J Community Health DOI 10.1007/s10900-014-9940-9

ORIGINAL PAPER

Provider Knowledge, Attitudes, and Practices Regarding Lyme Disease in Arkansas Dana Hill • Talmage Holmes

 Springer Science+Business Media New York 2014

Abstract Lyme disease (LD), a vector-borne disease, causes illness for many individuals in the United States. All of the conditions for the promulgation of LD are present in one Southern state in the United States; yet this state reports lower numbers of LD than adjacent states. The purpose of this study was to determine associations between this Southern state’s primary care providers’ knowledge and attitudes regarding the diagnosis and reporting of LD. A quantitative, cross-sectional study was conducted via a mailed questionnaire by the Arkansas Department of Health to 2,693 primary care providers. Respondents were 660 primary care providers from all regions of this state. Secondary data were analyzed using descriptive, Chi square, and logistic regression techniques. Analysis results included the following: a correct response rate of 59.1 % for symptom recognition, of 46.2 % for knowledge of recommended testing processes, and of 78.9 % for knowing LD is a reportable disease. These results compared to the expected norm were significant in every area with p values of .000. Specialty, region, and years of practice were found to be confounding influences in a number of assessment areas. Keywords Lyme disease
Vector-borne disease
Knowledge and attitudes regarding Lyme disease
Lyme disease testing D. Hill (&) Faculty MSN Nursing Programs, Western Governors University, 4001 S 700 E #700, Salt Lake City, UT 84107, USA e-mail: [email protected] T. Holmes Infectious Diseases Division, Illinois Department of Public Health, 525 W. Jefferson St., Springfield, IL 62761, USA e-mail: [email protected]

Introduction The zoonotic vector-borne disease, Lyme disease (LD), has caused debilitating illness in children and adults in the United States, Europe, and Asia for decades [1, 2]. All ages and genders are affected by LD; however, the most commonly reported cases of LD in the United States, from 2001 to 2010, were 5- to 9-year old males [3]. Emergence of this disease is not new; nevertheless, LD has become more frequently reported in recent years [1]. Disease burden has increased as known cases have reached the hundreds of thousands in probable and confirmed cases over the past 10 years [1, 4]. Over 20,000 cases of LD are reported to the CDC annually; but, Arkansas has reported only four cases of LD from 2002 to 2011 [5, 6]. Adjacent states, hosting similar terrain, climates, vegetation, animal populations, and seasonality report significantly higher numbers of LD cases to the CDC every year [6]. A minimal number of studies in the United States, and no known studies in Arkansas, have been published regarding knowledge, attitudes, and practices of physicians regarding LD surveillance; diagnosis; reporting; and treatment. Providers were found to be diagnosing LD at a 40 times greater rate than the reported case rates, and out of 262 cases, physicians chose to conduct serological testing on approximately half (132) of those cases as noted by Boltri et al. [7]. Magri et al. [8] found that physicians in New Hampshire were noted to have a good knowledge base regarding LD, but did not comprehensively understand diagnostic criteria or appropriate testing practices. A more recent study regarding provider knowledge, attitudes, and practices was conducted in British Columbia. Henry, Crabtree, Roth, Blackman, and Morshed (2012) used a survey tool to collect data from physicians in British Columbia (BC) to obtain information regarding physicians’

