Cracking the Glass Darkly: The Ancient Path to Lasting Happiness
During the mids through the early s, increases in the case numbers of reported spotted fever group rickettsioses were documented in several countries bordering the Mediterranean Sea, including Israel, Italy, and Spain Piras et al. Average annual incidence of Rocky Mountain spotted fever, per 1 million population in the United States, — Childs and Paddock, ; Openshaw et al.
Unfortunately, the reasons suggested for major periods of increased or diminished incidence of tick-borne diseases have, with few exceptions, been difficult to investigate and even more difficult to corroborate. These infections have circulated dynamically in nature for many thousands of years, and biological equilibria among the pathogen, tick, and vertebrate hosts parasitized by the tick or infected by the pathogen characteristically exist in the absence of humans.
Nonetheless, the emergence and flux of tick-borne diseases can most often be traced to specific human activities and behaviours that create disequilibrium in these cycles and position greater numbers of persons into disrupted ecosystems. Outbreaks of tick-borne disease are often linked to ecologic and social upheavals, resulting directly from human influence, that create circumstances advantageous for large numbers of ticks and reservoir hosts.
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During World War II, following the occupation of Crimea by Axis forces, there was abandonment of agricultural lands and diminished hunting of European hares Lepus europaeus because of combat activities. When Soviet troops reoccupied the Crimean steppes in , pastures and farms had become overgrown by weeds, and hares had become extremely abundant and were heavily parasitized with Hyalomma ticks.
The combination of these factors is believed to have contributed to an epidemic of CCHF among military personnel during —, involving especially signalmen and surveyors, who frequented brushy areas Hoogstraal, A careful analysis of climatic and vegetation features with georeferenced cases of CCHF in Turkey during — identified a recent expansion of extensively fragmented habitats in the Anatolia region as the most important factor for the CCHF epidemic in this region. In a similar manner, whole-scale clearing of primary old-growth forests by inhabitants in the northeastern United States in the late 18th and early 19th Centuries, followed by the abandonment of farms during the westward expansion of the late 19th Century, and subsequent deciduous successional growth that provided ideal habitats for white-tailed deer Odocoileus virginianus and deer ticks Ixodes scapularis dammini , fueled the emergence of Lyme disease in the second half of the 20th Century Spielman et al.
In Italy, changes in forest management practices during the last several decades of the 20th Century transitioned a greater percentage of coppice cover small areas of broad-leaved forest harvested regularly for firewood to high-stand forests and improving habitat suitability for small reservoir hosts of Ixodes ricinus ticks. This manipulation of forest structure is believed to have contributed to the steadily increasing incidence of TBE observed in 17 northern alpine provinces since the early s Rizzoli et al. Environmental disturbance is a frequent trigger for outbreaks of tick-borne infection.
The most extensively studied example, Lyme disease in the northeastern United States, resulted from reforestation, increased deer density, and increased development and use of forested sites by humans Spielman et al. It is likely that the deer tick vector and its microbial guild survived in relict sites during and after glaciation and through Colonial times Telford et al. Infestations of the deer tick were first recognized from the terminal moraine areas of southern New England and Long Island as well as northwest Wisconsin; these were also the sites where the first cases of Lyme disease or babesiosis were identified in the United States Spielman et al.
In the mids, Ipswich, Massachusetts represented the northernmost established infestation in the Northeast Lastavica et al. Within a decade, the distribution of the deer tick expanded on a north-south axis to the Bar Harbor region in Maine and the coastal peninsula of Delaware, Maryland, and Virginia Rand et al. Infestation of migratory birds by deer tick larvae and nymphs served as the primary mode of introduction Battaly et al.
Transport of adult ticks by deer along major waterways also contributed to a rapid spread, particularly in the Hudson River Valley Chen et al. Other recent examples of range expansions of medically important tick species include the establishment of Amblyomma americanum a vector of E. Conversely, loss of habitat or a host species may reduce the abundance of a historically dominant tick species.
From a tick surveillance program in Ohio during — D. From —, 1, adult D. The causes of these apparent shifts remain speculative; however, a hypothesis to explore is the effect of periodic scarcity of keystone hosts for D. The anthropogenic nature of tick-borne infections is considerable and sustained human activities that deplete or amplify the vertebrate host populations can manifest as surges of disease incidence in human populations.
In Brazil, capybara Hydochoerus hydrochaeris are important hosts to the tick Amblyomma cajennense , a vector of RMSF , and an effective amplifying host for R. Several arguments document the role of white-tailed deer in the emergence and expansion of Lyme disease, babesiosis, ehrlichiosis, and anaplasmosis Piesman et al. These 4 diseases were identified and characterized during the last 3 decades of the 20th century, following a period of near-exponential growth of white-tailed deer populations in multiple regions of the eastern United States.
