broccoliZeaxanthin Corn, red pepper

Flavonoids Anthocyanins Apple, berries, peachFlavanols/flavans Apple, nectarine, teaFlavanones Lemon, orange, tomatoFlavones Orange, carrot, pepperFlavonols Orange, berries, appleIsoflavones/ isoflavonoids Green beans, legumes

Tannins – Nuts, cocoa, wine, guavaAllyl/diallyl sulfides – Garlic, onion

Capsaicin – Hot pepper

Omega-3-fatty acids Conjugated linoleic acid Vegetable oils

Indoles – Broccoli, brussels sprouts,cabbage

Monoterpenes – Lemon, orange

Phenolic acids Cinnamic acids (caffeic , Apple, berrieschlorogenic, p-coumaric, ferulic)

Citric acid Citrus fruits, guavaEllagic acid BerriesGalic acid Cocoa, tea, wine

Plant sterols Beta sitosterol Apple, apricot bananas,almonds, peas, soybeans

Brassicasterol Sunflower seedsCampesterol Apple, fig, carrotPhytosterol Legumes, nuts, seedsSaponins GarlicStigmasterol Banana, fig, lemon

Pectin – Apple, cherries, guava

Resveratol – Red grapes, wine

*Adapted from Pennington (2002).



cherries and raspberries) has been observed, i.e. vitamin C, the sum oflutein and b-carotene and the anthocyanins. It is suggested that protectiveeffect of such compounds might be due to additive or synergistic actions(Olsson et al., 2004). Outstandingly, the seeds of several fruits (avocado,jackfruit, longan, mango and tamarind) have higher antioxidant activitiesthan the edible portion. These seeds are commonly discarded but if a lackof toxicity is confirmed, seeds could be used as a source of functionalcomponents (Soong and Barlow, 2004).

Table 3. Ethnobotanical uses of plants of the Psidium genus.*

Specie Use

P. cinereum Hemorrhage

P. guajava Analgesic, antiseptic, astringent, bactericide, bronchitis,cachexia, carbuncle, catarrh, cholera, chorea, cicatrizant,cold, colic, convulsion, cough, deafness, dentrifice,depurative, dermatosis, diarrhea, dropsy, dysentery,dyspepsia, emmenagogue, epilepsy, evil eye, fattening,fever, gingivitis, hemostat, hemorrhoid, hysteria,intestinal diseases, itch, jaundice, laxative, leucorrhoea,nausea, nephritis, respiratory diseases, rheumatism,scabies, skin diseases, sore, spasm, sprain, stomachdiseases, swelling, tonic, ulcer, vermifuge, vulnerary,wound

P. incanescens Astringent, hemorrhage

P. sartorianum Astringent, tonic

*EhtnobotDB (2004).

Uses in traditional medicine

Psidium plants are native to America but are worldwide distributed.Moreover, they are traditionally used in the prevention or treatment of alarge number of diseases (Table 3) (EthnobotDB, 2004). Preparations oftwigs or leaves of Psidium species are extensively used for the control ofgastrointestinal and respiratory disorders as well as in the treatment ofskin damage (Anesini and Perez, 1993; Caceres et al., 1993; Caceres et al.,1991). Within this genus, P. guajava is the most studied and used species.The traditional medicinal use of every part of the plant in the prevention ortreatment of diseases has been registered. Some of the traditional uses areshared between countries although the preparation and intake show somedifferences (Table 4).



Table 4. Traditional medicinal uses around the world, of different parts of Psidiumguajava.*

Use/treatment of Preparation Country(ies)

FruitDiabetes Dried fruit Brazil

Fresh fruit juice Taiwan

Diarrhea Dried fruit BrazilFresh fruit juice HaitiHot water extract Panama

Dysentery Hot water extract of green fruit Senegal

Digestive Hot water extract of fruit Mexico

Leaves

Cough Drops of boiled leaves are mixedwith oil fruit of Orbignya martiana Bolivia

Pain Dried leaves of P. guajava andCitrus aurantium are mixed andcrushed to treat pain aroundthe navel Cook IslandsInfusion of dried leaves to treatpostpartum pain

Sores Dried leaves macerated alone orwith coconut oil are applied tothe sores Cook Islands

Hot water extract is appliedexternally Guatemala,

Tanzania

Diarrhea Infusion of dried leaves and root FijiDecoction of dried leaves Haiti, India,

Sierra

Leone Hot water extract of young leaves Madagascar

Hot water extract or infusion of Mexico,leaves Peru, Senegal

Fresh leave juice Papua–New Guinea

Dysentery Fresh leaf juice is taken orally Fiji, RarotongaHot water extract of dried leaves Rwanda

Diabetes Hot water extract of dried leaves Thailand

RootsEmmenagogue Hot water extract IndonesiaDiarrhea Water extract of dried root Nigeria, Peru

Bark

Respiratory ailments Decoction of dried bark and leaves GuatemalaDiarrhea Hot water extract of fresh bark Panama

