**3. Findings of the application of eco‐epidemiological method in some focus studies on Colombia**

In Colombia, leishmaniasis has been identified in all its clinical forms. It may occur in the endemic form, causing natural outbreaks throughout almost all the national territory areas with altitudes lower 2000 meters above sea level, including wilderness areas, tropical dry forests, the Andean region where coffee is grown and plains and deserts areas located in the inter-Andean region, eastern region, and Guajira Peninsula.

Our group has studied the natural infection patterns of leishmaniasis in different foci of transmission, and these studies have demonstrated that women and children are affected by leishmaniasis with equal or greater frequency than men. This finding is in opposition with the belief that leishmaniasis is more common in men (previously considered as an occupational disease that affected men during the performance of rural labor activities in forested areas inhabited by the insect vector). However, studies have shown that women (adults and children) have less access to proper diagnosis and treatment, leading to infrequent case reporting. These studies have also shown that due the domestic adaptation of vector species, the occurrence of epidemic peaks of CL in different regions may affect entire families. It was observed that the presence of gender differences depended on the locations in which the consultations took place; however, no changes in the activities performed by women in the field were identified that could explain the increased frequency of contact with the vector observed [45].

In the different studied foci, three major leishmaniasis transmission cycles have been identified: sylvan, domestic/rural, and urban.


In Colombia, sylvatic and domestic-rural endemic foci are characterized by locations that are generally in remote and impoverished areas of cities with great social inequities and little state health institution presence. Because the lesions are visible (usually located on the exposed areas of the skin), these lesions may become chronic and disfigure the skin or mucous membranes, and indigenous peoples have developed their own medical systems for the disease.

**3. Findings of the application of eco‐epidemiological method in some** 

In Colombia, leishmaniasis has been identified in all its clinical forms. It may occur in the endemic form, causing natural outbreaks throughout almost all the national territory areas with altitudes lower 2000 meters above sea level, including wilderness areas, tropical dry forests, the Andean region where coffee is grown and plains and deserts areas located in the

Our group has studied the natural infection patterns of leishmaniasis in different foci of transmission, and these studies have demonstrated that women and children are affected by leishmaniasis with equal or greater frequency than men. This finding is in opposition with the belief that leishmaniasis is more common in men (previously considered as an occupational disease that affected men during the performance of rural labor activities in forested areas inhabited by the insect vector). However, studies have shown that women (adults and children) have less access to proper diagnosis and treatment, leading to infrequent case reporting. These studies have also shown that due the domestic adaptation of vector species, the occurrence of epidemic peaks of CL in different regions may affect entire families. It was observed that the presence of gender differences depended on the locations in which the consultations took place; however, no changes in the activities performed by women in the field were identified that could explain the increased frequency of contact with the vector observed [45].

In the different studied foci, three major leishmaniasis transmission cycles have been identi-

− Sylvatic cycle: Humans are infected when they enter into the proximity of forests or jungles and are bitten by the insect vectors; in this case, humans are an accidental host who are not involved in the transmission cycle. In Colombia, military members, miners, loggers, and

− Rural/domestic cycle: This cycle occurs mainly when intra-domiciliary transmission of the disease occurs (in which vectors are inside homes and affect the entire family without discrimination by age or sex). In foci, such as Montebello and San Roque (Antioquia) [6, 28, 33] and areas with traditional coffee cultivation [46], children under the age of 5 years have been found to have the highest incidence of leishmaniasis; in these areas, the most frequently incriminated vector has been identified as *Lu. gomezi*, which has increased biting activity during the early hours of the night. When an outbreak occurs in the epidemic form, the data have shown that humans are part of the transmission cycle

− Urban cycle: Similar to the rural/domestic cycle, in this cycle, vectors enter the peridomicile or home and may transmit the infection to the entire family; in this cycle, a higher rate of infection in children has been observed. Additionally, in this transmission cycle, humans can be accidental hosts not involved in the transmission cycle or act as

indigenous communities are the most affected by this transmission cycle.

**focus studies on Colombia**

42 The Epidemiology and Ecology of Leishmaniasis

fied: sylvan, domestic/rural, and urban.

and act as a reservoir [29, 34].

reservoirs.

inter-Andean region, eastern region, and Guajira Peninsula.

