From the School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom.
Received for publication May 7, 2002; accepted for publication October 7, 2002.
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ABSTRACT |
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climate; environment; humidity; Ixodes; Lyme disease; temperature; ticks; weather
Abbreviations: Abbreviations: NCDC, National Climatic Data Center; PHDI, Palmer Hydrological Drought Index.
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INTRODUCTION |
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In the US Northeast, approximately two thirds of human Lyme disease infections are transmitted during the months of June and July by infected nymphs in the second year of the tick life cycle, rather than by larvae or adults. A leading hypothesis relates changes in disease incidence in the US Northeast to periodic changes in acorn production in oak forests. Acorns are a mainstay of the diet of the white-footed mouse, which in the US Northeast is the main host for I. scapularis (1, 2). Periodic acorn abundance, known as masting, has been observed to precede local surges in the mouse population the following spring (3).
However, an environmental explanation for regional Lyme disease variability, such as weather, has also been proposed, because similar annual patterns of tick infection rates have been observed in forests dominated by species other than oaks and in regions without forests (4). Ticks require a relatively humid microclimate, such as decomposing plant matter, and soil humidity will affect their survival, particularly during quiescence and dormancy. Tick viability may also be impaired by a scarcity of suitable habitat in circumstances where drier weather has led to lower levels of vegetation available for questing and cover (5). A recent study in northern Illinois found a significant relation between cumulative rainfall and I. scapularis density and tick infection rates (6). Previous laboratory research demonstrated the low tolerance of I. scapularis to dry weather throughout its life cycle, but particularly in its subadult stages, because the smaller body size is particularly susceptible to water loss (5, 7, 8). Moisture levels during the growing season may also affect the food supply of rodent hosts, which tend to rely on seeds in winter (9).
In addition to drier conditions, cold winter weather may affect Lyme disease incidence because of reduced activity levels among adult ticks seeking their final blood meal (10) and because P. leucopus is relatively poorly adapted to cold weather. The white-footed mouse does not enter torpor as readily as other common mouse species, and numbers of white-footed mice tend to decline sharply during winter, especially when food resources are low (11). In the Lyme disease-endemic region of southeastern New York State, sharp drops in the white-footed mouse population following colder winters have been observed in local trapping experiments (3, 12). Analysis of data published by the Institute for Ecosystem Studies (3, 12) suggests that populations of P. leucopus trapped in June near Millbrook, New York, were lower following colder winters during the period 19911996 compared with the average December, January, and February temperatures during the preceding winter recorded by the National Climatic Data Center, region 0601 (northwestern Connecticut) (R2 = 0.65, p = 0.053). Long-term studies in the US Midwest indicate that the winter population decline of P. leucopus is temporary and that populations tend to recover by the end of the year (9). A decline in the rodent population during winter, however, reduces the probability that tick larvae that hatched in the spring will find a rodent host, become infected, and live to pass on the disease to humans when they enter the nymph stage the following year. Previous studies have shown a strong positive correlation between P. leucopus populations in spring and summer and the density of infected nymphs present the following year (12). In turn, nymphal tick abundance has been shown to be directly correlated with Lyme disease incidence in humans (13).
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MATERIALS AND METHODS |
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Lyme disease incidence was also considered in a regression equation with winter temperature during the same year (t) and in an equation with winter temperature during the previous year (t 1). A significant relation between Lyme disease incidence and same-year winter temperature (t) would provide some evidence of increased larval winter survival (14, 15). A relation with winter temperature lagged one period (t 1) would support the theory that winter temperature levels affect disease incidence, either through increased adult tick activity or because of greater white-footed mouse survival and activity and consequently higher larval tick infection and survival during the summer months.
These hypotheses were investigated for seven states in the US Northeast with the highest Lyme disease incidence ratesNew York, Connecticut, Massachusetts, Rhode Island, Pennsylvania, New Jersey, and Maryland. Together, these states accounted for 85 percent of the approximately 16,000 Lyme disease cases US states reported to the Centers for Disease Control and Prevention for 1999. Annual data on Lyme disease cases and data for the months of highest incidenceJune, July, and Augustwere used in the correlations. Data on the estimated monthly onset of Lyme disease in each state were provided by the states health departments.
