Abstract
Background
Ancylostoma spp., including A. duodenale, A. braziliense, A. caninum, and A. ceylanicum, are hookworms that are transmitted from infected soil and by contact with domestic animals and rodent hosts, and can cause systemic disease and cutaneous larva migrans. The objective of this study was to describe the ecoepidemiology of Ancylostoma caninum and Ancylostoma spp. in urban-marginal sectors and in rural sectors located in Ecuador.
Material/Methods
Through addressed sampling, a total of 498 domestic dogs and 40 synanthropic rodents were analyzed via the following coproparasitic methods: direct, flotation, sedimentation with centrifugation using saline (egg identification), modified Baermann (larval identification), and morphometric methods (confirmation). A total of 236 people were surveyed, and a clinical analysis was performed via physical examination. The environmental variables were obtained through reports from the INAMHI of Ecuador and the use of online environmental programs. Through surveys, data related to social determinants were obtained. Epidemiological indicators (prevalence, morbidity, and mortality) were obtained through microbial analysis and surveys.
Results
A total of 250 domestic dogs were diagnosed with Ancylostoma caninum (50, 20%), and 41 were diagnosed with Ancylostoma spp. (8.23%). One synanthropic rodent (2.5%) was positive for A. caninum. In the clinical analysis, 3 patients were identified as positive (1.27%) for cutaneous larva migrans (CLM). Likewise, environmental variables and social determinants influence the transmission, prevalence, and nature of parasitism by hookworm.
Conclusions
People, domestic dogs, and rodents were infected with these parasites. Consequently, there is a risk of ancylostomiasis and cutaneous larvae migrans spreading.
Keywords: Parasitology, Zoonoses, Tropical Medicine, Ancylostomiasis, Larva Migrans
Background
Ecoepidemiology is a branch of ecology in which the synthropism between a pathogen and its hosts (animal and human) and the environment is studied; this process usually manifests itself as the spread of infectious diseases in any region of the world, especially in countries with tropical and subtropical climates [1].
Ecuador is a tropical country located on the equator. It is one of 17 countries with the greatest biodiversity on the planet and is characterized by a range of climates in its 4 regions (coastal, Andes, Amazon, and Galapagos Islands), with abundant flora and fauna. The Ecuadorian coast is influenced by warm El Niño currents and cold Humboldt currents. Within the country, there is little information on soil-transmitted helminth infections, especially ancylostomiasis, which affects urban and rural populations and is related to tropical wildlife and the presence of certain animals in established risk areas [2].
Ancylostomiasis is one of the most common chronic infections, with an estimated 1.5 billion cases worldwide [3], and is directly responsible for 65 000 deaths per year. The disease is persistent in places with poor environmental sanitation and high humidity. Its clinical manifestations in humans include chronic intestinal blood loss, iron deficiency anemia and cutaneous larva migrans; it is a serious public health problem [4].
The nematodes that cause ancylostomiasis mainly in humans are Necator americanus and Ancylostoma (A.) duodenale [5]. The zoonotic canine hookworms Ancylostoma caninum, Ancylostoma ceylanicum, Uncynaria stenocephala, and Ancylostoma braziliense can cause larva migrans cutánea (CLM) in humans [6]. These are diagnosed through coproparasitic methods such as direct, flotation, sedimentation, Baerman, and Harada-Mori [3].
Cutaneous larva migrans manifests with a progressive migratory serpiginous dermal rash, with itching, and commonly appears on the foot. The prevalence worldwide is higher in tropical and very humid countries. The diagnostic method for identification is physical examination. Regarding treatment, albendazole and ivermectin are recommended for oral use; however, thiabendazole (topical) and mebendazole (oral) can be used [7].
Ancylostoma caninum is one of the most prevalent parasitic nematodes in dogs worldwide and is relatively common in puppies. Of all the hookworms in animals, A. caninum is much more common than other species and is the most pathogenic for pets (dogs and cats). This parasite can cause anemia, anorexia, hemorrhagic diarrhea, malnutrition, and other intestinal disorders, such as eosinophilic enteritis and aphthous ileitis [6,8].
Rodents are reservoirs and carriers of several zoonotic parasites that can be transmitted to humans [9]. Stray and house-dwelling dogs, as well as rodents, play an important role in disease transmission [9,10]. Furthermore, the presence of hookworm infections among domestic dogs, rodents, and humans, and the socioecoepidemiological relationships of these infections in Ecuador and Latin America are unknown [5,8].