Hot water extract of dried bark Peru



Scientific Evaluation of Biological Activities and theirAssociation with Phytochemical Components

Pharmacological effects of P. guajava extracts have been studied (Table 5)(Ross, 1999). An herbal extract of P. guajava leaf showed anti-adherenceand bacteriostatic activity against Streptococcus mutans. It is suggestedthat such activity was associated with the tannins acting by differentmechanisms. Thus, it is shown that this extract can be used in the controlof dental caries (Limsong et al., 2004). The aqueous extract of guava leafshowed a significant effect against Escherichia coli O157:H7, the minimalinhibitory concentration was less than 3.12 mg / ml (Sririak et al., 2004)and it also showed activity against rat induced salmonellosis by S. typhi.Extract was evaluated at doses of 10-50 mg / 100 g and up to 30 mg, secondaryreactions are not observed. The effectiveness of the aqueous extract wassimilar to that obtained with chloramphenicol, treatment of election forthis infection (Etuk and Francis, 2003). An aqueous extract of guava leafshowed anti-coughing activity in rats and guinea pig and antimicrobialagainst Staphylococcus aureus and b –Streptococcus group A (Gnan andDemello, 1999; Jaiarj et al., 1999). Interestingly, a methanolic extract of P.guajava leaf showed antidiarrhea activity acting as a growth inhibitoryagent of diarrhogenic pathogens (i.e. Salmonella ssp., Shigella ssp. andenterophatogenic E. coli); moreover in rats, methanolic extract reducesthe intestinal motility and the prostaglandin E2 induced enteropooling(Lin et al., 2002). In addition decoction of guava leaf and bark showedantiamoebic activity, the bark preparation was better than leaf preparationwith a MIC £ 7.81 m g / mL (Tona et al., 1998).

A butanol fraction from P. guajava leaf showed antihyperglycemicactivity in mice affected by diabetes type II. This fraction inhibited the

Hot water extract of young shoots SenegalDysentery Hot water extract of bark Mexico

Flowers

Antihelmintic Fresh flowers are crushed withthe juice of buds India

Emmenagogue Hot water extract of flowers andfruits Panama

Liver diseases Hot water extract of driedbranches Taiwan

* If any other way is indicated, preparation is taken orally.Adapted from Ross (1999).

Table 4. (Contd.)

Use / treatment of Preparation Country(ies)



protein tyrosin phosphatase 1B (PTP1B), an enzyme that is a major mediatorof insulin signaling and insulin resistance. Moreover, the butanol fractionreduces the accumulation of fat in liver. Thus, it is suggested that the butanolfraction of guava leaf can be used in the prevention and treatment of diabetestype II (Oh et al., 2005). The antidiabetic activity was also observed in anaqueous extract of P. guajava stem bark at a dose of 250 mg / kg in ratswith diabetes induced by alloxan. Moreover, the glucose tolerance wasincreased in normal rats (Mukhtar et al., 2004a); in the same model, ethanolextract of leaf showed hypoglycemic activity (Mukhtar et al., 2004b).

Table 5. Pharmacological activities of P. guajava extracts.*

Activity Observations

Analgesic Ethanol/water of aerial parts at a dose of 0.094 mg / kg inmice

Antibacterial Extracts of different polarity from aerial parts have ac-tivity against a large number of bacteria such as Staphy-lococcus aureus, Streptococcus pneumoniae, Pseudomonasaeruginosa, Salmonella typhi, Escherichia coli, Shigellaflexneri, S. dysenteriae, among others

Antidiarrheal Decoction of dried leaves at a dose of 10 ml / kg in rats.Ethanol (95%) extract of dried leaves at 750 mg / kg inmice

Antiedema Dried fruits at a dose of 100 mg/kg and ethanol / waterextract at 0.094 mg/kg, in rats

Antifungal Extracts of different polarity of aerial parts, were activeagainst Fusarium oxysporum F. sp. Lentis

Antihyperglycemic Ethanol/water extract of dried leaves at a dose of 200 mg /kg in rats. Water extract of fresh fruit at 5 and 8 g / kg inrats and at 1 g / kg in mice. Fruit juice at 1 g / kg wasactive in humans

Antimutagenic Extracts of different polarity of fresh fruits and other aerialparts in the Ames assay

Antispasmodic Ethanol / water extract of dried fruit on rat ileum

Antiyeast Ethanol extract of aerial parts against Candida albicans

Spasmogenic Water extract of dried leaves at a dose of 20 mg / kgadministred by gastric intubation to rats

Spasmolytic Butanol extract of dried leaves at a dose of 0.2 mg / ml onguinea pig illeum

* Adapted from Ross (1999).



An aqueous extract of P. guajava leaf showed cardioprotective activity,it controls the myocardial contractile dysfunction caused by the ischemia-reperfusion process. The loss of ATP and lipid peroxidation associated withthis process decreased. It is suggested that guava extract activity isassociated with its antiradical–antioxidant activity (Yamashiro et al., 2003).

