Epidemiology of Rodent Bites and Prediction of Rat Infestation in New York City
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American Journal of Epidemiology Vol. 148, No. 1 Printed in U.S.A. Epidemiology of Rodent Bites and Prediction of Rat Infestation in New York City James E. Childs,1 Sara L. McLafferty,2 Ramses Sadek,1 Gayle L Miller,1 Ali S. Khan,1 E. Randy DuPree,3 Ranjan Advani, 3 James N. Mills,1 and Gregory E. Glass4 The authors examined the epidemiology of rodent bites occurring in New York City from 1986 through 1994 to identify factors contributing to increased probability of rodent bite and rat infestation. City blocks on which a rodent bite case had been reported (n = 415) and three control blocks per bite block, matched by borough and randomly selected, were compared according to demographic characteristics obtained from US Census data. Environmental variables were defined using a geographic information system to extract distances to areas potentially providing food or refuge for rats, such as parks. Borough-specific models of bite risk were generated by logistic regression using data collected from 1991 to 1994; risk values were then generated for all city blocks. Field surveys for signs of rat infestation conducted on 31 randomly selected blocks indicated a significant association between degree of infestation and predicted risk. Spatial analyses comparing neighboring blocks showed that blocks with bite cases were significantly clustered. The models based on data from previous years correctly predicted 72 percent of 53 block addresses of rodent bite cases from 1995 as being locations of high or intermediate risk. A combination of geographic and epidemiologic analyses could help investigators identify the spatial occurrence of rat infestation over a large area and might help to focus control activities. Am J Epidemiol 1998; 148:78-87. bites and stings; geography; information systems; rats; risk assessment; rodent control; urban health In cities across the United States, introduced rodents United States and are reported from all states, while of the family Muridae (the Norway rat (Rattus norve- black rats are largely limited to coastal regions, pri- gicus), the black rat (Rattus rattus), and the house marily in the warmer South (5). mouse (Mus musculus)) are locally abundant and the Contact with rodents can result in bites. In 1970 and sources of considerable public health and economic 1971, the Center for Disease Control conducted a concern. Numerous zoonotic infections can be ac- national animal-bite surveillance program in 15 health quired through contact with these rodents or their jurisdictions; rodents accounted for 4.3 percent of the ectoparasites (1). Within the past decade, reports of 196,117 recorded bites (6). However, the epidemiol- human disease associated with a rat-borne Hantavirus ogy of rodent bites has received little attention, and the have been made from Baltimore, Maryland (2), and information available is negligible compared with data diseases such as leptospirosis (3) and murine typhus concerning dog and cat bites (7-10). Cases of rat bite (4) are ongoing concerns in many US cities. House sporadically catch public attention when the victims mice and Norway rats are common throughout the are infants, but most accounts are limited to case reports of rat-bite fever, a rare but potentially fatal infection primarily caused by Streptobacillus monili- formis in the United States (11). Received for publication September 2, 1997, and in final form January 16, 1998. In one of the few epidemiologic studies of rat bites, 1 Division of Viral and Rickettsial Diseases, National Center for investigators examined 50 consecutive bite patients Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA. appearing in a Los Angeles, California, emergency 2 Department of Geography, Hunter College, New York, NY. room (12). The majority of patients were under 15 3 4 New York City Department of Health, New York, NY. years of age, and most of the bites were not severe; Department of Molecular Microbiology and Immunology, Johns Hopkins University School of Public Health, Baltimore, MD. only one patient developed a bacterial infection that Reprint requests to Dr. James E. Childs, National Center for required antibiotic treatment. In contrast to bites from Infectious Diseases, Centers for Disease Control and Prevention, carnivores, bites from rodents (except the larger spe- 1600 Clifton Road NE, Mailstop G13, Atlanta, GA 30333. This paper was prepared under the auspices of the US Govern- cies such as beavers or woodchucks) are not consid- ment and is therefore not subject to copyright. ered to carry a high risk for rabies virus transmission 78
