Original Article
Cat Scratch Disease in Connecticut -- Epidemiology, Risk Factors, and Evaluation of a New Diagnostic Test
N Engl J Med 1993; 329:8-13July 1, 1993
- Abstract
Background
Although cat scratch disease is commonly diagnosed in patients who have unexplained regional lymphadenopathy after encounters with cats, its epidemiology and the risk factors for disease are not clearly defined, and there is no generally accepted diagnostic test.
Methods
We conducted a physician survey to identify cases of cat scratch disease occurring over a 13-month period in cat owners in Connecticut. We interviewed both the patients (or their parents) and controls matched for age who owned cats. Serum from the patients was tested for antibodies to Rochalimaea henselae with a new, indirect fluorescent-antibody test.
Results
We identified 60 patients with cat scratch disease and 56 age-matched, cat-owning control subjects. Patients were more likely than controls to have at least one pet kitten 12 months old or younger (odds ratio, 15), to have been scratched or bitten by a kitten (odds ratio, 27), and to have had at least one kitten with fleas (odds ratio, 29). A conditional logistic-regression analysis found that in kitten-owning households, patients were more likely than controls to have been scratched or bitten by a cat or kitten (odds ratio, 12.4; 95 percent confidence interval, 1.0 to 150).
Of 45 patients, 38 had serum samples with titers of 1:64 or higher for antibody to R. henselae, as compared with 4 of 112 samples from controls (P<0.001). The positive predictive value of the serologic test was 91 percent. Of 48 serum samples from patients' cats, 39 were positive for antibodies to R. henselae, as compared with positive samples from 11 of 29 control cats (P<0.001).
Conclusions
Cat scratch disease is strongly associated with owning a kitten, and fleas may be involved in its transmission. The serologic test for rochalimaea may be useful diagnostically, and our results suggest an etiologic role for this genus.
Media in This Article
Figure 1
Titers of Antibody to R. henselae Antigen as Measured by the Indirect Fluorescent-Antibody Test in Patients with Cat Scratch Disease.Table 1
Clinical Characteristics of 60 Patients with Cat Scratch Disease.Article Activity
- Article
Cat scratch disease was first described more than 40 years ago1. Its classic clinical feature is self-limited, regional lymphadenopathy occurring after a cat scratch or bite distal to the affected node. The etiologic agent has not been conclusively identified, and there has been no simple diagnostic test.
The majority of reported cases have occurred in persons under 20 years of age, who are usually male, and the number of cases has been consistently reported to peak in the fall and winter2,3. An estimated 22,000 cases are diagnosed each year in the United States, with more than 2000 hospitalizations4. More than 90 percent of the patients have a history of some type of contact with cats,2,5 and 57 to 83 percent have a history of a scratch from a cat6-9. Systematic evaluations of risk factors for the development of cat scratch disease have not been reported, however.
An indirect fluorescent-antibody test for the detection of humoral response to Rochalimaea henselae has recently been developed. Its relatively high sensitivity (88 percent) and specificity (94 percent) for cat scratch disease suggest that R. henselae or a closely related organism may have an etiologic role10.
In October and November 1991, two children in the same grade at an elementary school in Connecticut were hospitalized with encephalitis due to cat scratch disease. We conducted an investigation to define the epidemiologic features of cat scratch disease in Connecticut, to identify risk factors with the use of case-control methods, and to evaluate the R. henselae-based serologic test for the diagnosis of cat scratch disease.
Methods
Epidemiologic Investigation
A letter and a standardized case-report form were mailed to all licensed internists, family practitioners, pediatricians, and neurologists in the state of Connecticut (approximately 4900); they were asked to identify patients in whom they had diagnosed cat scratch disease from January 1991 through January 1992 and to complete and return the case-report form. The form requested information about the patients' contacts with cats and clinical information, including their history, presentation, diagnostic procedures, and therapeutic interventions.
Case-Control Study
Case Definition
A case of cat scratch disease was defined as the occurrence of unexplained lymphadenopathy in a resident of Connecticut who owned at least one pet cat or kitten during the three-month period before the onset of symptoms (the reference period). A pet cat or kitten was considered owned if anyone in the patient's home had fed it at least three times a week during the reference period. A kitten was defined as a cat that was 12 months of age or younger at the beginning of the reference period.