For the evaluation of medical systems in foci of transmission, qualitative ethnographic methods have been used in which participant observation techniques (requiring the presence of researchers within the community) are applied. Interviews also allow for the establishment of a personal dialogue with the community and key stakeholders such as healers and community leaders. Quantitative methods have also been applied through the use of surveys conducted by the investigator with questions designed in consultation with community members. Comparisons of CL cases seeking care at urban centers with cases identified through active surveillance have also shown that inhabitants in each region have developed their own conceptions about the origin and management of disease. These medical systems were found to vary between indigenous and peasant communities, such as those described below.

#### **3.1. Medical systems in indigenous communities: Zenú, Emberá and Tikuna**

The indigenous community Zenú, an endemic focus of VL in Colombia, is located in a tropical dry forest region on the Caribbean coast. The Emberá community, an endemic focus of CL, is located in a tropical wet forest region of the Colombian Pacific coast, while the Tikuna community lies within the Amazon rainforest. Despite differences in their culture and the ecological characteristics of the places they inhabit, the medical systems in these communities are similar. However, two types of disease that differ in these communities have been identified:

The first type of disease is called "bush illnesses," "Indian illnesses" or "*Esperajai*" in Emberá. The second type of disease includes Western diseases or "White diseases" that are treated by Western doctors and a type of facultative medicine called "Kapuniajai" in Emberá.

The "bush illnesses" or "Indian illnesses" are distinguished according to their etiology and include three types of diseases: (i) diseases caused by supernatural beings such as "Jais," which populate the jungle, "charms," "chimpine" or the spirits of ancestors or other evil spirits; (ii) diseases caused by jinxes resulting from an enemy administering a potion, usually in food, obtained from a sorcerer, healer or herbalist; and (iii) diseases caused by natural causes and due to a sudden contact between hot and cold matter.

"Bush illnesses" or "Indian illnesses" that relate to VL and are observed in the Zenú community include the following:

**1.** Diseases caused by supernatural beings: In this type of disease, it is believed that a "mushroom" or "wind mushroom" is produced by evil winds from the world of the dead. The symptoms of this disease include fever, body aches, headache, and possible unconsciousness or coma. This disease is also known as "wind sickness" or "mountain view" and is thought to be the separation of the "soul" from the body. When afflicted by this disease, the spirit is believed to wander aimlessly, sometimes resulting in death in sick children. The "soul" is thought to leave the body when a mother leaves the house with a child in her arms without providing any protection to prevent the evil wind that roams the mountains from taking over the child's soul while walking. The hours most conducive to this phenomenon are believed to occur at sunrise and sunset. When the mother takes the sleeping child from home to home, it is thought that the soul stays in the first location. This spirit loss may result in crying, loss of appetite, fever, hair loss, diarrhea, edema, and appearance of a "bun" or ball on the left side of the stomach.


Given these elements, it can be concluded that the VL is recognized in the Zenú medical system within the context of "bush illnesses" but is explained as originating from two different causes: the first being of supernatural origin and the second being due to natural reasons. For diagnosis, the patient's family may seek care from a "healer" or traditional doctor and provide a urine sample from the patient. Following observation of the urine, the healer diagnoses the patient with a disease and establishes a plant-based treatment that is administered and accompanied by a special diet for the child that includes chicken broth.

Medicinal plants used by a "healer" may be classified as "hot" or "cool." Hot plants include cinnamon (*Cinamomum zeilanicum*), pennyroyal (*Bistropogon mollis*), coriander (*Coriandrum sativum*), and "the happy" (*Lantana* spp.). "Cool" plants include basil (*Ocimum basilicum*), flaxseed (*Linum usitatis simum*), corn (*Zea mays*) and soursop leaves (*Annona muricata*). Some of these plants grow in the reserve, and others may be purchased at market places in nearby cities. The leaves are prepared in an infusion to drink or a concoction of leaves, stems and roots for baths, compresses, and poultices.

The Emberá Indians do not recognize CL as an individual clinical entity but consider it to be part of the skin conditions called "Aidá" in their language [47]. This disease is believed to occur in people who violate the social norms associated with menarche or widowhood. During menarche or widowhood, a person acquires a temporary taboo status that, if violated, is believed to then cause the disease. This disease is also thought to occur due to chance encounters with the "Jais" of the jungle, which are the forces that act on and control human well-being and comprise the spirits of ancestors (tutelary, protective and/or aggressive "Jais") and of prey animals, which are almost always aggressive "Jais" and agents of diseases who want to exact revenge on hunters [48].