Some of the biological activities observed in plant extracts of Psidiumssp. have been associated with specific compounds (Table 6). As a matter offact, the presence of lectins in guava fruits has been associated with thelow incidence in Mexico of enterohemorrhagic disease caused by E. coliO157:H7 because the high consumption of this fruit (Coutiño-Rodriguez etal., 2001); however, more studies are required in order to support suchhypothesis. The phytodrug QG-5 standardized for the flavonoid contentand evaluated with human patients with diarrhea, showed positive resultsand it was well tolerated (Lozoya et al., 2002). It is suggested that the painrelief properties of P. guajava and P. pohlianum leaf extracts could beassociated with an antinociceptive effect of their essential oils (Santos etal., 1996, 1998). An ethanolic extract of P. guajava leaf also showedantinociceptive activity; the effect was similar to equivalent doses ofmefenamic acid (Somchit et al., 2004). In addition, P. guajava leaf infusionsshowed analgesic and sedative activities. It produces a prolongation ofthe sleeping time induced by phenobarbitone suggesting an additivedepressant CNS effect (Shaheen et al., 2000). Bioactive compounds suchas carotenoids, flavonoids, phenolic acids, terpenoids and tannins have beencharacterized from different parts of P. cattleianum and P. guajava (Table2). Thus, the biological activities of Psidium genus have a clear correlationwith its composition (EthnobotDB, 2004; Pennington, 2002).

P. sartorianum

In order to get a rational exploitation of our natural resources, our researchgroup is interested in the establishment of the multipurpose potential ofnative plants to Mexico. To achieve such goal, the knowledge of native plantsmust be deep and wide from biology to biological activity. One of the mostinteresting models for our research group is P. sartorianum.

Traditional uses

In Mexico, the whole plant is used. Wood is used as a construction material,either for houses or railroads and as firewood as well. Furnituremanufactured with P. sartorianum wood is appreciated by its hardnessand its good finishes. It is also cultivated as orchards because of its ediblefruits and its natural beauty. Plants are also found in wild areas. Fruits arecollected from November to March and they are fresh products in traditionalmarkets. Fresh and dried fruits are frequently used in larger quantities for

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Psidium sartorianum

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Table 6. Biological activity and compounds in Psidium ssp.

Activity Observations Responsible compound Reference

Spasmolytic Leave extracts of P. guajava produce a relaxation Quercetin Lutterodt, 1989; of the intestinal muscle of rats, cobayo Lozoya et al., 1994;

Morales et al., 1994

Hyperglycemic inhibition Alcoholic extracts of P. guajava Isostricnine, stricnine Maruyama, 1985

Antifungic Dichlormethane extracts of P. acutangulum 3-Formil-2’,4’,6’-trihydroxi-5’- Miles et al., 1991leaves show activity against Rhizoctonia solani methyldihydrochalconeand Helminhosporium teres

Antimutagenic Leave methanolic extracts of P. guajava showed (+)-Gallocatechin Matsuo et al., 1994bio-antimutagenic activity in the Ames assay.The responsible compound is also present infruits altough it is lower than in leaves

Antibacterial The antibacterial activity of a methanolic extract Mainly associated to glycosides Arima and Danno, 2002of P. guajava is mainly due to flavonoids. Activity and aglycones of morin andwas evaluated against Salmonella enteritidis and querectin; e.g., morin-3-O-a-L-Bacillus cereus lyxopyranoside and morin-3-O-a-

L-arabopyranoside.

Gastrointestinal activity The fruits of P. guajava have a lectin that inhibits the Two guava galactosa-specific Coutiño-Rodriguezbacterial adhesion of E. coli O157:H7. Guava lectin lectins et al., 2001inhibits the E. coli Hemagglutinating activity

Antispasmodic A plant remedy (QG-5) elaborated from P. guajava Flavonoids Lozoya et al., 2002leaves and standarized for flavonoid concentrationof 1 mg/ 500 mg of quercetin equivalents, wasevaluated. QG-5 shows an spasmolytic effect andit decreased the duration of abdominal pain

Antinociceptive P. guajava essential oil was evaluated at doses in the a-Pinene Santos et al., 1998100- 400 mg / kg range. The essential oil reduced themean number of writhes, this activity is not correlatedwith the a-pinene content, but it is correlated with thereduction of the paw licking



the production of candies, conserves, flavored waters and ice lollies. Stembark and leaves have tannins. Aerial parts such as leaf are used by theirtonic and astringent properties, 10 g of leaf is boiled in 250 ml of water.This preparation is used to treat vomit, diarrhea, stomachache and coughing.Macerated fruit and leaf are used topically in wounds, infected parts andskin ulcers. This plant has also been used for the treatment of asthma andupset stomach. In Sinaloa, the stem is used in the treatment of dentalabscess and skin wounds (CIDE, 2005; Pennington and Sarukhan, 1968;Rebollar et al., 1994; Standley, 1924).

