Analysis of population-level determinants of legionellosis: spatial and geovisual methods for enhancing classification of high-risk areas
Gleason et al. Int J Health Geogr
Analysis of population-level determinants of legionellosis: spatial and geovisual methods for enhancing classification of high-risk areas
Jessie A. Gleason 0
Kathleen M. Ross 1 2
Rebecca D. Greeley 2
0 Environmental and Occupational Health Surveillance Program, New Jersey Department of Health , Trenton, NJ , USA
1 Council of State and Territorial Epidemiologists Applied Epidemiology Fellowship , Atlanta, GA , USA
2 Communicable Disease Service, New Jersey Department of Health , Trenton, NJ , USA
Background: Although the incidence of legionellosis throughout North America and Europe continues to increase, public health investigations have not been able to identify a common exposure in most cases. Over 80% of cases are sporadic with no known source. To better understand the role of the macro-environment in legionellosis risk, a retrospective ecological study assessed associations between population-level measures of demographic, socioeconomic, and environmental factors and high-risk areas. Methods: Geographic variability and clustering of legionellosis was explored in our study setting using the following methods: unadjusted and standardized incidence rate and SaTScan™ cluster detection methods using default scanning window of 1 and 50% as well as a reliability score methodology. Methods for classification of “high-risk” census tracts (areas roughly equivalent to a neighborhood with average population of 4000) for each of the spatial methods are presented. Univariate and multivariate logistic regression analyses were used to estimate associations with sociodemographic factors: population ≥ 65 years of age, non-white race, Hispanic ethnicity, poverty, less than or some high school education; housing factors: housing vacant, renter-occupied, and built pre-1950 and pre-1970; and whether drinking water is groundwater or surface water source. Results: Census tracts with high percentages of poverty, Hispanic population, and non-white population were more likely to be classified as high-risk for legionellosis versus a low-risk census tract. Vacant housing, renter-occupied housing, and homes built pre-1970 were also important positively associated risk factors. Drinking water source was not found to be associated with legionellosis incidence. Discussion: Census tract level demographic, socioeconomic, and environmental characteristics are important risk factors of legionellosis and add to our understanding of the macro-environment for legionellosis occurrence. Our findings can be used by public health professionals to target disease prevention communication to vulnerable populations. Future studies are needed to explore the exact mechanisms by which these risk factors may influence legionellosis clustering.
Legionellosis; Legionnaires' disease; Cluster analysis; GIS; SaTScan™; Ecological study
Background
Since the organism was first recognized during an
outbreak in 1976, Legionella pneumophila has been
identified as a relatively common cause of pneumonia in
community and healthcare settings and has continued to
garner attention globally [
1
]. Approximately 5000 cases
of Legionnaires’ disease are reported each year in the
United States [
2
]; however, the actual number of
hospitalized cases is estimated to be between 8000 and 18,000
[
3
] and the number of reported cases have been steadily
increasing in the United States, Europe and Canada
[
4–7
]. Although the first case of Legionnaire’s Disease
was recognized over 40 years ago, it remains a disease
of emerging concern particularly in developed countries
with more surveillance [1].
Legionellosis refers to two syndromes caused by
bacteria of the genus Legionella including: (1) Legionnaires’
disease, which is the more severe form of the infection
and associated with pneumonia; and (2) Pontiac fever,
which is milder and not associated with pneumonia [
8
].
Transmission to humans occurs through inhalation of
aerosolized water that is contaminated with the
bacteria. Legionellosis is not transmitted between individuals
or by swallowing contaminated water; however,
aspiration is also an important mode of disease transmission.
Legionella species are common worldwide in the natural
environment, including rivers, streams, and lakes and in
artificial water environments and can survive in a range
of environmental conditions, but grows best in warm
temperatures between 32 and 42 °C (90–108 F) [
1
].
The risk of contracting legionellosis is multifactorial,
including factors which promote the proliferation of
Legionella in the environment, host susceptibility
factors, and exposure to aerosols. Known host
susceptibility factors associated with the occurrence of legionellosis
include older age (> 50 years), male sex, history of
smoking, chronic lung disease, and poor immune function [
9
].
