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Journal of Clinical Microbiology, May 1998, p. 1240-1244, Vol. 36, No. 5
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Temporal Correlations between Tick Abundance and
Prevalence of Ticks Infected with Borrelia burgdorferi and
Increasing Incidence of Lyme Disease
Kirby C.
Stafford III,1,*
Matthew L.
Cartter,2
Louis A.
Magnarelli,1
Starr-Hope
Ertel,2 and
Patricia
A.
Mshar2
Department of Entomology, The Connecticut
Agricultural Experiment Station, New Haven, Connecticut
06504,1 and
Epidemiology Program, Bureau
of Community Health, Connecticut Department of Public Health,
Hartford, Connecticut 061342
Received 25 November 1997/Returned for modification 20 January
1998/Accepted 16 February 1998
 |
ABSTRACT |
The abundance of host-seeking Ixodes scapularis nymphs,
the principal vector for the Lyme disease agent, Borrelia
burgdorferi, in Old Lyme, Lyme, and East Haddam, Connecticut, was
compared with the incidence of reported human Lyme disease in the
12-town area around the Connecticut River and the State of Connecticut for the period 1989 to 1996. Ticks were sampled from lawns and woodlands by dragging flannel over the vegetation and examined for the
presence of B. burgdorferi by indirect fluorescent antibody staining. The infection rate of the nymphal ticks by B. burgdorferi during the 9-year period was 14.3% (of 3,866),
ranging from 8.6% (1993) to 24.4% (1996). The incidence of Lyme
disease was positively correlated with tick abundance in the 12 town
area (r = 0.828) and the State of Connecticut
(r = 0.741). An entomological risk index based upon
the number of I. scapularis ticks infected by B. burgdorferi was highest in 1992, 1994, and 1996 and was highly correlated with the incidence of Lyme disease in Connecticut
(r = 0.944). The number of Lyme disease cases has been
influenced, in part, by annual changes in population densities of
I. scapularis and, presumably, a corresponding change in
the risk of contact with infected ticks. Based upon tick activity and
spirochetal infection rates, epidemiologically based Lyme disease case
reports on a regional scale appear to reflect real trends in disease.
| |
INTRODUCTION |
Lyme disease is the most frequently
reported vector-borne illness in the United States (8). This
disease is a tick-borne zoonotic infection caused by the spirochete
Borrelia burgdorferi sensu lato. Since surveillance for Lyme
disease was begun by the Centers for Disease Control and Prevention
(CDC) in 1982, the number of human cases has increased from 491 to
16,461 in 1996 (6). The majority of these cases were
reported in the northeastern United States, where the principal vector
is the blacklegged tick, Ixodes scapularis (also commonly
known as the deer tick). The increase in reported cases can be
attributed to greater recognition, improved reporting, and a true
increase in incidence (4). This increase may also reflect a
change in tick abundance and, for Connecticut at least, an expansion of
the geographical distribution of the tick (11). The
incidence of Lyme disease in several Rhode Island communities was
strongly correlated with the density of spirochete-infected nymphal
I. scapularis (13). There were slight decreases
in reported cases nationally in 1993 and 1995, and vector surveillance
data in Connecticut, New York, and Rhode Island had indicated decreased
tick abundance during those years (3, 5). Rising numbers of
Lyme disease cases in Connecticut and Rhode Island in 1996 were
associated with increased population densities of I. scapularis (6).
Since 1991, Connecticut has reported the highest incidence of Lyme
disease, with 94 cases per 100,000 people reported in 1996. In a study
of the habitat distribution of I. scapularis in southeastern Connecticut from 1989 to 1991 (18), tick populations
appeared to correspond with the number of human cases of Lyme disease
reported in the state and the surveyed towns. The majority of Lyme
disease cases was associated with nymphal I. scapularis
during the summer months (10). Tick surveys were continued
from 1992 through 1997 to monitor the activity of host-seeking I. scapularis nymphs and the infection rate in those ticks. The
purpose of our study was to characterize the relationship between tick
abundance, the prevalence of B. burgdorferi in those ticks,
and the incidence of Lyme disease in Connecticut and the 12-town region
around the Connecticut River.
| |
MATERIALS AND METHODS |
Tick sampling.