Rodent Bites and Rat Infestation in New York City 79 (13), and victims are rarely prescribed postexposure incorrect addresses {n = 295). This left 514 bite pa- treatment (14). tients whose addresses could be mapped to 415 dis- The distribution of rodent populations within urban tinct blocks using Arclnfo software (Environmental centers has only rarely been determined directly by Systems Research Institute, Redlands, California) and trapping or by examining urban neighborhoods for the Bureau of the Census' enhanced TIGER files for signs of infestation (15). Mice are caught almost ex- New York City (19). Blocks were defined as the clusively within residences, while rats are found geographic units for study, which permitted the use of within dwellings and in alleys, sewers, and other lo- 1990 US Census data on demographic determinants at cations (16, 17). Indirect survey methods, such as either the block level or the census tract level. mapping of reports of rodent sightings in Baltimore (17) or of the home addresses of Detroit, Michigan, Demographic variables children found to be seropositive for Leptospira ic- terohaemorrhagiae (18), have permitted inferences Block statistics on total population, race (percentage about the urban conditions that support extensive ro- black, Asian, or white), percentage Hispanic, and dent infestation, particularly rat infestation. Although numbers of people younger than 18 years and older less affluent inner-city neighborhoods are typically the than 65 years were extracted from 1990 Census files areas identified as having the most severe problems, for determination of the demographic characteristics no studies have systematically defined factors that of each block. Information on median household in- might predict rat infestation and potentially the risk of come was available at the census tract level, and that rodent-associated problems. value was assigned to all blocks within each tract. For In this investigation, we examined the epidemiology assessment of crowding and the potential for environ- of rodent bites reported from New York City and used mental conditions which provide harborage for rodents these data and the environmental and social character- (e.g., vacant buildings), the total number of housing istics of the home blocks of bite patients to generate units in each block and the total number of units predictive models for rodent bite. After control blocks occupied were included. A density or crowding vari- were selected and the risk of a block's having a resi- able was computed by dividing the total block popu- dent bite case was modeled, a New York City-wide lation by the number of occupied housing units. map of rodent bite risk was produced. We then tested the predictions of statistical and spatial modeling by Environmental variables comparing block addresses of additional rodent bite victims from a subsequent year of surveillance with Environmental variables were assessed by determin- the addresses' predicted risk classification, and by ing the block's location relative to sites potentially environmental sampling of randomly selected blocks serving as rodent refuge or food resources. Arclnfo for evidence of rat activity. was used to query existing databases and to compute the distance (in meters) from the block center to the geographic feature. Attention was focused on parks, MATERIALS AND METHODS subways, railroad lines, and highways, because these areas can provide suitable habitat or exposed earth Rodent bite data which can be used as burrow sites by Norway rats. Animal bites to humans in the five boroughs of New Data files on sanitation records of street cleanliness York City (Brooklyn, Bronx, Manhattan, Queens, and were not available, but the distance to the nearest Staten Island) are reportable to the New York City waste transfer station was measured. Department of Health. Information on the descriptive epidemiology of rodent bite was derived from surveil- lance reports submitted to the health department from Analyses January 1986 through September 1994. A subsample For analysis of the effects of demographic and en- of reports from January 1991-September 1994 was vironmental factors on rodent bite risk, each block examined for statistical modeling and for use in the from which a bite had been reported was compared geographic information system analyses. The analysis with approximately three control blocks randomly se- was limited to the previous 4 years to reduce the lected from all of the remaining blocks in each bor- influence of environmental and neighborhood change ough. The final database consisted of 1,660 blocks: within the city. 528 in Brooklyn (132 bite blocks and 396 control Of the initial 829 reports of rodent bite, 315 cases blocks), 448 in Manhattan (112 and 336 blocks), 372 were excluded because they occurred in a work-related in the Bronx (93 and 279), 272 in Queens (68 and setting (mostly university laboratories; n = 20) or had 204), and 40 in Staten Island (10 and 30). For each Am J Epidemiol Vol. 148, No. 1, 1998