Outbreak investigations have identified the following
environmental and exposure to aerosol risk factors:
history of travel, residence in a healthcare facility, and
proximity to water systems including: domestic water services
(tanks, showers, faucets, stagnant warm pipes); cooling
towers and evaporative condensers; whirlpool spas;
respiratory therapy devices; vegetable misters; ice machines;
and decorative fountains systems [
1, 10, 11
]. However,
outbreaks of legionellosis account for only a minority of
cases. Up to 80% of legionellosis cases are sporadic and
public health investigations have not been able identify a
common source, although these cases are not randomly
distributed in time or space [
12–14
].
Research of population-level factors may be a useful
complement to individual-level factor research which is
the primary stream of research into causes and factors of
legionellosis [
15
]. Some research has identified potential
common population-level exposures including
meteorological factors such as temperature, humidity, and water
pressure [
11, 16, 17
], wastewater treatment plants [
18
],
certain public water system characteristics [
19
], and other
natural matrices and man-made water systems [
11
]; yet
further investigation into population-level factors is needed
to provide a better understanding of the complex nature
of legionellosis. Although other studies of area-based
predictors have assessed associations with infectious disease
including giardiasis [
20
], salmonellosis [
21
], and
campylobacteriosis [
22
], similar studies of legionellosis are limited.
Previous research has demonstrated methods for
detection of small areas of excess incidence of
Legionnaires’ disease [
23
] as well as cluster detection as a
prospective surveillance tool [
24
]. However, there is a paucity
of ecological studies comparing legionellosis rates across
geographic subsets (e.g., county, census tract) to
estimate the impact of environmental and sociodemographic
health disparities [
25
]. Incidence analyses are useful tools
to describe and compare disease rates across geographic
subsets. There is no steadfast rule to categorize incidence
rates to identify areas of high occurrence and choice of
cut point may lead to an over- or under- estimate of high
occurrence areas. Use of spatial cluster analyses to
identify areas of high occurrence can supplement findings
from incidence rate analysis.
Studies which focus on spatial disease clustering may
be successful at identifying macro-level factors, such as
socioeconomic, demographic, and environmental
factors, which contribute to the increase in disease [
26
].
SaTScan™ is a commonly used cluster detection
software which calculates a spatial scan statistic by gradually
scanning a window across space, noting the number of
observed and expected observations inside the window
at each location [
27
]. SaTScan™ users can adjust the size
of the cluster scanning window (i.e., percent of the total
population at risk); however, results can be misleading if
the size of the cluster scanning window is made
arbitrarily since a small scanning window can produce unstable
clusters whereas a large window can overestimate the
cluster area [
28
]. Researchers need to determine which
model (e.g., maximum window size) best represents the
true underlying clusters and how to quantitatively assess
the fit of a model [
29
].
As increases in the incidence of legionellosis are
observed, further investigation of population-level
determinants of legionellosis is needed to expand our
understanding of the complex mechanism of this disease. An
ecological analysis was performed to estimate the
association between legionellosis risk and the following
population-level risk factors: age, race, ethnicity, poverty,
education, housing factors including vacant,
renter-occupied, and housing age, as well as drinking water source.
To best classify census tracts at “high-risk” for
legionellosis we explored the following spatial variability
methods: (1) unadjusted and standardized incidence ratios
across census tracts; (2) cluster detection with
minimum and maximum window scanning and a reliability
score method for classification of homogenous, reliable
legionellosis clusters. The identification of geographic
areas with high burden of disease and subsequently
evaluating population-level determinants could allow for
targeted public health interventions.
Methods
Study population and design
Our study setting was the state of New Jersey, the most
densely populated of the 50 United States (U.S.), with a
population of just under 9 million people. New Jersey
is adjacent to New York City, New York the most
populous city in the U.S., and Philadelphia, Pennsylvania the
5th most populous city. This statewide study setting
provides a template for states/regions/countries to assess
the role of population-level factors and legionellosis and
not restrict research to urban city centers. Census tracts,
areas roughly equivalent to a neighborhood with an
average population of 4000, were used as geographic unit of
measure. Census tracts were developed and used by the
U.S. Bureau of Census to collect, tabulate and present
results of the decennial censuses. There are 2000
populated census tracts in New Jersey. Although U.S. census
blocks, which contain about 1000 people, may provide
finer scale geospatial analysis, data at that granular level
is more limited and information for all factors of interest
is not available.