Characteristics and nutritional components of fruit

Edible portion

Fresh fruit analyses are shown in Table 7. The outer color of the fresh fruitis green in unripe stages and color turn to yellow as ripening is advancing.Outer color is similar to that of ripe lime (Fig. 2C). The color of the ripefruit is clearly represented by the reflectance parameters. The peel color isbetter represented by the L* and b* parameters (Table 7). Fruit luminosityis high and color is dominated by a yellow hue. Moreover, although the a*parameter showed a high standard deviation, it took negative values,representing a green component in the color of ripe fruit.

The shape of P. sartorianum fruit is spherical but of heterogeneoussize ranging from 1 to 2.3 cm (Fig. 2C and Table 7). The ratio of the edibleportion to seed of ripe fruit corresponds to 88 % and 12 %, respectively.This ratio was better than that reported for some varieties of P. guajavafruit (64.6-79.3 % of edible portion) (Lakshminarayana and Moreno-Rivera,1978) and it was similar to that observed in other fruits (e.g. orange with 83and 17) and vegetables (e.g. chayote with 85 and 15) (Martinez-Correa etal., 1992). Fruit firmness evaluated with a digital penetrometer (JohnChatillon & Sons, Inc. US) was of 3.6 N. Pressure was applied in theequatorial part of the fruit and using a speed of 15 mm / min in order toproduce a depression of 1 mm.

P. sartorianum is a juicy fruit, acidic as indicated by its pH and acidityand sweet as indicated by its °Brix. The pH is lower than the reported for P.guajava fruit (3.6-4.48) (Chyau and Wu, 1989; Lakshminarayana andMoreno-Rivera, 1978) and it is in the range of values corresponding to limesand oranges (pH 2.6-4.3). In addition, P. sartorianum fruit is an excellentsource of vitamin C providing more than 20 % of the recommended dailyintake (60 mg / day) (FNB / FNIC, 2001).

The composition of the edible portion of P. sartorianum fruit is givenin Table 8. Values are compared in dry weight basis with the exemption ofmoisture. The moisture value (74.8 ± 0.13) is within the range of otherfruits. The protein content of P. sartorianum is lower than that reportedfor the fruit of P. guajava (5.9 g / 100g). The content of proteins of common



fruits is ranging from 1 g / 100 g (apples) to 14 g / 100 g (rhubarb). Proteincontent of P. sartorianum is toward the lower values (USDA, 2002) and ithas a low fat content; its content is similar to that reported for P. guajavaand it is lower than that observed in common fruits (0.37-4.99 g / 100 g)(Martinez-Correa et al., 1992; USDA, 2002; Yadava, 1996). The ash contentis similar to that observed in kiwi (3.78 g / 100 g) and higher to that observedin oranges (3.00-3.34 g / 100 g) (USDA, 2002). The crude fiber content of P.sartorianum is higher than that of P. guajava (5.1 %), apple (1.1 g / 100 g)and carrot (1.1 g / 100 g) (Yadava, 1996; Badui-Dergal, 1999). The energyvalue provided by the edible portion of P. sartorianum is comparable tothat observed in common fruits (1069-1579 kJ) (USDA, 2002).

Antinutritional compounds were also detected in P. sartorianum fruit(Table 8). The tannin content of P. sartorianum pulp is higher than thatreported for P. guajava (6-11 mg /g) and for other fruits (0.2-1 %)

Table 7. Physicochemical analyses of ripe and fresh P. sartorianum fruit.

Color parametersa

L* 74 ± 2.3

a* -6 ± 2.2

b* 47 ± 2.4Dimensions (cm)a

Height 1.6 ± 0.23Width 1.6 ± 0.26

Length 1.6 ± 0.27

Weight (g) a 4 ± 0.9

Edible portion/seed ratio a 7.6 ± 0.08pH b 2.86 ± 0.013

Total acidity b, c 1.9 ± 0.06

Total soluble solids (°Brix) b 17 ± 0.0

Vitamin C (g / 100g) b 53 ± 2.1

aValues are the mean ± SD of 25 measurements.Color was determined in the peel of ripe fruits. It was evaluated by reflectance using a

Minolta Colorimeter CR-310 (Minolta Co., Japan). Three equatoraial measurements sepa-rated from each other 120° were taken in every sample fruit.

Dimensioning was evaluated using a dial caliper (Precision Graphic Instruments Inc.,USA). Hardness of ripe fruits was measured using a Chatillon DFIS 50 apparatus (JohnChatillon & Sons, Inc., USA) as follows: a tip was used to perforate up to 1 mm of the pulp,maximum force was recorded as a hardness descriptor.

Weight was determinde using an analytical balance.bValues are the mean ± SD of at least five measurements.cIt is expressed as percentage of citric acid.Chemical analysis were carried out by standard methods (AOAC, 1990): soluble solids

with an Abbé refractometer (Milton Roy Co., USA) and represented as °Brix; pH with a digitalpotentiometer (OrionR, USA); total acidity; moisture; and vitamin C.