At the end of the 19th Century, following several decades of overhunting and habitat loss, an estimated ,—, deer existed in the United States. Intensive conservation efforts, coupled with expansive environmental changes that inadvertently provided ideal habitats for these animals to proliferate, caused an eruptive increase of the numbers of deer to approximately 18 million animals by Because these animals serve as keystone hosts for I.
Because O. Because roe deer are also considered crucial in maintaining and amplifying I. In , a dramatic resurgence of MSF in the region occurred simultaneously with the recovery of the wild rabbit population, suggesting to some investigators that these two events were linked ecologically and epidemiologically Le Gac et al. Disequilibrium among domesticated animals may create drastic changes as well. More than 90 cases of RMSF , including 11 deaths, have been reported from several small communities in the White Mountain area of eastern Arizona since This outbreak appears to be linked directly to enormous numbers of R.
Risk factors for human exposure to vectors, and human-associated factors that modify this risk, including activity patterns and the use of personal protection, remain poorly studied. In addition, incidence data of sufficient duration and at the appropriate temporal and spatial scales are often not available to validate existing quantitative models. Accordingly, if one cannot accurately predict incidence for a site over a short interval of time, despite readily measured surveillance variables, then any long-term prediction for the results of climate change remain conjectural.
Nonetheless, climate change has been implicated frequently as an important driver of incidence. The spread of tick-borne borreliosis in West Africa is possibly linked to a sub-Saharan drought that allowed the tick vector, Alectorobius sonrai , to colonize new savannah areas Trape et al. It has been suggested that warmer weather increases the frequency with which R.
Of the tick-borne diseases, TBE perhaps has the best incidence data across a range of scales, as well as ecological data, that permit detailed examination for causality. During the mids, the incidence of TBE in Sweden increased from 2 to 5 per , population, and two opposing factors confounded epidemiologic analyses: an increase in roe deer density, to suggest a greater abundance of I.
Even with confounding, a multiple regression analysis of meteorological data and TBE incidence suggested that a milder winter in the previous year, with 2 consecutive mild spring and fall seasons, predicted increased incidence. However, climate change alone does not adequately explain the remarkably rapid increase in the incidence of TBE across much of Europe during the last few decades, particularly in the Baltic States Figure A ; the factors that influence changes in TBE transmission, and ultimately human risk, appear to be more numerous and complex. What is known is that the risk of TBE in humans is dependent on the frequency of exposure to bites by infected ticks, which is dependent on human behaviour and on various biotic and abiotic factors, including climate Rizzoli et al.
Starting in , mean springtime temperatures increased across the Baltics; however, the change in TBE incidence among these counties was spatiotemporally heterogeneous and inconsistent with regional weather phenomena Sumilo et al. Simultaneously, a decline of collective farming in the post-communism Baltic States conceivably induced successional growth that promoted landscape changes, altering the fauna associated with I.
In addition, berry picking, mushroom gathering, and other socioeconomically related food-seeking activities placing individuals in more frequent contact with tick-infested habitats are believed to have increased during this same period, as a result of economic changes associated with the fall of the Soviet Union. In this context, short-term climate changes that provided optimal growing conditions for mushrooms and berries in Baltic forests may indeed have been a driver for risk, but only in direct association with human behaviors that resulted in increased exposure to tick-infested habitats Figure A Randolph, ; Randolph et al.
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Scientific, medical, or veterinary interest in a particular pathogen, or changes in the epidemiologic programs or organizational frameworks used to survey for a particular disease, may have enormous impact on the recorded incidence. By example, only 27 cases of Powassan encephalitis were reported in North America during the 3 decades after its discovery in ; however, the introduction of West Nile virus to the continent in the late s stimulated enhanced surveillance for arthropod-borne encephalitis by state and local health departments, and is believed to be the major factor in the recognition of 20 U.
Prior to the early s, research in tick-borne infections focused largely on RMSF , TBE , and diseases associated directly with animal health, such as babesiosis and theileriosis. The emergence of Lyme disease in the northeastern United States during the late s, particularly at sites where an affluent population lived or vacationed, stimulated a renaissance in tick biology and ecology that was driven, in part, by increased availability of state and federal funds for Lyme disease research.
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A single individual with interest in a specific disease, particularly one that is otherwise infrequently diagnosed and seldom reported, can have tremendous impact on the incidence of that disease. By example, no cases of MSF from Algeria were documented in the medical literature until 1 clinician identified 93 cases during a 4-month interval in Mouffok et al. Austria and Slovenia have among the highest reported rates of Lyme disease in Europe, with an average annual incidence of and per , population, respectively Smith and Takkinen, ; however, reporting in these countries is likely enhanced because of particularly energetic Lyme disease researchers who work in this region Stanek and Strle, Conversely, it has been suggested that the precipitous drop in reported cases of RMSF witnessed in the United States during the s might be attributable, in part, to the death in of R.
