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ORIGINAL ARTICLE
Year : 2021  |  Volume : 17  |  Issue : 73  |  Page : 23-30  

Vasorelaxant and antioxidant activity of some medicinal plants from Campeche, Mexico


1 Faculty of Chemical Biological Sciences, Autonomous University of Campeche, Campeche, Mexico
2 Department of Environmental Microbiology and Biotechnology, Autonomous University of Campeche, Campeche, Mexico
3 Historical and Social Research Center, Autonomous University of Campeche, Campeche, Mexico
4 Department of Marine Resources, Center for Research and Advanced Studies Merida, Yucatan; National Council for Science and Technology, Morelos, Mexico
5 Pharmacy Faculty, Autonomous University of Morelos State, Cuernavaca, Morelos, Mexico

Date of Submission09-Jul-2020
Date of Decision31-Aug-2020
Date of Acceptance22-Dec-2020
Date of Web Publication15-Apr-2021

Correspondence Address:
Francisco Javier Aguirre Crespo
Av. Agustín Melgar S/N entre Calle 20 y Juan de la Barrera, Col. Buenavista, CP 24039, San Francisco de Campeche, Campeche
Mexico
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/pm.pm_291_20

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   Abstract 


Context: Brosimum alicastrum, Cnidoscolus chayamansa, Tradescantia spathacea, Turnera diffusa, Manilkara zapota, and Jatropha gaumeri are medicinal plants recognized in Mexican Mayan Culture. Aim: Methanol leaves extracts of these plants were use as raw material to develop a phytochemical, spectroscopy, and pharmacological analysis. Subjects and Methods: Methanol maceration was carried out and were compared in terms of yield extraction, chlorophyll, simple phenolic and flavonoids content, antioxidant activity (DPPH and β-Carotene bleaching models), as well as isolated aorta rings (E+), precontracted with noradrenaline. Results: Best content of simple phenolic and flavonoids compounds was recorder in B. alicastrum, J. gaumeri and T. diffusa. J. gaumeri extract exert an antioxidant (β-carotene bleaching: EC50: 0.8 ± 0.1 μg/mL, Emax: 85.7% ± 0.4%; DPPH: EC50: 60.3 ± 1.8 μg/mL, Emax: 60.4% ± 1.8%; P < 0.05) and vasorelaxant (EC50: 161.61 ± 7.45 μg/mL; Emax: 79.71% ± 3.88%; P < 0.05) activity in a concentration dependent-manner. Fourier transform infrared spectroscopy analysis allowed estimating a 1.26 and 2.28% of quercetin (Q) and gallic acid (GA) in J. gaumeri. GA exerts antioxidant activity in DPPH model (EC50: 1.6 ± 0.2 μg/mL; Emax: 92.9% ± 3.3%) and Q/GA (1:2) mixture improves inhibition of β-carotene bleaching (EC50: 0.005 ± 0.005 μg/mL; Emax: 69.2% ± 0.7%; P < 0.05). Conclusion: J. gaumeri is a medicinal plant employed in Mayan traditional medicine and GA and Q could be related to traditional uses, as well as responsible for the pharmacological effects. GA and Q interactions improve inhibition β-Carotene bleaching activity, which suggests greater solubility in lipophilic systems and potential interactions at the plasma membrane level.

Keywords: Antioxidant, gallic acid, Jatropha gaumeri, quercetin, vasorelaxant


How to cite this article:
Aguirre Crespo FJ, Pérez EC, Valdovinos Estrella JD, Maldonado Velazquez MG, Ortega Morales BO, Crecencio PZ, Nuñez EH, Estrada Soto SE. Vasorelaxant and antioxidant activity of some medicinal plants from Campeche, Mexico. Phcog Mag 2021;17:23-30

How to cite this URL:
Aguirre Crespo FJ, Pérez EC, Valdovinos Estrella JD, Maldonado Velazquez MG, Ortega Morales BO, Crecencio PZ, Nuñez EH, Estrada Soto SE. Vasorelaxant and antioxidant activity of some medicinal plants from Campeche, Mexico. Phcog Mag [serial online] 2021 [cited 2021 May 9];17:23-30. Available from: http://www.phcog.com/text.asp?2021/17/73/23/313496



SUMMARY

  • Methanol extracts of Brosimum alicastrum, Cnidoscolus chayamansa, Tradescantia spathacea, Turnera diffusa, Manilkara zapota and Jatropha gaumeri exerts vasorelaxant and antioxidant activity in a Concentration-Dependent Manner. Fourier transform infrared spectroscopy analysis allows the identification of Q and GA in J. gaumeri extract. Q/GA (1:2) mix enhances the antioxidant activity in lipophilic environment.




