Control of pyrethroid-resistant Chagas disease vectors with entomopathogenic fungi - PubMed (original) (raw)
Control of pyrethroid-resistant Chagas disease vectors with entomopathogenic fungi
Nicolás Pedrini et al. PLoS Negl Trop Dis. 2009.
Abstract
Background: Triatoma infestans-mediated transmission of Tripanosoma cruzi, the causative agent of Chagas disease, remains as a major health issue in southern South America. Key factors of T. infestans prevalence in specific areas of the geographic Gran Chaco region-which extends through northern Argentina, Bolivia, and Paraguay-are both recurrent reinfestations after insecticide spraying and emerging pyrethroid-resistance over the past ten years. Among alternative control tools, the pathogenicity of entomopathogenic fungi against triatomines is already known; furthermore, these fungi have the ability to fully degrade hydrocarbons from T. infestans cuticle and to utilize them as fuel and for incorporation into cellular components.
Methodology and findings: Here we provide evidence of resistance-related cuticle differences; capillary gas chromatography coupled to mass spectrometry analyses revealed that pyrethroid-resistant bugs have significantly larger amounts of surface hydrocarbons, peaking 56.2+/-6.4% higher than susceptible specimens. Also, a thicker cuticle was detected by scanning electron microscopy (32.1+/-5.9 microm and 17.8+/-5.4 microm for pyrethroid-resistant and pyrethroid-susceptible, respectively). In laboratory bioassays, we showed that the virulence of the entomopathogenic fungi Beauveria bassiana against T. infestans was significantly enhanced after fungal adaptation to grow on a medium containing insect-like hydrocarbons as the carbon source, regardless of bug susceptibility to pyrethroids. We designed an attraction-infection trap based on manipulating T. infestans behavior in order to facilitate close contact with B. bassiana. Field assays performed in rural village houses infested with pyrethroid-resistant insects showed 52.4% bug mortality. Using available mathematical models, we predicted that further fungal applications could eventually halt infection transmission.
Conclusions: This low cost, low tech, ecologically friendly methodology could help in controlling the spread of pyrethroid-resistant bugs.
Conflict of interest statement
NP, SJM, JRG, and MPJ have a patent pending on a blood-sucking insect trap, and a method to detect and control those insects.
Figures
Figure 1. The cuticle of T. infestans fourth-instar nymphs.
Scanning electron micrograph (SEM) of a transversal cut of the second tergite of pyrethroid-resistant (A) and pyrethroid-susceptible (B) bugs. The cuticle width was estimated in 32.1±5.9 µm and 17.8±5.4 µm respectively, P<0.0001. Magnification: 1,400×.
Figure 2. Median lethal time of both pyrethroid-susceptible (Py-S) and pyrethroid-resistant (Py-R) T. infestans treated with B. bassiana grown on two different carbon sources, under laboratory conditions.
Fifth-instar nymphs were immersed for 6 seconds in a fungal suspension (2×108 con/ml). Values are means±SD. Significant differences (P<0.05) between glucose-grown (GG) and hydrocarbon-grown (HCG) fungi are shown with an asterisk.
Figure 3. Horizontal transmission (autodissemination) of conidia from previously contaminated nymphs to initially non-infected nymphs.
Three replicates were performed per experiment, and the experiment was repeated three times at bimonthly periods. The asterisk show significant differences (P<0.05). At the end of the experiment, only 3.7% of the fungus-treated survivors were able to molt, whereas 28.2% of the control bugs did molt.
Figure 4. Efficacy of fungal intervention in rural villages, and estimation of bug population reduction on potential transmission risk.
A) Relationship between the number of insects collected and the number of insects killed by B. bassiana after the intervention. The field experiment was performed in 9 houses from two rural villages in the Argentina/Bolivia border (Fig. S1A). Insects were collected manually, no chemical-trapping methodologies were used in order to avoid potential alterations in the process of fungal infection, and therefore they account for a small number of the actual catchable bug population. Adults were 40.3±7.0% of the total insects collected; 57.1±10.4% of the adults, and 55.1±10.4% of the nymphs were killed by fungi. Most of the nymphs collected (67.6%) belonged to fourth- and fifth-instar. These stages, along with adults, account for almost all bugs that are infected . Linear regression: y = −4.98+0.90 x; r = 0.95. B) Estimation of potential T. cruzi transmission risk index (TcTRIp) after intervention with _B. bassiana_-based traps at village level. Solid lines show the predicted TcTRIp without intervention (circles), and after bug population reduction due to the experimental fungal infection shown in A) (triangles). Dotted lines indicate the predicted values of TcTRIp after 2 (squares) or 3 (diamonds) hypothetical successive interventions. Initial bug density corresponds to an arbitrary number of insects prior intervention.
References
- Schofield CJ, Jannin J, Salvatella R. The future of Chagas disease control. Trends Parasitol. 2006;22:583–588. -PubMed
- Santo Orihuela PL, Vassena CV, Zerba EN, Picollo MI. Relative contribution of monooxygenase and esterase to pyrethroid resistance in Triatoma infestans (Hemiptera: Reduviidae) from Argentina and Bolivia. J Med Entomol. 2008;45:298–306. -PubMed
- Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, et al. Evolution of supergene families associated with insecticide resistance. Science. 2002;298:179–181. -PubMed
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