A clinically compatible legionellosis case is classified
as confirmed if it meets at least one of the confirmatory
laboratory criteria: (1) culture isolation of any Legionella
organism from respiratory secretions, lung tissue,
pleural fluid, or other normally sterile fluid; (2) detection of L.
pneumophila serogroup 1 antigen in urine [
30
]; or
seroconversion of fourfold or greater rise in specific serum
antibody titer to L. pneumophila serogroup 1. In
accordance with communicable disease reporting regulations
set by the New Jersey Department of Health (NJDOH),
healthcare providers must report diagnosed cases of
legionellosis within 24 h of laboratory confirmation to
the local health department where the case resides. Local
health departments are responsible for initiating a public
health investigation and subsequently reporting the case
to the State health department through NJDOH’s
Communicable Disease Reporting and Surveillance System
(CDRSS).
Confirmed legionellosis cases from 2003 to 2013 were
extracted from CDRSS. Cases that were out-of-state
during the entire incubation period (2–10 days prior to
illness onset) were excluded from the study. Cases were
also excluded if the CDRSS record did not contain age
at onset, gender, date of symptom onset, or address.
Legionellosis cases were geocoded to census tract
based on their street address using ArcGIS version 10.2.
Each census tract was assigned the aggregated count of
legionellosis cases, the total 2010 U.S. Census population,
and geographic coordinates of the census tract centroid
for utilization in SaTScan™ software.
Census tract level demographic and socioeconomic
variables of interest were obtained from the 2010
U.S. Census including percentages of total
population ≥ 65 years of age, non-white race, Hispanic ethnicity,
below poverty, less than or some high school education.
Housing variables included percentages of housing units
which are vacant, renter-occupied, and built pre-1950
and pre-1970. Both pre-1950 and pre-1970 housing
were explored in univariate analyses allowing for a
simple comparison of effect estimate magnitude, but only
pre-1950 was included in multivariate analyses. Each
continuous exposure variable was categorized using the
lower and upper quartiles rounded to the nearest 5% as
cutoffs. The cutoffs, with distributions, for each variable
can be found in Table 2. Additionally, each census tract
population-weighted centroid was spatially joined to the
public water system in which it fell. The primary drinking
water source of each public water system was classified
into ground water, surface water, and unknown.
Spatial methods
The following methods were used to explore geographic
variability and clustering of legionellosis and to identify
associations with population-level factors: (1) unadjusted
and standardized incidence rate methods and (2) cluster
detection using both 1 and 50% window size sensitivity
as well as a reliability score method to minimize window
size sensitivity. Unadjusted legionellosis incidence rates
were calculated for the 10-year study period for each
census tract by dividing the number of confirmed
legionellosis cases per census tract by total census tract population.
Age- and sex-adjusted standardized incidence rates were
calculated for the 10-year study period for each census
tract using direct standardization. New Jersey’s age- and
sex-category population estimates available from the
2010 U.S. Census were used as the standard
population. A choropleth map of the unadjusted and age- and
sex-adjusted incidence rates was created using ArcGIS.
Adjusted and unadjusted incidence rates were
categorized into five intervals (0, > 0 and ≤ 2; > 2 and ≤ 4; > 4
and ≤ 6; and > 6) for visualization.
Cluster analysis
Discrete Poisson models were used to identify
retrospective, purely spatial clusters of legionellosis, using
SaTScan™ software [
31
]. Standard clusters were defined as
statistically significant clusters identified with SaTScan™
using the maximum scanning window size (50% of the
population at risk) and a minimum window size of 1%.
To mitigate SaTScan™ window size sensitivity and
maximize the detection of stable legionellosis clusters, we
calculated individual reliability scores for each census
tract utilizing a methodology introduced by Chen et al.