The relative abundance of host-seeking
I. scapularis nymphs from 1989 to 1997 was determined by
"dragging" a 1.2-m2 piece of flannel cloth over the
vegetation at 10 residential properties in the four towns of East
Haddam (three sites), Old Lyme (two sites), Lyme (four sites), and
Chester (one site) (18) (Fig.
1). The flannel cloth (95 by 130 cm) was
stapled along a 105-cm wooden dowel with the ends of a rope attached to
each end of the dowel. The sites included woodlands and woodland edge, where I. scapularis predominates, and generally both lawns
and forested areas were sampled. The total area sampled ranged from 0.15 to 0.50 ha, with woodlands comprising 0.024 to 0.25 ha at each
site. The area sampled at each site was determined by measuring the
site with a metric measuring wheel. From 1992, samples were taken from
10- by 25-m woodland subplots in the same locations at eight of the
residences in East Haddam, Lyme, and Old Lyme. Host-seeking I. scapularis at each site was sampled once a month from April
through October in 1989, twice each month from April through October
from 1990 through 1993, and twice each month from May through August in
1994. Any ticks found on the drag cloth were placed in vials with a
blade of grass for moisture and returned to the laboratory for
identification and testing for B. burgdorferi. The presence
of B. burgdorferi in host-seeking nymphs was determined by
indirect fluorescent antibody staining of tick midgut tissues with
murine monoclonal antibody (H5332) as previously described (12).
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FIG. 1.
The 12-town region of Connecticut. The towns of Old
Lyme, Lyme, and East Haddam lie east of the Connecticut River, while
the remaining nine towns are west of the river.
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|
Disease surveillance.
Connecticut has had a passive,
physician-based surveillance system for Lyme disease since July 1987 (1). The CDC case definition for Lyme disease acquired in an
area of endemicity was used to classify cases (7). In 1989, the Lyme disease surveillance system was expanded by the Connecticut
Department of Public Health to include a supplemental Lyme disease case
report form. Follow-up questionnaires were sent to physicians who
reported a case of Lyme disease without supplying clinical information.
Reports without clinical information were not counted as cases. In
1990, Connecticut case reports were based upon the new national
surveillance case definition for Lyme disease adopted by the Council of
State and Territorial Epidemiologists in 1990 (2).
Therefore, the case reports for 1989 were based on the previous CDC
case definition. Active surveillance for Lyme disease in the original
12-town area studied by Steere et al. (19) (i.e., Lyme, Old
Lyme, East Haddam, Haddam, Chester, Deep River, Essex, Old Saybrook,
Westbrook, Clinton, Killingworth, and Madison) began in 1991 (Fig. 1).
Case reports for the 12-town area were used as a measure of Lyme
disease incidence in the region for the period 1989 through 1996.
Methods of analysis.
The number of ticks collected from each
woodland plot and lawn for each site was standardized by conversion to
the number collected per hectare. Nymphal abundance for each month and
year was the average for all site visits during each month and from mid-May through mid-August, respectively. Tick populations between years were compared by analysis of variance on log-transformed biweekly
tick abundance and Fisher's protected least significance difference
(LSD) test (17). Patterns of tick activity within each month
for each year were examined by their departure from the overall mean
for each month for the entire study period (e.g., difference in mean
tick abundance for May 1989 from mean tick abundance for May, 1989 to
1997). An annual entomological risk index (ERI), similar to that used
by Mather et al. (13), was calculated as the product of tick
abundance (average number of nymphs per hectare) and the proportion of
ticks infected by B. burgdorferi. The ERI is the average
number of infected ticks per hectare and reflects the risk of acquiring
a bite from an infected tick. Differences between years in the rate of
infection by B. burgdorferi were compared by analysis of
variance on transformed (arcsin 
x) site-specific
infection rates. The incidences of reported human Lyme disease for the
state and 12-town area were compared to annual tick abundance and the
ERI by simple linear regression for the period 1989 to 1996. A
projection of the number of cases in Connecticut and the 12-town area
is based upon a simple linear regression of tick abundance and the
number of Lyme disease cases for the 8-year period.
| |
RESULTS |
Tick abundance and prevalence of infection.