(Lakshminarayana and Moreno-Rivera, 1978; Sánchez-Regueiro and Bilbao-Reboredo, 1996); whereas the phytic acid content was similar to that ofbeans (0.84-1.12 g / 100 g) and defatted soy (1.64 g / 100 g) (Oatway et al.,2001). Fruits are consumed in lower quantities than legumes and cereals.It is not expected to observe antinutritional effects by P. sartorianumconsumption. Moreover, the presence of these compounds could be beneficialin the prevention or treatment of infectious diseases and cancer (Lachance,1997; Oatway et al., 2001; Ross, 1999; Shamsuddin, 2002; Spiller, 1993).

Seed

The composition of the seed of P. sartorianum is shown in Table 8. Seedhas low protein content as compared with other common seeds such asblack beans (24.32 g / 100 g) and soybeans (39.90 g / 100 g) (USDA, 2002). Thefat content is low as compared with other seeds such as soybeans (21.80 g / 100g), flaxseed (37.26 g / 100 g) and sunflower (49.26 g / 100 g) (USDA, 2002).The ash content of P. sartorianum seeds is lower than that observed insome common nuts and seeds ranging from 2.49 (peanuts) to 5.24 g / 100 g(pumpkin seeds) (USDA, 2002). The crude fiber is higher than that of peanutand two varieties of Leucaena leucocephala, K8 and K28, whose content is2, 16 and 13 mg / 100 g, respectively (Muller and Tobin, 1986; Sethi andKulkarni, 1994). The energy value of P. sartorianum seeds is lower thanthat of some common nuts and seeds, reflecting a low fat content (USDA,2002). The tannins content is lower than that of some varieties of Leucaenaleucocephala seeds, K8 and K28, whose content is 7.12 and 5.47 g of tannicacid / 100g, respectively (Sethi and Kulkarni, 1994). The phytic acid contentis lower than that established for some varieties of Vigna unguiculata suchas CS-46, CS-88, GC-89691 and Cherodi, with 8.2, 9.3, 9.5 and 9.4 g / 100 g,respectively (Preet and Punia, 2000) being similar to the observed values ofsome common seeds and vegetables (Oatway et al., 2001).

Chemical components in other parts of the plant

The chemical components in the different parts of P. sartorianum are mainlyunknown. However, the yield of the leaf essential oil obtained by stemdistillation was 0.12 %. This yield was higher than that obtained from otherPsidium ssp.: P. cattleianum (0.07 %), P. fridrichsthalianum Land (0.01%), P. guajava (0.06 %) and P. guineense (0.02 %) (Tucker et al., 1995). Thechemical composition of the essential oil of P. sartorianum leaf is shown inTable 9. Remarkably, every species of the Psidium genus is characterizedby a specific pattern of the leaf essential oil components, being a -pineneone of the highest represented compounds (da Silva et al., 2003; Tucker etal., 1995; Yañez et al., 2002). Nevertheless, the chemical composition isclearly affected by a locality effect factor. In the leaf essential oil obtainedfrom Cuban P. sartorianum plants, 21 components were identified beingthe main components limonene (43 %) and a -pinene (39.5 %) (Pino et al.,



2003). In addition, in the leaf essential oils obtained from Cuban P.parvifolium and P. cattleianum, a -pinene is not represented and the maincomponents were viridiflorol (31.9 %) and epi- a -muurolol (21.9 %),respectively (Pino et al., 2004).

Scientific evaluation of antimicrobial activities

Leaf, stem and fruit of Psidium ssp. have been widely used for the treatmentof different infectious diseases affecting the digestive, respiratory, urinarytract and the skin and mucosus structures as well. Thus, we are interestedin P. sartorianum, an indigenous plant to Sinaloa, Mexico, because it ischaracterized by its ample spectrum of uses.

Antifungal and antibacterial activities

We studied the antifungal activity of P. sartorianum fruit. The methanolicextract was evaluated against different fungal species of the genus Candidaand Trichophyton (Camacho-Hernandez et al., 2004). These fungi are theetiological agents of superficial mycosis. Candida albicans is an opportunist

Table 8. Composition of P. sartorianum fruit per 100 g dry weight.

Edible portion Seed

Proximatea

Protein (g) 3.7 ± 0.21 4.0 ± 0.28

Fat (g) 0.23 ± 0.020 3.5 ± 0.22

Crude fiber (g) 14 ± 0.5 59.6 ± 0.34

Ash (g) 3.98 ± 0.030 1.63 ± 0.020

Energy (kJ) 1235 644

Tanninsa,b (g) 11 ± 0.9 0.9 ± 0.07

Phytic acida (g) 0.82 ± 0.010 0.83 ± 0.015

All values are expressed as:a the mean ± SD of five measurements.b tannins as catechin equivalents.

The moisture, crude protein (Micro Kjeldahl, N × 6.25), fat, crude fiber and ashvalues were estimated by standard methods (AOAC, 1990). For computing the energyvalues, carbohydrate content was determined by difference (not shown) and theMerrill and Watt (1973) conversion factors were used.

