Graham J. Hickling

Adaptive human behavior in epidemiological models

The science and management of infectious disease are entering a new stage. Increasingly public policy to manage epidemics focuses on motivating people, through social distancing policies, to alter their behavior to reduce contacts and reduce public disease risk. Person-to-person contacts drive human disease dynamics. People value such contacts and are willing to accept some disease risk to gain contact-related benefits. The cost–benefit trade-offs that shape contact behavior, and hence the course of epidemics, are often only implicitly incorporated in epidemiological models. This approach creates difficulty in parsing out the effects of adaptive behavior. We use an epidemiological–economic model of disease dynamics to explicitly model the trade-offs that drive person-to-person contact decisions. Results indicate that including adaptive human behavior significantly changes the predicted course of epidemics and that this inclusion has implications for parameter estimation and interpretation and for the development of social distancing policies. Acknowledging adaptive behavior requires a shift in thinking about epidemiological processes and parameters.

Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States.

The geographic pattern of human risk for infection with Borrelia burgdorferi sensu stricto, the tick-borne pathogen that causes Lyme disease, was mapped for the eastern United States. The map is based on standardized field sampling in 304 sites of the density of Ixodes scapularis host-seeking nymphs infected with B. burgdorferi, which is closely associated with human infection risk. Risk factors for the presence and density of infected nymphs were used to model a continuous 8 km×8 km resolution predictive surface of human risk, including confidence intervals for each pixel. Discontinuous Lyme disease risk foci were identified in the Northeast and upper Midwest, with a transitional zone including sites with uninfected I. scapularis populations. Given frequent under- and over-diagnoses of Lyme disease, this map could act as a tool to guide surveillance, control, and prevention efforts and act as a baseline for studies tracking the spread of infection.

Use of tick surveys and serosurveys to evaluate pet dogs as a sentinel species for emerging Lyme disease.

OBJECTIVE To evaluate dogs as a sentinel species for emergence of Lyme disease in a region undergoing invasion by Ixodes scapularis. SAMPLE POPULATION 353 serum samples and 78 ticks obtained from dogs brought to 18 veterinary clinics located in the lower peninsula of Michigan from July 15, 2005, through August 15, 2005. PROCEDURES Serum samples were evaluated for specific antibodies against Borrelia burgdorferi by use of 3 serologic assays. Ticks from dogs were subjected to PCR assays for detection of pathogens. RESULTS Of 353 serum samples from dogs in 18 counties in 2005, only 2 (0.6%) contained western blot analysis-confirmed antibodies against B burgdorferi. Ten of 13 dogs with I scapularis were from clinics within or immediately adjacent to the known tick invasion zone. Six of 18 I scapularis and 12 of 60 noncompetent vector ticks were infected with B burgdorferi. No ticks were infected with Anaplasma phagocytophilum, and 3 were infected with Babesia spp. CONCLUSIONS AND CLINICAL RELEVANCE Serosurvey in dogs was found to be ineffective in tracking early invasion dynamics of I scapularis in this area. Tick chemoprophylaxis likely reduces serosurvey sensitivity in dogs. Ticks infected with B burgdorferi were more common and widely dispersed than seropositive dogs. In areas of low tick density, use of dogs as a source of ticks is preferable to serosurvey for surveillance of emerging Lyme disease. IMPACT FOR HUMAN MEDICINE By retaining ticks from dogs for identification and pathogen testing, veterinarians can play an important role in early detection in areas with increasing risk of Lyme disease.

Diverse Borrelia burgdorferi Strains in a Bird-Tick Cryptic Cycle†

ABSTRACT The blacklegged tick Ixodes scapularis is the primary vector of the most prevalent vector-borne zoonosis in North America, Lyme disease (LD). Enzootic maintenance of the pathogen Borrelia burgdorferi by I. scapularis and small mammals is well documented, whereas its “cryptic” maintenance by other specialist ticks and wildlife hosts remains largely unexplored because these ticks rarely bite humans. We quantified B. burgdorferi infection in a cryptic bird-rabbit-tick cycle. Furthermore, we explored the role of birds in maintaining and moving B. burgdorferi strains by comparing their genetic diversity in this cryptic cycle to that found in cycles vectored by I. scapularis. We examined birds, rabbits, and small mammals for ticks and infection over a 4-year period at a focal site in Michigan, 90 km east of a zone of I. scapularis invasion. We mist netted 19,631 birds that yielded 12,301 ticks, of which 86% were I. dentatus, a bird-rabbit specialist. No resident wildlife harbored I. scapularis, and yet 3.5% of bird-derived ticks, 3.6% of rabbit-derived ticks, and 20% of rabbit ear biopsy specimens were infected with B. burgdorferi. We identified 25 closely related B. burgdorferi strains using an rRNA gene intergenic spacer marker, the majority (68%) of which had not been reported previously. The presence of strains common to both cryptic and endemic cycles strongly implies bird-mediated dispersal. Given continued large-scale expansion of I. scapularis populations, we predict that its invasion into zones of cryptic transmission will allow for bridging of novel pathogen strains to humans and animals.