Lyme disease has been under surveillance by the US Centers for Disease Control and Prevention since 1982, but a systematic case definition was only introduced beginning with the 1991 reporting year. Improvements in education and outreach continued after that time, and most state health departments in the Northeast reported an improvement in Lyme disease data quality after the early 1990s. For this analysis, state data on reported annual Lyme disease incidence for the period 19932001 provided by each states department of health were used. Annual numbers of cases reported to the Centers for Disease Control and Prevention as of December 15, 2001, were used for the year 2001, instead of 2001 data from the states health departments, which were not yet available. For reported onset of Lyme disease by month, only data for the period 19932000 were available for all seven states.
In this analysis, summer moisture was represented by Palmer Hydrological Drought Index (PHDI) monthly averages for June, July, and August, the months in which nymphal ticks are most active. The PHDI measures the intensity and duration of long-term drought by considering levels of precipitation, evapo-transpiration, and runoff. Positive values for the index represent moist conditions, and negative values represent drier conditions; for example, severe drought has an index of 3.0 or lower. The influence of winter temperature on disease incidence is tested using average monthly temperatures for the climatologic winter (December, January, and February). Monthly weather data published by the National Climatic Data Center (NCDC) of the National Oceanic and Atmospheric Administration were used in all cases. For the smaller states, the NCDC region in the geographic center of the state was selected, and for the others, the NCDC region that most represented the area of Lyme disease concentration was used. The NCDC regions selected included the southern Hudson Valley in New York (NCDC region 5), southeastern Pennsylvania (NCDC region 3), northwestern New Jersey (NCDC region 1), and eastern Maryland (NCDC region 6).
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RESULTS |
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In four of the seven states examined, significant positive relations were found between annual Lyme disease incidence in 19932001 and the summer moisture index from two prior periods (t 2). The relations were significant at p < 0.05 for Connecticut, Massachusetts, New York, and Pennsylvania; the relations were correlated at only p < 0.10 for Rhode Island and Maryland (see figure 2). (The correlation was weaker for New Jersey, which is not included in figure 2.)
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The three most important weather variablesPHDI 2 years previously (t 2), winter temperature during the previous year (t 1), and PHDI during the same year (t)were also correlated with reported Lyme disease onset for each of the summer months. Significant correlations with summer disease onset and same-month drought index were evident for only two states. However, the correlations with June- and July-onset disease incidence and same-month drought index for t 2 were strong and consistent, and over half of the human infections occurred during those months. All of the states reported disease cases for the month of June were correlated with June PHDI (t 2) at p < 0.05, except those for Pennsylvania (p = 0.053) (see table 1).
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DISCUSSION |
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The results are also consistent with a theory that moisture affects rodent host populations, such as that of P. leucopus, because less food is produced in the growing season to sustain mice during the critical winter/spring months (6, 9). The current analysis shows that drought may affect the broader pattern of Lyme disease incidence despite the possibility of local host migration from specific study sites. The lack of correlation observed for PHDI (t 1) and disease incidence undermines an expectation of enhanced larval survival related to moister weather. These results may be consistent with recent findings that ticks in the larval stage may show a more adaptive response to drier weather through quiescence than do nymphs (17).
The lack of correlation observed for same-year moisture (PHDI t) is surprising considering that a higher survival rate would be expected in moister conditions for the unfed nymphs, as well as the fed nymphs. One possible explanation is that people are less likely to spend time outdoors in wetter weather in early summer, so higher tick survival under these conditions is offset by fewer opportunities for humans to encounter ticks. In the United Kingdom, for example, higher Lyme disease incidence has been observed during warmer, drier summers, perhaps because people spend more time outdoors and summer weather tends to be mild (18). However, in the warmer climate of the northeastern United States, drier, hotter conditions may serve to discourage outdoor activities later in the summer. The data show some correspondence in New England between lower Lyme disease incidence and drier conditions in the same month for the months of August and July.
No significant relations were found between annual Lyme disease incidence and same-year winter temperature, which would have provided evidence of increased larval survival related to warmer winter weather (13). The theorized associations between warmer winter weather in the previous year (t 1) and Lyme disease related to an increase in rodent survival and/or increased adult tick activity over the winter months are tentative. Significant multicollinearity with spring/summer moisture (t 2) was seen in two out of the three states where winter temperature (t 1) was found to be a significant predictor of Lyme disease. Further research would be needed to confirm the influence of winter weather on P. leucopus survival and transmission of Lyme disease. Preliminary analysis suggests only limited evidence for the other theorythat enhanced adult tick activity in warmer winter weather contributes to a rise in nymph tick populations during the following year. An increase in the activity of adult ticks would be expected to affect winter disease incidence in humans and other hosts, but analysis of disease incidence during the months of December, January, and February, as compared with temperature for each of these months, revealed only a few significant relations. Significant results for onset of disease correlated with same-month temperature for January, February, and December (19932000) are as follows: Rhode Island: January, r = 0.71, p = 0.049; February, r = 0.83, p = 0.011; New York: December, r = 0.74, p = 0.036; Connecticut: February, r = 0.84, p = 0.009. Significant relations were not found for the remaining 17 months tested.