Abbreviations used: DPPH: 1,1diphenyl2picrylhydrazyl; E+: Aorta with endothelium; EC50: Half-maximal effective concentration; Emax: Maximum response achievable; FTIR: Fourier transform infrared spectroscopy; Q: Quercetin; GA: Gallic acid; NA: Noradrenaline; DMSO: Dimethylsulfoxide; BHT: Dibutylhydroxytoluene; FC: Folin-ciocalteu reagent; ChlTOT: Total chlorophyll content; βE: β-Carotene emulsion; PLS: Partial least-square; CRC: Concentration-response curve; ANOVA: Analysis of variance; AUC: Area under curve; ROS: Reactive oxygen species; RNS: Reactive nitrogen species.


   Introduction Top


Mexican healthcare agency reports that one-third of deaths correspond to diabetes mellitus, ischemic heart disease, and cerebrovascular diseases.[1] The Mexican National Health Survey 2016 reports a prevalence of hypertension of 25.5%, of these, 40% were unaware of having hypertension. On the other hand, 79.3% of hypertensive adults diagnosed are under pharmacological treatment but only 45.6% are under control.[2]

Hypertension depends of volume ejected by the heart into the arteries, the elastance of arteries and the rate of blood flow.[3] In hypertension, endothelium relaxant or contraction soluble factors regulate vascular tone and alterations are associated with morphological and functional alterations of the endothelium.[4]

In addition, oxidative stress increases arterial stiffness and it is associated with arterial remodeling.[5] It should be noted that lipid peroxidation is enhanced in hypertensive patients.[6]

Physiological stress are involved in the generation of oxidative lesions, metabolic disorders, and the development of chronic degenerative diseases.[7] In the vascular system, superoxide anion (O2) determines the biosynthesis and bioavailability of nitric oxide (NO) and together with hydrogen peroxide (H2O2) regulates the functionality of the vascular system. Reactive species play an important role in the pathophysiology of arterial hypertension.[8]

One of the worldwide research lines is focusing on the research and development of synthetic and/or natural antioxidant agents,[9] which allows the generation of prophylactic and/or therapeutic options to physiological stress associated with free radicals, among other conditions. In this sense, chemical entities present in medicinal plants could have beneficial effects by reducing oxidative stress and simultaneously favoring physiological functions such as relaxation of vascular smooth muscle. In Mexico, herbal medicine is recognized as part of Traditional Medicine and is used in the maintenance and reestablishment of health as well as in the improvement of quality of life;[10] however, few documents support the safety and efficacy of traditional use. In this context, the current research was carried out to screen the antioxidant and vasorelaxant properties of Brosimum alicastrum Sw. (Moraceae), Cnidoscolus chayamansa McVaugh (Euphorbiaceae), Tradescantia spathacea Sw. (Commelinaceae), Turnera diffusa Willd ex Schult (Turneraceae), Manilkara zapota (L.) P. Royen (Sapotaceae) and Jatropha gaumeri Greenm (Euphorbiaceae) to establish bases for the systematic search of chemical entities with potential applications to physiological stress and hypertensive diseases.


   Subjects and Methods Top


Chemical and drugs

Noradrenaline (NA), papaverine, dimethylsulfoxide (DMSO), 2,2-diphenyl-1-picrylhydrazyl (DPPH), gallic acid, quercetin, dibutylhydroxytoluene (BHT), β-carotene, linoleic acid, Tween 40, and Folin Ciocalteu reagent (FC) were purchased from Sigma-Aldrich Co (St. Louis, MO, USA). All other reagents were analytical grade from local sources. Every day, extract solutions were made using distilled water.

