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Halophyte Plants as Sources of Antiprotozoal Agents: History
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Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor: Maria João Rodrigues , Catarina Guerreiro Pereira ,
Marta Oliveira
, Gökhan Zengin , Luísa Custódio

Aligned to their traditional uses as antiparasitic agents, halophytes have proven by in vitro and in vivo research approaches their potential as sources of molecules with activity towards different protozoa species. Most antiprotozoal studies on natural products focus particularly on neglected tropical diseases (NTDs), a group of twenty infectious illnesses that include, for example, leishmaniasis, human African trypanosomiasis (HAT), Chagas disease, and schistosomiasis. NTDs affect more than 1 billion people worldwide, particularly very poor populations in tropical and subtropical areas in 149 countries). Leishmaniasis is caused by more than 20 Leishmania species, while trypanosomiasis is ascribed to Trypanosoma, either the Trypanosoma brucei complex (sleeping sickness, human African trypanosomiasis) or T. cruzi (Chagas disease, American trypanosomiasis). Malaria, referred to as a “disease of poverty”, is no longer recognized as an NTD and is caused by protozoa of the genus Plasmodium, namely P. falciparum, P. vivax, P. malariae, and P. ovale, which are specific for humans.

  • halophyte plants
  • diseases
  • halophyte species
  • antiparasitic
  • salt tolerant plants

1. In Vitro Activities and Bioactive Constituents

Most of the reports on the antiparasitic activity of halophyte species include an in vitro screening, followed by the determination of the chemical composition of raw extracts, and less frequently of purified fractions or pure compounds. Sixteen species belonging to 14 different families have been described with in vitro antiprotozoal activity, and those reports are summarized in Table 1.
Essential oils are described as a composite mixture of volatile molecules obtained from aromatic plants, mostly by hydrodistillation, and display highly relevant biological properties, including antiparasitic activities. Essential oils were the main target to evaluate the potential antiprotozoal properties of halophyte species, mostly against Leishmania and Trypanosoma parasites. For example, the essential oil of flowering aerial parts of Crithmum maritimum was highly effective towards T. brucei parasites (EC50 = 5.0 µg/mL), which was linked to its mono-terpene hydrocarbon content, such as in limonene (EC50 = 5.6 µM; Figure 1) and sabinene (EC50 = 6.0 µM; Figure 1) [1]. However, they were less effective against L. infantum promastigotes (IC50 = 122 and 205 µg/mL, respectively) [2]. The antiparasitic features of major compounds, including monoterpene hydrocarbons, sesquiterpene hydrocarbons, oxygen-containing sesquiterpenoids, and diterpenoids, are well described [2]. In turn, the essential oil of leaves and fruits of Pistacia lentiscus exerted high inhibitory effects against promastigotes of Leishmania major, L. tropica, and L. infantum, with IC50 values varying between 8 and 26.2 µg/mL [3]. The major volatile components were myrcene and α-pinene in leaves, and α-pinene and limonene, in fruits, all reported with antileishmanial activities [4][5]. In another work, essential oils from leaves of P. lentiscus collected from two areas in Tunisia were tested against L. major intramacrophage and axenic amastigote forms [6], displaying moderate activities against intracellular amastigote (IC50 = 12.5–35.6 µg/mL), and high activity against L. major axenic amastigote forms (IC50 = 0.5 µg/mL) [6]. The main compounds were identified as pinene, β-myrcene, d-limonene, O-cymene, terpinen-4-ol, β-pinene, and α-phellandrene, which may disrupt parasite intracellular metabolic pathways [6].
Table 1. In vitro antiprotozoal activity of halophyte species.