80 Childs et al. control block, a suite of variables identical to that of rodent bite classification. A list of 31 randomly se- the corresponding bite block was derived. lected blocks in Manhattan and Brooklyn (13 pre- Preliminary analyses included univariate compari- dicted to be low risk, 13 predicted to be high risk, and sons of variables by means of nonparametric statistical five predicted to be intermediate risk) was provided to tests performed independently for each borough. The a survey team that was blinded to their predicted spatial aggregation of blocks with rat bites, through value. Surveys were performed using a standardized the 10th nearest neighboring block, was tested by environmental survey form (25) designed to assess rat comparing the distances (in meters) from the centers infestation. of bite and control blocks using the method of Cuzick The housing characteristics of each block were as- and Edwards (20), with Simes correction for multiple sessed by determining the proportions of addresses comparisons (21). that were residential, commercial (businesses), mixed Logistic regression analyses for the New York City (residential and commercial), and food-oriented (gro- data set and for each borough were used to generate ceries or restaurants). Proportions of vacant buildings equations for prediction of the risk of a block's con- and empty lots were determined. The proportion of taining a rat-bite case. Data on most demographic and properties without proper refuse containers or with environmental variables were dichotomized at the me- accessible garbage, pet food, and/or animal feces pro- dian value before being entered into the model. Blocks vided an indicator of food resources for rats, and the were assigned a value of 1 if their value exceeded the presence of abandoned vehicles, lumber piles, appli- median value for the entire borough and a 0 otherwise. ances, and other large items was recorded as a measure When continuous variables fitted the model better, of potential harborage for rats. The proportion of they were retained. In each analysis, logistic regres- houses with physical evidence of infestation or other sion was performed for all subsets to determine the indicators of rat activity was also recorded. two best subsets of different numbers of variables All proportions were transformed by taking the arc- (22). Subsets were examined for their fit to the data sin of the square root, and one-way analysis of vari- (Hosmer-Lemeshow goodness-of-fit statistic (C)), for ance was used, with predicted risk classification as the sensitivity (number of bite blocks correctly classified categorical variable. Analytical results with two-tailed as bite blocks/[number of bite blocks correctly classi- p values less than 0.050 were considered statistically fied as bite blocks plus number of bite blocks incor- significant. rectly classified as nonbite blocks]), for specificity (number of nonbite blocks correctly classified as non- Prediction of future block sites of rat-bite cases bite blocks/fnumber of nonbite blocks correctly clas- sified as nonbite blocks plus number of nonbite blocks Addresses of rodent bite cases reported to the New incorrectly classified as bite blocks]), and for overall York City Department of Health in 1995 were ana- correct classification. The contribution of each com- lyzed by the methods described above. Rodent bite bination of variables was assessed by selectively re- risk values generated by the borough-specific logistic moving variables and evaluating the data using partial regression analysis were computed for each geocoded F tests. In some analyses, variables that were not block for ascertainment of how accurately sites had statistically significant were retained because they been predicted. contributed to increased model sensitivity. Final logistic regression models were selected to RESULTS maximize sensitivity and overall correct classification, Demographic characteristics and 2-5 variables without interaction terms were re- The 514 evaluated cases of rodent bite occurred tained. For each borough, the logistic regression equa- throughout the five boroughs of New York City (table tion was used with the Arclnfo data layers to generate 1 and figure 1). The bite cases were evenly distributed a rodent bite risk score for every block with a nonzero by sex, and the median age of case-patients was 22 residential population. Statistical analyses were per- years (range,