Plant material

Plant species were select using an ethnomedical criterion. Leaves of B. alicastrum, C. chayamansa, T. spathacea, T. diffusa, M. zapota, and J. gaumeri were employed. [Table 1] lists voucher numbers, ethnomedical, phytochemical and pharmacological aspects of each species. All species were collected in June-2017 in San Francisco de Campeche, Campeche, México and voucher specimen were deposit in University Herbarium. Plant material dry at room temperature under shade; later it was ground and stored in hermetic plastic bags (Ziploc®).
Table 1: Botanical and common names of the selected plants, voucher and their ethnobotanical, phytochemical and pharmacological studies

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Extraction

Crude extracts were prepared by maceration and were carried out with a constant mass/volume ratio (2:28), time (72 h periods), and temperature (T: 25°C). Methanol extracts were recovered, filter, concentrated under reduce pressure (Buchi® Rotaevaporator) and store in the refrigerator for further analysis. Three independent experiments were performed with three replicates each (n = 9).

Determination of chlorophyll content

Chlorophyll estimation was calculated by recording the absorbance at λ = 645 and 663 nm as well as the use of the formula ChlTOT (μg/mL): 20.2 (A645) +8.02 (A663), previously described.[47] Each evaluated sample was subjected to three-independent experiments with three replicates each.

Determination of simple phenolic content

From GA (1.04–8.2 μg/mL) or stock extract solution (10 μg/mL) 0.4 mL were transferred 0.4 mL of FC reagent in 1 mL of distilled and incubated for 20 min in darkness. The reaction was stopped with Na2CO3 10% (1.6 mL) and the absorbance was recorded at 765 nm. The simple phenolic content was expressed as equivalents (mg/g) of GA present in the plant material.[48]

Determination of the flavonoid content

From a Q (1–10 μg/mL) or extract stock solution (10 mg/mL), 0.3 mL were add to 0.9 mL of MeOH, 0.15 mL AlCl310%, 0.15 mL of CH3CO2 K 1M and 1.8 mL of distilled water. Mixtures were incubated for 30 min at room temperature and in dark conditions and absorbance was read at 415 nm. The content of flavonoids in the aqueous extracts is expressed as equivalents (mg/g) of quercetin present in leaves of each medicinal plant.[48]

Antioxidant activity (1,1-diphenyl-2-picrylhydrazyl)

From extract stock solution (1 mg/mL), serial dilutions were made until reaching final concentrations (1 → 100 μg/mL). For this, 200 μL of each concentration was added to 1.8 mL of DPPH 0.1M in MeOH; they were mixed and incubated for 30 min in the dark and then, the absorbance (λ = 517 nm) was recorded. Methanol solutions of C. sinensis (1–50 μg/mL; positive control), GA, Q and Q/GA (0.03–32 μg/mL) were used. The percentage of remaining of DPPH was calculated using the formula:

.[49] Finally, the use of a non-linear model was employed to determine the potency (EC50, [μg/mL]) and efficacy (Emax, [%]) of the antioxidant activity exerted by the extracts. Each evaluated sample was subject to three independent experiments with three replicates each.

β-Carotene bleaching test

To obtain β-Carotene emulsion (βE), 1 mg of β-Carotene were dissolved in 5 mL of chloroform and 1 mL was added to 25 μL of linoleic acid with 20 μL of Tween 40; chloroform was evaporated at 40°C, 50 mL of pure water was added and shake (βE).[50] 0.3 mL of methanolic samples were added to 2.5 mL of βE to reach 0.05 → 1.5 μg/mL for BHT, 0.05 → 280 μg/mL for extracts and 0.0005 → 5.0 μg/mL for GA, Q and (Q/GA; 1:2); methanol was use as a blank sample. Absorbencies were measure at 492 nm each 15 min during 2 h. Antioxidant activity was given by the equation ([AA − AB]/[AB0 − AB120]) × 100. AA and AB are the absorbencies of the test samples at each time and blank sample at 120 min, respectively, and AB,0 and AB,120 is the absorbance of the blank sample at t = 0 and t = 120 min, respectively. For each concentration, degradation rate was recorded and then potency and efficacy of inhibition of β-Carotene bleaching was calculated using a non-linear model. Six independent experiments were carried out on each sample evaluated.

Vasorelaxant activity

The experimental procedures were developed in concordance with recommendations of NOM-062-ZOO-1999.[51] For this, rats (Rattus norvergicus; male, Wistar, 275 ± 25 g) were maintained in a cycle of 12 h light/dark at 25°C; food and water consumption were ad libitum. The abdominal dissection allowed obtain in the thoracic aorta, it was clean of the adjacent tissue and kept in the Ringer-Krebs-Henselit solution. For evaluation, 0.3 mm segments were stabilized (3 g; 30 min). The vasorelaxant activity induced by the extracts (0.03 → 560 μg/mL) was developed according to the methodology described.[52] Test samples and positive control (Papaverine: 0.1 → 3 μg/mL) were compared with respect to the maximum contraction induced by NA (1 × 10−7 M) by using Acqknowledge software (BIOPAC®, CA, USA). Six independent experiments were carried out on each sample.

Infrared Fourier transform-infrared spectroscopy

FTIR experiments were made from crude extracts and use the powder diffuse reflectance technique; the samples pellets were prepared with 1 mg of GA or Q, 1 mg of the extract, 199 mg of KBr, and then were mix in an agate mortar. Subsequently, pellets were loaded in Thermo Nicolet Nexus 670, under the following conditions: 400–4000 cm−1 for scan ranging and 4 cm−1 of resolution.[53] FTIR spectrum of GA, Q and Q/GA mixture (25/75, 50/50, and 75/25) has been employed for estimation of GA and Q content in the extracts derived from the species under study. The weighting of the area under the curve (AUC) at 721 y 762 cm−1 presents in the FTIR spectrum of Q, GA and mixtures were used to estimate Q and GA content in crude extracts from medicinal plants under study. For this, the partial least square model was used to quantify Q and GA in complex mixtures such as medicinal plants extracts.

Statistical analysis

The experimental results are shown as the average ± the standard error of the mean. Experimental data of concentration-response curves (CRCs) were plot and adjusted by the non-linear employing curve-fitting program MicrocalTM Origin 8.0 (Microcal Software Inc., USA). Significance was evaluated using an analysis of variance; values of P < 0.05 were considered statistically significant.


   Results Top


Effect of methanol maceration on leaves extraction

The methanol maceration procedure was suitable to obtain raw material from leaves of medicinal plants. The yield was significant (P < 0.05) lower in arboreal species. Methanol maceration in arboreal species (B. alicastrum, M. zapota and J. gaumeri) also showed the significant (P < 0.05) reduction in chlorophyll extraction. Whereas the maceration with methanol ameliorates the yield and chlorophyll extraction in T. spathacea, C. chayamansa and T. diffusa. The chemical and spectroscopic analysis allows to the estimation of simple phenolic and flavonoid compounds content in all experimental methanolic extracts. Herbal species showed low content of simple phenolic and flavonoids compounds with respect to arboreal species as well as methanol extract of C. sinensis, internal control employed. In this sense, B. alicastrum and J. gaumeri extracts registered the best content of simple phenols and flavonoids compounds [Table 2].
Table 2: Quantitative analysis of methanolic extracts derived of medicinal plants from Campeche, Campeche, Mexico

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In vitro and ex vivo pharmacological evaluations

B. alicastrum, J. gaumeri and M. zapota methanolic extracts exert an antioxidant activity in a concentration-dependent manner on the DPPH antioxidant model [Graph 1] and [Table 3]. CRC analysis revealed that methanolic extract of B. alicastrum and M. zapota exerts a significant antioxidant activity with better potency and efficacy than C. sinensis (EC50: 22.9 ± 2.4 μg/mL; Emax: 98.7% ± 6.4%; EC50: 30.6 ± 0.9 μg/mL; Emax: 85.8% ± 1.7% vs. EC50: 41.8 ± 0.3 μg/mL; Emax: 94.6 ± 0.8; P < 0.05%) extract. On the other hand, among herbaceous species only T. diffusa extract exerts a great potency (EC50: 28.9 ± 3.6 μg/mL) of antioxidant activity but with low efficacy (Emax: 34.9% ± 14.2%) as free radical scavenger.

Table 3: Antioxidant (2,2-diphenyl-1-picrylhydrazyl, β-carotene bleaching) and vasorelaxant activity induced by methanolic extracts derived of the selected plants

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Extracts derived from arboreal species showed a significant (P < 0.05) inhibition of β-carotene bleaching activity. J. gaumeri (EC50: 0.8 ± 0.01 μg/mL; Emax: 85.7 ± 0.4%), B. alicastrum (EC50: 6.3 ± 0.1 μg/mL; Emax: 83.0 ± 0.1%) and M. zapota (EC50: 55.6 ± 1.6 μg/mL; Emax: 85.4 ± 0.1%) extracts exhibited an inhibition of β-Carotene bleaching activity in a concentration-dependent manner with better potency and efficacy than C. sinensis (EC50: 113.4 ± 0.04 μg/mL; Emax: 64.6 ± 1.2%) extract. Finally, methanol extracts of C. chaymansa, T. spathacea and T. diffusa do not exert a significant bleaching activity [Graph 2] and [Table 3].



Evaluation in aortic rings (E+) pre-contracted with noradrenaline (1 μM) allows to identify that the extracts of B. alicastrum, C. chayamansa, T. spathacea, M. zapota and T. diffusa do not exert a significant vasorelaxant activity. However, CRC analysis revealed that J. gaumeri extract exerts a similar smooth muscle relaxant effect than papaverine but less potency [Graph 3] and [Table 3].



Fourier transform-infrared spectroscopy analysis and estimation of gallic acid and quercetin content

Bands observed between 3600 and 3300 cm−1 correspond to stretching vibrations of OH groups typical of water, alcohols, phenols, flavonoids as well as amides [Graph 4]. Peaks at 2900–2800 cm−1 are associated with narrowing and deformation vibrations specific to -CH3 and -CH2 from lipids, methoxy derivatives, aldehydes, and cis double bonds. 1750–1600 cm−1 complex area corresponds to bending vibration of N-H (amino acids), C = O stretching (ketones, aldehydes, esters), free fatty acids (1710 cm−1), and glycerides (1740 cm−1). A 1600–1500 cm−1 area corresponds to aromatic domains and N-H bending vibrations. 1450–1300 corresponds to stretching vibrations C-O and C-C present in amides and phenyl groups, respectively. Stretching vibrations of carbonyl C-O or O-H bending were observed at 1300–1100 cm−1 area. Signals at 1030, 1050, 1105, and 1130 cm−1 were associated with stretching vibrations C-O of mono-, oligo- and carbohydrates. Finally, <1000 cm−1 area was observed C-H bending vibrations that could correspond to isoprenoids.[54],[55],[56],[57]



Quantitative determination of the inorganic and organic matter,[58] as well as natural products[59],[60] are demonstrated by KBr-FTIR in the transmission mode. In this sense, the presence of GA and Q in methanol extracts was carried out by analysis of peaks into a fingerprint-FTIR region. The FTIR spectra of Q, GA and Q/GA mixtures (25/75, 50/50, and 75/25) are presented in [Graph 5]. In 1100–600 cm−1 region, Q and GA showed 10 and 13 bands, respectively. AUC at (725–717 cm−1) and (756.5–767.8 cm−1) were employed to estimates Q and GA, respectively. AUC of Q, GA and mixtures (25/75, 50/50, and 75/25) of FTIR spectrum allow us identified a high linear correlation (r2 = 0.87) and (r2 = 0.93), respectively. This allows estimating 1.26 and 2.28% of Q and GA in J. gaumeri methanol extract. These metabolites are not identified in T. spathacea, T. diffusa, M. zapota, B. alicastrum and C. chayamansa, however, their presence is not ruled out.



In vitro evaluations of Q, GA and Q/GA (1:2) mixture

Finally, the antioxidant activity of GA, Q, and Q/GA (1:2) mix was evaluated by using the DPPH and bleaching of β-carotene models. GA, Q, and Q/GA exerts antioxidant activities in both DPPH and β-carotene bleaching models in a concentration-dependent manner [Graph 6], [Graph 7] and [Table 4]. The CRC analysis allows identified that Q/GA (1:2) mixture was markedly shifting to the right and reduce the radical scavenging activity in the DPPH model, with respect to GA. On the other hand, the CRC of inhibition β-carotene bleaching activity exerted for Q/GA mix was significant (P < 0.05) shift to the left with respect to GA and Q as well as BHT (positive control).
Table 4: Antioxidant activity induced by Quercetin, Gallic Acid and mix (1:2)

