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Revista mexicana de ciencias pecuarias
versão On-line ISSN 2448-6698versão impressa ISSN 2007-1124
Rev. mex. de cienc. pecuarias vol.11 no.4 Mérida Out./Dez. 2020 Epub 02-Mar-2021
https://doi.org/10.22319/rmcp.v11i4.5182
Articles
Presence of Hymenolepis nana and diminuta in rodents of the Las Pinas citadel, in Milagro, Ecuador, and its risk for public health
a Universidad de Guayaquil. Facultad de Medicina Veterinaria y Zootecnia. Km 27 ½ vía a Daule, Guayaquil, Ecuador.
b Universidad Estatal de Milagro. Facultad Ciencias de la Salud, Milagro, Ecuador.
Hymenolepidiosis is a zoonosis of worldwide prevalence, especially in children, and it is caused by rodent cestodes called Hymenolepis (H) nana and Hymenolepis diminuta. It is very common in developing countries with hot, temperate and dry climates. The life cycle of H. nana does not require intermediate hosts, and its usual transmission is fecal-oral (by ingestion of infective eggs); and infection of H. diminuta occurs through ingestion of tenebrionid arthropods with the larval form (cysticercoids). The objective of this study was to determine the presence of H. nana and H. diminuta in the “Las Piñas” citadel, in the city of Milagro (Ecuador) and to make the public health risk known, through informative talks. For this research, the rodents were captured with the help of Tomahawk and Sherman traps with non-toxic baits (meat, mortadella, fish, bread). A descriptive, prospective cross-sectional study with qualitative approach, carried out between February 1st and July 30th, 2018, analyzed fecal samples using direct methods and flotation-centrifugation with a supersaturated saline solution. Out of 87 captured and processed rodents, 20 cases (22.99 %) were determined for Hymenolepis nana, and 10 cases (11.49 %), for H. diminuta. This was the first report of Hymenolepis nana and diminuta in rodents in the country. It can be concluded that the presence of these parasites at the study site is evident and may become a serious public health problem, due to the risk of transmission to the inhabitants of the sector.
Keywords Trapping; Coproparasitoscopic methods; Parasitism in rodents; Public health
La Hymenolepidiosis es una zoonosis de prevalencia mundial, sobre todo en niños, es causada por cestodos de roedores denominados Hymenolepis (H) nana e Hymenolepis diminuta, es muy frecuente en países en vías de desarrollo, con climas cálidos, templados y secos. El ciclo biológico de la H. nana no requiere de hospederos intermediarios, y su transmisión habitual es fecal-oral (por ingesta de huevos infectivos); y la infección de H. diminuta se da a través de la ingestión de artrópodos tenebriónidos con la forma larvaria cisticercoides. El objetivo de este estudio fue determinar la presencia de H. nana e H. diminuta en la ciudadela Las Piñas, de la ciudad de Milagro (Ecuador) y dar a conocer a través de charlas informativas el riesgo en salud pública; para esta investigación se capturaron roedores con ayuda de trampas Tomahawk y Sherman en complementariedad con cebos no tóxicos (carne, mortadela, pescado, pan). Mediante un estudio aplicado, con enfoque cualitativo, de tipo descriptivo-prospectivo-transversal, realizado entre el 1 de febrero al 30 de julio del 2018, se analizaron las muestras fecales por métodos directos y de flotación-centrifugación con solución salina sobresaturada. De 87 roedores capturados y procesados, 20 casos (22.99 %) se determinó para Hymenolepis nana y 10 casos (11.49 %) para H. diminuta. Constituyéndose en el primer reporte de Hymenolepis nana y diminuta en roedores en el país. Se concluye que es evidente la presencia de estos parásitos en el sitio de estudio, lo que podría convertirse en un serio problema de salud pública, por el riesgo de transmitirse a los habitantes del sector.
Palabras clave Trampeo; Métodos coproparasitarios; Parasitismo en roedores; Salud pública
Introduction
Infectious agents transmitted from animals to humans account for the majority of new pathogen outbreaks worldwide1, with over one billion cases of human disease attributable to zoonotic diseases each year, making the identification of wild reservoirs of zoonotic pathogens a public health priority2.