Family/Species Plant Organ Extract/Fraction/Compound Chemical Components Protozoal Species Results * References
Amaranthaceae            
Dysphania ambrosioides (L.) Mosyakin & Clemants (syn. Chenopodium ambrosioides L.) Aerial organs Essential oil Terpinolene L. amazonensis, L. donovani Epimastigotes (IC50 = 21.3 µg/mL), and trypomastigotes (IC50 = 28.1 µg/mL) [7]
        T. cruzi Epimastigotes (IC50 = 21.3 µg/mL), trypomastigotes (IC50 = 28.1 µg/mL), and amastigotes (IC50 = 50.2 µg/mL) [7]
  Aerial parts containing immature seeds Ethanol ethylacetate extract Ascaridole [8]; (−)-(2S,4S)-p-mentha-1(7),8-dien-2-hydroperoxide [9];
(−)-(2R,4S)-p-mentha-1(7),8-dien-2-hydroperoxide [10]
(−)-(1R,4S)-p-mentha-2,8-dien-1-hydroperoxide [11]
(−)-(1S,4S)-p-mentha-2,8-dien-1-hydroperoxide [12].		 T. cruzi (epimastigotes) MLC [8] = 23 μM; MLC [9] = 1.2 μM;
MLC [10] = 1.6 μM;
MLC [11]= 3.1 μM; and MLC [12]= 0.8 μM		 [13]
  Leaves Hydroalchoholic extract ND Giardia lamblia (trophozoites) IC50 = 198 µg/mL [14]
  Leaves 70 % Ethanol extract ND Plasmodium falciparum IC50 = 25.4 μg/mL [15]
  Leaves Essential oil Ascaridole Entamoeba histolytica (trophozoites) IC50 = 700 µg/mL [16]
Anacardiaceae            
Pistacia lentiscus L. Leaves and fruits Essential oil Leaves: Myrcene and α-pinene; Fruits: α-pinene and limonene Leishmania major, L. tropica, L. infantum (clinical isolates) IC50 = 8–26.2 µg/mL [3]
  Leaves Essential oil α-pinene, β-myrcene, D-limonene, o-cymene, terpinen-4- ol, β-pinene, α-phellandrene Leishmania major Intramacrophage amastigote: IC50 = 12.5–35.6 µg/mL; Axenic amastigote: IC50 = 0.5–56.1 µg/mL [6]
Apiaceae            
Crithmum maritimum L. Aerial organs Essential oil Limonene, γ-terpinene and sabinene Trypanossoma brucei IC50 = 5.0 µg/mL [1]
  Limonene, sabinene       Limonene: EC50 = 5.6 µM
Sabinene: EC50 = 6.0 µM		  
  Aerial organs Essential oil α-pinene, p-cymene β-phellandrene, Z-β -ocimene, γ-terpinene, thymyl-methyl oxide, dillapiole L. infantum (promastigotes) IC50 = 122 µg/mL [2]
  Flowers Decoction Falcarindiol Trypanosoma cruzi Extract: EC50 = 17.7 µg/mL, SI > 5.65
Fraction: EC50 = 0.47 µg/mL, SI = 59.6		 [17]
Eryngium maritimum L. Aerial organs Essential oil α-pinene, germacrene D, bicyclogermacrene, germacrene, δ-cadinene L. infantum (promastigotes) IC50 = 205 µg/mL [2]
Foeniculum vulgare Mill. Seeds Essential oil, n-hexane, methanol, and water extracts E-anethole Trichomonas vaginalis Methanol and hexane extracts: MLC = 360 µg/mL
Essential oil and anethole: MLC = 1600 µg/ml		 [18]
  Seeds Water extract Hesperidin, ferulic acid, chlorogenic acid Blastocystis spp. 48h: IC50 = 224 µg/mL; 72h: IC50 = 175 µg/mL [19]
Asteraceae            
Inula crithmoides L. Aerial organs Dichloromethane extract Gallic, syringic, salicylic caffeic, coumaric, and rosmarinic acids; epicatechin, epigalocatechin gallate, catechin hydrate, quercetin, and apigenin Leishmania infantum Intracellular amastigotes: 70% at 125 µg/mL; Promastigotes: 26.5% at 125 µg/mL [20]
Caryophyllaceae            