Rodent Bites and Rat Infestation in New York City 81 TABLE 1. Characteristics of 514 New York City residents Characterization of block of residence reported to have received a rodent bite during the period 1991-1994 Most people who had been bitten by rodents lived on blocks with significantly lower median incomes Characteristic No.* % than those of control blocks (table 2). In addition to Year containing more residents per block (four of five bor- 1991 73 14.2 oughs), case blocks also had a higher percentage of 1992 166 32.3 1993 residents younger than 18 years of age and a lower 155 30.2 1994 120 23.3 percentage of residents older than 65 years of age. The mean number of housing units per block and the mean Borough Brooklyn 150 31.3 percentage of rental units per block were greater for Bronx 123 25.6 case blocks in each borough (table 2). In each bor- Manhattan 136 28.3 ough, the percentage of the population characterized Queens 61 12.7 as black or Hispanic was higher on the case blocks. Staten Island 10 2.1 Blocks with more than one bite case showed trends Sex identical to those of blocks with single bite cases; only Male 235 48.5 in Manhattan were significant differences found be- Female 250 51.5 tween blocks with different numbers of reported bite Bite site cases. Blocks with multiple bites in Manhattan had Finger/hand 264 53.3 Toe/foot 100 20.2 lower median incomes, lower percentages of Asian Leg 41 8.3 and white residents, higher percentages of black resi- Head/face/neck 46 9.3 dents, and higher percentages of residents under 18 Arm 32 6.5 years of age (Wilcoxon rank sum test: all p's < 0.05) Body/trunk 12 2.4 in comparison with single-bite blocks or control Biting animal blocks. These differences were similar to those be- Rat 416 80.9 tween all bite blocks and control blocks, and therefore Mouse 95 18.5 Other 3 0.6 blocks with any number of bite cases were pooled for future analyses. Situation Asleep 221 54.6 Distances to environmental features varied substan- Awake 184 45.4 tially by borough, but some patterns in their associa- Treatment tion with rodent bite blocks were discernable (table 2). Medical 334 94.6 Distances to subways (five of five boroughs), waste None 13 3.7 stations (four of five), railroads (four of five), and Surgical 6 1.7 parks (five of five) were shorter for case blocks. Disposition No pattern was apparent in distance to the nearest Released 335 97.7 highway. Admitted 8 2.3 * Numbers do not total 514 in some categories because of missing values. Logistic regression modeling of rodent bite blocks The best subset logistic regression models for New cases, through the 10th nearest neighboring block, was York City and for each borough contained 2-5 vari- statistically significant (all z scores > 6.0; all p val- ables (table 3). Variables included in the models of ues < 0.0001; Simes correction: p < 0.0001). Bites more than one borough or of New York City overall were most common in northern Brooklyn, the southern were median income, total population of block, dis- Bronx, and the southern and northern extremes of tance to subway, percentage Hispanic, and percentage Manhattan (figure 1). Overall, 371 (89.4 percent) of younger than 18 years. Seven other variables were the 415 blocks contained a single bite case, 34 (8.2 used in individual borough models (table 3). percent) contained two cases, nine (2.2 percent) con- The fit of each model varied considerably, and in- tained three, and one contained four. The number of dividual borough models provided better fits to the blocks reporting more than one bite case was 13 for data than did the overall New York City model (table the Bronx (14 percent of all bite blocks), eight for 4). Four of the five borough models provided good Brooklyn (6.1 percent), 22 for Manhattan (19.6 per- fits to the data, as indicated by Hosmer-Lemeshow cent), zero for Queens, and one for Staten Island (10 goodness-of-fit statistics (table 4). In each case, these percent). models provided a sensitivity greater than 60 percent Am J Epidemiol Vol. 148, No. 1, 1998