[
28
]. SaTScan™ was run 50 times adjusting the size of the
cluster scanning window (1–50%) by 1% with each run.
Each SaTScan™ run used a maximum likelihood function
that identified the most likely cluster and secondary
statistically significant clusters. P values obtained through
Monte Carlo hypothesis testing using 999 replications
and relative risk values were assigned to each census
tract.
Using the output from the 50 SaTScan™ runs, reliability
scores were calculated for each census tract as described
in Chen et al. [
28
]. Reliability score is calculated by
Ri = Ci/S, where Ri is the reliability score for location i, Ci
is the number of scans for which that location i is within
a significant cluster, and S is the total number of
SaTScan™ runs; and is defined as the likelihood that a census
tract is reported within a significant cluster among
systematically varying cluster scanning window sizes.
Reliability scores can range from zero to one; zero indicates
that the census tract was not identified within any
statistically significant clusters in any SaTScan™ scans and one
means that the census tract was identified within a
statistically significant cluster in every SaTScan™ run.
Public health analyses routinely use choropleth maps
to display incidence and cluster data, however Roth et al.
[
32
] describe methods to improve the visualization of
reliable, homogenous, and high-risk clusters. By utilizing
this proposed methodology, reliability scores and
relative risk values were concurrently illustrated with
bivariate choropleth map using ArcGIS. This technique used a
two-dimensional color and transparency legend (Fig. 3).
Statistical analysis
Univariate logistic regression modeling was used to
explore associations between population-level factors
and three types of legionellosis occurrence (i.e.,
census tract identified through conventional incidence rate;
default cluster methods; and reliable, high-risk
cluster methods) with demographic, socioeconomic, and
environmental risk factors. Census tracts were
categorized as high-risk if the incidence rate was > 2 cases per
100,000 persons per year (incidence rate during 10-year
study period was divided by 10 to estimate annual rate)
or if the census tract was located within a statistically
significant cluster detected by the default cluster detection
methods. Census tracts with a reliability score ≥ 0.5 and
a RR ≥ 2 were categorized as high-risk for cluster
detection using the reliability score method. These
classification criteria are presented in Table 1.
Multivariate analyses explored associations of
demographic, socioeconomic, and environmental risk factors
of reliable, high-risk cluster census tracts compared to
low-risk census tracts (RS = 0 and RR < 2) while
simultaneously controlling for the other factors. Census
tracts which were associated with a cluster but did not
meet the criteria of a reliable, high-risk cluster were not
included in the multivariate analyses. Pairwise
correlations between each continuous exposure variable,
precategorization, was examined. Collinearity diagnostics
were assessed with an a priori cutoff of 30 for the
condition indices (CI). Stepwise logistic regression was used to
create a model that required a significance level of 0.05
to allow a variable into the model and a significance level
of 0.05 to remain in the model. Forward and backward
model selection resulted in the same final model; while
the full model had the lowest AIC value. Results are
reported as adjusted odds ratios with 95% confidence
intervals.
Results
Descriptive data
From 2003 to 2013, 1634 reported legionellosis cases in
New Jersey met the study’s inclusion criteria. Pairwise
Pearson correlation coefficients between continuous
predictor factors identified only weak and very weak
correlations (r < 0.39) except for a moderate positive correlation
between education and non-white race (r = 0.42),
poverty and Hispanic ethnicity (r = 0.49), and a strong a
correlation between renter-occupied and some high school
IR incidence rate, RS reliability score, RR relative risk
IR ≥ 2 per 100,000
IR ≥ 2 per 100,000
Detected within a cluster
Detected within a cluster
RS ≥ 0.5 and a RR ≥ 2
education (r = 0.61) and renter-occupied and non-white
race (r = 0.61).
Incidence rate
Although incidence rate methods included the largest
number of cases, these methods also have a
correspondingly large number of census tracts and population size
which will likely result in dampened effect estimates
when modeled (Table 1). Cluster analyses had fewer
census tracts identified, with the reliability score method
appearing to maximize the number of cases included
against number of census tracts as compared to the
default 1 and 50% cluster methods. Among the 2000
populated census tracts in New Jersey, 969 (49%) tracts had
at least one confirmed case of legionellosis between 2003
and 2013 (range 1–10 cases). The average 10-year
unadjusted incidence rate was 19.5 cases per 100,000 persons
(range 0–264) and the average 10-year adjusted incidence
rate was 20.8 cases per 100,000 persons (range 0–1694)
(Fig. 1a, b).