Selection of Controls
We used a modified random-digit dialing technique11 to recruit controls. Cat owners were matched with the patients for age as follows: the cat owner's age had to be within 6 months of the patient's age if the patient was 2 years old or younger (but ≥ 3 months); within 1 year, if the patient was 3 to 10 years old; within 3 years, if the patient was 11 to 18 years old; and within 5 years, if the patient was 19 years old or older. We generated lists of telephone numbers with the same prefix (exchange) as the patient's telephone number and attempted a maximum of three calls for each number. A total of 2453 telephone numbers were called: 2167 numbers (88 percent) were those of businesses, unavailable parties, or households without cats. The telephone was allowed to ring 10 times before the party was considered unavailable. Of the remaining 286 numbers, 220 (77 percent) were those of persons who did not fulfill age-matching criteria and 10 (3.5 percent) were those of persons who declined to participate.
Data Collection
A standardized questionnaire was used to collect data on interactions between the subjects and their cats, between the subjects and their environment, and between the cats and their environment; specific characteristics relating to the cats; exposure to other animals; and environmental factors. The questionnaire also asked for limited demographic information about the subjects and the cats as well as about the vaccination and medical history of the cats. All interviews were conducted in person or by telephone by one of two investigators, both of whom knew whether the subjects were patients or controls. Information was requested about the patients and controls for the reference period defined above and was collected on each cat in each household.
Laboratory Testing
Serum samples were obtained from the patients, their families, and their cats and kittens. Control human samples (n = 112) were obtained from among samples received by the Laboratory Division of the Connecticut Department of Health Services from Connecticut residents from October 1, 1991, through January 31, 1992, primarily for testing for measles or varicella antibody. The age distribution of these residents (in five-year age groups) was similar to that of the patients. Control serum was also obtained from 29 healthy cats and kittens at three veterinary clinics in Connecticut.
The samples from the patients and the control subjects were evaluated with a R. henselae-based indirect fluorescent-antibody test as previously described10. The samples from the cats were evaluated with the use of fluorescein-labeled anticat IgG immunoglobulin. Serologic testing was performed without knowledge of whether the samples were those of the patients and their cats or of the controls (Connecticut residents and cats).
Statistical Analysis
Multivariate analysis was used to assess effect modification and confounding with variables found to have elevated odds ratios according to univariate analysis12. Multivariate modeling was hypothesis-oriented and did not use stepwise selection of variables.
Results
Descriptive Epidemiology
Seventy-two cases of suspected cat scratch disease were reported in Connecticut. Twelve patients did not meet the case definition because we could not verify whether these patients owned cats (six patients) or because they did not own cats (six patients)5. Therefore, 60 cases fulfilled the case definition. Three study families contained two patients each; two other patients had been exposed to the same cats. The median age of the patients was 15 years (range, 1 to 57), and 43 percent were more than 20 years of age. Thirty-one patients (52 percent) were female, and 58 (97 percent) were white. In 56 patients (93 percent), symptoms began during the six months from August 1991 through January 1992. The patients were distributed throughout Connecticut. Overall, the statewide incidence of cat scratch disease was 1.8 cases per 100,000 population.
Clinical Information
The median interval between the onset of lymphadenopathy or constitutional symptoms (if present) and diagnosis by a health care provider was 8 days (range, 0 to 55). The most common sites of lymphadenopathy were the axillae and the neck (Table 1Table 1
Clinical Characteristics of 60 Patients with Cat Scratch Disease.). Other signs and symptoms of illness accompanying lymphadenopathy were reported by 49 patients (82 percent) -- most commonly, fever, malaise, or a skin lesion at the site of a cat scratch. Two of the four patients with encephalopathy had seizures and a period of coma, but all four recovered without sequelae. None of the patients were evaluated with use of the skin-test antigen for cat scratch disease, which is not standardized or approved for general use. Antibiotics were prescribed for 47 patients (78 percent). Nine patients (15 percent) underwent lymph-node biopsy. Ten patients (17 percent) were hospitalized for a mean of 5 days (range, 1 to 15). None of the patients died.Case-Control Study
Of the 60 patients whose cases met the case definition, 4 were not successfully matched with controls for age and cat ownership; therefore, 56 patients and their controls were enrolled in the case-control study. The controls did not differ significantly from the patients in race, sex, family size, level of maternal education, or socioeconomic status.
