**4. Conclusions and recommendations**

Leishmaniasis is a complex disease of multifactorial origin in which different species of parasites, reservoirs, vectors, and ecological and social factors interact. The focal nature of the transmission of leishmaniasis in each endemic area has been found to be associated with the particular environmental conditions in a given area, such as climate, humidity, altitude, temperature, and vegetation, that favor the vector's presence. Like other vector-borne diseases, leishmaniasis has been found to be strongly influenced by global warming and climate variability, which affect the dynamics of the vectors, reservoirs and human populations. The use of eco-epidemiological assessments provides a multidisciplinary approach to understanding heterogeneities and dynamics that occur in the foci of leishmaniasis transmission.

that require adaptability to both urban environment and novel areas. Such is the case of *Lu. longipalpis,* which had been reported at a maximum altitude of 1100 meters above sea level until 2006, when we identified this species in the Andean region of the country (Caldas) at 1387 meters above sea level; this was the second global report of the prevalence of this species at a higher altitude [59]. *Lu. panamensis*, one of the main vector species of CL in Colombia, has become the predominant species in the most urbanized areas, showing its high capacity for adaptation, unlike other species present in the jungle areas of Darien Colombia (Department

While the biting activity of insect vectors has been found to be crepuscular and nocturnal, these species have variable hours of activity. For example, in Montebello and Antioquia, *Lu. gomezi* has been found to have greater biting activity from 6 to 8 pm. In the municipality of La Guaira, Valle del Cauca, *Lu. youngi* has generally been identified as having increased biting activity between 7:00and 9:00 pm [60]. *Lu. evansi* in San Andres de Sotavento has been found to have increased biting activity from 11:00 pm to 1 am [7]. Specifying the peak hours

Seasonal variations in the density of vectors have been identified. For example, in sub‐tropical countries, the period of greatest activity of a vector has been found to correspond to the warmer months of the year. In France, *Ph. ariasi* has been found to be active from June to September, with its highest density identified at the end of July [5, 60, 61]; however, after examining the physiological age of the insects, it was found that the highest proportion of calved females and natural infections with *Leishmania* occurred in August and early September. In tropical regions and notably in Colombia, we have found that the period of greatest risk corresponds to the rainy season. In San Andres de Sotavento (*Lu. evansi*) [27], Montebello (*Lu. gomezi*) [6] and Choco (*Lu. panamensis* and *Lu. trapidoi*) (Carrillo LM, unpublished data) a significant increase in vector density during the rainy season has been identified. At the end of this period, the rate of calved females and natural *Leishmania* infections has also been determined to be significantly higher. In the area of Urabá during the phenomenon "*El Niño*" a tendency towards decreased

of biting is important for the selection of the control measure to be used.

vectors has been identified, contrary to what was reported by Cardenas et al. [62].

**4. Conclusions and recommendations**

Over longer periods, disease outbreaks (e.g., Montebello, San Roque, and Saiza) have been observed that correspond to the confluence of multiple factors such as the presence of infected reservoirs and vector abundance; in all of these outbreaks, it was found that transmission occurred in the intra‐ and peridomicile, with children highly affected and no gender difference identified. Additionally, humans were identified as a possible reservoir due to the large number of active lesions present at any given time and high number of bites (see the photo of the girl with bites and photos of extensive lesions). Climatic factors, such as a phenomenon of "*La Niña*,*"* characterized in Colombia by the rainy season, could favor higher vector densities and outbreaks; however, studies confirming this hypothesis are needed.

Leishmaniasis is a complex disease of multifactorial origin in which different species of parasites, reservoirs, vectors, and ecological and social factors interact. The focal nature of the

Choco) (Carillo LM, unpublished data).

48 The Epidemiology and Ecology of Leishmaniasis

The application of the eco-epidemiological method then enables the following processes to occur in the natural foci of transmission: (a) identification of the species of *Leishmania* and role of phlebotomines and wild and domestic reservoirs; (b) definition of the geographical areas or macrofoci and description of the environmental characteristics that may become ecological markers of the presence of a vector, such as temperature, vegetation, soil type, and altitude; (c) establishment of the time of the year (spatio-temporal) associated with increased risk of transmission based on the rates of natural infection and biting activity; (d) establishment, with respect to housing (microfocus), of the risk of infection for inhabitants in the intra‐, peri‐ and extradomicile; (e) determination of the different age groups in a community that are most affected or at risk of becoming ill; and (f) identification of the conceptions, attitudes, and practices in communities related to the disease. The improvement of eco‐epidemiological surveillance for leishmaniasis should be based on the identification of these parameters to facilitate the design and implementation of cost‐effective prevention and control measures. In addition, the sustainability of these measures is dependent on intersector collaboration and support (municipal/Department of Health) and active participation of the community.