123

J Community Health

knowledgeable about LD and comfort in treating LD [9]. Henry et al. concluded that physicians in BC were knowledgeable about LD and were comfortable with treatment practices; however, education was needed regarding the awareness of erythema migrans (EM) rash as diagnostic of LD [9]. A study of Arkansas providers’ awareness of surveillance techniques and diagnosis of LD was relevant to understanding the effect of knowledge and attitudes regarding the diagnostic and reporting practices of LD in Arkansas. Understanding the true incidence of LD throughout the world is complicated by multiple factors. The case definition has become more complex as more knowledge has been gained regarding disease symptom expression and testing specificity and validity [10]. Specificity of testing, complexity of required testing, and the absence of laboratory markers early in LD onset also contribute to inadequate diagnosis of LD, thus affecting LD incidence [11, 12]. The deficient knowledge of LD incidence rates may also be attributed to misdiagnosis of symptoms or the lack of recognition of late development of symptoms by providers [13, 14]. Some beliefs regarding the minimal presence of ticks infected with B. burgdorferi or the absence of competent reservoirs for Ixodes ticks may influence attitudes about LD and subsequently affect the numbers of persons diagnosed with LD [15–17]. Other issues potentially affecting attitudes and practices regarding LD diagnosis include differences in host ecology [18, 19], climate of some areas [17, 20, 21], varying human contacts and behaviors [17, 18], genetic strain variation [17, 22], and, reporting inconsistencies [5]. The purpose of this study was to compare the knowledge and attitudes to the practice for diagnosing and reporting LD for primary care providers in Arkansas. A need for such a study was established through the observance of various views among the scientific community and because reported incidences of LD in Arkansas are low compared to adjacent states. The Arkansas Department of Health (ADH) receives numerous LD reports from providers indicating their belief of positive results from testing; however, test results are not indicative of adherence to recommended testing protocols and cannot be considered as truly positive [10; ADH staff, personal communications, January, 2012]. The one-type testing used by Arkansas providers as a positive test does not coincide with the two-tier testing recommended by the CDC [10]. There also is no indication, per the present reporting mechanism, of presentation of symptoms, exposure, or other information relevant for diagnosing LD [23; ADH staff, personal communications, January, 2012]. The lack of presentation of test results per current recommendations or other information regarding differential diagnostic techniques, via LD reports, makes it difficult to ascertain Arkansas providers’ LD knowledge,

123

attitudes, and beliefs. To obtain insight into the knowledge, attitudes, and practices of Arkansas providers regarding LD diagnosis and reporting, a questionnaire was distributed by ADH and secondary data were used for analysis of the survey. This article offers some background information; the problem prompting the study; analysis of the data; and resulting recommendations.

Background Numerous persons in the United States are burdened with LD; however, Arkansas has reported low rates of the population with LD [4]. The CDC recognizes the complexity and limitations of surveillance and attributes it to three aspects: underreporting and over diagnosis of cases, significant variation and differences among states for testing and reporting practices, and incomplete observation or nonvalidation of clinical symptoms. Additionally, the burden of surveillance with increases in desired laboratory confirmation and the complexity of testing have potentially reduced the number of cases identified; yet, no evidence has been presented demonstrating a decreased incidence of LD [5]. Diagnosis of LD may be affected by the many controversial beliefs including the following: host absence and competence, infected tick presence, presence of other similar tick-borne diseases which complicate diagnosis, and issues surrounding recommended testing protocols. Researchers have revealed that some of these contentious beliefs are present in Arkansas. For instance, all factors for the development of the vectors for transmission (ticks) and the transmission of B. burgdorferi are present in Arkansas; however, Arkansas is not considered to be endemic for LD [5, 16]. Patil et al. (2010) stated, ‘‘Lyme disease is not endemic in Arkansas, and testing for Borrelia burgdorferi can lead to clinical confusion, unnecessary treatment and excess cost’’ (p. 186). Patil et al. also claimed that the ticks feed on lizards in Arkansas, rather than white footed mice, which are believed to be superior competent reservoirs for LD. Also, due to the similarities in symptoms of LD and Southern Tick Associated Rash Illness (STARI), accuracy of diagnosing LD is believed to be challenging and may lead to misdiagnosis [16, 24]. Despite these findings, some of the medical community in Arkansas has continued to test patients for the presence of this disease. Positivity for the presence of B. burgdorferi in enzyme immunoassay (EIA) screening and positive reactions to significant kDa bands in IgM western blot testing have been demonstrated in one-type testing conducted and reported to ADH from the medical community in Arkansas [ADH staff, personal communications, January, 2012]. The one-type testing conducted by Arkansas providers does not coincide with