Associations of passerine birds, rabbits, and ticks with Borrelia miyamotoi and Borrelia andersonii in Michigan, U.S.A.

BackgroundWild birds contribute to maintenance and dissemination of vectors and microbes, including those that impact human, domestic animal, and wildlife health. Here we elucidate roles of wild passerine birds, eastern cottontail rabbits (Sylvilagus floridanus), and Ixodes dentatus ticks in enzootic cycles of two spirochetes, Borrelia miyamotoi and B. andersonii in a region of Michigan where the zoonotic pathogen B. burgdorferi co-circulates.MethodsOver a four-year period, wild birds (n = 19,631) and rabbits (n = 20) were inspected for tick presence and ear tissue was obtained from rabbits. Samples were tested for Borrelia spirochetes using nested PCR of the 16S-23S rRNA intergenic spacer region (IGS) and bidirectional DNA sequencing. Natural xenodiagnosis was used to implicate wildlife reservoirs.ResultsIxodes dentatus, a tick that specializes on birds and rabbits and rarely bites humans, was the most common tick found, comprising 86.5% of the 12,432 ticks collected in the study. The relapsing fever group spirochete B. miyamotoi was documented for the first time in ticks removed from wild birds (0.7% minimum infection prevalence; MIP, in I. dentatus), and included two IGS strains. The majority of B. miyamotoi-positive ticks were removed from Northern Cardinals (Cardinalis cardinalis). Borrelia andersonii infected ticks removed from birds (1.6% MIP), ticks removed from rabbits (5.3% MIP), and rabbit ear biopsies (5%) comprised twelve novel IGS strains. Six species of wild birds were implicated as reservoirs for B. andersonii. Frequency of I. dentatus larval and nymphal co-feeding on birds was ten times greater than expected by chance. The relatively well-studied ecology of I. scapularis and the Lyme disease pathogen provides a context for understanding how the phenology of bird ticks may impact B. miyamotoi and B. andersonii prevalence and host associations.ConclusionsGiven the current invasion of I. scapularis, a human biting species that serves as a bridge vector for Borrelia spirochetes, human exposure to B. miyamotoi and B. andersonii in this region may increase. The presence of these spirochetes underscores the ecological complexity within which Borrelia organisms are maintained and the need for diagnostic tests to differentiate among these organisms.

Different Populations of Blacklegged Tick Nymphs Exhibit Differences in Questing Behavior That Have Implications for Human Lyme Disease Risk

Animal behavior can have profound effects on pathogen transmission and disease incidence. We studied the questing (= host-seeking) behavior of blacklegged tick (Ixodes scapularis) nymphs, which are the primary vectors of Lyme disease in the eastern United States. Lyme disease is common in northern but not in southern regions, and prior ecological studies have found that standard methods used to collect host-seeking nymphs in northern regions are unsuccessful in the south. This led us to hypothesize that there are behavior differences between northern and southern nymphs that alter how readily they are collected, and how likely they are to transmit the etiological agent of Lyme disease to humans. To examine this question, we compared the questing behavior of I. scapularis nymphs originating from one northern (Lyme disease endemic) and two southern (non-endemic) US regions at field sites in Wisconsin, Rhode Island, Tennessee, and Florida. Laboratory-raised uninfected nymphs were monitored in circular 0.2 m2 arenas containing wooden dowels (mimicking stems of understory vegetation) for 10 (2011) and 19 (2012) weeks. The probability of observing nymphs questing on these stems (2011), and on stems, on top of leaf litter, and on arena walls (2012) was much greater for northern than for southern origin ticks in both years and at all field sites (19.5 times greater in 2011; 3.6–11.6 times greater in 2012). Our findings suggest that southern origin I. scapularis nymphs rarely emerge from the leaf litter, and consequently are unlikely to contact passing humans. We propose that this difference in questing behavior accounts for observed geographic differences in the efficacy of the standard sampling techniques used to collect questing nymphs. These findings also support our hypothesis that very low Lyme disease incidence in southern states is, in part, a consequence of the type of host-seeking behavior exhibited by southern populations of the key Lyme disease vector.