Cluster detection
SaTScan™ cluster detection was performed with a
minimum and maximum size scanning window of 1 and 50%
(Fig. 2a, b). The 1% scanning window resulted in 11
statistically significant clusters comprised of 93 census
tracts, while the scanning window of 50% resulted in six
statistically significant clusters comprised of 259 census
tracts. Alternatively, the methodology proposed by Chen
et al. [
28
] identified 322 (16%) census tracts as
belonging within at least one statistically significant cluster,
of which 136 census tracts met the high-risk definition
(RS ≥ 0.5 and RR ≥ 2) (Fig. 3).
Statistical analyses
Unadjusted odds ratios and 95% confidence
intervals of associations with population-level risk
factors highlights differences among spatial methods of
legionellosis occurrence (i.e., conventional incidence
rate; default cluster census tracts; reliable, high-risk
cluster census tracts) (Table 2). Census tracts
classified as high-risk through the incidence rate method
were more likely to be categorized into the highest
non-white population category (OR 1.67; 95% CI 1.28,
2.17); percentage of poverty category (OR 1.49; 95% CI
1.17, 1.90); lower education level; and housing units
that are renter- occupied or built pre-1950 or
pre1970 as compared with census tracts with lower rates
of legionellosis. Comparatively, census tracts classified
as high-risk through cluster analysis, both default and
reliability score methods, found similar patterns of
positive associations with population-level factors as those
from incidence analysis methods, but effect estimates
were much stronger for all factors explored. For
example, census tracts classified as high-risk for incidence
analysis were approximately 1.5 times more likely to be
categorized into high poverty than lower risk census
tracts compared with 3.8 times more likely that
cluster-based high-risk census tracts would be categorized
as high poverty. Cluster methods also found
statistically significant associations with older age and vacant
housing. Only minor, non-significant, differences were
noted between findings from default cluster analyses
and reliability score methods. The final multivariate
logistic regression model found that census tracts with
the highest percentages of older age (OR 0.38; 95% CI
0.22, 0.67); Hispanic populations (OR 0.10; 95% CI 0.05,
0.19); poverty (OR 7.21; 95% CI 4.04, 12.86); and
housing units built pre-1950 (OR 5.69; 95% CI 2.82, 11.50)
were positively statistically significantly associated with
reliable, high-risk legionellosis cluster areas (Table 3). It
is important to note that once other factors were
controlled for, Hispanic ethnicity had a negative,
statistically significant association.
Discussion
Our study assessed the relationship between
populationlevel factors and areas of higher legionellosis occurrence.
Census tracts classified as high-risk for legionellosis were
more likely to have a high percentage of non-white
population, poverty; low education level; and high
percentage of housing units that are renter- occupied or built
pre-1950 or pre-1970. Following adjustment of
covariates, high percentage of older age, poverty, and housing
units built pre-1950 were positively associated while high
percentage of Hispanic populations was negatively
associated. Cluster detection methods for classifying
highrisk census tracts were preferred from the incidence rate
method.
Spatial methods
Little guidance exists for determining cut-off
selection for incidence rates to classify high-risk census
tracts. In 2009, the crude U.S. national incidence rate
for legionellosis was 1.15 per 100,000 persons, the
ageadjusted was 1.08 per 100,000 persons [
33
]. Therefore, a
priori, study investigators selected an IR > 2 (or IR > 20
for 10-year rate) as a “high-risk” cut-off; which appears
to have over-selected for high-risk census tract, with
almost a third of the state’s population included in a
high-risk census tract. In general, our findings suggest
that the potential over-selection led to limited ability of
both univariate and multivariate models to either detect
significant associations or resulted in more moderated
effect estimates as compared with the cluster-based
methodologies. Population-level analyses are important
for contributing to our understanding of the macro-level
determinants of legionellosis, and these analyses require
accurate identification of at-risk areas.