J Community Health

the current two-tier testing recommended by CDC [10] and as is presented in the most recent case definition for LD. Arkansas providers may fall within the CDC’s recognized complexity and limitation issues surrounding diagnosis and reporting of LD. It is unknown if the diagnostic and reporting practices regarding LD by Arkansas providers are affected by controversial beliefs in the scientific community or by knowledge and attitudes. The Problem In recent years, much controversy has arisen regarding the presence of LD in Arkansas and the absence of competent reservoirs [16, 25]. However, numerous persons in Arkansas seek medical attention annually for the occurrence of symptoms resembling that of LD [ADH staff, personal communications, January, 2012]. Arkansas providers report positive test results to ADH, but test results do not indicate understanding of current testing recommendations which require further testing including two tier testing of performing an ELISA first, followed by IgM and IgG western blot [26; D. Haselow, personal communication, January 11, 2013]. The ADH conducted a review of 75 reports from June 25, 2012 through August 16, 2012, received by the ADH of persons tested for LD, and found incomplete testing, inappropriate testing, and inconsistent reporting [23; ADH staff, personal communications, January, 2012]. LD was reported as positive following screenings alone, Western immunoblot testing with both IgG and IgM or IgM alone, and Western immunoblot not specified. Testing was reported in multiple ways with variations in screenings and Western immunoblot, but was performed more frequently using IgM Western immunoblot testing only. Of all of the reports reviewed, only three performed the screening test followed by appropriate IgG and IgM Western immunoblot testing. In these 75 reports, there was incomplete testing and reporting of reactions and inappropriate testing (lack of second confirmatory test), possibly affecting the diagnosis of LD and subsequent treatment. Reporting consisted of only serological results and did not disclose information regarding symptoms, history, physician confirmation of positivity for LD, or treatment, if given, as ADH reporting requirements do not include descriptive patient information regarding symptoms or history [23]. Review of test results reported gave insight to the potential for true positive tests, indicating the potential for Arkansas to join the list of states with endemic LD [ADH staff, personal communications, January, 2012]. Furthermore, case definitions have changed over the past 12 years, creating the potential for a lack of knowledge among Arkansas providers regarding current recommendations for surveillance, diagnosis, and reporting [10, 27]. Additionally, debates have been presented regarding many

factors associated with LD potential in Arkansas, but most significantly surrounding competent reservoirs, creating the potential for variances in beliefs regarding LD and subsequent testing, diagnosis, and treatment of LD in Arkansas [16]. Due to the inconsistencies of testing and reporting practices, the changes in case definitions over recent years and the debatable factors associated with LD, the knowledge and attitudes of Arkansas providers regarding LD were not understood. Arkansas providers’ knowledge and attitudes may impact the practices of diagnosis, reporting, and treatment.

Methodology A cross-sectional, quantitative survey analysis was conducted, via the use of a survey tool, to determine knowledge and attitudes as they related to the practices of Arkansas primary care providers in the practice of diagnosing and reporting LD. Insight was also sought related to differences in practice for diagnosing and reporting LD between physician specialty groups, number of years in practice, and county of practice. Population The target population was providers in Arkansas including physicians (MD) who worked in the area of pediatrics, internal medicine, and family medicine/family practice/ general medicine. Approximate numbers of each of these providers was as follows: 500 pediatricians, 1,200 internal medicine specialists, and 1,300 family medicine/family practice/general medicine physicians. These provider names, specialization information, and mailing addresses were retrieved from the Arkansas Medical Board Association public search database. Search criteria for MDs included MD specified, specific specialty, any certification, any city, and any county in Arkansas. The entire population of providers (3,017) was included in the survey distribution. Analysis was conducted for all of the completed and returned surveys. Sample Size The survey was distributed to 3,017 primary care providers in Arkansas; however, the actual sample used for data analysis was a convenience sample of returned and completed questionnaires. An online sample size calculator from Raosoft, Inc. [28] was used to determine the most appropriate number of surveys for margin of errors of 1–5 %. A response distribution of 50 % was chosen for this calculation as, historically, response rates to a similar