This study was part of the FCI-029 Project (Competitive Research Fund) approved and financed by the University of Guayaquil (UG) of Ecuador: Ecoepidemiology of Neglected Intestinal Helminthiases in Urban-Marginal and Rural Areas of the Guayas Province. Therefore, this study aimed to evaluate the prevalence of Ancylostoma spp. infection in 498 domestic dogs and 40 synanthropic rodents and human cutaneous larva migrans in 236 people in suburban and urban areas of the Ecuadorian coast. Environmental variables, social determinants, and epidemiological indicators were analyzed between March and September 2023.
Material and Methods
Ethics Statement
This study was reviewed and approved by the Research Council of the Faculty of Veterinary Medicine and Zootechnics (FMVZ) of the University of Guayaquil (UG), the Research Department of the University of Guayaquil (DIUG) and the Ethics Committee of the University of Guayaquil, Ecuador. This was an observational, cross-sectional study with a mixed approach.
Sampling Areas
Fecal samples of domestic dogs, synanthropic rodents, and humans were collected through non-probabilistic addressed sampling from the urban-marginal sectors of Guayaquil, including Balerio Estacio and La Ladrillera (2°11′24″ S; 79°53′15″ W; 4 masl), and from rural sectors including Loma Larga (1°55′00″ S; 80°00′42″ W; 7 masl) (of the Nobol Canton) and Santa Rosa (1°52′00″ S; 79°59′00″ W; 9 masl) (of the Daule Canton), which are located in the province of Guayas on the Ecuadorian coast and have a tropical savanna climate. The sites investigated differ markedly between winter (rainy and hot) and summer (dry and cooler), with temperatures ranging from 20°C to 37°C.
Universe and Sample
Due to the absence of a census of domestic dogs, the total human population was used to determine the sample size of the dogs. The population of the 4 zones is 38 057 inhabitants (Balerio Estacio, 32 000 inhabitants; La Ladrillera, 3607, Loma Larga, 1000 inhabitants, and Santa Rosa 1450), housed in 7212 dwellings/households. To calculate the sample size, the WinEpi program was used, with a confidence interval of 95%, a sampling error of 5%, a population size of 7212 (households), and a minimum expected incidence of 5% [11]. According to the calculations, the following were sampled: 59 households per area, with 2 or more dogs and 1 person (the one who is most in contact with the animal) for each household.
Recognition of Areas, Informed Consent, Surveys, and Diagnostic Criteria
Prior to the investigation, a survey of the areas was carried out, and a talk was held with the local inhabitants, who were told about the ecoepidemiology of the parasite and the risk of acquiring cutaneous larva migrans in humans. In addition, the importance of conducting the study was raised, and the collection and identification of samples from their domestic dogs was explained [12].
Similarly, a survey was conducted with prior informed consent with people who had more than 2 domestic dogs. The topics of the survey were presented as figures and images to help the interviewee answer the questions. Included in these images were epidemiological indicators (prevalence, morbidity and mortality); social variables (number of family members, ages of family members, occupation, tendency to walk barefoot, health system, household infrastructure, presence of sewers and type of water supply, disposal of excreta, keeping of animals and presence of CLM); and environmental parameters (temperature, humidity, precipitation, solar radiation, soil texture, type of vegetation, pH, deforestation, and fauna).
To identify A. caninum, the criteria described by Bowman [13], Botero and Restrepo [14], and Romero Cabello [15] were considered. Coproparasitic methods used – direct, flotation, and sedimentation with centrifugation using saline solution – for identification of eggs, and the modified Baermann method was used for identification of larvae. Finally, the morphometric method was used to confirm the parasite.
Estimation of Epidemiological Indicators and Social Determinants
Estimation of epidemiological indicators was carried out with the results of the diagnoses obtained and with the help of the surveys carried out. In the case of social determinants, the results of the surveys were taken into account.
Characterization of the Environmental Variables
Environmental variables were obtained through environmental programs such as Weather Spark [16], Weather Atlas [17], and meteorological bulletins from the INAMHI [18]. In addition, we used studies described in the Development and Land Management plans carried out by the Decentralized Autonomous Governments of the cities of Guayaquil [19], Nobol [20], and Daule [21].