Spergularia rubra (L.) J.Presl & C.Presl and Aerial organs Dichloromethane extract Catechin hydrate Leishmania infantum Intracellular amastigotes: 25% at 125 µg/mL; promastigotes: 16.7% at 125 µg/mL [20]
Cyperaceae            
Cyperus rotundus L. Tuber of root Ethyl acetate extract ND Plasmodium falciparum Sensitive strain 3D7: IC50 = 5.1 µg/mL; resistant strain INDO: IC50 = 4 µg/mL [21]
Combretaceae            
Laguncularia racemosa (L.) C.F. Gaertn. Leaves Chloroform:methanol (1:1) extract Triterpenoids, phenols P. falciparum 60.1 % at 6.25 μg/mL [22]
Fabaceae            
Glycyrrhiza glabra L. Roots Water extract Licochalcone A Leishmania major (promastigotes) Extract: > 90% death at 1:100 and 1:200 dilutions [23]
        L. donovani (promastigotes) > 90% death at 1:100 dilution [23]
    Licochalcone A   L. major Amastigotes: 0 % infection at 5 and 10 μg/mL
Promastigotes: 0.4 % at 1:100		 [23]
Juncaceae            
Juncus acutus L. Roots Dichloromethane extract and Fraction 8 Phenanthrenes, dihydrophenanthrenes, and benzocoumarins Trypanosoma cruzi (trypomastigotes) Extract: IC50 < 20 µg/mL; Fraction 8: IC50 = 4.1 µg/mL, SI: 1.5 [24]
Nitrariaceae            
Peganum harmala L. Seeds Water extract ND L. major
(Promastigotes, amastigotes)		 Promastigotes: IC50 = 40 µg/mL; Amastigotes: 50% reduction of infection at 10 and 40 µg/mL at 48h [25]
  Seeds Hydroalchoholic extract Harmaline, harmine, and beta-carboline L. major
(promastigotes)		 IC50 = 59.4 µg/mL [26]
  Seeds Water extract ND L. donovani
(promastigotes, axenic amastigotes)		 Promastigotes: ED50 = 458,000 µg/mL at 72 h; Axenic amastigotes: ED50 = 6000 µg/mL at 72 h [27]
  Seeds, Roots Methanol extract ND L. tropica Seeds: IC50 = 18.6
µg/mL; Roots: IC50 = 16.4
µg/mL		 [28]
Plantaginaceae            
Plantago major Seeds 80% Ethanol ND P. falciparum IC50 = 40.0 µg/mL [29]
Polygonaceae            
Rumex crispus L. Leaves, roots Methanol and ethanol extract ND Trypanosoma brucei brucei Etanol root: IC50: 9.7 μg/mL [30]
        Plasmodium falciparum 3D7 strain Methanol leaves: IC50 = 15 μg/mL [30]
Portulacaceae            
Portulaca oleraceae Leaves, stems Essential oils Phytol, squalene, palmitic acid, ethyllinoleate, ferulic acid, linolenic acid, scopoletin, linoleic acid, rhein, apigenin, bergapten L. major (promastigotes) Leaves: IC50 = 360 µg/mL; Stems: IC50 = 680 µg/mL [31]
Tetrameristaceae            
Pelliciera rhizophorae Planch. & Triana Leaves Methanol:Chloroform (1:1) fraction α-amyrin, β-amyrine, ursolic acid, oleanolic acid, betulinic acid, brugierol, iso-brugierol, kaempferol, quercetin, and quercetin Leishmania donovani Oleanolic acid: IC50 = 5.3 μM
Kaempferol: IC50 = 22.9 μM
Quercetin:IC50 = 3.4 μM		 [32]
        Trypanosoma cruzi α-Amyrin: IC50 = 19.0 μM [32]
        Plasmodium falciparum Betulinic acid: IC50 = 18.0 μM [32]
ND: not determined. IC50: half-maximal inhibitory concentration; EC50: half-maximal effective concentration; LC50: median lethal concentration; MLC: minimum lethal
Marinedrugs 21 00066 g001 550
Figure 1. Chemical structures of pure compounds reported with antiprotozoal properties.