123

J Community Health

survey were within the 30 % range [9]. Also, survey response rate as studied by Hager et al. [29] was considered adequate if responses reached the 50 % mark. According to Instructional Assessment Resources [30], a 50 % response rate for mailed surveys is considered to be adequate for acceptability, with 60 % being good, and 70 % or higher being very good. A population of 3,000 (for the approximate number of Arkansas primary care providers) was chosen with confidence levels (CL) of 90, 95, and 99 %. Recruitment of Participants The ADH recruited participants by sending a letter requesting participation. The letter included an explanation of the survey intent, a paper copy of the survey, a stamped and preaddressed envelope for survey return, an explanation of participation, and requested survey completion deadlines. Participation was voluntary; ADH de-identified the questionnaire answers to the participant to ensure anonymity. Each survey had a unique code to identify returned surveys for the purposes of sending a reminder letter and additional survey to accomplish receipt of the largest number of surveys possible. The code was used only for mailing purposes and was not included in data analysis or for any other purposes. Descriptive demographic information included practice specialty, number of years in practice, and the county of practice. Questions regarding physician practice did not include any patient identification information; therefore, no personal information was collected for either the provider or their patients. Survey Period Participants were asked by ADH to complete a four-page survey via hard copy within 6 weeks of receipt of the request. Reminder letters and an additional survey were sent via mail by ADH to providers who had not completed the questionnaire within 2 weeks after the first distribution of the survey and again prior to the participation deadline to primary care providers who had not returned a survey. Aggregated data from the survey were analyzed using SPSS. Survey Information The survey instrument used for this study had been previously validated and used for two similar studies regarding physician knowledge, beliefs, and practices. A survey using this tool was first conducted in a cross-sectional survey method in New Hampshire. The tool was developed as a four-page, 21-item questionnaire and was tested prior to use [8]. The instrument was again used for a study of

123

physicians in British Columbia after modifications were made to remove a question about vaccination and to add questions to collect data regarding geographical risk [9]. Modifications resulted in a change in the number of items in the instrument to 23-items rather than 21-items [9]. Modifications made by ADH to the survey tool did not change the number of questions. The purpose of modification by ADH was to disallow extraneous data collection not needed for the focus in the areas of knowledge and attitudes potentially affecting diagnosis and reporting of LD in Arkansas. Validity of the survey was not affected as any modifications to the questions. A pilot test of the survey was conducted by a small group of ADH-employed physicians. The questionnaire was also reviewed by the ADH Science Advisory Committee and approval was sought for survey distribution before any surveys were distributed. Questions specifically mentioning area of study were changed from British Columbia to Arkansas and the date of data collection was changed from 2007 to 2012.

Findings and Discussion Response Out of the 3,017 questionnaires mailed, the number of returned surveys was 984 (32.6 %): four were returned blank (0.1 %), 222 (7.3 %) responders indicated they did not work in clinical practices and 98 (3.2 %) were undeliverable. The undeliverable surveys, blank surveys, and those indicating not working in clinical practice were excluded from the numerator and denominator, leaving a total of 2,693 possible participants. The remaining 660 returned completed surveys resulted in a response rate of 24.5 % (660/2,693). All completed and partially completed surveys were included in the data base. Surveys were distributed to primary care providers throughout Arkansas. Participants indicated the county of their practice; however, for analysis purposes, regions of practice for the state were determined by the county of practice. The ADH has divided the state into five regions: Northwest, Northeast, Central, Southwest, and, Southeast. The percentage of distribution for the 2,693 possible participants was as follows: 799 (29.7 %) to the Northwest region, 411 (15.3 %) to the Northeast region, 1,153 (42.8 %) to the Central region, 170 (6.3 %) to the Southwest region and 160 (5.9 %) to the Southeast region. Returned surveys used for analysis represented practicing primary care providers in all regions and were equivalent to distributed surveys. Surveys returned from primary care providers for each region were as follows: 181 (27.4 %) from the Northwest region, 112 (16.9 %) from the Northeast region, 263 (39.8 %) from the Central region, 62