Collection, Transport, and Analysis of the Sample of Domestic Dogs
For the collection of fecal samples from domestic dogs (from March to September 2023), the owners were given sterile jars, their address and contact number were registered, and a data form was completed. In cases where pet owners could not collect the sample, a technical team collected it [22].
The stool samples of the dogs were immediately transported to the Laboratory of the Veterinary Clinic “Besito Vet Pet Lab” in the city of Guayaquil, where they were analyzed by coproparasitic methods including direct, flotation (Willis), sedimentation with centrifugation using saline solution, and Baermann modified methods. The sections were stained with Lugol solution and observed by light microscopy at 10× and 40× [15,23].
To determine the morbidity of symptomatic animals, the following stool analyses were performed: bacterial (culture and Gram staining), fungal (AFB and lactophenol staining), and viral (antigen for parvovirus and canine distemper).
Notably, all participants or, if the participants were children, guardians, signed the consent form before participating in the study. The participants were fully familiarized with the procedure. The request to sample domestic dogs and rodents was analyzed and approved by the Institutional Committee for the Care and Use of Animals of the FMVZ of the UG.
Sampling of Synanthropic Rodents
The rodents were captured between March 1 to April 28, 2023, in the “La Ladrillera” sector by using 30 Tomahawk and 10 Sherman traps. Nontoxic bait was used (100 g of oats with a quantity of 20 g of peanuts and 5 ml of vanilla, tuna, meat, fish, or fried chicken skin). The traps were strategically placed in landfills, drains, market peripheries, and other places that presented evidence of rodents. Once the live animals were captured, they were sprayed with “Fipronil” insecticide. In the laboratory, the rodents were euthanized by an overdose of 10% ketamine. Subsequently, each rodent was dissected, and its digestive tract was removed. The stool was placed in a Petri dish with physiological solution [24].
The intestinal contents of the animals were analyzed by applying the following coproparasitic methods: direct, flotation and sedimentation-centrifugation with saline solution. Then, the samples were analyzed via optical microscopy using the 10× and 40× objectives [13,15]. The following parameters were recorded: species, sex, and age group following the procedures described by De Sotomayor et al [24].
Morphometry of the Parasitic Forms
All samples that were positive (from domestic dogs and rodents) according to the indicated coproparasitic methods were confirmed by morphometry following the criteria of Bowman [13], Botero and Restrepo [14], Romero Cabello [15], and Lucio et al [25].
Identification of Cutaneous Larva Migrans
The presence of cutaneous larva migrans was determined by physical examination of each patient.
Statistical Analysis
The data obtained were tabulated and are presented in tables generated using the Microsoft Excel 2010 program. In addition, the prevalence of canine ancylostomiasis and CLM was related to social, environmental, and epidemiological indicators through inferential statistical analysis performed with RStudio statistical software. Fisher’s exact test was used to analyze these data. Finally, a generalized linear model (GLM) was implemented.
Results
Epidemiological Indicators
Of the 498 dogs analyzed in the 4 areas studied, 250 (50.20%) were positive for A. caninum (Figure 1), and 41 (8.23%) were positive for Ancylostoma spp. (Figure 2; Table 1). Forty-seven dogs presented vomiting, diarrhea, dehydration, decay, weakness, and pale mucous membranes. A total of 9.4% morbidity and 1.2% mortality were observed (6 dogs died).
Figure 1.
Microscopic identification of (A) egg of Ancylostoma caninum (red arrow) in feces of domestic dogs, (B) egg of Ancylostoma caninum (red arrow) in feces of rodent through the technique of sedimentation by centrifugation using saline solution and (C) larvae of Ancylostoma caninum in feces of domestic dog (red arrow) obtained by the technique of modified Baermann, observed by optical microscopy at 40× and stained/not with Lugol. (Taken by the authors).
Figure 2.
Microscopic identification of (A) egg of Ancylostoma spp. (red arrow) through the technique of sedimentation by centrifugation using saline solution and (B) larvae of Ancylostoma spp. (red arrow) obtained by the technique of modified Baermann, in the feces of domestic dogs observed by optical microscopy at 40× and stained/not with Lugol. (Taken by the authors).
Table 1.