In the Emberá community, a patient may be taken to the Jaibaná (shaman) who is in charge of controlling both evil and beneficial spiritual forces. Through ritual singing to the "Jai," the Jaibaná is thought to "see" the agent that has possessed the body of the victim and look for a way to exorcise it and heal the person. The Jaibaná also provides answers and defines the disease. According to this diagnosis, the Jaibaná can cure the patient or sends him/her to the herbalist or hospital to receive treatment. The agents causing "Aidá," represented as the "Jais," are thought to be small worms found in the forest. When treatment is provided by an herbalist, he or she may diagnose the disease by examining the urine of the patient. The herbalist may then add a plant to the urine, which may produce the typical signs that result when someone has made a curse on a person. When treatment is provided by a Jaibaná, he or she uses the songs of the "Jai" and plants, purification rituals or daily allowances, depending on what the "Jais" advises. Meanwhile, herbalists also prescribe a special diet without sweet or salty foods.

For Tikunas Indians, CL is thought to be produced by an encounter inside the forest with the sloths (*Choloepus hoffmanni*) that transmit the disease by staring at the person, and this belief is consistent with the epidemiological findings of higher disease prevalence in hunters and the presence of vector insects that live in the forest. For treatment, the doctor uses indigenous macerated bark of a tree, which is highly caustic and helps to heal the lesions.

#### **3.2. Medical systems in rural communities**

the spirit is believed to wander aimlessly, sometimes resulting in death in sick children. The "soul" is thought to leave the body when a mother leaves the house with a child in her arms without providing any protection to prevent the evil wind that roams the mountains from taking over the child's soul while walking. The hours most conducive to this phenomenon are believed to occur at sunrise and sunset. When the mother takes the sleeping child from home to home, it is thought that the soul stays in the first location. This spirit loss may result in crying, loss of appetite, fever, hair loss, diarrhea, edema, and appearance of

**2.** This feature is important because 100% of interviewed mothers who had children with VL consulted a healer as their first medical resource, with all cases of diseases diagnosed as

**3.** Diseases caused by natural causes: These diseases are believed to be the result of sudden contact between hot and cold matter. For example, indigestion is thought to be caused by walking barefoot or bathing in hot weather. These diseases include the "milkbun illness" or "child in *Chime*," which is believed to occur when a pregnant mother breastfeeds another child. Through this process, breast milk is damaged, and the child that drinks the milk suffers from constant fever, loss of appetite, and stomach swelling (liver, spleen). A "bun" or ball is then believed to grow in the navel, and then the child dies. Elderly people say that this disease is very old, and many children have died from fever because they

Given these elements, it can be concluded that the VL is recognized in the Zenú medical system within the context of "bush illnesses" but is explained as originating from two different causes: the first being of supernatural origin and the second being due to natural reasons. For diagnosis, the patient's family may seek care from a "healer" or traditional doctor and provide a urine sample from the patient. Following observation of the urine, the healer diagnoses the patient with a disease and establishes a plant-based treatment that is administered and

Medicinal plants used by a "healer" may be classified as "hot" or "cool." Hot plants include cinnamon (*Cinamomum zeilanicum*), pennyroyal (*Bistropogon mollis*), coriander (*Coriandrum sativum*), and "the happy" (*Lantana* spp.). "Cool" plants include basil (*Ocimum basilicum*), flaxseed (*Linum usitatis simum*), corn (*Zea mays*) and soursop leaves (*Annona muricata*). Some of these plants grow in the reserve, and others may be purchased at market places in nearby cities. The leaves are prepared in an infusion to drink or a concoction of leaves, stems and

The Emberá Indians do not recognize CL as an individual clinical entity but consider it to be part of the skin conditions called "Aidá" in their language [47]. This disease is believed to occur in people who violate the social norms associated with menarche or widowhood. During menarche or widowhood, a person acquires a temporary taboo status that, if violated, is believed to then cause the disease. This disease is also thought to occur due to chance encounters with the "Jais" of the jungle, which are the forces that act on and control human well-being and comprise the spirits of ancestors (tutelary, protective and/or aggressive "Jais")

a "bun" or ball on the left side of the stomach.