Rattus norvegicus (brown rat) and Rattus rattus (black rat) are known reservoirs of bacteria, viruses and zoonotic parasites of veterinary importance3,4. Helminthiasis affects 20 % of the Latin American population and is considered a neglected disease, infecting approximately 3.8 billion people worldwide5. These infections are common in rural populations and overcrowded areas, especially in countries with tropical and subtropical climates, associated with poverty and marginalization, and do not receive adequate national or international attention6,7. The social determinants of these diseases include poor housing conditions (without adequate roofs, walls, or floors), lack of access to safe drinking water, basic sanitation and hygiene, low income, poor education, and barriers to accessing health services in general and primary health care in particular7,8.
Hymenolepidiasis is a globally prevalent parasitism caused by cestodes of the genus Hymenolepis and Rodentolepis (Hymenolepipidae: Cyclophyllidea). The life cycles of these parasites involve humans, rats and mice as definitive hosts, and arthropods (Tenebrionids) as intermediate hosts. The presence of tenebrionids in the houses and unhealthy conditions generated by the lack of basic services and environmental and socio-economic factors favor the development of the disease in hot and humid areas, causing greater affectations to the child population9,10.
Rats and mice act as definitive hosts of Hymenolepis, and the occurrence of this parasite in humans is usually transmitted by fecal-oral route, by egg ingestion (H. nana); however, occasionally it can also be transmitted by ingestion of an arthropod, which will thus complete its life cycle (H. diminuta)11,12. It has been estimated that 20 million people in the world are infested with these two parasites13. However, both parasites share some epidemiological characteristics, such as prevalence in children from marginalized areas with poor hygiene habits, sanitary conditions and overcrowding12.
Ecuador is a country with a great variety of climates with four delimited regions: coast, sierra, east and insular region. The "Las Piñas" citadel is located on the Ecuadorian coast; it is characterized by a tropical climate in addition to high percentages of moisture due to its rivers and plains. The citadel has a marginal urban sector with 2,500 houses, where it is possible to find unoccupied houses; sugarcane, cocoa, and banana plantations, and pastures; in addition, there are ditches and septic wells. On the other hand, it does not have sewage, and few homes have drinking water; therefore, it meets the necessary conditions to have the presence of rodents that represent a health risk14. In addition, the presence of Hymenolepis nana and diminuta in rodents has not been reported in the country. Rodents must be reported, as they are potential sources of parasites that may cause public health problems as a result of their transmission to humans. On the other hand, the purpose of this study is to inform public health authorities and health professionals about cases of Hymenolepidiasis in rodents, as well as to inform the population and guiding them in prevention efforts.
Material and methods
Study area and period
The study was conducted in the urban-marginal citadel called "Las Piñas", located in the northern part of the canton Milagro, province of Guayas, on the Ecuadorian coast, at the geographical coordinates 2° 7' 0" S and 79° 36' 0" W. The community "Las Piñas" has 12,000 inhabitants; its climate is tropical-humid, with a marked difference between winter and summer, and with temperatures ranging from 22 to 36 °C 14, 15.
Survey
Each one of the selected households was visited, explained about the study and the risk of parasitosis in their environment, and once they gave their consent and signed a consent form for themselves and for the minors, a directed survey was applied, after which a sterile vial was given to each person.
The survey included the following questions: Do you know about hymenolepidiasis? What is the source of your drinking water? How are excreta handled in your home? Are intra- or peridomestic rodents present? Do you store farinaceous foods (rice, corn, barley, etc.)? Are there tenebrionids (beetles, fleas, weevils, etc.) in the farinaceous food deposits? Do you have a sewer system?
Sampling
Before carrying out the study, permission was requested from the authorities of the Faculty of Veterinary Medicine and Zootechnics (FMVZ) of the University of Guayaquil to carry out the study in the Microbiology Laboratory of the FMVZ; permission and collaboration were obtained as well from the “Las Piñas’ New Horizons” Improvement Committee (“Nuevos Horizontes de Las Piñas”). In addition, the research methodology was analyzed and approved by the Research Coordination of the FMVZ.
A descriptive, transversal and prospective study was carried out between February 1 and July 31, 2018; 70 homes with a total population of 320 people were researched between winter and summer, at an approximate temperature of 27 to 32 °C.