Comparatively, results from incidence analyses and
cluster detection methods supported each other; yet
cluster detection methods, both default and
reliability score methods, detected much stronger associations
for all factors explored. However, we found that results
did not meaningfully differ based on cluster detection
method and default window scanning sizes are effective
in estimating associations. Public health authorities can
apply Chen’s methodology for retrospective surveillance
to identify homogenous, reliable, high-risk disease
clusters for prioritizing targeted prevention outreach.
Missing values were excluded from analysis
Values in italics are statistically significantly at a significance level of 5%
Ecological study design at the census tract level
a Age- and sex-adjusted incidence greater or equal to 2 cases per 100,000 persons
b Significant cluster with 50% of population at risk, relative risk greater or equal to 2 cases per 100,000 persons
c Exposed census tracts defined as RR > 2 and reliability score > 0.5
d Population-weighted centroids of census tracts were joined with public water system polygons
Study results and literature
As the percent of persons aged ≥ 65 years increases
from 10 to 14% to greater than 15%, the negative
association with legionellosis clustering becomes stronger.
Since people 50 years of age or older are known to be
at increased risk for acquiring legionellosis [
1
], further
research is required to determine why older age was a
protective factor in this study. After controlling for other
factors, census tracts with a ≥ 5 to < 20% Hispanic
population and ≥ 20% Hispanic population were 54 and 90%
times less likely, respectively, to be classified as high-risk
for legionellosis clustering. As with older age, Hispanic
ethnicity was less likely to be associated with increased
incidence or clustering or legionellosis. A recently
published study that assessed race/ethnicity and
Legionnaires’ Disease incidence in New York (2002–2011) had
similar findings; the average incidence per year for
nonHispanic blacks was significantly higher than that for
Hispanics [
10
]. Census tracts with more than 50%
nonwhite populations were significantly more likely to be
associated with legionellosis incidence and clustering,
although, this effect was not seen while controlling for
other factors, such as poverty. Associations with
legionellosis and race were therefore largely driven by
confounding from poverty, which was anticipated by a moderate
correlation between the two continuous variables, and as
suggested by previous research [
15
].
In both multivariate models, poverty level remained the
strongest risk factor for legionellosis. The positive
association between poverty level and legionellosis clustering
strengthened as other factors, such as ethnicity and race
were controlled for. The data show a distinct gradient in
risk as the percentage of poverty level increases. Overall,
incidence of Legionnaires’ disease in the city of New York
increased 230% from 2002 to 2009 and followed a
socioeconomic gradient, with highest incidence occurring in
the highest poverty areas [
10, 26
]. Among patients with
community-acquired cases, the probability of working
in transportation, repair, protective services, cleaning,
or construction was significantly higher for those with
Legionnaires’ disease than for the general working
population. Although socioeconomic status may be linked
with risk factors for legionellosis (e.g., smoking, travel,
underlying illness), a direct association between
socioeconomic status and the risk of legionellosis has not been
identified [34]. Factors related to socioeconomic
status, recognized as an important determinant of certain
chronic conditions, has not been extensively evaluated
for its role in the incidence of infectious diseases.
Incomplete information in case reports regarding individual
level socioeconomic factors in many U.S. disease
surveillance systems reduces the usefulness of surveillance data
for these determinants. To our knowledge, no prior
studies using group level data investigated the relationship
between socioeconomic factors and legionellosis.