Some essential oils from other species have been described with antiparasitic activities, but with higher IC50 values, such as those from P. oleracea leaves and stems (IC50 = 360 and 680 µg/mL) on L. major promastigotes [31], or from F. vulgare seeds against T. vaginalis (MLC = 1600 µg/mL) [18]. The essential oil of D. ambrosioides aerial organs have been investigated for its in vitro activity against L. amazonensis and L. donovani, being highly active towards their epimastigotes (IC50 = 21.3 µg/mL) and trypomastigotes (IC50 = 28.1 µg/mL), as well as towards T. cruzi amastigotes (IC50 = 50.2 µg/mL) [7]. Terpinolene was the major active component [7]. In addition, ascaridole, identified as the main component of D. ambrosioides leaves’ essential oil, also exhibited in vitro activity against E. histolytica parasites, which are responsible for amebiasis, a parasitic disease considered a public health problem in developing countries [16].
Extraction with organic solvents has less expression than the extraction of essential oils, but even so, it also proves to be very effective in the extraction of compounds with antiprotozoal activity from salt-tolerant species. In this context, Oliveira and colleagues [24] performed an in vitro screening of T. cruzi trypomastigotes on 94 samples belonging to 31 halophytes species from Southern Portugal. From those, the dichloromethane extract of Juncus acutus roots was the most active (IC50 < 20 µg/mL), which was further fractionated, affording one active fraction with an IC50 of 4.1 µg/mL and selectivity index (SI) of 1.5. The active constituents were identified as phenanthrenes, dihydrophenanthrenes, and benzocoumarins [24]. C. maritimum flower decoction also presented anti-T. cruzi activity with an EC50 value of 17.7 µg/mL and SI of 5.65, and a fraction rich in falcarindiol has an increased activity (EC50 = 0.47 µg/mL) and selectivity (SI = 59.6) [17].
The same research group also screened 25 salt-tolerant plant species from southern Portugal for promastigotes and intracellular amastigotes of L. infantum, and the highest activity was obtained with the dichloromethane extract of S. rubra and I. crithmoides aerial organs [20]. The active extracts from I. crithmoides were rich in phenolic acids (gallic, syringic, salicylic caffeic, coumaric, and rosmarinic acids) and flavonoids (epicatechin, epigallocatechin gallate, catechin hydrate, quercetin, and apigenin), while catechin hydrate was detected in S. rubra [20].
In addition, hexane and methanol extracts of F. vulgare seeds were highly active against T. vaginalis (MLC = 360 µg/mL) [18], whereas aqueous extracts exhibit anti-Blastocystis activity with IC50 values ranging between 223.8 and 174.9 µg/mL [19]. The predominant compounds in F. vulgare were hesperidin, ferulic, and chlorogenic acid [19]. Several authors reported the in vitro antimalarial properties of G. glabra, particularly of root and aerial part extracts [29][33][34]. Furthermore, Licochalcone A (Figure 1) was isolated from its root water extract, with activity against L. major amastigotes (0% infected cells at 5 and 10 µg/mL) and promastigotes (0.4% infected cells at 1:100). Moreover, major components of a methanol:chloroform fraction obtained from the leaves of the tea mangrove Pelliciera rhizophorae, showed high antiprotozoal activity against L. donovani (Oleanolic acid: IC50 = 5.3 μM; Kaempferol: IC50 = 22.9 μM; Quercetin: IC50 = 3.4 μM), T. cruzi (α-amyrin: IC50 = 19.0 μM), as well as P. falciparum (Betulinic acid: IC50 = 18.0 μM) (Figure 1) [32].