During the research, 87 rodents were sampled from three selected areas: (1) rodents in inhabited houses, vacant lots, ditches, and garbage dumps; 2) ditches and garbage dumps, and 3) Community Police Unit (CPU), ditches, garbage dumps, and vacant lots. It is important to mention that concentrations of garbage were found in all the researched areas. On the other hand, the survey was conducted with 90 people from the sector, divided into 30 for each one of the three abovementioned sectors.
Rodent Capture
Rodents were captured with the help of Tomahawk and Sherman traps and non-toxic baits (meat, bologna, fish, bread) taking recommended biosecurity measures. These traps were strategically placed in "Las Piñas" which is an urban-marginal citadel, which has places at risk such as: garbage dumps, ditches, pastures, and in the homes of certain community members who claim to have rodents16.
Those rodents that were captured alive were euthanized with pure chloroform soaked in cotton, according to the method suggested by the CICUAL of the School of Veterinary Medicine and Animal Husbandry of the University of Guayaquil. In addition, fipronil was sprayed at 0.15% before proceeding with the necropsy, as a biosafety rule for the professionals who performed it.
Once the animals were captured, they were transported alive to the Microbiology Laboratory of the FMVZ of the University of Guayaquil, where the necropsy was performed on them and the sample was extracted to be later analyzed using the techniques reported by Aluja and Constantino17,18.
Laboratory analysis
The samples were analyzed using direct methods and sedimentation with saturated salt solution17,19, then examined under the optical microscope with 10X and 40X objective lenses.
The parameters to be followed during the necropsy for the removal of the gastrointestinal tract from the rodents were those reported by de Aluja and Constantine18. In addition, the Travassos qualitative technique was applied in order to obtain adult parasites18,20. The mucous membranes of already washed organs were checked for adult or juvenile helminths attached to, or underneath the mucous membrane.
Results
After setting up and baiting the traps at the different study sites, it was waited for a period of 12 h. The traps were subsequently checked, and the rodent species were taxonomically identified16,17; a total of 87 rodents (40 Rattus rattus and 47 Rattus norvegicus) were thus captured and analyzed using the direct coproparasitic method and sedimentation with saturated salt solution. 20 (22.99 %) of the rodents were positive for H. nana, and 10 (11.49 %) were positive for H. diminuta.
Furthermore, it was possible to identify the distribution of the parasite in the rodent species studied: H. nana 12 (100 %) and H. diminuta (0 %) in Rattus rattus, and H. diminuta 10 (55.5 %) and H. nana 8 (44.5 %) in Rattus norvegicus.
Cases of Hymenolepis nana and diminuta were found in all the study areas. In area 1, there were a total of 4 cases of H. nana and 2 cases of H. diminuta. In area 2, there were 7 cases of H. nana and 3 cases of H. diminuta. In area 3, a total of 9 cases of H. nana and 5 cases of H. diminuta were determined (Table 1).
Table 1 Total number of parasites per area
| Area 1 (%) | Area 2 (%) | Area 3 (%) | Total | % | |
|---|---|---|---|---|---|
| Hymenolepis nana | 4 (4.59) | 7 (8.04) | 9(10.34) | 20 | 22.97 |
| Hymenolepis diminuta | 2 (2.29) | 3 (3.44) | 5(5.74) | 10 | 11.47 |
In addition, 90 people were surveyed with questions about the risk of transmission of diseases from rodents to humans, all of whom said that they did not know about Hymenolepidiasis; 60 individuals (66.67 %) said they consumed water from drums and 30 (33.33 %) mentioned buying water from tankers. All respondents reported that they discarded their excreta through septic tanks. In the case of rodent excreta, the respondents indicated that they assumed that they fell to the ground.
As for the presence of intra and peridomestic rodents, 32 individuals (35.55 %) reported seeing intradomestic rodents; 48 individuals (53.33 %) reported seeing peridomestic rodents; 10 individuals (11.11 %) reported seeing no rodents inside or outside their home. On the other hand, only 17 individuals (18.88 %) declared to have in their home deposits of farinaceous food. Likewise, 13 individuals (14.44 %) reported having seen tenebrionids in their deposits of farinaceous food located in their homes. Regarding the sanitary situation, 70 surveyed individuals (77.78 %) reported not having drinking water, and all 90 said that they did not have a sewerage system.