Prevalence of ancylostomiasis in domestic dogs and synanthropic rodents and presence of CLM in people in urban-marginal and rural sectors of the Ecuadorian coast.
| Total cases studied | Ancylostoma caninum (cases) | Ancylostoma spp. (cases) | CLM (cases) | Prevalence |
|---|---|---|---|---|
| 498 domestic dogs | 250 | 50.20% | ||
| 41 | 8.23% | |||
| 40 synanthropic rodents | 1 | 2.5% | ||
| 236 humans | 3 | 1.27% |
Regarding the morbidity of domestic dogs with clinical manifestations, when performing stool tests, the bacteria (culture and Gram staining), fungi (AFB and lactophenol staining), and viruses (antigens for parvovirus and canine distemper) were all negative.
Of the 40 synanthropic rodents captured and analyzed, 14 (35%) were identified as Rattus rattus and 26 (65%) as Rattus norvegicus. Of these, 19 (47.5%) were female and 21 (52.5%) were male; furthermore, 24 (60%) weighed more than 250 g, and 16 (40%) weighed less than 250 g. Of the 40 rodents analyzed, only 1 (2.5%) was positive for Ancylostoma caninum (Figure 1; Table 1).
Of the 236 people examined, 3 (1.27%) had cutaneous larva migrans. In the Cooperativa Balerio Estacio sector, 2 cases of CLM were diagnosed (a 13-year-old and a 34-year-old), and in La Ladrillera, 1 case of CLM was diagnosed in a 14-year-old. In these 3 cases, the households had dogs who tested positive for A. caninum (Figure 3; Table 1).
Figure 3.
A 14-year-old boy with a palpable serginous lesion on his right foot was diagnosed with cutaneous larva migrans (MCI). (Taken by the authors).
Notably, dogs with ancylostomiasis were orally administered a single dose of 0.5 mg/kg (0.23 mg/lb) milbemycin oxime and praziquantel. After 1 month, the dogs were tested to confirm the absence of the parasite. The 3 people with MCL received oral ivermectin administered as a single dose of 200 μg/kg. Seven days after treatment, skin lesions on the soles of their feet were dry, and they no longer had itching; the symptoms disappeared during the following week [23].
Social Determinants
Of the 236 people who participated in the survey, all had 2 to 6 domestic dogs. The average number of people per household ranged from 5 to 6. The age range was from 2 to 85 years, and the household members had various occupations (22.8% informal trade, 6.1% formal trade, 26.4% dependence, and 44.7%% agriculture). Furthermore, 49% of the people did not wear shoes inside or outside the house; 10% had health insurance (4.4% social insurance and 5.6% farmer insurance). A total of 79.3% of the households studied had houses with mixed construction, and 20.7% had cane wood construction. The areas studied did not have sewerage; various types of water supplies were present (63.7% of the water was drinking water, 33.6% was purchased from a tanker, 2.1% was from the river, and 0.6% was obtained from a deep well). Finally, excreta were disposed of through latrines (30.8%), septic tanks (65.8%) and outdoor locations (3.4%).
Environmental Parameters
In the urban-marginal sectors (Balerio Estacio and Ladrillera), the average temperature is 23.54°C to 33.23°C, the humidity is 86.92%, and rainfall occurs mostly in March and April (93.4 to 203 mm), while solar radiation occurs every month for 12 hours and 3 minutes per day. In addition, the climate is tropical savanna, with an overall soil texture of soft clay, although certain sectors are sandy, with a pH between 6.5 (Balerio Estacio) and 6.7 (Ladrillera). In addition, a great variety of animals are present (eg, dogs, cats, birds, rodents, opossums); these areas are deforested due to the growth of the city.
In rural areas (Loma Larga and Santa Rosa), temperatures are between 23.35 and 32.43°C, with 87.99% humidity. Precipitation occurs mostly in March and April (622.5 to 930 mm) and solar radiation occurs every month for 12 hours and 4 minutes per day; the climate is tropical savanna with clay soil, though some areas are sandy; Santa Rosa has a pH of 6, and Loma Larga has a pH of 6.4. Both sites are mostly forested, and the main crops are rice and livestock. There is a great diversity of domestic and wild animals (eg, dogs, cats, birds, pigs, cows, horses, fish, monkeys, rodents, possums, squirrels, and snakes); but some areas are deforested for agricultural purposes.