Phytic acid was extracted and measured colorimetrically as described by Lattaand Eskin (1980), at 500 nm with a Spectronic 21D spectrophotometer (Milton Roy,USA).

Tannins were determined as described by Price et al. (1978). Catechin (Sigma)was used as a standard reference.



fungus, it produces different clinical forms of mycosis, being the mostcommon the monocutaneous such as the stomatitis (Bonifaz, 2000).Nowadays, C. albicans has been commonly observed in systemic infections,associated with AIDS or whatever disease or situation producingimmunosuppresion . Trichophyton is a dermatophyte and the agent thatcontributes to a high prevalence of ringworm of nail (Tinea unguis), athlete’sfoot (T. pedis), inguinal (T. cruris), body (T. corporis), head (T. capitis) andof hand (T. manis) (Bonifaz, 2000). Moreover, it has been registered thatallergens are produced by Trichophyton ssp. and they induce ahypersensibility reaction, mediated by IgE. Thus, asthma could be inducedby Trichophyton infections (Woodfolk, 2005).

In our study, we establish the Minimal Inhibitory Concentration (MIC)using the tube dilution methodology. Trichophyton ssp. were more sensitiveto the methanolic extract of P. sartorianum than Candida spp. The strongestactivity was against Trichophyton mentagrophytes FM 538 (MIC = 1 mg /ml); T. rubrum FM 626, T. rubrum FM 628 and T. schoenleinii FM 48 alsoshowed a good sensitivity. On the other hand, only one strain of Candidashowed sensitivity at the evaluated concentrations. Remarkably, this strainshowed a low sensitivity to the referential antibiotic (Table 10). The responseof the fungal strains to the antifungal agent was in agreement with that ofprevious reports (Esppinel-Ingroff and Pfaller, 1995; Shadomy et al., 1987).

Our research group produced the first report on the antifungal activityof P. sartorianum fruit. Antifungal activity has been reported for P.sartorianum leaf. The polar and non-polar extracts showed activity againstCandida albicans. However, the MIC value was not determined (Ankli etal., 2002). Studies about the antimicrobial activities of other Psidium specieshave been compiled by Ross (Ross, 1999) and it is not reported any activityagainst filamentous fungi of methanolic extracts of P. guajava. Moreover,Candida albicans showed resistance against leaf methanolic extracts of P.cattleianum (Coehlo-de-Souza et al., 2004).

We have established that P. sartorianum fruit has a high content oftannins (Table 8). Such compounds could be associated with the observedantifungal activity. In our studies with extracts of Bromelia pinguin, similarresults were obtained with 13 out 19 studied strains but Candida albicansFM 206, Trycophyton rubrum FM 48 and T. schoenleinii FM 48 showeddifferent MIC values (Camacho-Hernandez et al., 2002). In B. pinguin,tannins were also found in high concentration. Moreover, the antifungalactivity of Lysiloma acapulsencis plant was also associated with the tannincomponents (Navarro et al., 2003). However, the antifungal activity of P.sartorianum could be associated with its essential oils. As an example,Backousia citridora oils showed activity against 17 filamentous fungi andone Candida sp. strain (Wilkinson et al., 2003).

Although P. sartorianum has been traditionally used for the treatmentof infectious diseases, infusions and macerated preparations of different



plant parts (CIDE, 2005; Pennington and Sarukhan, 1968; Rebollar et al.,1994; Standley, 1924), scientific information is scarce. In our laboratory,we are researching antibacterial activity against bacterial pathogens ofhumans (Streptococcus pyogenes, Staphylococcus aureus, Enterococcusfaecalis, Salmonella ssp., Salmonella typhi, Shigella ssp., Escherichia coliand Pseudomonas auruginosa). Some of these strains were isolated fromhospitalized patients or obtained from the American Type Culture Collection(ATCC). In our preliminary results, extracts of P. sartorianum fruit showeda strong activity against Staphylococcus aureus and Enterococcus faecalis,these bacterias are known by their ability to develop multiresistance; thus,it is interesting to complete our studies of antibacterial activity and toestablish which components are involved with such activity.

Polar extracts of P. sartorianum leaf have shown antimicrobial activityagainst Pseudomonas aeruginosa, Escherichia coli, Candida albicans,Staphylococcus epidermidis, Helicobacter pylori, Campylobacter jejuni,Bacillus cereus and Giardia lamblia (Ankli et al., 2002). It was alsointeresting that Escherichia coli O157:H7 is inhibited by a polar extract ofP. guajava (2.5 mg / ml) in the agar diffusion method (inhibitory zone = 7-17 mm diameter) (Voravuthinkunchai et al., 2004).