The abundance of
nymphal I. scapularis in residential woodlots in
southeastern Connecticut increased dramatically in 1991 over that of
1989 or 1990 (Fig. 2). Tick numbers
increased again by 70% in 1992 compared to relative abundance in 1991. Tick abundance increased in 1994 by 57% over that recorded in 1993 and
again by 14% in 1996 compared to 1995. Nymphal densities were lower in
1993 and 1995. In 1997, densities of I. scapularis nymphs
were higher than in 1996. Similar trends were observed in tick activity on the lawn. These differences in the annual fluctuation of tick abundance were highly significant, both in the woods (F = 7.801, df = 8, 402; P 
0.001) and on the lawns
(F = 4.691, df = 8, 429; P 0.001). Tick abundance in 1992, 1994, and 1997 was significantly higher
than in most other years on both the lawn (LSD = 0.3578; P 0.044) and woodlands (LSD = 0.7856;
P 0.048), although the number of I. scapularis nymphs in 1994 was not significantly higher than that
in 1991. There was little difference in the overall annual trends
between the three seasonal periods used to initially tabulate tick
abundance (i.e., mid-May through mid-August, mid-May through July, and
June and July only) (Fig. 1). However, variation in the seasonal
activity of the I. scapularis nymphs each year could
influence risk of exposure to tick bites and number of human cases of
Lyme disease, particularly during the beginning and end of the tick
season.
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FIG. 2.
Numbers of I. scapularis nymphs per hectare
for three seasonal periods (mid-May through mid-August, mid-May through
July, and June and July only) collected from woods or lawns during the
period 1989 to 1997 in Old Lyme, Lyme, and East Haddam.
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There were pronounced differences in nymphal tick activity during each
month of the summer tick season over the 9-year study
(Fig.
3). Not only was nymphal tick activity in
the woodland plots
above the 9-year baseline for each month of May,
June, July, and
August in 1992, 1994, and 1997, but
I. scapularis nymphs were
also more abundant at the beginning (May)
and end (August) of
the tick season. In 1995,
I. scapularis
was abundant in the late-May
and early-June samples, with subsequent
tick activity dropping
rapidly through July and August, when
Connecticut was experiencing
a drought. Tick activity was below the
long-term baseline for
all 4 months in 1989, 1990, and 1993. In 1996, nymphal blacklegged
ticks were abundant during the peak months of June
and July, but
their activity was low in May and August. The abundance
of
I. scapularis nymphs on the lawns shows a pattern similar
to that
in the woods with above-average activity in 1992, 1994, and
1997.
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FIG. 3.
Departures of the mean number of I. scapularis nymphs collected during the months of May, June, July,
and August from the woods in Old Lyme, Lyme, and East Haddam, for each
year, 1989 to 1997, from a grand average baseline (0 on the graph) for
the entire study period. Values do not represent measures of tick
abundance.
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|
The overall infection rate of the host-seeking nymphal ticks by
B. burgdorferi during the 8-year period was 14.3% (of
3,866).
However, the infection rate varied significantly between years
(
F = 2.538, df = 8,179;
P = 0.012)
during the study period (Table
1). The
fewest ticks were found to be infected in 1993 (8.6%),
and the highest
infection rate was recorded in 1996 (24.4%). While
infection rate
estimates are highly variable among individual
samples, values for most
years are based on testing several hundred
ticks from all the sites
over the entire period of nymphal tick
activity and, consequently, is
probably a reasonable estimate
of the general infection rate in the
region for any given year.
There was no significant difference between
the months of May,
June, July, and August in the proportion of nymphs
infected with
B. burgdorferi. Based upon the ERI, the years
of greatest overall
risk for Lyme disease were 1991, 1992, 1994, and
particularly
1996 (Table
1). During 1992 and 1994, the risk of
acquiring a
bite from an infected nymph was high even in May and
August.
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TABLE 1.