82 Childs et al. FIGURE 1. Distribution of 415 blocks in the five boroughs of New York City on which a person reporting a rodent bite lived, 1991-1994. The boundaries of each borough are defined by thicker lines. A single dot is displayed even for blocks from which more than one bite was reported. Data on rodent bite, a reportable condition in New York City, were analyzed for 1991-1994, but not all addresses could be coded and mapped. (range, 61.8 percent to 70.0 percent) and a specificity of values between 0.7 and 0.9. Risk scores were not near or above 70 percent (range, 69.8 percent to 86.7 generated for blocks without human residents. percent). The citywide and Brooklyn models provided the poorest fits to the data, with sensitivities below 60 percent, although both the overall percentage of blocks Field assessment correctly characterized and the percent specificities High risk blocks were only marginally more likely were over 70 percent (table 4). to be infested than were low and intermediate risk blocks, but the degree of infestation was significantly greater. Among the 31 blocks surveyed, 10 of 13 Mapping risk of rodent bite predicted to be high risk had evidence of active rat Overall, 28,478 (85 percent) of the 33,468 blocks in infestation in one or more residences, compared with the five boroughs had nonzero populations, and a eight of 13 predicted to be low risk and three of five rodent bite risk score could be obtained for each bor- predicted to be intermediate risk. However, in blocks ough using the logistic regression models (table 5). predicted to be high risk, the average proportion of Maps were drawn by stratifying risk probabilities at addresses infested was 27.3 percent as compared with the median value (0.041) and the 72nd percentile (0.7) 8.3 percent for intermediate risk blocks and 9.1 per- (figure 2 (Staten Island not shown)); this formed three cent for low risk blocks. An initial one-way analysis of classes of blocks: high risk (22 percent of blocks), variance indicated no difference between intermediate intermediate risk (28 percent), and low risk (50 per- risk and low risk blocks, and when these blocks were cent) blocks (table 5). The second cutoff point was combined, a significant difference was evident in the selected after exploratory analyses revealed a cluster proportion of addresses infested on high risk blocks Am J Epidemiol Vol. 148, No. 1, 1998
Rodent Bites and Rat Infestation in New York City 83 TABLE 2. Comparison of demographic data (mean values) from 415 city blocks on which rodent bite patients resided and 1,245 randomly selected control blocks from each borough, New York City, 1991-1994t Brooklyn Bronx Manhattan Staten Island Queens Characteristic No No No No No Bite Bite Bite Bite Bite bite bite bite bite bite Total population ot block 519"* 289 873" 588 759*** 322 192 87 584*** 189 %65 years of age 8 13"* 12 14 9 13"* 12 17 12 16" Median annual income (dollars)* 26,025 32,966"* 31,911 53,757'" 19,731 32,880"* 36,946 51,861" 33,562 43,259*" Race/ethnlclty (%)§ White 28 53*" 45 64*** 26 49**. 65 89* 50 58* Black 54... 31 33"* 20 41 « • 31 23 4 26* 23 Hispanic 29"* 21 35«* 21 53«* 34 13 8 25"* 16 Asian 3 5 7 7 2 3 5 3 15* 11 No. of housing units/block 186"* 112 396* 320 259"* 122 62 29 218"* 72 % of rental units 82«* 69 85*" 74 90"* 55 76 34 82"* 58 Distance (m) to a geographic feature Highway 500 646" 2,601" 2,136 4,911 4,184" 3,331 5,552* 563 624 Waste station 5,269 4,822 2,621 2,836 5,281 6,008" 9,294 11,539* 6,615 7,743** Subway 380 560"* 183 189 332 758"* 6,669 8,997 921 2,167*" Railroad 2,198 2,203 1,220 1.582" 617 1,124"* 648 1,203* 1,914 1,484 Park 233 264 153 161 213 261 324 370 295 313 * pi 0.05; " p
84 Childs et al. reported within residences (6 percent for rat infesta- • •*; r-: in tion, 49 percent for mice) and were rarely associated ! oi o oj with bites (1.2 percent of respondents reported expe- CNI •* ci r^ d r^ ••* c o riencing any rodent bite during their lifetime). Further- § more, rodent bites are underreported. Previous studies •a in New York City have indicated that only 41 percent 2. lO CO (O t b CO 8 S) q I I I I I I I I of animal bites treated in emergency rooms are re- o r-: ci w ported to health authorities (28). Even bites inflicted by dogs are frequently not reported: In Pennsylvania, 2 a study of children aged 4-18 years found that the rate O of dog bite was 36 times greater than the rate reported X to health authorities (29). o In addition to underreporting, we were unable to & I I I II I I I I I I « I geocode a high percentage of addresses, primarily o because inaccurate addresses were given or recorded at the treatment centers. These limitations would result # a T^ T^ 4 i - J> 0) in some bite blocks' being classified as nonbite blocks Io i-m 1 o> ^ odd a> and would reduce precision, biasing our model results toward the null (30). However, the subsequent assess- s I I IS I ments of the models and the evidence of clustering among bite blocks provided confidence that character- I a 2 istics relevant to rat infestation and risk of rodent bite o were captured. i 2J Another concern was that the field assessment mea- sured only rat infestation, but the statistical models 1 used to classify blocks were based on reported rat or ?-|0)| I I I ^(O I I I I •a CO '