No significant difference was found in the presence of Ancylostomas in domestic dogs according to location. However, in relation to the presence of CLM in the human population, a significant difference was found between Balerio Estacio and the other localities. Similarly, there was a significant difference in the housing conditions according to locality. In La Ladrillera, more than 50% of the people live in cane houses, and in Loma Larga, approximately 90% of the houses are made of wood. Finally, with respect to the disposal of excreta, there was a significant difference in that in Loma Larga, 72% of the inhabitants had latrines.
Finally, notably, the people and their domestic dogs that participated in the study received the results of their diagnoses. The domestic dogs that had ancylostomiasis were treated and the people who had CLM received expert medical advice for their treatment. In addition, a rodent elimination campaign was implemented.
Discussion
This is the first study carried out in Ecuador on the ecoepidemiology of Ancylostoma caninum in rodents and domestic dogs and its relationship with the prevalence of CLM in humans. In this investigation, a 50.20% prevalence rate of canine ancylostomiasis was determined, which is similar to the prevalence rate reported in urban and rural areas worldwide (40–100%) [26] and very close to the higher prevalence rate of 60% reported in endemic areas of South America [27]. The prevalence rate observed in this study is higher than that of domestic dogs in Europe, which is 1.7–33% [28]; and it is within the range of prevalences described in Asia 3.5% [10] to 79.1% [29], Africa 31.9% [30] to 53.8% [31], and Australia 6.9% [32] to 77.3% [33].
We detected a 8.23% rate of Ancylostomas spp., which is lower than the prevalence rates described by Brahmbhatt et al [8], Pratap et al [29], and Calvopiña et al [34].
Our results on canine morbidity (9.4%) and mortality (1.2%) are similar to the values mentioned by Aziz and Ramphul Brahmbhatt [3], lower than those of Kagira and Kanyari [35], and higher than those determined by Loukas et al [36].
The prevalence of A. caninum (2.5%) that we observed in a synanthropic rodent is lower than that in Peru (4.3%) [37] and in Malaysia (76.67%) [38].
Lucio et al [39] reported that parasitological parameters such as helminth prevalence and parasite load may be related to rodent variables, such as sex, age, and body condition, and tend to differ according to locality or ecological environment. The above results indicate that the presence of A. caninum in dogs and rodents are reliable indicators of the poor environmental conditions of the sector and the hygienic conditions of the people [9].
In this study, 3 cases of CLM were identified (1.27% prevalence), similar to the findings of Coello et al [23], but less than the 2% reported by Sears [40]. Suarez [41] reported 217 cases in men and 244 in women at the national level in Ecuador from 2007 to 2017. The pathology is directly related to exposure to filariform larvae (infective form) in the soil, which percutaneously penetrate the human skin, and this is often underdiagnosed [7,23].
Environmental variables and social determinants influence the transmission, prevalence, and nature of parasitic diseases. In addition, enteroparasite infections are commonly associated with age, hygiene habits, and nutritional or immunological conditions [42].
The social determinants obtained are similar to those described by Elfu Feleke [43], Dhaka et al [44], and Tiruneh et al. [45]. Hookworms are associated with the urban-marginal and rural sectors of underdeveloped tropical countries with low socioeconomic and educational levels, which is why the WHO classifies them as neglected parasitoses [23].
The environmental parameters obtained in this study are higher than those described in previous years in Ecuador by Weather Spark [16], Weather Atlas [17], INAMHI meteorological bulletins [18], and Development and Land Management plans carried out by the Decentralized Autonomous Governments of the cities of Guayaquil [19], Nobol [20], and Daule [21]. The ecological changes in sectors (deforestation) and environmental factors (how our study was conducted) influence the transmission dynamics of ancylostomiasis, as described by Seguel and Gottdenker [46] worldwide and Riess et al [47] in Tanzania. This last author stated that the hookworms in the study population were strongly associated with ecological factors such as temperature, rainfall, vegetation, composition, and soil moisture, which provide the infecting hookworm larvae the warm and humid conditions it requires for survival.
Regarding the ecological and environmental conditions necessary for the transmission of A. caninum to animal and human hosts, the optimum temperature for transmission is 20–30°C. However, transmission can occur at up to 39°C [47], with a higher prevalence in summer when humidity levels are 70–90% [8] and abundant rainfall, temperate climates, loose humid and fertile soils [48], fragile solar radiation [49], deforestation [50], and abundant vegetation and fauna [45] are present. All these parameters influence parasite persistence [45] and are similar to those reported in our study. However, importantly, in the studied areas (urban-marginal and rural), which differed in deforestation, vegetation and fauna, all cases of A. caninum were diagnosed among domestic dogs.
