Factors Related to Missed Diagnosis of Incidental Scabies Infestations in Patients Admitted Through the Emergency Department to Inpatient Services

Ming-Yuan Hong, MD, Ching-Chi Lee, MD, Ming-Che Chuang, MD, Sheau-Chiou Chao, MD, Ming-Che Tsai, MD, and Chih-Hsien Chi, MD

Abstract
Objectives: Scabies is highly contagious and requires prompt diagnosis and implementation of infection control measures to prevent transmission and outbreaks. This study investigated the clinical and administrative correlates associated with missed diagnosis of scabies in an emergency department (ED). Methods: This was a retrospective study of patients with incidental scabies infestations who were admitted to a university hospital via the ED during a 4-year period. Results: A total of 135 inpatients were identied as having scabies; among them, 111 patients (82%) had visited the ED. Scabies were diagnosed during the ED stay in 39 of 111 patients (35%), while the diagnosis was missed in the ED in 72 patients (65%). Although no geographic clusters suggestive of nosocomial scabies transmission were registered, 160 medical workers and one hospitalized patient received prophylactic treatment due to direct skin-to-skin contact with inpatient scabies cases during the study period. Overcrowding (odds ratio [OR] = 8.4; 95% condence interval [CI] = 1.9 to 38.0) and time constraints (OR = 8.2; 95% CI = 1.9 to 34.7) in the ED were associated with a missed diagnosis of scabies during ED stay. Patients with lower illness severity scores were at higher risk for failure to diagnose and to treat scabies prior to hospital admission (OR = 5.7; 95% CI = 1.6 to 20.9). Conclusions: Missed diagnoses of scabies during ED stay may result in nosocomial spread and increase the unnecessary use of prophylactic treatments. ED overcrowding, time constraints, and less severe illness compromise ED recognition of scabies. Health care workers should be especially alert for signs of scabies infestations under these conditions. ACADEMIC EMERGENCY MEDICINE 2010; 17:958964 2010 by the Society for Academic Emergency Medicine Keywords: scabies, diagnosis, crowding, emergency department

cabies, caused by the mite Sarcoptes scabiei var. hominis, is highly contagious, and worldwide prevalence has reached an estimated 300 million individuals annually.1 Scabies is an important infectious skin disease in Taiwan, and surveys have revealed a prevalence of 1.4%.2 Scabies causes intensely pruritic eruptions at the affected sites and is transmitted by direct
From the Department of Emergency Medicine (MYH, CCL, MCC, MCT, CHC) and the Department of Dermatology (SCC), National Cheng-Kung University Hospital; and the Graduate Institute of Clinical Medicine, College of Medicine, National Cheng-Kung University (MYH, CCL), Tainan, Taiwan. Received November 1, 2010; revision received January 1, 2010; accepted January 1, 2010. Supervising Editor: Sandy Bogucki, MD, PhD. Address for correspondence and reprints: Chih-Hsien Chi, MD; e-mail: chich@mail.ncku.edu.tw.

contact. The prevalence in nursing home staff members is up to 10.7%, indicating that occupational contact with patients may be an important risk factor for scabies infestations.3 Scabies outbreaks have also been reported in various settings, including long-term care facilities and hospitals, and often originate with a single undiagnosed or incompletely treated case.410 Low awareness of and unfamiliarity with scabies among health care workers may delay diagnosis and infection control and are associated with considerable nancial and working burdens.6,11 Prompt clinical diagnosis and implementation of infection control measures are important to achieve effective treatment and avoid scabies outbreaks.1,5,6,12 The emergency department (ED) is a signicant point of admission for hospitalized patients. The ED is focused on rapid patient assessment, stabilization and decides on hospital admission or discharge based on

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2010 by the Society for Academic Emergency Medicine doi: 10.1111/j.1553-2712.2010.00811.x