Synchronous phenology of juvenile Ixodes scapularis, vertebrate host relationships, and associated patterns of Borrelia burgdorferi ribotypes in the midwestern United States

To elucidate features of enzootic maintenance of the Lyme disease bacterium that affect human risk of infection, we conducted a longitudinal study of the phenology of the vector tick, Ixodes scapularis, at a newly invaded site in the north-central United States. Surveys for questing ticks and ticks parasitizing white-footed mice and eastern chipmunks revealed that I. scapularis nymphal and larval activity peaked synchronously in June and exhibited an atypical, unimodal seasonality. Adult seasonal activity was bimodal and distributed evenly in spring and fall. We discuss implications of these phenology data for the duration of the I. scapularis life cycle. Densities of Borrelia burgdorferi-infected, questing nymphs were comparable to those found in endemic areas elsewhere in the midwestern and northeastern U.S. Molecular genetic diversity of B. burgdorferi infecting these ticks and rodents was assessed by analysis of the ribosomal spacer types (RSTs). RST 1, a clade that includes strains with highly pathogenic properties, was relatively uncommon (3.4%) in contrast to the northeastern U.S., whereas less pathogenic ribotypes of the RST 2 and 3 clades were more common. These features of the ecology of this midwestern Lyme disease system likely contribute to the lower incidence of Lyme disease in humans in the Upper Midwest compared with that of the Northeast owing to reduced exposure to pathogenic strains of B. burgdorferi.

Effects of predation and rabbit haemorrhagic disease on population dynamics of rabbits (Oryctolagus cuniculus) in North Canterbury, New Zealand

The impact of predation and rabbit haemorrhagic disease (RHD) on population dynamics of rabbits, and the survival of juvenile rabbits, was investigated between July 1999 and March 2000 in North Canterbury, New Zealand. Rabbit abundance and pre- and post-emergent rabbit mortality were monitored on four sites, two of which were subject to predator control. RHD spread naturally through all sites from late November to early December. Rabbit densities declined on all sites, but after the RHD epidemic, declines were significantly greater where populations of predators had not been controlled. Survival of rabbit nestlings was lower where predators were not controlled. All post-emergent radio-collared rabbits died at sites where predators were not controlled, whereas 18% of those collared at sites where predators were controlled survived to maturity. In contrast to the results from previous studies, rabbits born at the start of the breeding season had very high rates of post-emergent mortality, as they appeared to be susceptible to the RHD virus later in the breeding season. The age at which juvenile rabbits become susceptible to RHD, the timing of RHD epidemics, and the abundance of predators are likely to be important in determining survival of juvenile rabbits. This study demonstrates that predation can reduce rabbit populations to low levels, but only in combination with other factors, in this case RHD.

Management of infectious wildlife diseases: Bridging conventional and bioeconomic approaches

The primary goal of disease ecology is to understand disease systems and then use this information to inform management. The purpose of this paper is to show that conventional disease ecology models are limited in their ability to inform management of systems that are already infected, and to show how such models can be integrated with economic decision models to improve upon management recommendations. Management strategies based solely on disease ecology entail managing infected host populations or reservoir populations below a threshold value based on R0, the basic reproductive ratio of the pathogen, or a multiple-host version of this metric. These metrics measure a pathogens ability to invade uninfected systems and do not account for postinfection dynamics. Once a pathogen has invaded a population, alternative management criteria are needed. Bioeconomic modeling offers a useful alternative approach to developing management criteria and facilitates the consideration of ecological-economic trade-offs so that diseases are managed in a cost-effective manner. The threshold concept takes on a more profound role under a bioeconomic paradigm: rather than unilaterally determining disease control choices, thresholds inform control choices and are influenced by them.

High-Prevalence Borrelia miyamotoi Infection Among Wild Turkeys (Meleagris gallopavo) in Tennessee

ABSTRACT During spring and fall 2009, 60 wild turkeys (Meleagris gallopavo) harvested by Tennessee hunters were surveyed for Borrelia spp. by sampling their blood, tissue, and attached ticks. In both seasons, 70% of turkeys were infested with juvenile Amblyomma americanum; one spring turkey hosted an adult female Ixodes brunneus. Polymerase chain reaction assays followed by DNA sequencing indicated that 58% of the turkeys were positive for the spirochete Borrelia miyamotoi, with tissue testing positive more frequently than blood (P = 0.015). Sequencing of the 16S–23S rRNA intergenic spacer indicated ≥99% similarity to previously published sequences of the North American strain of this spirochete. Positive turkeys were present in both seasons and from all seven middle Tennessee counties sampled. No ticks from the turkeys tested positive for any Borrelia spp. This is the first report of B. miyamotoi in birds; the transmission pathways and epidemiological significance of this high-prevalence spirochetal infection remain uncertain.