44 The Epidemiology and Ecology of Leishmaniasis

"wind illness" or "milkbun illness" [19, 47].

would not "refresh" and had a swollen abdomen.

roots for baths, compresses, and poultices.

accompanied by a special diet for the child that includes chicken broth.

The first descriptions of CL in Colombia were made during the last century under the name "sows" and attributed to poor hygiene. This view persists in rural eastern Colombia, where the cause of the disease is attributed to the bite of flies from pig pens known as "pigflies." Meanwhile, the peasants of northwestern Colombia believe that the disease is caused by the bite of the "pito," which is the designated name for both CL and for some herbivorous and hematophagous hemipteran, and specifically reduviid, insects that live in logs and decaying timbers found near houses. These insects cause skin lesions by biting and defecating on people. Additionally, this disease is recognized by the name "vine" in these communities due to the bite of small animals that have a thread-like appearance and are called "vines" or "I saw you"; these animals have been found to often bite people while in the forests and in the branches of trees. Peasants in northwestern Colombia say that if a person sees this animal, he or she can shout, "Saw you," and the animal is paralyzed and does not cause itching or disease [46]. In these communities, the diagnosis of this condition is made by examining the lesion or urine.

Other communities believe that the etiology of the disease is due to the action of the "warty louse," a small parasite of *Lachesis muta* snakes, known as rattlesnakes or "warty" snakes. People believe that when they kill these snakes, they are exposed to and bitten by these "lice" thus causing the disease.

Treatment of CL in rural communities varies according to the community's conception of the origin of the disease and the degree of antiquity of the human settlement. Despite sharing the same geographic area, the CAP of rural populations may be very different. For example, populations that have been settled in this area for a longer period are of African descent. These populations fear the disease and strongly prefer to avoid jobs that involve entering the jungle to prevent infection. People in these communities also believe that leishmaniasis is a "hallmark of the jungle" and that having the disease means that the jungle is welcoming your arrival; therefore, they have no preventive measures against it.

Another population, known as "paisas," is a recent settlement of people from coffee cultivating areas who came to this region over the last 30 years; this region has an endemic focus of CL produced by *L. panamensis*, and people in this population use caustic agents and plants to treat the disease. Treatment with caustic agents consists of the local application of various substances such as silver nitrate, sulfuric acid, hot water, and hot brown sugar and, frequently, cauterization of the lesion with a spoon or the tip of a machete that has been placed in a fire and is applied without anesthesia to the ulcer, leaving a smooth scar [49]. Treatment with plants consists of the local application of macerated leaves or bark of various trees and shrubs and some latex from vines, many with leishmanicidal action previously demonstrated in the laboratory [50]. In recent settlement communities, no preference for a plant or group of plants exists, and a wide range of plants is used; however, moxa is one of the most popular.

Conceptions of the disease are closely associated with not only culture but also social relations. For example, gender relations are represented by the provision of feminine or masculine attributes to ulcers, the papular, silent type of ulcers that are not easily observed and generally isolated and difficult to treat are called "male pito" and the ulcerous lesions that are often numerous, "weep" (produce fluid), and more easily observed and treated are called "female pito" [49].

Nonspecific medications are often used, including antifungal drugs, ointments, salves, local application antibiotics, and veterinary medicines; these medications are generally self‐made or prescribed by doctors who have had no possibility to confirm the diagnosis with laboratory tests. Among the most commonly used veterinary drugs is ivermectin, which has been recently approved for human use and has been found to be effective in some studies [51].

In our studies conducted in indigenous communities, it was not possible to verify the use of urine as a healing element, which has been described in black communities in central San Juan [52]; in these communities, in addition to using urine for diagnosis, it has been used for treatment of various skin diseases, rheumatism, and snakebites and smeared on the skin or drank.

It is interesting to compare the observations described here with the Igun model [53], which showed that the selection of a given treatment or system of health care is determined by personal, family, and sociocultural conceptualizations related to the cause, severity, and potential consequences of the diseases as well as the effectiveness and cost and difficulty in obtaining different types of health care (traditional or modern).