Proportions of nymphal I. scapularis ticks
infected with B. burgdorferi collected by sampling the
vegetation at 8 to 10 residential sites in Old Lyme, Lyme, and East
Haddam and ERIs, 1989 to 1996
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|
Lyme disease incidence and tick abundance.
The incidence of
human cases of Lyme disease in Connecticut increased dramatically in
1991, 1992, 1994, and 1996, with rates of 36, 54, 62, and 94 per
100,000 people, respectively (Fig. 4). A
similar trend for the same years was observed in the 12-town region
with an incidence of 340, 560, 320, and 450 per 100,000, respectively.
The rate per 100,000 residents exceeded 1,000 in the town of Old Lyme
in 1991, 1992, and 1994 and exceeded 1,000 for the town of Lyme in 1992 and Chester in 1996. The number of cases in the state decreased in 1993 and 1995 from the previous years. These periods of higher and lower
incidence of Lyme disease coincide with the activity of I. scapularis nymphs. In 1991, the density of I. scapularis nymphs increased 170%. The number of Lyme disease
cases increased by 69 and 106% in the state and 12-town region,
respectively. The years that had the highest number of reported cases
in Connecticut were 1992, 1994, and 1996, years with the greatest
nymphal-tick activity. The number of Lyme disease cases statewide
decreased by about 23% in 1993 and 1995 from the previous years, which
coincided with 45.4 and 19.6% decreases in nymphal-tick densities for
1993 and 1995, respectively. A similar pattern was observed for the
12-town region (Fig. 4).
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FIG. 4.
Lyme disease incidence rate (per 100,000) for
Connecticut and the 12-town region for 1989 to 1996; abundance (number
per hectare) of nymphal I. scapularis in residential
woodlots in the towns of Old Lyme, Lyme, and East Haddam; and the
corresponding ERI, 1989 to 1997.
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|
The least-squares linear regression of the incidence of Lyme disease
for the state and 12-town region on tick abundance (number
per hectare)
for the 8-year period from 1989 through 1996 is presented
in Table
2. Tick abundance in residential woodlots
was significantly
correlated with the incidence of Lyme disease in the
12-town area
and in Connecticut, especially for the period from 1989 to
1995.
Tick abundance increased by only 14% in 1996, but the infection
rate was higher, resulting in an increased risk for Lyme disease.
The
ERI was highly correlated with the number of reported cases
in
Connecticut during the entire 8-year period (
r = 0.944)
(Fig.
4). The ERI based upon ticks recovered from the lawn was
correlated
significantly only with the incidence of Lyme disease in the
12-town
area. By contrast, the relationship between tick abundance on
the lawn and the incidence of Lyme disease statewide was insignificant
(
P > 0.05).
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TABLE 2.
Regression of nymphal tick abundance and ERI on the
number of reported human Lyme disease cases for Connecticut and the
12-town area, 1989 to 1996
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|
| |
DISCUSSION |
The incidence of Lyme disease in Connecticut was positively and
significantly correlated with long-term trends in the abundance of
nymphal I. scapularis and the abundance of
spirochete-infected ticks from woodland plots in the communities of Old
Lyme, Lyme, and East Haddam. This suggests that recent increases in
tick abundance may be responsible, in part, for much of the rise in
Lyme disease infection in Connecticut, although the tick is also
spreading geographically within the state (11). Trends in
tick abundance in these woodlands probably reflected general activity
across the state or, at least, in southeastern Connecticut, which has had the highest incidence of Lyme disease. However, in the established foci of Old Lyme, Lyme, and East Haddam, the incidence of Lyme disease
increased by 64% from 1995 to 1996, while tick densities increased by
only 14%. Annual patterns of tick activity in this study corresponded
more closely with Lyme disease in the 12-town area. Unfortunately, the
factors that influence the annual abundance of I. scapularis
are poorly understood. The population dynamics of the tick population
is complex, and future abundance of I. scapularis cannot be
predicted (10). Future monitoring of I. scapularis may be required in other regions of the state in order to accurately assess tick trends in relation to the incidence of Lyme
disease. Based upon the abundance of I. scapularis per hectare in the 12-town region or the abundance of infected ticks (ERI)
in the summer of 1997, 2,329 and 1,708 cases of Lyme disease, respectively, might be expected for 1997. However, increased tick activity and reporting of Lyme disease from other portions of the state
could increase the incidence of the disease in 1997 above a rate
determined by past trends in the 12-town region. For example, the
incidence of reported Lyme disease from Windham and Tolland counties in
northern Connecticut has increased from 11 and 27 cases per 100,000, respectively, in 1989 to 257 and 155 cases per 100,000, in 1996, which
may be a result of increased tick activity. This could be determined
from a broader-based surveillance of the abundance of I. scapularis nymphs in Connecticut.