Other authors reported the in vitro anti-Plasmodium efficacy of ethanolic extracts of Plantago major seeds (P. falciparum: IC50 = 40.0 µg/mL) [29] and C. rotundus tuber root ethyl acetate extract (P. falciparum IC50 = 5.1 µg/mL and 4 µg/mL for sensitive and resistant strains, respectively) [21]. Peganum harmala seeds and aerial parts extracts have been extensively studied for their antileishmanial properties against L. major, L. donovani, and L. tropica as sustained by different authors [25][26][27][28].
Overall, some authors defined that extracts with IC50 values below 15 µg/mL and selectivity above 3 can be considered promising for further development as drug leads [35]. Following this guideline, the fraction of flower decoction of C. maritimum can be considered the most promising sample with anti-T. cruzi activity by coupling both criteria (EC50 = 0.47 µg/mL; SI = 59.6) [17].

2. In Vivo Studies

Only a few authors evaluated the in vivo antiprotozoal potential of halophytes, including only three species and using mainly rodents as models. These reports are summarized in Table 2.
The most studied species was D. ambrosioides, investigated by five different authors. For instance, essential oil from its aerial parts was more effective against experimental cutaneous leishmaniasis by L. amazonensis in BALB/c mice than its pure main components, namely ascaridole, carvacol, and caryophyllene oxide [36]. In turn, hydroalcoholic extracts of its leaves displayed in vivo antimalarial properties against BALB/c mice infected with P. berghei intraperitoneally [15], and in vivo effects on C3H/HePas mice infected with L. amazonensis promastigotes [37]. Moreover, ascaridole was the main component in D. ambrosioides leaves’ essential oil and exhibited in vitro and in vivo activity against E. histolytica parasites [16]. Besides, other authors reported the anti-Plasmodium efficacy of ethanolic extracts of A. officinalis flowers (P. falciparum IC50 = 62.7 µg/mL; P. berghei suppression of parasitemia in vivo [400 mg/kg] = 62.86 %), and of P. major seeds (P. falciparum: IC50 = 40.0 µg/mL; P. berghei suppression of parasitemia in vivo [400 mg/kg] = 22.5%) [29].
Table 2. In vivo antiprotozoal activity of halophyte species.
Family/Species Plant Organ Extract/Fraction/Compound Chemical Components Assay Results References
Amaranthaceae            
Dysphania ambrosioides (L.) Mosyakin & Clemants (syn. Chenopodium ambrosioides L.) Aerial organs Essential oils Ascaridole, carvacrol, caryophyllene oxide Cutaneous leishmaniasis-L. amazonensis in BALB/c mice Prevented lesion development compared with untreated animals [36]
    Mix of ascaridole, carvacrol, caryophyllene oxide   Cutaneous leishmaniasis-L. amazonensis in BALB/c mice Cause death of animals after 3 days of treatment [36]
  Leaves Essential oil Ascaridole Entamoeba histolytica HM-1 in IMSS strain
Golden hamsters infected with trophozoites		 8 mg/kg and 80 mg/kg reverted the infection [16]
  Leaves 70% Ethanol ND BALB/c mice infected with P. berghei Increased survival and decreased parasitaemia [15]
  Leaves 70% Ethanol ND C3H/HePas mice infected with Leishmania amazonensis promastigotes Reduced nitric oxide production and the parasite load [37]
Malvaceae            
Althaea officinalis L. Flowers 80% Ethanol ND P. berghei infected female Swiss albino mice Suppression of parasitemia = 62.86 %, at a dose of 400 mg/kg [29]
Plantaginaceae            
Plantago major L. Seeds 80% Ethanol ND P. berghei infected female Swiss albino mice Suppression of parasitemia = 22.46 %, at a dose of 400 mg/kg [29]
ND: not determined.

This entry is adapted from the peer-reviewed paper 10.3390/md21020066

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