As for the capture sites, in area 1, cases of intestinal parasites were determined in rodents that roamed areas such as inhabited houses, vacant lots, ditches and garbage dumps. In area 2, intestinal parasites were determined in rodents that prowled in ditches and garbage cans. In area 3, cases of intestinal parasites were detected in rodents around the Community Police Unit (CPU); ditch, garbage dump and vacant lots.
In order to estimate the number of houses affected by the close presence of rodents, a radius of action of 40 to 50 m was used for the species Rattus rattus, and of 30 to 45 m for Rattus novergicus21.
The study of impact on the population showed that the perimeter of affectation of area 1 where positive rodents were found comprised an average of 10 to 18 houses, which suggests a direct damage of 10 to 18 families respectively. In area 2, the radius of action of the traps where positive rodents were found included 15 to 18 houses. In Area 3, it comprised 10 to 25 houses.
Discussion
The estimated prevalence of Hymenolepis nana, of 22.99 %, is higher than that determined in Costa Rica (0.97 %)22, in Cuba (2.56 %)23, in Peru (6.8 %)17, in Brazil (8.8 %)24, and in Argentina (8.2 %)19. Likewise, low prevalences of H. nana have been registered in countries of other continents, such as 2.5 % in Iran25, 3.3 to 10.3 % in China, and 3.3 to 4.1% in the Netherlands26; however, higher prevalences have been recorded in Taiwan (21.8 %)26, Brazil (35.7 %)27 and Italy (100 %)26. It should be noted that the coastal region of Ecuador is an area where there is a high, constant environmental temperature throughout the year, due to the presence of two annual seasons (winter/summer), which are characterized by high humidity and the presence of moderate to torrential rains in the former, and low rainfall and high environmental temperatures in the latter.
The 10.64 % of determined Hymenolepis diminuta is less than the one expressed in Cuba with 11.5 %23, in Argentina with 12.2 %19, in Peru between 25.7 and 43.8 %28 and in Costa Rica with 43.6822. Also, low prevalences of H. diminuta were determined in countries of other continents, such as Taiwan, with 6.3 %26, and Iran, with 1.7 %25, in contrast with prevalences (10.64 %) above that found in countries such as China (27.8 %)26, Iran (38.8 %)25, The Netherlands (10.2 to 50 %), Serbia (30.5 %), and India (62.5 %)26.
Notably, in all the studied areas there were cases of H. diminuta and H. nana, zoonotic parasites, regarding which the surveyed individuals said they had no knowledge of the disease they produce. On the other hand, 33.33 % mentioned buying water from tankers. All the individuals said that they discarded their excreta through septic tanks; 35.56 % said they saw rodents in their homes, and 53.33 % said they saw rodents in their homes. Likewise, 18.88 % mentioned having in their homes deposits of farinaceous food, which are the main source of tenebrionids, intermediate hosts of the H. diminuta29, which may transmit the parasites to humans, especially in the winter season, when the number of vectors increases25.
The 77.78 % of the respondents mentioned that they do not have drinking water, and also all the respondents stated that they do not have sewage, which is a potential risk for the increase of rodents in the face of the present increase in population21; the latter, in turn, are important indicators of neglected parasitosis in vulnerable populations7,30.
Finally, cases of intestinal parasites were determined in rodents of inhabited houses, ditches, garbage dumps, plots of land and vacant lots, which are places where there is greater proliferation of these mammals21.
Conclusions and implications
This study determined the presence of H. diminuta and H. nana in rodent feces from the "Las Piñas" citadel in the Milagro canton, and concluded that the presence of these helminth parasites is evident at the study site, which constitutes a public health problem and involves a risk of new cases. On the other hand, emphasis is placed on promoting an in-depth epidemiological study to identify the most vulnerable members within the family nuclei, for the development of awareness campaigns aimed at age groups at risk of suffering from the parasite.
Acknowledgements and conflict of interest
The authors are grateful for the collaboration of the Faculty of Veterinary Medicine and Animal Husbandry of the University of Guayaquil and the Committee for the Improvement of New Horizons of "Las Piñas’, whose participation and openness to this study made it possible for us to reveal the data presented herein.
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Received: December 05, 2018; Accepted: September 03, 2019
Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons
