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Vector transmission: how it works, what transmits, where it occurs

S.F. Breniere1, A. Villacis2 and C. Aznar3

  • 11nstitut de Recherche pour le Developpement (IRD), Montpellier, France,
  • 2Center for Infectious and Chronic Disease Research, School of Biological Sciences, Pontifical Catholic University of Ecuador, Quito, Ecuador, 3Universite des Antilles et de la Guyane, Cayenne, French Guyana

Chapter Outline

How does transmission work? 497 Who transmits the parasite? 499

Vector capacity 500 Eclectic species 501

Chagas disease in the Amazonian region 503 Where does the transmission occur? 504

In dwellings 504

In rural, urban, and periurban areas 505 Risk factors of domiciliary infestation by triatomines 505 Does vector transmission occur outside human dwellings? 507 The perception of vectors and a need for education 507 References 508

How does transmission work?

Chagas disease is commonly transmitted by bloodsucking triatomine vectors living in residential dwellings (domestic vectors) in close contact with humans. Indeed, the main interventions implemented to decrease transmission focus on eliminating vectors that live in dwellings. Generally, transmission occurs during the night when the insects are most active, at which time they take their blood meal on sleeping humans. The parasite is transmitted during this contact, but the free-infection form (flagellated) is in the feces of the insect rather than the salivary glands, as in most other arthropod vectors. The parasites are concentrated in the rectal bulb in the terminal part of the digestive tube of the insect, and during the blood meal or soon after, the bugs defecate and deposit the infected feces on the skin or near mucosa. The bite causes a skin abrasion that allows the parasite to enter underneath the skin. This transmission is complex, and all the steps are not well understood. Its load

American Trypanosomiasis Chagas Disease. DOI: http://dx.doi.org/10.1016/B978-0-12-801029-7.00023-X

Copyright © 2017 Elsevier Inc. All rights reserved.

Rhodnius prolixus taking a meal on human skin

Figure 22.1 Rhodnius prolixus taking a meal on human skin.

Source: Electronic publication from “Centro de Analisis de Imagenes Biomtsdicas Computarizadas,” CAIBCO, Instituto de Medicina, Tropical, Facultad de Medicina, Universidad Central de Venezuela.

depends on many factors including those that promote human—vector contact and those that allow the parasite to enter its host (Fig. 22.1).

The first step is the contact between the vector and the mammal. What attracts the bugs to their prey? Heat, carbon dioxide, and odors could be cues and lures that direct the bugs. Triatoma dimidiata and Rhodnius prolixus are major vectors of Chagas disease in Central and South America: in experimental tests, these vectors were more attracted by heat or CO2 alone than by selected chemicals.1 In experiments where the breathing of a host was mimicked by pulses of CO2 and where a continuous flow of CO2 was provided, Triatoma infestans, the main vector in the Southern Cone, was attracted.2 However, CO2 may not be an essential component to attract triatomines.3 In 2002, it was speculated that T. infestans possess thermoreceptors as do other animals and insects, which aids in hunting and feeding.4 Additional studies have shown that heat has a significant attractive effect, such as the heat emitted by the face, which can attract a triatomine bug from a distance of 2 m.5 Furthermore, moisture could increase the attraction of a hot spot, but this effect may be limited to short distances.6 A double-choice olfactometer was used to test volatile substances and showed that R. prolixus is also attracted by the odors of human skin and even microflora compounds present mainly on the face, which would explain why the bites frequently occur on the human face.7 Among the factors that influence the movement of the bugs toward their prey, infrared radiation could be a cue, as recently suggested when analyzing the infrared emission in landscapes from sunset to the early hours of the night.8

The duration of the blood meal of triatomines is long because the insect must obtain a large quantity of blood. It is important that the host does not react in a hostile manner because of the pain caused by the bite. A number of biological properties of triatomine saliva are similar to that of other arthropods and help the vector obtain its meal while also facilitating the transmission of the pathogenic agents. Among others, the saliva proteomic analyses have identified a large number of these factors.9 Thus, saliva contains anesthetic factors, anticoagulants, and vasodilators that facilitate the intake of blood.10,11 Although the anesthetic effect has been little studied, parasitological xenodiagnosis was used with different species of triatomine. The patient was exposed to the bite of 30—40 nymphs, and the bites were rather painless.12 Interestingly, the use of triatomines to obtain blood from small animals with cryptic veins was proposed as an alternative to conventional blood sampling13; the authors reported that the animals may be less stressed and possibly did not notice the bloodsucking insect. However, it should be noted that the inhabitants of hyperendemic areas frequently testified that the bug density was so high in their house (T. infestans) that they would be awakened at night by the attack of bugs, and they were forced to sleep elsewhere (“nos sacaban de la casa”).

The parasites contained in feces can penetrate skin cells through the abrasion made by the bite. In fact, intact skin is an effective barrier against Trypanosoma cruzi, but very small abrasions of the skin (e.g., triggered by scraping) could allow the parasite to penetrate the skin. In experimental trials on mice of the natural route of infection via skin, cells were invaded very quickly.14 The results showed that the parasite spread rapidly (<15 min) from the site of inoculation. At least a few parasitic forms can be immediately transported, possibly through the lymphatic or blood system, and then disseminated to other tissues of the host. Of course, if the parasites are transmitted via the mucosa, cells are easier to infect. In the invasion process, triatomine saliva still plays a role. It has an inhibitory effect on the activation of the classical complement pathway that acts in the lysis of foreign agents.15 The role of the complex salivary secretion of triatomines is not well known, but immunomodulating proteins exist in the saliva of several hematophagous arthropods, and it has been widely observed that saliva can enhance the infectivity of pathogens.16 Saliva particularly affects the activation of T- and B-lymphocytes, macrophages, and dendritic cells. Interestingly, lyso- phosphatidylcholine, a component present in the saliva of R. prolixus, acts as a powerful chemoattractant for inflammatory cells at the site of the bug bite, leading to a concentration of available cells for infection.17 Thus, saliva is able to create a local environment conducive to cell invasion by the parasite.

Human infection requires the multiplication of the parasite, which occurs only in the host cells in the amastigote form. In fact, T. cruzi invades a wide variety of vertebrate cells by endocytosis, including phagocytic cells, using a mechanism distinct from phagocytosis.18 There are many mechanisms of recognition between the parasite and host cells, and T. cruzi has adapted to invade a wide variety of specialized cells.19—21

 
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