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the patients medical condition. Consequently, the ED has rapid patient turnover and higher patient ow volume, both of which are considered risk factors for introduction of scabies to hospitals.4 Admitting patients with undiagnosed scabies increases the risk of nosocomial outbreaks.9 However, only limited data exist regarding how many diagnoses of scabies are missed in the ED. This study investigated clinical and administrative correlates for missed diagnosis of incidental scabies infection in the ED.1 METHODS Study Design This was a retrospective chart review of incidental scabies infestations in inpatients admitted via the ED between January 2003 and January 2007. The local institutional review board approved the study protocol. Study Setting and Population This study was conducted in a 1,080-bed tertiary medical center with approximately 65,000 annual ED visits. The hospital-based National Emergency Department Overcrowding Scale (NEDOCS) score (mean standard deviation [SD]) was 112 (19), and the ED length of stay (LOS) for inpatients was 14 (2) hours during the study period. Adult patients (aged 18 years and older) admitted to our hospital via the ED who were diagnosed with scabies infestations according to the International Classication of Disease, 9th version (ICD-9 133.0), and those who were prescribed topical gamma-benzene hexachloride at any time during their ED or in-hospital course, were identied via a computer-generated search. The search looked for two situations: medication orders and infection control investigations. Medication orders and triage times are automatically time-stamped in a computerized database and printed in the medical chart. ED discharge times are not automatically time-stamped; instead, nurses enter the ED discharge times when patients are transferred to inpatient wards. After patients are admitted to the ward services, the times that medications are ordered are recorded by nurses after the order is checked. In ED patients or inpatients who admit through the ED, scabies is diagnosed in two ways that include the presence of pathognomonic scabies lesions (the burrow sign) or the nding of S. scabiei adult mites, larvae, or eggs on a microscopic examination of skin scrapings. Infested patients and hospital workers with skin-toskin physical contact were treated simultaneously with topical gamma-benzene hexachloride. Infection control measures were carried out that included washing and bagging infested patients clothing and linens for at least 3 days and instituting contact isolation and barrier nursing procedures until scabies eradication was conrmed by a dermatologist.1 The hospital-based data were collected from infection control investigations of inpatients that ruled out the occurrence of geographic clusters suggestive of nosocomial scabies transmission and also from the hospital workers who received prophylactic treatment for scabies due to occupational contact.

Patients who were specically referred to the ED for presumed scabies, and whose chief complaints were found by the triage nurse to be consistent with scabies, were referred to the dermatology service and were excluded from this study. We excluded patients for whom scabies treatment was initiated more than 1 month after presentation to the ED, to distinguish scabies that was likely present on admission from infections that were more likely to have been acquired in the hospital.4 The patient ow algorithm is summarized in Figure 1. Study Protocol Data from medical records were collected, including demographic information, data on the timing of care (e.g., triage, medication order, and ED discharge times), comorbidities,13 clinical features (including distributions of skin rash), whether patients were residents of chronic care facilities, and laboratory data. The chart review followed published guidelines on retrospective chart review methods in emergency medicine to ensure accurate data abstraction and to limit the biases inherent to such studies.14 The ED LOS or total period until initiation of therapy was dened as the time period following triage time until ED discharge or medication order times. Patients with a history of cerebrovascular disorder, dementia, intracranial hemorrhage, or Parkinsonism were classied as having neurologic disability. If multiple values were available for laboratory data (e.g., leukocyte and eosinophil counts), the rst values obtained after arrival in the ED were used. Thirteen random charts (10%) were reviewed independently and completely. For the timing variables, and laboratory results recorded directly from the patient chart, there was 100% accuracy in chart abstraction. There was disagreement on the presence of neurologic disorder in two patients (j = 0.77). For the components of demographic distribution of scabies, there was 100% agreement (j = 1.0) on 12 of 14 components. Physiologic variables for the Rapid Acute Physiology Score (RAPS)15 were obtained from triage records. For the components of the RAPS, including pulse rate, blood pressure, respiratory rate, and Glasgow Coma Scale, there was 100% agreement (j = 1.0) on all components. The NEDOCS was administered on patient arrival at the ED, and the result was obtained from ED administration records.16 For NEDOCS values abstracted from administrative data, there was 100% agreement (j = 1.0). The patients who underwent therapy and infection control measures for scabies during their ED stays were classied as the ED-diagnosed group. Patients with a discharge diagnosis of scabies who did not undergo scabies treatment or initiation of infection control measures during their ED stay were sorted into the missed-diagnosis group. Four dichotomous variables were derived from these events. A severely overcrowded ED was dened as NEDOCS score exceeding 140 according to Weiss et al.,16 and the mean score plus 1 SD was approximately 140 in our hospital. We therefore chose a cutoff of 140 to represent ED congestion. The mean ED LOS for inpatients minus 1 SD was around 12 hours in our hospital, and the variable ED time constraints was dened as an

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Figure 1. Flow chart of a common pathway in the diagnosis and treatment of scabies infestations in the ED. *Infection control (IC) measures included 1) washing and bagging infested patients clothing and linens for at least 3 days and 2) instituting contact isolation and barrier nursing procedures until scabies eradication was conrmed by a dermatologist.