The relative length of the tick season is another factor in the risk
for tick bites. Host-seeking nymphs of I. scapularis in the
northeast begin their activity in May, peak in June, and slowly decline
in activity through July and August (10, 16, 18). Sampling
nymphs of I. scapularis only during the June seasonal peak
appears to be an adequate measure of tick abundance in relation to the
annual incidence of Lyme disease, but early and late seasonal tick
activity will be missed. There was considerable variation in the basic
pattern in the level of activity each month through the period of this
study. Interestingly, two years, 1992 and 1994, that had a high
incidence of Lyme disease not only had a higher peak abundance of
nymphal ticks but also had greater tick activity for a longer period.
Nymphal-tick activity was extended into August in 1997 as well.
Infection rates were found to vary tremendously among the residential
sites in Connecticut, and this may account, in part, for the weak
relationship between the lawn ERI and Lyme disease incidence at the
local level. The abundance of infected ticks on the lawn more
accurately reflected the regional incidence of Lyme disease. Areas of
high risk and low risk can be expected between the lawns of individual
residences. The lawn is probably where most tick bites are acquired by
residents, although only a small proportion (2 to 13%) of the tick
population is found there (9, 14, 18).
The risk for Lyme disease is currently assessed from human case
reports, isolation from or detection of Lyme disease borrelliae in mice
and ticks, serosurveys of animals, collection of host-seeking I. scapularis, or collection of ticks attached to deer, mice, or
other animals. Each of these methods has inherent biases and limitations in geographical scale. The number of reported human cases
as a measure of the true distribution and incidence of Lyme disease is
subject to the surveillance case definition and type of surveillance
method used. Despite these limitations, the abundance of host-seeking
nymphs was closely associated with the incidence of human Lyme disease
based upon case reports over an 8-year period in Connecticut. The
incidence of Lyme disease at the state and regional levels closely
paralleled the abundance of I. scapularis nymphs and the
abundance of spirochete-infected nymphs. The relative abundance of
nymphal ticks within the woodland habitat has been a reliable, and
independently measured, predictor for Lyme disease at the regional and
state levels. Epidemiologically based Lyme disease case reports on
regional, state, and national scales appear to reflect real trends in
the disease based upon tick activity and spirochetal infection rates,
although Lyme disease is clearly underreported (15). The use
of active surveillance of human cases and more intensive sampling of
I. scapularis nymphs may provide a better assessment of risk
within an area of endemicity and for the state.
| |
ACKNOWLEDGMENTS |
This study was supported in part by the CDC cooperative agreement
U50-CCU106598.
We acknowledge Frank Campbell, Kathryn Gorski, Cynthia Phillips,
Patricia Noyes, Collen Moser, Tia Blevins, Shanon Trueman, Vickie
Bomba, Cynthia Musante, Curtis Gibson, Michael Harma, Brandon Brei, and
Michael Burelle for assistance in collecting ticks over the years. We
also thank Alan G. Barbour, University of California
Irvine, for
providing murine monoclonal antibody (H3552). The map of Connecticut and the 12-town area was provided by Ellen Cromley, Department of
Geography, University of Connecticut.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Forestry and Horticulture, The Connecticut Agricultural Experiment
Station, 123 Huntington St., Box 1106, New Haven, CT 06504-1106. Phone: (203) 789-7252. Fax: (203) 789-7232. E-mail:
kcstaff{at}caes.state.ct.us.
| |
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Journal of Clinical Microbiology, May 1998, p. 1240-1244, Vol. 36, No. 5
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