J Community Health

(9.4 %) from the Southwest region and, 33 (5.0 %) from the Southeast region. Survey respondents indicated specialty of practice as follows: Family practice, 314 (47.6 %); Pediatrics, 117 (17.7 %); Internal medicine, 126 (19.1 %); and other 103 (15.6 %). All participants in the category indicated as other also had a credential of Internal medicine. The combination of other and Internal medicine equaled a response rate of 229 (34.7 %). The response rate from participants regarding specialty of practice mimicked the percentages as distributed for each specialty. Distribution included 1,242 (46.1 %) to family practice providers, 475 (17.6 %) to pediatricians, and 976 (36.2 %) to providers in internal medicine. Respondents’ years of practice ranged from less than 1–60 years, with a mean of 20.59. Over 75 % of the participants’ years of practice fell within the less than 1–30 year range for number of years in practice. Participants represented all regions and multiple disciplines. Survey participation was representative of the geographical boundaries and practice specialties of the intended population, but is not generalizable to the entire cohort.

practice characteristics indicated the patient brought up the possibility of LD (52.3 %); treatment was initiated when LD was not believed to be present (39.6 %); and LD would be reported to ADH if suspected (78.2 %). Chi square analysis was used to determine if differences were noted in the knowledge and practices of Arkansas primary care providers regarding the practice of LD diagnosis and reporting. Significant differences were noted for each question as indicated by wide ranges in percentages of correctly answered questions and p values of .000. Confounders were also noted for specialty of practice, years in practice, and years of practice as determined by logistic regression analysis. Examples of the confounders noted were: •

•

Analysis Descriptive analysis of each question in the survey was performed to determine the knowledge and attitudes of Arkansas primary care providers as they relate to the practices of diagnosis and reporting of LD. Questions on the survey in the knowledge categories were written with the option to choose ‘‘do not know’’; however, some participants did not answer the questions. Only two questions allowed for multiple answers. If participants chose more than one answer on single answer questions, that answer was considered as invalid. In addition to aggregate analysis, a selection was made of the data to include all of the correctly answered questions per respondent for knowledge regarding symptoms, testing, and reporting to determine what proportion of respondents correctly answered all of these questions. Many respondents answered several questions correctly; however, out of 660 respondents, only one respondent answered all of these questions correctly or 0.15 %. The answers to questions regarding knowledge of symptoms ranged from 17.9 % (as indicated by answering the question correctly) to 96.0 % (Table 1). Percentages of correct answers for LD testing ranged from 18.4 to 61.7 % (Table 2). In addition to lesser knowledge noted for symptoms and testing, the perception of unreliable tests and whether or not LD is endemic to Arkansas was notable as both of these beliefs were 51.8 %. Answers to questions regarding

•

Odd ratios were higher for incorrect responses for all specialties with the symptom of third degree heart block as noted by significant p values of .000–.007. Odds of incorrectly responding to the recognition of this symptom were 3.252 times greater for family medicine providers and 1.999 times greater for pediatricians. Years in practice was a confounding variable identified for responses to the assessment of performing additional tests if the first test for LD was positive as noted with an odds ratio of 0.875. Assessment of the responses regarding the symptom of radioculoneuropathy revealed confounding in both family medicine and for providers in the Northwest region of the state. Respondents in the specialty of family medicine were 1.594 times more likely to incorrectly respond to the recognition of radioculoneuropathy as a symptom of LD. Respondents from the Northwest region of the state were 0.388 times more likely to incorrectly answer this assessment.

Limitations Prior to the initiation of the study, potential limitations were recognized as dependency of completion of the survey by an adequate number of respondents who represented the entire cohort, the potential for recall bias, and social desirability bias. Actual limitations were similar to expected limitations. Questionnaires were either fully or partially completed by 660 participants out of 2,693 possible participants. A greater number of responses may have better represented the cohort; however, analysis of survey returns revealed ratio proportionate representation of primary care providers per specialty of practice and region of practice. The number of respondents did not equal the number of possible respondents; however, similarities were noted in the distribution of surveys to specialty of practice

123

J Community Health Table 1 Assessment of knowledge of symptoms of LD

EM erythema migrans rash; HB heart block; HD heart disease

Symptom

Correctly answered (%)

Unanswered (%)

EM occurs in \60 %

False

147 (22.3)

2 (.3)

EM is sufficient for diagnosis

True

116 (25.4)

2 (.3)

Incubation period of LD

3–30 days

490 (76.3)

17 (2.6)

Invalid (%)

1 (0.2)