ED LOS that did not exceed 12 hours. The RAPS, a truncated version of the Acute Physiology and Chronic Health Evaluation (APACHE-II), was calculated on patient arrival to the ED in this investigation. A RAPS greater than or equal to 5 indicates a mortality rate over 20%,15,17 and such cases were at a higher risk of requiring critical care. Therefore, less severe illness was dened as RAPS less than 5. Eosinophilia was dened as blood eosinophil count exceeding 600 eosinophils per microliter.18 Data Analysis Statistical analyses were performed using the Statistical Package for Social Science for Windows (version 17.0, SPSS, Chicago, IL). Continuous variables, including age, total period of initial therapy for scabies following ED registration, and leukocyte counts, were expressed as mean (SD) and medians (interquartile range [IQR])

and were compared using Students t-tests. Categorical variables, including sex, presence of comorbidities, eosinophilia, resident status in a chronic care facility, overcrowded ED, ED time constraints, less severe illness, and skin distribution of scabies, were expressed as absolute number and percentage and were compared with the chi-square or Fishers exact tests. Variables with p-values less than 0.10 were processed using multivariate analysis with a stepwise backward elimination model. Interactions between variables with signicance (dened as p < 0.05) by multiple analysis were subsequently checked with a goodness-of-t test. RESULTS During the 4-year period, 135 patients were diagnosed with scabies infestations, and 111 of those were admitted to the hospital via the ED. The 111 patients enrolled

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in this study included 39 patients (35%) in the ED-diagnosed group and 72 patients (65%) in the missed-diagnosis group. The mean (SD) age of all patients was 73 (12) years. The sample contained 51 females (46%) and 60 males (54%). The most common comorbidities were neurologic disability (64%), hypertension (64%), and diabetes (43%). The site most commonly affected by scabies was the abdomen (57%), followed by the axillae (54%), nger webs (42%), and wrists (34%). Infection control investigations revealed that 161 persons received prophylactic topical gamma-benzene hexachloride treatment due to direct skin-to-skin contact with inpatient scabies cases during the study period, included 160 medical workers and one hospitalized patient. Five medical workers and the hospitalized patient reported pruritis, although scabies was not identied in the six symptomatic persons. No geographic clusters suggestive of nosocomial scabies transmission were registered, according to infection control investigations. Table 1 lists the results of our univariate analysis of demographic information, comorbidities, ED LOS, laboratory data, and the severity score between the two groups. The two groups did not differ signicantly in sex, age, comorbidities, or laboratory data. However, the ED-diagnosed group had a higher percentage of resident status in a chronic care facility, a lower percentage of overcrowded ED, fewer ED time constraints, less severe illness, and shorter total period to initiation of scabies therapy following ED registration than did the missed-diagnosis group. Table 2 lists the skin distributions of scabies infestations. The ED-diagnosed group contained a higher percentage of lesions involving the nger webs than the missed-diagnosis group did.

Table 3 lists the results of our multivariate analysis. Overcrowded ED, ED time constraints, and less severe illness were signicantly associated with missed diagnosis. No signicant interactions between ED time constraints, overcrowded ED, and less severe illness were noted; in other words, these three factors were independently associated with a delay in the diagnosis of scabies (p-value of each pair: ED time constraints vs. overcrowded ED, p = 0.874; overcrowded ED vs. less severe illness, p = 0.868; ED time constraints vs. less severe illness, p = 0.555). DISCUSSION The ED is an important route by which patients arrive at the hospital. However, the information on scabies in the ED population remains limited. This investigation is the rst to characterize the clinical features of scabies in the ED. In the study population, 82% of patients with scabies infestations were admitted via the ED, and missed diagnosis of scabies signicantly impeded prompt treatment and infectious control measures. While the gravity of the condition or apparent delays in its diagnosis would not generally incur severe clinical consequences, there are two compelling aspects of this study: 1) the potential implications of nosocomial infection of staff and other patients in the hospital if a common diagnosis is missed during ED evaluation and, 2) the possible relationship between both ED crowding and acuity of illness and the failure to diagnose and treat scabies prior to hospital admission. Scabies occasionally appears in atypical forms, including truncal distribution or nonpruritic dermatoses

