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Elucidating the Mechanism of Trypanosoma Cruzi Acquisition by Triatomine Insects: Evidence from a Large Field Survey of Triatoma Infestans

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Elucidating the Mechanism of Trypanosoma Cruzi Acquisition by Triatomine Insects: Evidence from a Large Field Survey of Triatoma Infestans Tropical Medicine and Infectious Disease Article Elucidating the Mechanism of Trypanosoma cruzi Acquisition by Triatomine Insects: Evidence from a Large Field Survey of Triatoma infestans Aaron W. Tustin 1, Ricardo Castillo-Neyra 2,3 , Laura D. Tamayo 2, Renzo Salazar 2 , Katty Borini-Mayorí 2 and Michael Z. Levy 2,3,* 1 Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USA; [email protected] 2 Zoonotic Disease Research Lab, One Health Unit, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Lima Province 15102, Peru; [email protected] (R.C.-N.); [email protected] (L.D.T.); [email protected] (R.S.); [email protected] (K.B.-M.) 3 Department of Biostatistics, Epidemiology & Informatics, Perelman School of Medicine of the University of Pennsylvania, Philadelphia, PA 19104, USA * Correspondence: [email protected]; Tel.: +1-215-746-8131 Received: 25 March 2020; Accepted: 26 May 2020; Published: 1 June 2020 Abstract: Blood-sucking triatomine bugs transmit the protozoan parasite Trypanosoma cruzi, the etiologic agent of Chagas disease. We measured the prevalence of T. cruzi infection in 58,519 Triatoma infestans captured in residences in and near Arequipa, Peru. Among bugs from infected colonies, T. cruzi prevalence increased with stage from 12% in second instars to 36% in adults. Regression models demonstrated that the probability of parasite acquisition was roughly the same for each developmental stage. Prevalence increased by 5.9% with each additional stage. We postulate that the probability of acquiring the parasite may be related to the number of feeding events. Transmission of the parasite does not appear to be correlated with the amount of blood ingested during feeding. Similarly, other hypothesized transmission routes such as coprophagy fail to explain the observed pattern of prevalence. Our results could have implications for the feasibility of late-acting control strategies that preferentially kill older insects. Keywords: Trypanosoma cruzi; Triatoma infestans; Chagas disease; parasite prevalence; coprophagy 1. Introduction Trypanosoma cruzi, the protozoan parasite that causes Chagas disease, is transmitted to humans via the feces of blood-sucking triatomine insects (Hemiptera: Reduviidae) such as Triatoma infestans, the major vector of Chagas disease in much of South America [1]. Triatomines pass through five nymphal instar stages before becoming adults. All triatomine stages are at risk for acquiring T. cruzi because they all ingest blood meals. Insects may also become infected when they engage in behaviors such as coprophagy [2]. Once acquired, infection with T. cruzi is persistent [3]. Therefore, in well-stablished colonies with stable transmission patterns, T. cruzi prevalence is expected to increase monotonically with the insects’ developmental stage. The general shape (e.g., linear, exponential, logarithmic) of the rising prevalence curve may give clues as to the method of transmission. With respect to Chagas disease control, it may be important to ascertain the shape of this relationship between T. cruzi prevalence and stage. In this report we show the stage-prevalence of T. cruzi in a large sample of T. infestans captured during vector control and surveillance activities in Arequipa, Peru. These data allow us to test three hypotheses of T. cruzi acquisition by triatomines. Our first hypothesis, hereafter called the Blood Trop. Med. Infect. Dis. 2020, 5, 87; doi:10.3390/tropicalmed5020087 www.mdpi.com/journal/tropicalmed Trop. Med. Infect. Dis. 2020, 5, 87 2 of 10 Hypothesis,Trop. Med. Infect. is thatDis. 2020 the, 5 probability, x FOR PEER REVIEW of infection with T. cruzi depends upon the amount of2 bloodof 10 ingested. Observations of laboratory-reared insects indicate that the quantity of blood ingested by ingested. Observations of laboratory-reared insects indicate that the quantity of blood ingested by T. T. infestans increases rapidly and nonlinearly with stage [4] Thus, if the Blood Hypothesis is correct, infestans increases rapidly and nonlinearly with stage [4] Thus, if the Blood Hypothesis is correct, there might be a rapid nonlinear rise in T. cruzi prevalence with stage (Figure1A). A second possibility there might be a rapid nonlinear rise in T. cruzi prevalence with stage (Figure 1A). A second is thatpossibility an insect’s is that risk an of insect’s infection risk depends of infection upon depends the number upon the of opportunitiesnumber of opportunities to acquire theto acquire parasite (Bitesthe Hypothesis), parasite (Bites rather Hypothesis), than the rather