This analysis relied on a limited times series of nine observations on reported Lyme disease incidence. Formal analyses of the quality of the data over time were not available, but some state epidemiologists maintain that reporting has improved over the past decade as awareness by the public and health-care providers has grown. It is also the case for most states that wetter summers and warmer winters predominated in the latter half of the time series. Averaging across the states, the PHDI was greater by about 0.7 and the winters were warmer by about 1°C in the second half of the series compared with the first half. Therefore, the prospect of some positive bias in the correlation results cannot be ruled out, because underreporting in the first half of the series may have coincided with a cooler, drier weather trend. However, although the New York region exhibited the greatest homogeneity in the moisture index, revealing no significant trend, disease incidence in this state was most highly correlated with the moisture index (t 2).
While the results demonstrate that higher Lyme disease incidence is correlated with wetter weather, it might be presumed that excessive rainfall would have an adverse effect on tick populations. For example, a recent study of I. scapularis populations at an Illinois site found a steep decline in larval populations in bottomlands following flooding (6). In the series examined for this analysis, only one example of a very high moisture index was available. In this instance, in the state of Rhode Island, the summer PHDI exceeded 4.0 in 1998 and Lyme disease incidence in 2000 was at above-average, but not record, levels. For the other states, higher disease incidence was correlated positively with the highest moisture index, and if a threshold exists after which extreme moisture is negatively correlated, it was not apparent in the limited time series examined.
Summer moisture effects on Lyme disease incidence provide an alternative to the acorn masting theory, which seeks to correlate Lyme disease variability in the US Northeast with changes in the rodent host food supply. More widespread monitoring of acorn production than is currently available would be needed to test the broader implications of masting cycles on Lyme disease incidence. However, in central Massachusetts, where some regional acorn production monitoring has been attempted (3, 19, 20), county Lyme disease data can be examined for elevated disease incidence two summers after major acorn production years. It appears that in the 2 years (1993 and 1995) following the best acorn production years of 1991 and 1993 in central Massachusetts (19), reported disease incidence in central Massachusetts counties was at a record low for the 1990s: at 76 percent and 78 percent below the 19932001 mean, respectively. The lack of correspondence between observed acorn production peaks and county-level disease incidence could be due to a lack of synchronization among oak trees, a lack of importance of acorns in the overall mouse food supply, or the fact that other factors, such as those identified in this study, are playing a greater role in disease variability.
The analysis presented may have some implications for the prevention and control of Lyme disease. Currently, some health authorities issue warnings of heightened Lyme disease risk due to recent climatic conditions, that is, a warm winter and a wet spring. The current analysis suggests that warnings of enhanced risk should be revised to take into account knowledge of the lag times between measured climate conditions and human risk. Therefore, warnings of enhanced Lyme disease risk in late spring/early summer would reflect spring moisture conditions that existed 2 years previously. Secondarily, disease risk in late summer is more likely to reflect current soil moisture levels. Regardless of disease variability, authorities can continue to encourage programs for controlling the populations of both the black-legged tick and its main host, the white-footed mouse.
This study has offered evidence of weather-related predictors of Lyme disease incidence that reveals broadly consistent relations in the seven states considered. The relevant changes in weather variables analyzedwetter springs and summers and warmer wintersare projected to increase in frequency according to recent climate-change scenarios for the northeastern United States. For example, the Global Circulation Models recommended by the Intergovernmental Panel on Climate Change for regional studies project a slight increase in precipitation and an increase in winter temperatures in the US Northeast over the next half century (21). Winter temperatures in the New England region increased by approximately 2°C during the last century (22); and higher survival rates for P. leucopus and wetter summers, which improve the survival prospects of nymph ticks, may be contributing factors behind the increasingly high levels of Lyme disease seen in the region.
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ACKNOWLEDGMENTS |
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The author thanks E. Backlund, F. Kohn, M. Rosenthal, and Dr. D. Kimberling for helpful discussions.
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NOTES |
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REFERENCES |
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