Table 1 Demographic Data and Clinical Characteristics of Patients Diagnosed With Scabies in the ED (ED-diagnosed Group) and Outside the ED (Missed-diagnosis Group) Number of Cases (%) Clinical Variables Male Age (yr), mean SD Comorbidities Hypertension Neurologic disability Diabetes mellitus Laboratory data in ED Leukocyte counts (1000 mm3), mean SD Eosinophilia* Resident status in a chronic care facility Total period of initial therapy for scabies following ED registration (days), median (IQR) Overcrowded ED ED time constraints Less severe illness ED-diagnosed Group (n = 39) 19 (49) 73 13 28 (72) 24 (62) 14 (36) 14.6 5 34 1 7.1 (13) (87) (11) Missed-diagnosis Group (n = 72) 41 (57) 73 12 43 (60) 47 (65) 34 (47) 13.2 7 49 4 7.7 (10) (68) (211) p-value 0.431 0.961 0.222 0.836 0.317c 0.332 0.750 0.038a <0.001c 0.036a 0.007b 0.022a

4 (15) 7 (18) 19 (49)

18 (40) 32 (44) 52 (72)

IQR = interquartile range. a p < 0.05; bp < 0.01; cp < 0.001. *Eosinophilia is dened as blood eosinophil count exceeding 600 eosinophils per microliter. National Emergency Department Overcrowding Scale (NEDOCS) scores exceed 140, n=71. Length of ED stay is less than 12 hours. Rapid Acute Physiology Score (RAPS) is less than 5.

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Table 2 Difference in Skin Rash Distributions Between Patients Diagnosed in the ED (ED-diagnosed Group) and Outside the ED (Misseddiagnosis Group) Number of Cases (%) Distributions of Skin Rash Finger webs Wrists Elbows Axillae Knees Abdomen Buttock Typical sites ED-diagnosed Group (n = 39) 22 14 9 18 9 25 5 22 (56) (36) (23) (46) (23) (64) (13) (56) Missed-diagnosis Group (n = 72) 25 24 24 41 18 38 6 45 (35) (33) (33) (57) (25) (53) (8) (63) p-value 0.044* 0.836 0.285 0.322 1.000 0.317 0.513 0.549

*p < 0.05. Presence of visible lesions involving at least two typical sites for scabies, including nger webs, exor surfaces of the wrists and elbows, axillae, knees, external genitalia in males, and breasts in females.

Table 3 Risk Factors for Missed Scabies Diagnosis, Based on Multivariate Analysis Clinical Variables Overcrowded ED ED time constraints Less severely illness Skin rash with nger webs involvement Resident status in a chronic care facility OR 8.4 8.2 5.7 0.8 0.7 95% CI 1.938.0 1.934.7 1.620.9 0.22.7 0.22.8 p-value 0.005* 0.004* 0.009* 0.719 0.584

*p < 0.01. National Emergency Department Overcrowding Scale (NEDOCS) scores exceed 140. Length of ED stay is less than 12 hours. Rapid Acute Physiology Score (RAPS) is less than 5.

in elderly or institutionalized patients, which confounds the diagnosis and delays treatment.12,19,20 Our patients had atypical rash distributions, with the most commonly affected site being the abdomen, rather than the typical presentation at the nger webs or wrists. The diagnosis of scabies depends mainly on skin lesion history and distribution, and lesions most commonly occur in the nger webs, exor surfaces of the wrists and elbows, axillae, knees, external genitalia in males, and breasts in females.1,5,21 In a report from a region with a high prevalence of scabies (13%), skin presentation was a useful diagnostic tool for scabies infestations, and the presence of itching at two or more typical locations was 96% sensitive and 97% specic for scabies identication.21 However, only 60% of the cases in our study population had at least two typical sites of scabies infestations. The study patients were characterized by advanced age, and 75% were residents of chronic care facilities. These results are consistent with those reported in previous works, in that atypical features of skin rash distributions are occasionally seen in elderly or institutionalized patients. Unusual features of scabies infestations are commonly seen in institutionalized patients and may delay diagnosis and treatment.12,19 However, most patients (87%) diagnosed in the ED in our investigation came from chronic care facilities, and the percentage of