amount than of bloodthe amount ingested. of blood Under ingested. this hypothesis, Under thisT. cruzihypothesis,prevalence T. amongcruzi instarsprevalence might among risein instars a roughly might linear rise in fashion a roughl withy linear stage fashion (Figure with1B), stage as all (Figure nymphs 1B), probably as all takenymphs roughly probably equal numbers take roughl of bites.y equal numbers of bites. Figure 1. Hypothetical shapes of the relationship between triatomine stage and prevalence of infection withFigureTrypanosoma 1. Hypothetical cruzi under shapes three of the hypotheses. relationship between (A) Acquisition triatomine of stage the parasiteand prevalence depends of infection upon the quantitywith Trypanosoma of blood ingested cruzi under (Blood three Hypothesis); hypotheses. (B )(A Parasite) Acquisition acquisition of the depends parasite upondepends the upon number the of exposurequantity opportunities of blood ingested (Bites (Blood Hypothesis); Hypothesis); (C) Early(B) Parasite instar acquisition nymphs frequently depends upon acquire the thenumber parasite of exposure opportunities (Bites Hypothesis); (C) Early instar nymphs frequently acquire the parasite via coprophagy, while older instars acquire the parasite at a lower rate via ingestion of blood from via coprophagy, while older instars acquire the parasite at a lower rate via ingestion of blood from mammalian hosts (Coprophagy Hypothesis). Note: the scale of the vertical axis is for illustrative mammalian hosts (Coprophagy Hypothesis). Note: the scale of the vertical axis is for illustrative purpose only and does not correspond to actual data; rather, panels (A) through (C) demonstrate three purpose only and does not correspond to actual data; rather, panels (A) through (C) demonstrate different theoretical shapes that could each produce 25% prevalence in fifth instars. three different theoretical shapes that could each produce 25% prevalence in fifth instars. The third hypothesis is that triatomines frequently acquire T. cruzi via coprophagy The third hypothesis is that triatomines frequently acquire T. cruzi via coprophagy (Coprophagy (Coprophagy Hypothesis). Triatomines ingest small amounts of feces of older insects in order to Hypothesis). Triatomines ingest small amounts of feces of older insects in order to acquire bacterial acquire bacterial symbionts necessary for digestion of blood meals [5]. Presumably, it is the early symbionts necessary for digestion of blood meals [5]. Presumably, it is the early instars that ingest instarsfeces, that as ingestnymphs feces, of some as nymphs species offail some to mature species in fail the to absence mature inof thesymbionts absence [6]. of symbiontsAn isolated [6 ]. Anexperiment isolated experiment has suggested has suggestedthat T. infestans that T.may infestans also acquiremay alsoT. cruzi acquire by thisT. cruzirouteby [2]. this If parasite route [2 ]. If parasitetransmission transmission via coprophagy via coprophagy is common is under common field conditions, under field then conditions, T. cruzi prevalence then T. cruzi mayprevalence increase mayrelatively increase quickly relatively among quickly first and among second first instars, and second followed instars, by a less followed rapid byincrease a less in rapid older increase nymphs in olderthat nymphs acquire thatthe parasite acquire only theparasite via blood only feeding viablood (Figure feeding 1C). (Figure1C). 2. Materials2. Materials and and Methods Methods BetweenBetween 2008 2008 and and 2014, 2014, workers workers from from thethe ArequipaArequipa Ministry of of Health Health and and the the Universidad Universidad PeruanaPeruana Cayetano Cayetano Heredia Heredia/University/University ofof PennsylvaniaPennsylvania (UPCH(UPCH/Penn)/Penn) Zoon Zoonoticotic Disease Disease Research Research LaboratoryLaboratory collected collected triatomines triatomines from from urban urban andand peri-urbanperi-urban households in in and and around around the the city city of of Arequipa.Arequipa. Located Located at 2300at 2300 m abovem above sea sea level level in anin aridan arid zone, zone, Arequipa Arequipa is the is the second second largest largest city city in Per in ú, homePerú, to 1,008,290home to 1,008,290 people [ 7people]. Since [7]. the Since 1960s, the the 1960s, population the population has been has growing been growing rapidly rapidly due to andue influx to of immigrants,an influx of immigrants, most of whom most have of whom settled have on hillsides settled on in hillsides the periphery in the ofperiphery the city. of These the city. settlements These aresettlements characterized are bycharacterized poorly built by housing, poorly built mostly hous constructeding, mostly with constructed volcanic with stone volcanic and bricks stone without and mortar,bricks where without there mortar, is a greater where presencethere is
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