Fever is a symptom

Yes

621 (96.0)

13 (2.0)

3rd degree HB is a symptom

Yes

420 (66.9)

30 (4.5)

2 (0.4)

Valvular HD is a symptom

No

257 (42.8)

58 (8.8)

1 (0.2)

Meningitis is a symptom

Yes

476 (75.3)

27 (4.1)

1 (0.2)

Diarrhea is a symptom

No

267 (44.9)

65 (9.8)

1 (0.2) 3 (0.6)

Radiculoneuropathy is a symptom

Yes

493 (79.8)

41 (6.2)

Arthritis is a symptom

Yes

620 (96.0)

14 (2.1)

Goiter is a symptom Other diseases by black-legged ticks

No Anaplasmosis

392 (66.0) 97 (17.9)

66 (10.0) 25 (3.8)

and region of practice and the proportion of returned surveys for both of these indices. Therefore, results may or may not be generalizable to the primary care providers who did not participate in the study, but are generalizable to those who did participate in the study. The biases of recall and social desirability were minimized due to the construction of the survey (requesting current knowledge) and the aggregate data collection.

Recommendations Primary care providers’ lesser knowledge of LD, as compared to the currently accepted evidence-based standards of knowledge, revealed an opportunity for education related to basic understanding of LD transmission, LD symptoms, evidentiary diagnostic tools, and required reporting practices. For reasons of privacy and anonymity, respondents were not asked for information regarding where they received medical education or what type of education they received regarding LD. However, some participants indicated instruction from professors at the University of Arkansas for Medical Sciences regarding the nonexistence of LD in Arkansas. Many of the primary care providers in Arkansas may have attended this university as it is the only educational institution in Arkansas for medical practice. For future studies, it would be helpful to have this type of information so that education might be tailored more specifically for providers. Primary care providers should have the opportunity to have frequent updates from current literature regarding LD. The need for immediate education also became apparent as providers not only incorrectly answered survey questions, but a large proportion answered not knowing the answer (not sure, do not know) or did not mark any answer

123

Correct answer

93 (14.3)

Table 2 Assessment of knowledge of testing for LD Testing

Correct answer

Correctly answered (%)

Unanswered (%)

Invalid (%)

When is testing appropriate?

Initial pres.

294 (47.0)

13 (2.0)

21 (21.4)

If the patient presents with EM and initial testing is negative, should they be retested in 2 weeks?

No

120 (18.4)

8 (1.2)

What is the first test to be performed?

ELISA

355 (55.2)

15 (2.3)

If ELISA is positive, should additional tests be performed?

Yes

397 (61.7)

17 (2.6)

What is the second test that should be performed if ELISA is positive?

WB IgG/ IgM

321 (48.6)

17 (2.6)

2 (0.4)

1 (0.2)

Initial pres initial presentation; WB western blot

at all to several survey questions. Only one respondent correctly answered all of the questions regarding LD diagnosis, symptoms, testing, and reporting. Current and evidence-based information about LD needs to be disseminated to all Arkansas primary care providers. A follow-up survey post education and monitoring of reported test results from suspected cases of LD may then be helpful in determining if the education disseminated was effective. Education delivered through various venues (conferences, presentations, and articles) could be beneficial for all

J Community Health

providers, but should be tailored for providers in family medicine as this group was identified as more likely to have a lessened awareness of symptoms related to LD. The lack of knowledge regarding LD and the comments on the survey by respondents led us to believe that LD may not be considered for diagnosis when it may actually be present, leading to events of under-diagnosis and underreporting. ADH entertained the possibility of conducting a study to physically test individuals presenting with any signs or symptoms of LD using the two-tier method for the purposes of identifying any cases of LD in the state. The CDC was approached for the possibility of helping to fund such a project and agreements were tentatively met. This type of study may be useful in helping to determine if LD does exist in Arkansas and if it is underreported. A challenge for this type of study would be involving primary care providers in being observant for potential LD infections and then referring the patients to the ADH for testing. Patients referred by primary care providers to ADH would also have to agree to participate and would have to comply with initial testing and then follow-up testing as indicated. Compensation may be necessary for participants for such as study and may not be financially feasible. Four providers mentioned that some physicians were over-diagnosing patients with LD. If these events are occurring, additional opportunities for study may include how providers are diagnosing patients without confirmatory lab results, why they are not reporting cases they have diagnosed, and if the treatment of LD is appropriate and adheres to current treatment protocols. Types of surveillance to answer these questions may include additional surveys, interviews, shadowing, requiring more information to be presented with preliminary tests, prescription monitoring (for medications prescribed for LD), or closer monitoring of tests performed within the state. To empower the community, a public service announcement regarding LD might also be considered for public health education for prevention measures and information regarding symptoms and questions to ask primary care providers. This type of empowerment of the community, in combination with education for the providers, could increase overall knowledge regarding LD.