In our study, census tracts with higher proportions of
rented (vs. owned) housing units were strongly associated
with legionellosis incidence and clustering, although,
this effect was not seen while controlling for other
factors, such as poverty and pre-1950 housing. According
to the American Housing Survey, rental units are more
likely to be structurally inadequate than owner occupied
units [
35
]. Given that older housing is also more likely to
be inadequate, more than 13% of rentals built before 1960
have some structural deficiencies [
36
]. Older housing
stock was also strongly associated with legionellosis
clustering and areas of high occurrence. These effects appear
to have a dose–response such that effect estimates were
stronger for census tracts from the moderate to highest
category of older housing for both pre-1950 or pre-1970,
and were more elevate for older pre-1950 versus
pre1970 housing stock. Older housing stock issues may be
two-fold at both the individual and area-based level. Not
only are older homes at risk of deteriorating plumbing
systems leading to poor water quality, census tracts with
older housing stock may also have an aging community
water infrastructure providing homes with poorer water
quality. Even when controlling for poverty and source
of water, pre-1950 housing was strongly associated with
legionellosis occurrence. Transmission of legionellosis
has been reported to occur in private homes, yet as most
outbreak investigations are focused on public buildings,
outbreaks are more easily associated with large public
buildings as compared with private residences [
25
]. There
is a need for investigations to address how individuals
acquire Legionella from their home, especially as these
residential homes and infrastructures continue to age
[
37–39
].
Public water distribution systems have been shown
to play a role in the transmission of Legionella
including potential contamination of the plumbing systems of
buildings [
40, 41
]. Since surface water is exposed to the
environment, it was hypothesized that Legionella may be
found at higher concentrations in census tracts served by
these systems. Therefore, census tracts served by surface
water sources may be at an increased risk of legionellosis
occurrence compared with groundwater sources.
However, no statistically significant associations with drinking
water source water were found.
Pairwise correlations between population-level factors
were not as strongly correlated as we predicted, since
macro-environment factors are often predictive of one
another (e.g. poverty and race, older housing stock,
education levels). Area-based measures may be inherently
collinear which may make multivariate analyses
problematic. Condition indices were well below the cutoff of
30 and stepwise regression appears to have removed the
more highly correlated factors. Future studies are needed
to explore the exact mechanisms by which these risk
factors may influence disease.
Limitations
Our study has inherent limitations based on its
ecological study design. The associations identified between
legionellosis and risk factors were measured at the census
tract level and cannot be used to make individual
inferences—this would result in biased interpretations known
as ecological fallacy. Our cluster detection methods are
limited to use of home address only; which could
potentially result in exposure misclassification. This study did
not have the capability to detect work-related or
travelrelated clusters. A similar study conducted in New York
City found that certain occupations might be associated
with increased risk for community-acquired
legionellosis [
10
]. We recommend that in the future, public health
investigations collect work addresses during patient
interviews and medical record reviews to enable
prospective cluster detection surveillance to identify
workrelated disease clusters. Due to limited data availability at
the census tract level additional risk factors such as
comorbidities and smoking were not explored and future
research should include these important factors.
Conclusion
Along with well-established risk factors (e.g., older age,
sex, immunocompromised), emerging variables such as
socioeconomic and environmental factors may be
significant indicators for legionellosis risk at the census tract
level. The findings from this study are particularly
important because they create an opportunity for public health
authorities to better target communication for disease
prevention. While geographic patterns alone are
insufficient to conclude that these factors are causally related to
the risk of legionellosis, these methods can be regarded
as a first step approach in the evaluation of census tract
level factors and the risk of legionellosis.
Author’s contributions
JAG and KMR made substantial contributions to conception and design,
acquisition of data, and analysis and interpretation of data; all authors
contributed to drafting and revising of the work. All authors read and approved the
final manuscript.
Acknowledgements
None.
Competing interests
The authors declare they have no competing interests.
Availability of data and materials
The case data used in this study are not publicly available to protect the
Personal Health Identifiers of study participants but are available to investigators
who obtain approval for human subjects’ research for use of the data by the
Rowan University Institutional Review board which serves as the New Jersey
Department of Health (NJDOH) IRB of record. Additional information can be
obtained by the NJDOH’s Ethics Liaison.
Consent for publication
Not applicable.
Ethics approval and consent to participate
State of New Jersey Department of Health Institutional Review Board which
was transferred to Rowan University Institutional Review Board which now
serves as the IRB of record for this study has approved this study for human
subjects’ research.
Funding
This study/report was supported in part by an appointment to the Applied
Epidemiology Fellowship Program administered by the Council of State and
Territorial Epidemiologists (CSTE) and funded by the Centers for Disease
Control and Prevention [
8
] Cooperative Agreement Number 1U38OT000143-05.
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