Table 9. Chemical composition of the essential oil obtained from P. sartorianum leaves.*

a -pinene (16.66) a -ylangene (2.00)

b -caryophyllene (12.35) a -humulene (1.54)

a -phellandrene (9.81) T-cadinol (1.51)

(Z)-nerolidol (5.24) b -phellandrene (1.29)

b -selinene (4.31) terpinolene (1.28)

linalool (3.55) selin-11-3n-4?-ol (1.25)

allo-aromadendrene (3.42) b -pinene (0.67)

p-cymene (3.38) aromadendrene (0.62)

viridiflorol (3.28) myrcene (0.56)

limonene (3.12) a -cadinol (0.55)

a -selinene (3.09) a -terpinene (0.35)

a -terpineol (2.71) b -bisabolene (0.34)

caryopyllene oxide (2.65) viridiflorene (0.33)

(E)- b -ocimene (2.39) b -sesquiphellandrene (0.21)

d -cadinene (2.36) d -3-carene (0.12)

(Z)- b -ocimene (2.20)

*Adapted from Tucker and Maciarello (1995). Data were obtained by GC-MS and valuesin parentheses are the mean percentage.



Antibacterial activity could be also associated with the tannins andessential oil components of P. sartorianum fruit, as it has been found withthe activity of other plants (Abdelrahim et al., 2002; Annuk et al., 1999;Caceres et al., 1993; Mandal et al., 2000; Navarro et al., 1996; Santos et al.,1997; Viljoen et al., 2005).

Nowadays, we are characterizing the antifungal and antibacterialactivities, established for extracts of P. sartorianum fruit and also in thechemical compounds associated with such activities.

Antiparasitary activity

Parasitary diseases are a public health concern and current available drugsare not effective. Thus, we have to develop new compounds, emphasizingthose that act by novel mechanisms of action to fight back the resistancephenomenon. In a previous report, a polar extract of P. sartorianum leafshowed a low activity against Giardia lamblia (Ankli et al., 2002). In ourresearch group, we are studying the antiparasitary activity of fruits ofnative plants from the State of Sinaloa, Mexico and particularly the P.sartorianum fruit.

In our research, we have developed in vitro bioassays to evaluate theactivity of plant extracts against Hymenolepis nana and Giardia lamblia.The selection of such parasites was based on two main aspects: the highprevalence and morbility of these parasitoses in most of the underdevelopedcountries and the lack of efficiency of current available drugs to eradicatethem (Drake and Bundy, 2001; Harris et al., 2001; Quhui-Cota et al., 2004;Sirivichayakul et al., 2000).

Giardia lamblia is the most prevalent pathogen protozoan in humans,mainly in children; its common habitat is the duodenum, where thetrophozoite is firmly adhered to the mucous membrane. This interactioninduces an inflammatory reaction and a mechanical obstruction of theabsorption process. Thus, host showed nutrimental deficiency of glucose,lactose, vitamins A and B12, fatty acids and folic acid among other nutrients.Symptomatology of giardiosis goes from asymptomatic to the presence ofdiarrhea, vomit, abdominal pain, lose of weight, general weakness, fatigueand hyporexia (Olson et al., 2002).

Hymenolepis nana is the most prevalent cestode in humans; it is morecommon in children than in adults. The symptomatology depends on patientsensibility and infection intensity; sometimes it is asymptomatic, but insome patients with the same parasitary charge, mesogastric pain, nausea,vomit, headache, sickness, diarrhea and / or constipation, enteritis, asthenia,hypodinamy, hyporexia, disorders in carbohydrate absorption andmalnutrition could be observed. Nervous symptoms such as insomnia,dizziness and spasms could be present as well (Becerril and Romero, 2004).

We have evaluated the antigiardiasic activity of a methanolic extractof the P. sartorianum fruit. Different concentrations were evaluated and



metronidazole was used as antiparasitary control. Parasites were incubatedin TY-S-33 culture media. The dose-response curve showed a great in vitroeffect, 50 mg / ml dose produce 100 % death of parasites in 10 min. Whenmetronidazole was evaluated at the same concentration, it showed the sameeffect only after 12 h of incubation. In Thailand, the antiparasitary activityof chloroformic and methanolic extracts of medicinal plants (e.g. Alpiniagalanga, Boesenbergia pandurata, Edipta prostrata, Piper betle, P. chaba,Zingiber zerumbet) against Giardia lamblia has been observed(Sawangjaroen et al., 2005). Moreover, the effectiveness of flower extractsof Calendula sp., Thymus sp. and Aloe barbadensis and essential oils ofCucurbita pepo and Zea mays, among others, was within 65-86 % range(Sawangjaroen et al., 2005). Some of the more active compounds isolatedfrom plant extracts against Giardia lamblia, were melitoside (coumaricacid derivative) from Teloxys graveolans and epicatechin from Rubuscoriifolius; the effect of the last compound was similar to that observedwith emetin but it was not higher than that of metronidazole (Alanis et al.,2003; Calzada et al., 2003) .