Interactions between Humans and Cats
Matched univariate analysis revealed that the patients were more likely than the controls to have had several different types of exposure to cats (Table 2Table 2
Cat-Related Risk Factors for Cat Scratch Disease.). Patients were more likely than controls to have had at least one pet kitten. Specific types of contact significantly associated with cat scratch disease included being scratched or bitten by a kitten, being licked on the face by a kitten, sleeping with a kitten, and combing a kitten. Similar exposures to adult cats were not significantly associated with the development of disease. No significant risk factors were identified among patients who did not own at least one kitten.Interactions among Humans, Cats, and Environments
Patients were more likely than controls to have had at least one pet kitten with fleas, to have had a kitten that dug outside, and to have found at least one tick on their own body (Table 2). Patients were no more likely than controls to report that they had mice in their home, that construction, excavation, remodeling, or plowing had recently been carried out within 100 yd (90 m) of their home, that they had sustained an injury that broke the skin, or that they kept houseplants. Patients' cats were no more likely than controls' cats to have spent more time outside the home, used a litter box, or caught or killed small animals.
Cat-Specific Factors
The age and sex of the pet cats were significantly associated with the development of cat scratch disease (Table 2). The patients' cats were significantly younger than the controls' cats (mean age, 33 vs. 59 months; P<0.002), a finding consistent with the previously noted association between ownership of a kitten and disease. Patients were also more likely to own a male cat. There was no significant difference between the patients' cats and the controls' cats in breed, vaccination status during the first year of life, likelihood of being examined by a veterinarian during the previous two years, frequency of illnesses, or need for medications or in the proportion that had been neutered, spayed, or declawed.
Bivariate Analysis
Owning a kitten, owning a kitten with fleas, and being scratched or bitten by a kitten were the variables most strongly associated with cat scratch disease. To evaluate the independent effects of these three variables, we constructed two matched conditional logistic-regression models. Each bivariate model included kitten ownership and either the presence of a pet cat with fleas or cat scratches or bites, with appropriate interaction terms. Being scratched or bitten by a cat was significantly associated with disease among persons in households with kittens; this risk was nearly seven times the risk associated with disease among persons in households without kittens (Table 3Table 3
Odds Ratios for Cat Scratch Disease, According to Kitten Ownership (Bivariate Analysis).). The presence of a cat with fleas in households with kittens was associated with a sixfold increase in the risk of disease, but this difference was not statistically significant. The risk of disease, however, was nearly 10 times higher than the risk associated with the presence of a cat with fleas in households without kittens. Other factors associated with disease in the univariate analysis (such as the sex of a cat or sleeping with a cat) were no longer significant after adjustment for the variable of kitten ownership.Laboratory Testing
The indirect fluorescent-antibody test for R. henselae was positive (titers ≥ 1:64) for 38 of the 45 patient serum samples evaluated and 4 of the 112 control samples (84 percent vs. 3.6 percent; P<0.001). This serologic test had a sensitivity of 84 percent, a specificity of 96 percent, and a positive predictive value of 91 percent. One of four patients with paired acute-phase and convalescent-phase samples had a fourfold rise in titer; the other three patients had titers of 1:512 or higher in both samples. Five of seven patients with negative titers were adults.
Figure 1Figure 1
Titers of Antibody to R. henselae Antigen as Measured by the Indirect Fluorescent-Antibody Test in Patients with Cat Scratch Disease. shows antibody titers in the serum samples from all 45 patients; the samples were obtained at various times after the onset of lymphadenopathy. The titers for antibody to R. henselae were highest in the early weeks after the onset of lymphadenopathy and appeared to decline over time. Excluding patients with serologic tests negative for R. henselae did not alter the findings of the case-control study. Fourteen of 77 samples (18 percent) from asymptomatic members of patients' families were positive (P<0.001 for the comparison with the rate among patients; P<0.002 for the comparison with the rate among controls [Connecticut residents]). A follow-up telephone survey of these 14 family members revealed that 6 (43 percent) had had symptoms consistent with cat scratch disease during the two months before the serum was obtained; 5 of these 6 reported a history of recent cat scratches.Thirty-nine of 48 serum samples (81 percent) from patients' cats and 11 of 29 samples (38 percent) from control cats (veterinary-clinic cats) were positive for R. henselae (P<0.001). The magnitude of the elevation in the titers in the cats was similar to that in the patients.
Discussion
Most children with cat scratch disease have mild symptoms and a benign clinical course13. The cases of two children with encephalitis that prompted the present investigation, however, are reminders that cat scratch disease can be a severe, protracted illness and may require costly and painful diagnostic evaluation because of the broad differential diagnosis14 and the lack of a reliable diagnostic test.
The epidemiology of cat scratch disease and the risk factors for this disorder are not fully understood, a fact that underlines the need for systematic studies of the illness. The incidence of 1.8 cases of cat scratch disease per 100,000 population that we found in this study is lower than the incidence of 9.3 cases per 100,000 reported from a national data base,4 and since our case ascertainment was retrospective and voluntary, it probably represents an underestimate of the true disease burden.
The clinical characteristics and seasonal distribution of cat scratch disease in Connecticut were similar to those described in previous reports2,3. There were more older patients in our study (43 percent of our patients were more than 20 years old) than in previous studies2,3. This age distribution, however, was similar to that in the only study of the national incidence of cat scratch disease among ambulatory and hospitalized patients4. The higher proportion of younger patients in previous reports may reflect selection bias on the part of pediatrician investigators toward their patient population. Our study suggests that cat scratch disease may be more common among adults than previously recognized.
Ownership of a kitten was the risk factor most strongly associated with the development of cat scratch disease, according to univariate analysis. A number of other variables related to contact with a kitten were also associated with disease, although in bivariate analyses controlling for kitten ownership, only the variable of receiving a scratch or bite remained significant. Ascertainment bias among the patients could have increased the likelihood that being scratched by a cat would be identified as a risk factor for disease. The association with other traumatic contact with a kitten, including bites, however, suggests that these exposures are of primary importance. A scratch or bite may introduce an infectious agent, as anecdotal data on the natural history of cat scratch disease suggest. The association with a scratch or bite by a kitten may reflect a particular characteristic of kittens that facilitates the propagation of the etiologic agent to a greater extent than would characteristics of adult cats. Alternatively, kittens may scratch and bite more because they are held or played with more frequently than older cats.
Cats implicated in cases of cat scratch disease do not appear ill, but the significant difference in seropositivity between patients' cats and control cats suggests that cats may become infected with R. henselae. This suggestion is supported by the recent isolation of R. henselae from blood from a sick cat15. The natural reservoir of this organism is otherwise unknown. If cats frequently have bacteremia due to R. henselae or other rochalimaea species, then contamination of bite wounds with saliva or other body fluids of cats could lead to direct transmission of the organism to humans.
Our study raises the possibility of a role for fleas in the transmission of cat scratch disease. Fleas are well-known vectors for several human and animal diseases16 and could be involved in transmission as biologic or mechanical vectors, or both. Fleas may, however, be markers for other risk factors for illness, such as poor general hygiene, exposure to other arthropods, or exposure to the outdoors.
The seasonality of cat scratch disease may be explained in part by the breeding patterns of cats and fleas. Female cats are polyestrous but usually become pregnant in the spring or early fall; gestation lasts about nine weeks, and weaning six to seven weeks. Thus, a cohort of kittens may become available for the transmission of the disease in late summer or midwinter. Flea breeding also peaks in the late summer,17 coinciding with an increase in the number of cases of cat scratch disease. Because kittens are indoors more frequently in winter than in summer, physical contact with them, and possibly transmission of the etiologic agent, is increased. There is, however, no similar incidence peak in the late winter or early spring.