Parker, who had been the driving force behind U. RMSF surveillance activities for more than 3 decades Burgdorfer, In the United States, surveillance data for tick-borne diseases are acquired voluntarily through separate but complementary reporting instruments that collectively comprise a national system of passive surveillance.
Incidence statistics for all U. Understandably, compliance with requests to physicians and state and local health department staff to provide supplemental data is problematic. The non-submission of CRFs and the incompleteness of supplementary data collection suggest that a considerable percentage of cases tick-borne disease in the United States are unavailable for detailed analyses, including analysis of risk factors that determine severity Childs and Paddock, Establishing an accurate and specific case definition that couples well-defined clinical characteristics with specific laboratory confirmation is fundamentally important in all forms of surveillance and provides the foundation from which subsequent epidemiologic parameters are derived.
The absence of standardized case definitions for tick-borne diseases that cross regional or national borders remains a crucial problem in the accumulation of broad scale incidence data for many of these infections. Case definitions are not immutable, and as clinical knowledge about a particular disease expands and evolves, the case definition may be remodeled to include clinical or laboratory data specific to the disease.
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Because so many tick-borne infections are relatively new to science and medicine, it is not surprising that case definitions and surveillance systems for several of these diseases have required years or decades of refinement Table A In this context, incidence statistics, particularly early in the evolution of these systems, should be interpreted cautiously, and comparisons of data from year-to-year, or even decade-to-decade, may be misleading. While passive surveillance requires a reasonably high level of stability to maintain its effectiveness, it must also remain malleable, and responsive to new information gained about a particular disease.
A well-crafted case definition provides more robust surveillance for the recognized disease and better positions investigators to detect clinically or epidemiologically similar diseases that otherwise might be embedded in data gathered by using a non-specific case definition.
Erythema migrans rashes were noted on many patients in the southern and southcentral United States during the late s Masters et al. In the following year, however, only cases were reported from Georgia CDC, , and even fewer cases in subsequent years. The decline in reported cases reflected the adoption of the CDC surveillance case definition in by the Georgia Department of Public Health. Indeed, blood cultures subsequently revealed a relapsing fever Borrelia sp.
In this case, discovery of a novel disease agent occurred because these patients did not meet the established case definition for Lyme borreliosis Anda, et al. Recent discoveries of novel rickettsioses in the United States caused by R. The efforts required to verify that reported data comply with an established case definition are considerable and are magnified further when clinical data and exposure history are uncoupled from laboratory results.
Electronic laboratory reporting, used increasingly by states to expand case identification of Lyme disease, captures positive test results, but does not provide supportive information about clinical findings or exposure history. Instead, these data must be collected by public health personnel, creating added burden to surveillance endeavors that often exceeds investigative capacity Kudish et al.
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In response, CSTE Epidemiologists modified the national surveillance case definition for Lyme disease in to allow reporting of probable cases, i. The most accurate incidence rates are obtained through active surveillance, but these apply to relatively small catchment areas defined for the investigation, and typically provide a snapshot of incidence in a specified region during a relatively short interval of time. This process allows greater control in the selection of clinical specimens and data collected, but is labor-intensive and requires a level of funding that is prohibitive to sustain indefinitely.
Indeed, most contemporary active surveillance endeavors are supported by federal grants and have a defined period of patient enrollment that spans, at most, only a few years IJdo et al. In contrast, passive surveillance systems provide data that define endemicity and provide long-term trends over larger geographic regions; however, there is generally less control over the quality and quantity of the acquired data, and this activity requires sustained commitment and appropriate infrastructure at local, state, and national levels to collect, collate, and analyze data collected over broad intervals of time and space.
Inherent differences between these systems preclude direct comparisons of the data generated by each method. By example, prospective active surveillance for ehrlichiosis in southeast Missouri identified 29 confirmed and probable cases from —, for a calculated average annual incidence of 3.
By comparison, the average annual incidence of ehrlichiosis for the entire state of Missouri, determined by passive surveillance, was only 0. The nature of active and passive surveillance explains these marked differences in incidence rates. Catchment areas for active surveillance are not chosen at random; rather, these are selected by investigators using passive surveillance estimates that indicate the disease exists in relative abundance in that region Wilfert et al.
In the case of the Missouri investigation, patient ascertainment was facilitated by a motivated clinician who was skilled at identifying potential cases of ehrlichiosis. Additionally, national surveillance for ehrlichiosis was initiated only in , and several years of maturation may be required before passive surveillance systems reach a level of familiarity and frequent use by clinicians and epidemiologists. Even for epidemiological statistics that document outcomes as important as death, there is considerable underreporting to public health authorities.
Prospective cohort studies provide the best estimates of incidence but the resources that are needed to undertake such research preclude their use over larger scales. Phase II dose-ranging studies were done during — in coastal New England with enrolled subjects.