Nowadays, we are evaluating the in vitro effect of methanolic andaqueous extracts of fruit pericarp of P. sartorianum against adults ofHymenolepis nana. Praziquantel is being used as reference antiparasitary

Tabla 10. Sensitive strains to the antifungal activity (MIC) of the P. satorianum fruitpulp methanol extract.*

Strain Methanol Referenceextract** (mg / ml) agent*** (mg / ml)

Candida albicans FM 206 16 16

Trichophyton mentagrophytes FM 538 1 0.5

T. mentagrophytes FM 614 16 0.25

T. rubrum FM 245 32 0.5

T. rubrum FM 626 4 0.13

T. rubrum FM 628 4 0.5

T. schoenleinii FM 48 4 1

T. tonsurans FM 164 32 0.5

Paecilomyces varioti ATCC 22319 32 0.5

* Adapted from Camacho-Hernandez et al. (2004).** The highest concentration of methanol extract used was 32 mg/ml. The non-

sensitive strains were C. albicans FM 210, C. albicans FM 211, C. albicans FM 208, C.albicans FM 342, C. krusei FM 074, C. albicans ATCC 10231 and T. rubrum FM 639.

*** Reference agent: nystatin for the Candida strains, ketoconzole for other fungalstrains.



agent. Parasites are maintained in Hank’s modified broth. In our assay,both extracts showed activity; using, 5 and 15 mg / ml, paralysis and deathof H. nana have been observed at 5 and 15 min, respectively. Effectivenesswas higher than that observed with praziquantel evaluated at the sameconcentration, paralysis (17 min) and death (45 min). Remarkably, 25 mg /ml of P. sartorianum methanolic extract showed similar results thanpraziquantel at 50 mg / ml. We have to consider that praziquantel is a purecompound whereas the methanolic extract is a mixture of compounds.

The paralysis of cestodes induced by phytochemical compounds hasbeen reported for alcoholic extracts of root-peel of Flemingia vestitaevaluated against Raillietina echinobothrida. Flemingia vestita istraditionally used as antihelmintic agent by natives to Meghalaya, India.The activity of this plant has been associated with their flavonoidcomponents, mainly to the isoflavone genistein and by formononetin,pseudobaptigenin and daidzein. Plant extract induced a decrement in theglycogen levels associated with an activation of glycogenolytic enzymes (Daset al., 2004).

The morphologic studies by optic and electronic microscopy of treatedparasites showed swelled sections on the strobila, disorganization of thetegument characterized by damage of the basal membrane and a largenumber of vacuoles; in addition, crater-like structures were observed inthe external part of H. nana. Swelling of proglottids was observed with thetreatment with both P. sartorianum extracts; similar effects have beenreported for Hymenolepis microstoma treated with cyclosporine A. It hasbeen suggested that such effect could be associated with changes in themembrane permeability, although up to date, the mechanism of action ofthis drug is not completely clear (Wastling et al., 1992). Interestingly,damage induced by the treatment with cyclosporine A was not as severe asthat observed with P. sartorianum extracts.

Similar effects have been registered for the cysticercos of Taeniataeniformis treated in vitro with mebendazole. Observed damages includedholes in tegument, crater-like structures and disappearance of microtriches(Borgers et al., 1975).

Our results have showed clear evidence of the in vitro antiparasitaryactivity of P. sartorianum fruits. Nowadays, we are studying thephytochemical and pharmacological effects to identify the active compounds,which are related with this important biological activity.

Remarks

Psidium species belong to the Myrtaceae family. They produce an interestingrange of secondary metabolites and many of these are considered functionalcomponents.

Psidium preparations have been traditionally used for the preventionand treatment of infectious, parasitic and chronic diseases. P. guajava isthe best studied species and their health benefits have been demonstrated.



The fruit of P. guajava is a functional food considering its componentsand biological activities.

The whole plant of P. sartorianum has been traditionally used by peopleof Sinaloa, Mexico. Remarkably, fruit is edible and aerial parts have beenused to treat different diseases such as diarrhea, cough and ulcers, amongothers. However, scientific studies about the components and biologicalactivities on P. sartorianum are scarce.

The edible portion of P. sartorianum is an excellent source of vitaminC; it shows a high content of crude fiber and ash. The tannin and phyticacid content is also high. If included in diet, these characteristics couldcontribute with nutrients and biological active compounds to maintain agood health of the consumer.

P. sartorianum has components with interesting biological propertiesof importance for humans. Specially, we are looking for components thatshow activity against bacterias, fungi and parasites that have developedresistance.

Our preliminary results showed that extracts of P. sartorianum fruitinhibit the growth of dermatophytes and Candida spp. The extracts alsoinhibited Gram positive and Gram negative pathogen bacterias and theyproduce severe damages to Giardia lamblia and Hymenolepis nana. Theseinfectious agents represent a serious public health concern over the world.

P. sartorianum is an ecological resource that has not been adequatelyused in Mexico. Its traditional use and the properties of plants of this genusshowed that this species has also other potential values such as: mealproduction, medicinal uses and construction.

Acknowledgments

We would like to thank the ‘‘Consejo Nacional de Ciencia y Tecnologia’’,CECYT and FOMES for the financial support provided and to MSc JesusEspinoza-Alvarez, UAS, Culiacan, Sinaloa, Mexico, for his technicalassistance.

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