### **3.3. Characterization of the macro‐, meso‐ and microfoci**

the same geographic area, the CAP of rural populations may be very different. For example, populations that have been settled in this area for a longer period are of African descent. These populations fear the disease and strongly prefer to avoid jobs that involve entering the jungle to prevent infection. People in these communities also believe that leishmaniasis is a "hallmark of the jungle" and that having the disease means that the jungle is welcoming your

Another population, known as "paisas," is a recent settlement of people from coffee cultivating areas who came to this region over the last 30 years; this region has an endemic focus of CL produced by *L. panamensis*, and people in this population use caustic agents and plants to treat the disease. Treatment with caustic agents consists of the local application of various substances such as silver nitrate, sulfuric acid, hot water, and hot brown sugar and, frequently, cauterization of the lesion with a spoon or the tip of a machete that has been placed in a fire and is applied without anesthesia to the ulcer, leaving a smooth scar [49]. Treatment with plants consists of the local application of macerated leaves or bark of various trees and shrubs and some latex from vines, many with leishmanicidal action previously demonstrated in the laboratory [50]. In recent settlement communities, no preference for a plant or group of plants exists, and a wide range of plants is used; however, moxa is

Conceptions of the disease are closely associated with not only culture but also social relations. For example, gender relations are represented by the provision of feminine or masculine attributes to ulcers, the papular, silent type of ulcers that are not easily observed and generally isolated and difficult to treat are called "male pito" and the ulcerous lesions that are often numerous, "weep" (produce fluid), and more easily observed and treated are called

Nonspecific medications are often used, including antifungal drugs, ointments, salves, local application antibiotics, and veterinary medicines; these medications are generally self‐made or prescribed by doctors who have had no possibility to confirm the diagnosis with laboratory tests. Among the most commonly used veterinary drugs is ivermectin, which has been recently approved for human use and has been found to be effective in

In our studies conducted in indigenous communities, it was not possible to verify the use of urine as a healing element, which has been described in black communities in central San Juan [52]; in these communities, in addition to using urine for diagnosis, it has been used for treatment of various skin diseases, rheumatism, and snakebites and smeared on the skin

It is interesting to compare the observations described here with the Igun model [53], which showed that the selection of a given treatment or system of health care is determined by personal, family, and sociocultural conceptualizations related to the cause, severity, and potential consequences of the diseases as well as the effectiveness and cost and difficulty in obtaining

different types of health care (traditional or modern).

arrival; therefore, they have no preventive measures against it.

one of the most popular.

46 The Epidemiology and Ecology of Leishmaniasis

"female pito" [49].

some studies [51].

or drank.

Although the first record of leishmaniasis in Colombia was reported in 1872 by Indalecio Camacho, it was not until the early 1980s that the study of the macrofoci of leishmaniasis began. During this decade, leishmaniasis was defined as a sylvan disease affecting men working in affected areas as loggers, soldiers, and hunters. One of the first eco‐epidemiologic studies was conducted in Montebello in 1986; in this mesofocus, the risk of infection in homes (microfocus) as opposed to in the extradomiciliary environment was characterized for the first time because the vectors were identified in the intradomicile and much of the affected and at risk populations was identified to be women and children under the age of 5 [6, 54].

In the indigenous community of San Andres de Sotavento-Cordoba on Colombia's Caribbean coast, a microfocus for VL has been identified in homes that were located near the gallery forest. In these cases, *Lu. evansi* species were found to be able to easily access homes and bite entire families, including the population group that is most at risk of developing VL, children under the age of 5 years. In the same region, a high rate of infected dogs with *Leishmania* has been identified, as have vectors, which have even been found to be present in areas with a low incidence of VL; these infected vectors and reservoirs have been found in the extradomicile, but *Lu. evansi* has not been found to enter homes, and therefore VL cases have not been identified. In the evening hours when increased biting activity of *Lu. evansi* has been identified, children are often inside homes and within the reach of infected vectors. However, adults that have been bitten in the extradomicile have not been found to develop the disease [7].

Humans play a modulatory role in facilitating or hindering the risk of transmission. For example, in the Magdalena River valley region, deforestation and rangeland establishment have confined the CL insect vectors to the forest. These species have been found to not reach the home when a paddock belt is more than 100 meters away. However, deforestation, while increasing the distance from some vector species, also creates favorable environments for the establishment of others. Such is the case of *Lu. longipalpis*, a VL vector in the Magdalena River valley region, which has been found to invade new areas and create new risks for populations living in these regions.

Characterization of microfoci has helped the creation of proposals for prevention and control.