Conclusion The participants indicated an opportunity to educate primary care providers in Arkansas, providing them with the tools needed to adequately and appropriately diagnose and report LD. Underreporting and under-diagnoses of LD is a probability as demonstrated by the inaccuracy and lesser knowledge involving LD than what is currently accepted as evidencebased standards of knowledge. Providing education and

support to primary care providers in Arkansas for diagnosing and reporting LD may change treatment and care of Arkansas and reduce the burdens associated with this disease as primary care providers would have the knowledge base to lead them to more appropriate and adequate diagnoses of LD and implementation of appropriate pharmaceutical interventions. Acknowledgments Thanks to the Arkansas Department of Health and Dr. Dirk Haselow, State Epidemiologist, who distributed the surveys and allowed for the research through a secondary data use agreement.

References 1. Griffin, D. (2007). Lyme disease. In K. Nelson & C. Williams (Eds.), Infectious disease epidemiology: Theory and practice (2nd ed., pp. 1063–1086). Sudbury, MA: Jones and Bartlett Publishers. 2. World Health Organization. (2013). Lyme borreliosis (lyme disease). Retrieved from http://www.who.int/ith/diseases/lyme/ en/index.html. 3. Centers for Disease Control and Prevention. (2012). Confirmed lyme disease cases by age and sex—United States, 2001–2010. Retrieved from http://www.cdc.gov/lyme/stats/chartstables/inci dencebyagesex.html. 4. Centers for Disease Control and Prevention. (2012). Lyme disease: Reported lyme disease cases by state, 2000–2010. Retrieved from http://www.cdc.gov/lyme/stats/chartstables/reportedcases_ statelocality.html. 5. Centers for Disease Control and Prevention. (2007). Lyme disease—United States, 2003–2005. Morbidity and Mortality Weekly Report, 56(23), 573–576. 6. Centers for Disease Control and Prevention. (2012). Lyme disease: Reported cases of lyme disease by year, United States, 2002–2011. Retrieved from http://www.cdc.gov/lyme/stats/chart stables/casesbyyear.html. 7. Boltri, J., Hash, R., & Vogel, R. (2002). Patterns of Lyme disease diagnosis and treatment by family physicians in a southeastern state. Journal of Community Health, 27(6), 395–402. 8. Magri, J., Johnson, M., Herring, T., & Greenblatt, J. (2002). Lyme disease knowledge, beliefs, and practices of New Hampshire primary care physicians. Journal of American Board of Family Medicine, 15(4), 277–284. 9. Henry, B., Crabtree, A., Roth, D., Blackman, D., & Morshed, M. (2012). Lyme disease: Knowledge, beliefs, and practices of physicians in a low-endemic area. Canadian Family Physician, 58, e289–e295. 10. Centers for Disease Control and Prevention. (2012). 2012 case definitions: Nationally notifiable conditions infectious and noninfectious case. Retrieved from http://wwwn.cdc.gov/nndss/docu ment/2012_Case%20Definitions.pdf. 11. Bhate, C., & Schwartz, R. (2011). Lyme disease: Part II. Management and prevention. Journal of American Academy of Dermatology, 64(4), 639–653. doi:10.1016/j.jaad.2010.03.047. 12. Stanek, G., Wormser, G., Gray, J., & Strle, F. (2012). Lyme borreliosis. The Lancet, 379, 461–473. doi:10.1016/501406736(11)60103-7. 13. Aucott, J., Seifter, A., & Rebman, A. (2012). Probable late lyme disease: A variant manifestation of untreated Borrelia burgdorferi infection. BMC Infectious Diseases, 12(173), 1–10. 14. Feder, H., Johnson, B., O’Connell, S., Shapiro, E., Steere, A., & Wormser, G. (2007). A critical appraisal of ‘‘chronic lyme disease’’. The New England Journal of Medicine, 357, 1422–1430.