Rodent Bites and Rat Infestation in New York City 85 TABLE 4. Summary statistics for final regression models used to predict blocks with cases of rodent bite, New York City, 1991-1994 Hosmer- Adjusted P Borough Lemeshow FP statistic value correct* sensitivity* specificity* All boroughs 0.20 29.83 0.0002 71.8 59.3 76.0 Brooklyn 0.18 18.20 0.02 72.7 59.1 77.2 Bronx 0.15 6.39 0.60 68.1 63.4 69.6 Manhattan 0.33 5.73 0.68 76.4 65.6 80 Queens 0.20 9.20 0.32 75.5 61.8 80.4 Staten Island 0.92 0.13 0.94 82.5 70.0 86.7 * Calculated at a probability of being a block with a rodent bite case of 0.28-0.34. subways, railroads, and parks, all of which are a po- stations also tended to be shorter for bite blocks, tential source of exposed ground in which Norway rats although it was not clear whether this was related to can burrow. Parks and subways can also be sources of potential food sources or other neighborhood charac- food through human refuse. Zoologic parks have been teristics. Still, the significance of environmental vari- associated with major foci of rat infestations in other ables in the logistic regression models controlling for cities (32). However, living in proximity to noisy socioeconomic variation suggests some independent transportation systems may also be a characteristic of effect on the incidence of rat bites. less affluent neighborhoods. Mean distance to waste The restriction of our sample base to bite patients Risk Probability tm o • 0.041 H 0.041 - 0.7 0.7-1.00 No Data Scale 1:250,000 FIGURE 2. Risk of a block's being a site where a rodent bite could have occurred, based on logistic regression modeling of bite risk for each of five boroughs (Staten Island not shown), New York City, 1991-1994. Risk was stratified into three classifications, with half of the blocks being low risk and 22% and 28% being intermediate and high risk, respectively. Am J Epidemiol Vol. 148, No. 1, 1998
86 Childs et al. TABLE 5. Classification of all blocks in New York City into Some of the most useful applications of this type have areas of varying rodent bite risk using common cutoff values, been studies of zoonotic diseases, a category which New York City, 1991-1994* can include animal bites (35). The potential use of Bite risk these methods for assessing human risk for rat-borne Borough H '9h flHVti^ Low population diseases such as leptospirosis and murine typhus re- >0 7 ( (p p7o,7* Brooklyn 3,290 (43)t 0 4,287(57) 1,223 tion of these methods in helping to focus control Bronx 2,118(60) 33 1,404(40) 1,034 efforts is apparent, although the means of implement- Manhattan 849 (34) 839 (34) 781 (32) 564 ing control may be lacking. Many cities have rodent Queens 8 6,508 (58) 4,715(42) 1,727 Staten Island 0 682 (19) 2,963(81) 441 control programs that are understaffed, and efforts are typically reactive rather than proactive. Responding to All boroughs 6,265(22) 8,062(28) 14,150(50) 4,989 public complaints of rodent infestation does not ensure * This scheme was used to select blocks for field surveys of rat that efforts are directed toward locations with the infestation for assessment of the scoring indices in terms of their greatest problem. In addition, the fact that borough- usefulness in predicting locations of rat abundance. t Numbers in parentheses, percentage of area in that risk specific models provided substantially better fits to the category. data indicates that generalization of these models to other cities would not necessarily be useful. The re- finement of methods explored in this study would hold with geocoded addresses raises questions concerning promise in terms of helping to direct control efforts how representative of rodent bite victims our sample through a process that is less costly than field surveys was. However, few data on rodent bites with which to and less prone to misdirection by differences in the compare our results are available. In a case series from degree of tolerance of rodent infestation among Los Angeles (12), the mean age of treated patients was communities. 10.8 years, approximately half of our figure, and fewer bites to the lower extremities were reported (~14 percent vs. >28 percent). These differences may re- flect the epidemiology of rat bite in various geographic REFERENCES locations or different methods of case selection. In southern areas of the United States, especially in port 1. Gratz NR. Rodents and human disease: a global appreciation. In: Prakash I, ed. Rodent pest management. Boca Raton, FL: cities, the most common rat may be the black or roof CRC Press, 1988:101-23. rat, R. rattus (33). The black rat is highly arboreal, and 2. Glass GE, Watson AJ, LeDuc JW, et al. 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