The results of different studies have shown that in a focus, transmission may be intra‐, peri‐ and extradomiciliary, and while women and children may be as substantially affected by leishmaniasis as men, women have less access to healthcare. These data have also shown that official statistics are not a good reflection of the true epidemiology of leishmaniasis in the rural areas where a greater number of cases are recorded.

The fact that women less frequently seek care causes the prevalence in this population to be underestimated, and therefore there are inaccurate estimates of the gender‐specific rate of infection. Implementation of better governmental strategies will be required to correct the inequality in access to the treatment for women, and strategies for controlling the disease that are oriented towards preventing intra- and peridomiciliary transmission are also required. There is also a need to increase the focus within health departments towards correcting the unequal access to health services in women (regarding leishmaniasis), as this disparity can reflect other problematic situations in the rural health setting.

Based on these different findings, it is suggested that the design of control strategies take into account the following considerations:

When it is determined (through the study of a focus) that transmission is occurring in the interior of a domicile, then measures for vector control and the prevention of leishmaniasis can be used to prevent people from becoming infected with the parasite by preventing bites from the infected vectors.

Control measure should be applied before the period of greatest risk and aimed at the protecting people at higher risk in the geographical area in which there has been transmission, whether that area is intradomiciliary or extradomiciliary. Additionally, the hours of greatest risk should be considered. The rainy season has been identified as the time when there is a greater risk transmission in foci and a higher density of vectors; therefore, control measures should be implemented before the rainy season begins. However, these findings must be validated in each foci.

Various vector control measures are available, including the use of bed nets or curtains impregnated with insecticides (even hammocks) and spraying of insecticides inside houses (in those foci where transmission is intra- and peridomiciliary).

In the case of bed nets, it is necessary to take into account the type of material and size of the holes and educate the community so they will not wash the mosquito net and damage the residual effect and nature of the material (regardless of whether it is impregnated). For example, nylon tulle or polyester bed nets are most effective because the residual effects of the insecticide are much higher; additionally, in these bed nets, the holes are very small and prevent *Lutzomyia* passing through the mosquito net. While bed nets are generally well accepted by most communities, acceptance must be considered individually in each community because it can vary from one community to another. For example, color has been identified as one factor that may affect the degree of acceptance of bed nets. If a mosquito net is not impregnated with insecticide, *Lutzomyia* species may get through even very small holes. However, when it is impregnated, vectors will not go through the bed net.

In foci where transmission occurs in an intra- and/or peridomicile, the infection of pets (and people with lesions) has been hypothesized to demonstrate that in these foci, the disease affects both women and men. Proper treatment of people may serve as a control measure of transmission in foci where humans are reservoirs and provide support for the implementation of better methods of control.

Finally, implementing primary health education to inform the community about issues related to the disease will increase knowledge about why the disease occurs, what causes it, what transmits it and how it heals. Recognizing the parasite that causes the disease (causative agent), transmitting insect, its behavioral habits, clinical manifestations of the disease, and mucosal compromise will help to promote disease control.

Individuals in these communities need to understand that it is necessary to perform some diagnostic procedures before initiating treatment and that there are options for treating the disease. These treatments are provided free of charge by the Ministry of Health through the sectional health services for all people with a diagnosis of leishmaniasis with any of its clinical presentations. Additionally, explaining the need to complete treatment to prevent the emergence of drug resistance, relapse, and complications in the mucosae and educating community members about some important measures that can contribute to avoiding contact with insect vectors are crucial.

It is important to emphasize during primary education that control measures (mosquito nets) should be provided to the populations at greatest risk. Specifically, children should be protected, as they are the population at highest risk of visceral leishmaniasis. It is also necessary to protect the family unit in general in the intra-domicile through the use of mosquito nets every night.

Through the use of primary health education, the community itself may help to guide control efforts by reporting increases in the intradomiciliary density of *Lutzomyia* species. Informing health providers to recognize early disease (leishmaniasis) is also important. A provider may then diagnose the patient or refer the patient for diagnosis (in early cases). Through community participation, it is possible for this disease become a priority issue for community activities.