123

J Community Health 15. Nadelman, R., & Wormser, G. (2007). Reinfection in patients with Lyme disease. Clinical Infectious Diseases, 45, 1032–1038. doi:10.1086/521256. 16. Patil, N., Baiola, R., Saccente, M., Vyas, K., & Bradsher, R. (2010). A clinical review of Lyme disease in Arkansas. The Journal of the Arkansas Medical Society, 106(8), 186–188. 17. Pepin, K., Eisen, R., Mead, P., Piesman, J., Fish, D., Hoen, A., et al. (2012). Geographic variation in the relationship between human lyme disease incidence and density of infected hostseeking Ixodes scapularis nymphs in the Eastern United States. The American Journal of Tropical Medicine and Hygiene, 86(6), 1062–1071. doi:10.4269/ajtmh/2012.11-0630. 18. Eisen, R., Piesman, J., Zielinski-Gutierrez, E., & Eisen, L. (2012). What do we need to know about disease ecology to prevent Lyme disease in the northeastern United States? Journal of Medical Entomology, 49(1), 11–22. 19. LoGiudice, K., Ostfeld, R., Schmidt, K. A., & Keesing, F. (2003). The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, 100(2), 567–571. doi:10.1073/ pnas.023733100. 20. Brownstein, J., Holford, T., & Fish, D. (2005). Effect of climate change on lyme disease risk in North America. EcoHealth, 1(2), 38–46. doi:10.1007/s10393-004-0139-x. 21. Subak, S. (2003). Effects of climate on variability in Lyme disease incidence in the Northeastern United States. American Journal of Epidemiology, 157, 531–538. 22. Singh, S., & Girschick, H. (2004). Lyme borreliosis: From infection to autoimmunity. Clinical Microbiology and Infection, 10, 598–614. doi:10.1111/j.1469-0691.2004.00895x.

123

23. Arkansas Department of Health. (2012). Instructions for reporting communicable diseases to the Arkansas Department of Health. Retrieved from http://www.healthy.arkansas.gov/programsServices/ epidemiology/Documents/ReportableDisease2004.pdf. 24. Philipp, M., Masters, E., Wormser, G., Hogrefe, W., & Martin, D. (2006). Serologic evaluation of patients from Missouri with erythema migrans-like skin lesions with the C6 lyme test. Clinical and Vaccine Immunology, 13(10), 1170–1171. doi:10.1128/ CVI.00238-06. 25. Wheeler, J. G., & Romero, J. R. (2012). Tick-related illnesses in Arkansas: Myths and management. Journal of Arkansas Medical Society, 108(12), 272–273. 26. Centers for Disease Control and Prevention. (2011). Lyme disease: Two-step laboratory testing process. Retrieved from http:// www.cdc.gov/lyme/diagnosistreatment/LabTest/TwoStep/. 27. Centers for Disease Control and Prevention. (1990). Case definitions for public health surveillance. Morbidity and Mortality Weekly Report, 39(RR-13), 1–50. Retrieved from ftp://cdc.gov/ pub/Publications/mmwr/rr/rr3913.pdf. 28. Raosoft, Inc. (2004). Sample size calculator. Retrieved from http://www.raosoft.com/samplesize.html. 29. Hager, M., Wilson, S., Pollak, T., & Rooney, P. (2003). Response rates for mail surveys of nonprofit organizations: A review and empirical test. Nonprofit and Voluntary Sector Quarterly, 32(2), 252–267. 30. Instructional Assessment Resources. (2007). Assess teaching: Response rates. Retrieved from http://www.utexas.edu/academic/ ctl/assessment/iar/teaching/gather/method/survey-Response.php.