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   Discussion Top


Plantae kingdom registers a huge diversity of chemical structures, which represent an important source of new drugs. For the present work, B. alicastrum, C. chayamansa, T. spathacea, T. diffusa, M. zapota and J. gaumeri were select for their ethnomedical and pharmacological reports as well as the presence of secondary metabolites with pharmacological reports [Table 1]. Maceration is a method included in the Mexican Pharmacopoeia[61] and it is relatively advantageous to obtain the raw material from tissues derived of medicinal plants because solvents dissolve secondary metabolites in function to the polarity, temperature, and time. The assay can be employed with other polar or nonpolar solvents to obtain both lipophilic and hydrophilic chemical entities. As can be seen in [Table 2], variations in the yield as well as in the estimation of the content of chlorophyll, simple phenolic compounds, and flavonoids were registered. These results allow demonstrating the interspecies biological variability and need to use specific standard conditions for harvest and extraction of the raw material. In the study of natural products, seasonal variations, drying, and storage influence in the production of high-quality herbal products.[62] In the same way, different extraction methods are distinguished and each one presents advantages and disadvantages.[63] This context reflects the need for the employment of diverse strategies and technologies for the characterization, identification, and production of natural products.[64]

The potential emergent area is the natural antioxidants agents for their actions on ROS and RNS species generated in endothelial and smooth muscle cells from the vascular system.[65] In this sense, to explore the antioxidant and vasorelaxant effects of methanolic extracts from medicinal plants were employed DPPH and β-Carotene in vitro tests and noradrenaline-precontracted aorta rings as an ex vivo model. Methanol extracts exert antioxidant activity and the best potency and efficacy were observed in extracts derived from arboreal species (B. alicastrum, M. zapota and J. gaumeri), and no polar metabolites and polar compounds could be related with high radical scavenging activity [Graph 1], [Graph 2] and [Table 3]. The increased potency in the inhibition β-carotene bleaching test with respect to DPPH model [Table 3] suggests that J. gaumeri methanol extract could have nonpolar antioxidant metabolites. In fact, metabolites such as as α/β-amyrin,[66] sterols,[67] gallic acid,[68] and quercetin[69] act as lipid peroxidation inhibitors, however, previous studies suggest that the DPPH method is independent of the substrate polarity,[50] in this sense, metabolites as β-amyrin,[70] taraxerol,[34] β-sitosterol,[71] gallic acid[35] and quercetin[72] exert DPPH free radical scavenging activity. Quantification of natural products using FTIR has been previously reported.[73],[74] Analysis of the FTIR spectrum of Q and GA allow the estimation of these metabolites in a 1:2 ratio [Graph 4] and [Graph 5]. The mix of Q/GA exert the best parameter of potency and efficacy in the inhibition β-carotene bleaching test [Graph 7] and [Table 4] these results suggesting that lipophilic environment favor the interaction between them, reduction of ionized species, increase of non-ionized species and better interaction with lipophilic molecules.

Simple phenolic compounds, flavonoids,[75] and triterpenes[76] have been reported to exert vasorelaxant effects on rat aortic rings. α/β-amyrin open K+ channel.[77] β-sitosterol does not affect acetylcholine-induced relaxation.[78] GA modulate hemodynamic parameters[79] and quercetin, induce relaxation in a concentration-dependent manner.[80] Partial vasorelaxant effects induced by J. gaumeri [Graph 3] and [Table 3] methanol extract suggest a great diversity of chemical entities and a low abundance of those with vasorelaxant activity. In this context, metabolites such as taraxerol, β-sitosterol, α/β-amyrin as well as gallic acid and quercetin identified in leaves methanolic extracts of J. gaumeri work together in a lipophilic environment and could be participating in the antioxidant and vasorelaxant effects.


   Conclusion Top


J. gaumeri is a medicinal plant employed in Mayan traditional medicine and GA and Q could be related to traditional uses, as well as responsible for the pharmacological effects. GA and Q interactions improve inhibition β Carotene bleaching activity, which suggests greater solubility in lipophilic systems and potential interactions at the plasma membrane level.

Acknowledgements

Elias Cerino Pérez acknowledges UAC fellowship. We are also grateful to Faculty of Chemical Biological Sciences, Autonomous University of Campeche for providing the necessary facilities with which to conduct this research. We are indebted to Emanuel Gaona (Pharmacy Faculty- Autonomous University of Morelos State) and Iliana Osorio Horta (Faculty of Chemical Biological Sciences, Autonomous University of Campeche) for technical assistance.

Financial support and sponsorship

CONACYT FOMIX Campeche (286944).

Conflicts of interest

There are no conflicts of interest.



 
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