Our results with the R. henselae-based serologic test, along with other reported results,10 provide further evidence that this test may be useful in diagnosing cat scratch disease. We found that it had a high sensitivity (84 percent) and specificity (96 percent). The apparently high proportion of asymptomatic family members with positive titers (18 percent) was similar to the proportion of asymptomatic family members with positive reactions to the skin-test preparation18. Although these reactions may represent false positive results, six of the family members with positive tests had symptoms consistent with cat scratch disease. It is possible that the other family members without classic symptoms of the disease had atypical or subclinical infections. Thus, the results of the indirect fluorescent-antibody test suggest that the spectrum of the disease may be broader than previously recognized.
Our data on the seroprevalence of R. henselae among cats showed a significant difference between patients' cats and control cats, but the limited number of control cats did not allow us to evaluate the effects of age and sex. These data do, however, suggest that cats may frequently be infected with rochalimaea or a related organism.
A number of different viruses,19,20 bacteria,21 and mycobacteria22 have been proposed as the etiologic agent of cat scratch disease. Recently, rochalimaea species have been detected with the skin-test antigen for the disease,23 and R. henselae has been isolated from two patients with clinical disease24. These data and the serologic data presented here suggest that R. henselae or a related organism has an etiologic role in cat scratch disease.
R. henselae is genetically similar to the Bartonellaceae family25,26. Bartonella bacilliformis is transmitted by the sandfly. The other rochalimaea species known to cause human disease, R. quintana (trench fever), is transmitted by lice. It has been suggested on the basis of two case reports that ticks play a part in R. henselae infection27. In our study, rochalimaea DNA was detected by polymerase chain reaction28 in collections of fleas obtained from two cats owned by one of the patients whose illness precipitated our investigation. This information, along with the findings of the case-control study, supports the possibility of a role for arthropods in cat scratch disease.
More than 27 million households in the United States (over 30 percent) have at least one cat29. If prospective surveillance data reveal that cat scratch disease is truly a common cause of chronic lymphadenopathy in children,30 preventive strategies may have a substantial impact on public health. The findings of this study are the first step in identifying specific risk factors for infection, which may lead to recommendations for prevention. This study clearly demonstrates the important role of traumatic contact with kittens (scratches or bites) in cat scratch disease, but further evaluation of the relation between this illness and arthropods (such as fleas and ticks) and kittens is needed. The serologic results support the hypothesis that R. henselae or a closely related organism has an etiologic role in this disorder. The indirect fluorescent-antibody test for antibody to R. henselae organisms appears to be a sensitive and specific diagnostic tool, which may greatly reduce the effort and expense often associated with the diagnosis of cat scratch disease.
Presented in part at the 32nd Interscience Conference on Antimicrobial Agents and Chemotherapy, Anaheim, Calif., October 11-14, 1992.
We are indebted to the participating physicians and veterinarians in Connecticut, to the staff at the epidemiology and laboratory divisions of the Connecticut Department of Health Services, and to Georgia Malcolm for their time and effort spent in this investigation.
Source Information
From the Meningitis and Special Pathogens Branch (K.M.Z., B.A.P., J.D.W.) and the Biostatistics and Information Management Branch (B.D.P.), Division of Bacterial and Mycotic Diseases, and the Viral and Rickettsial Zoonoses Branch, Division of Viral and Rickettsial Diseases (R.L.R.), National Center for Infectious Diseases, and the Epidemic Intelligence Service (K.M.Z.), Centers for Disease Control and Prevention, Atlanta; the Division of Field Services, Epidemiology Program Office, and the Epidemic Intelligence Service, Centers for Disease Control and Prevention, Hartford, Conn. (D.H.H.); and the Connecticut Department of Health Services, Bureau of Health Promotion, Epidemiology Section, Hartford (J.L.H., M.L.C.).
Address reprint requests to Dr. Zangwill at the Meningitis and Special Pathogens Branch, Division of Bacterial and Mycotic Diseases, Centers for Disease Control and Prevention, Mailstop C-09, 1600 Clifton Rd., Atlanta, GA 30333.
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