Although a direct relationship with contamination could not be established through statistical analysis in this study, there is a potential risk for people who walk barefoot in urban-marginal areas where there are CLM-positive dogs and for farmers who work barefoot in the field. However, transmission can also occur when people handle untreated feces that are used to directly fertilize crops, when poor hygienic habits are present, or when unwashed fruits and vegetables are consumed [48].
The porosity of sandy soils facilitates the movement of larvae, allowing them to burrow and escape desiccation and to move upward to escape water after heavy rains. However, soils with a high clay content are less porous and thus inhibit the motility of these larvae [47]. The people who had CLM lived in areas with sandy soils of the Balerio Estacio and La Ladrillera Cooperatives.
This study and many others have shown that vigorous vegetation, unaltered soils, high temperatures, and porous soils with more acidic pH are strongly associated with a higher prevalence of hookworms. Hookworms tolerate a pH range of 4.6 to 9.4 (especially when the pH is slightly acidic), which allows them to hatch and infect humans and dogs; our results coincide with these previous findings. The presence of vigorous vegetation also favors defecation outdoors since it provides privacy to individuals, who, along with domestic dogs, release the parasite’s eggs with their feces, which subsequently transform into infective larvae [51].
Notably, this study was carried out after theCOVID-19 pandemic, when presumably the people in previous years had experienced extensive contact with their domestic dogs. In addition to the heat wave in Ecuadorian coasts caused by Cyclone Yaku, the beginning of the warm current of El Niño and the altered climatic conditions of the country created the riskiest situations for the appearance of outbreaks, epizootics, and epidemics.
In addition, this research contributes to the epidemiological surveillance system of animal and public health related to ancylostomiasis for the benefit of Ecuadorian society.
Limitations of the Study
A greater number of samples, sample size of both domestic dogs, synanthropic rodents and people, and the inclusion of more vulnerable sectors would have improved this research. For example, the areas of Balerio Estacio, Loma Larga, and Santa Rosa could be sampled. On the other hand, during the research the need to measure new sociocultural variables was observed, such as informing people about the presence of the parasite, knowing their habits and customs that can increase the risk of contamination. Regarding coproparasitic methods, the PCR technique could be applied for better identification of the parasite.
Conclusions
Ancylostomiasis is a highly prevalent zoonotic disease in developing countries that can affect the population in endemic areas. In this study, 50.20% of the infections with A. caninum and 8.23% of the Ancylostoma spp. were identified in domestic dogs, and 1 (2.5%) of the A. caninum infection was identified in a synanthropic rodent. Likewise, 3 (1.27%) cases of CLM were diagnosed (2 adolescents and 1 adult). To obtain the parasites, direct coproparasitic methods, flotation, sedimentation with centrifugation using saline solution, and the modified Baermann method were used. Optical microscopy was used to identify the eggs and larvae of A. caininum and Ancylostoma sp., and the presence of these parasites was confirmed via morphometry.
The following information was collected: social variables through surveys; territorial planning plans for the GADs of the cities of Guayaquil, Nobol and Daule; and environmental parameters through environmental programs (Weather Atlas and Weather Spark), INAMHI meteorological bulletins, GAD land use plans for the cities of Guayaquil, Nobol, and Daule, and through observation. The results obtained suggest that several zoonotic transmissions could occur; however, additional studies are needed to confirm this fact. If such is the case, the community is exposed to significant environmental risk from ancylostomiasis. Therefore, the population should be educated about the sanitary measures needed and about the obligation of periodic deworming of their domestic animals to prevent the transmission of this and other parasites.
Acknowledgments
We would like to acknowledge the University of Guayaquil for financial support and the MVZ as well as Jonathan Cordero Velasco, who spoke with neighborhood leaders, police units, and residents, providing us with support, including his help in the logistical part of the investigation.
Footnotes
Conflict of interest: None declared
Declaration of Figures’ Authenticity: All figures submitted have been created by the authors, who confirm that the images are original with no duplication and have not been previously published in whole or in part.
Financial support: Universidad de Guayaquil
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