residents of chronic care facilities was also higher in the ED-diagnosed group than in the missed-diagnosis group. One possible explanation for this nding is the high prevalence of scabies in patients from chronic care facilities (3.3% in one study22), so perhaps health care workers maintained high alertness for scabies and instituted early investigations in patients from chronic care facilities. In general, physicians may diagnose scabies in patients with typical or obvious rashes, while ignoring atypical or obscure lesions. The percentage of typical presentations with nger web involvement was higher in the ED-diagnosed group than in the missed-diagnosis group in our investigation. The classic demographic presentations and distributions of scabies are well known.1 During visits by medical staff, a patient with skin lesions that involved the nger webs generally triggered scabies screening and further evaluation of the skin lesion facilitated early recognition of scabies. Additionally, the supercial veins of the dorsal hands are commonly used for intravascular access. When preparing the skin prior to venous catheterization, medical staff thoroughly examined the hands, even during resuscitation, thus prompting the diagnosis of scabies in the ED. The RAPS was used as a simple measure of initial patient care.15,17 The physical scoring system (the

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APACHE-II) scoring is not done very well in the ED, particularly early in the ED stay.23 Nguyen et al.23 also suggested that nontraditional use of APACHE-II may not accurately describe disease severity in the preintensive care unit period and should be recalibrated to include physiologic parameters during the ED stay. To evaluate the acuity of illness in our ED-based population, we used the RAPS system. Less severely ill patients with lower RAPS severity scores on ED arrival exhibited higher risk of a missed scabies diagnosis. This may be explained intuitively from a patient-care perspective. For more severely ill patients, evaluation and treatment should be prioritized, and a more detailed history-taking and physical examination is conducted for such patients, perhaps facilitating the diagnosis of scabies.6,11,12 Similarly, a delay has been shown in providing antibiotics for patients with pneumonia: in one study, patients who were less ill or had atypical presentations were at higher risk of delayed antibiotic administration.24 In the ED-diagnosed group, 68% of patients were diagnosed with scabies within the rst 8 hours of arrival at ED. This suggests that the medical staff tended to diagnose scabies during their initial evaluation. The initial level of ED congestion inuenced the diagnosis rate, making the initial NEDOCS score particularly important for diagnosing scabies. In the overcrowded ED, it was difcult for medical staff to remain alert to the possibility of scabies. ED crowding is a serious problem globally, including in Taiwan, and may inuence clinical care and performance.2527 Excessive workloads in overcrowded EDs have been recognized as contributing to delayed and missed diagnoses, which may threaten public health by compromising patient safety.26,28,29 Weiss et al.3033 modied the NEDOCS model to estimate the severity of ED crowding and established a scale for forecasting ED overcrowding that predicted the rate of patients leaving the ED without being seen. A NEDOCS score over 140 indicates severe ED overcrowding and contributed to missed diagnosis of scabies in our investigation. This nding is consistent with previous works suggesting that ED overcrowding may affect clinical care and performance of health care workers.2527,34 In addition to combating overcrowding through administrative and political channels, medical staff must also be aware that overcrowding in the ED may compromise clinical performance and should therefore increase their alertness during times of ED congestion. The low percentage of scabies identication may in part have resulted from the ED pathway in our hospital. Patients complaining chiey of dermatologic disorders, including skin pruritis or rash, are transferred to dermatologists by the triage nurse and were excluded from this study. Because of this pathway for diagnosis and treatment of scabies infestations in our ED, it is understandable that scabies in a patient with other complaints not involving skin problems might have been overlooked. It is possible that medical staff tend to focus on major patient complaints while ignoring infectious diseases, which might lead to nosocomial spread. Scabies may present atypically in physically incapacitated, immunocompromised, or institutionalized persons and is also associated with developmental delay, Downs syndrome, and neurologic disorders.12,3537

Maintaining a high threshold of suspicion in high-risk patients and instituting screening of suspicious skin lesions may be of great assistance in preventing missed diagnosis and outbreaks. Therefore, to improve detection of scabies, EDs should consider strategies for detecting infested patients early, possibly utilizing early screening of high-risk patients in EDs. LIMITATIONS This investigation was conducted at a single center, and the results are not necessarily applicable to other institutions with different settings or with patients with different level of illness severity. Another important limitation is the possibility of misclassication bias. If the diagnosis of scabies was not coded, the patient was not identied for study inclusion. To minimize this bias, we also performed a hospital-based search for patients who had been prescribed topical gamma-benzene hexachloride during the study period. These medical charts were reviewed using the same protocol as for patients with the code for scabies (ICD-9 133.0). Because this was a retrospective study, chart-based documentation was limited, and certain factors related to scabies infestations could not be measured, including type of skin presentation, presence of skin pruritis, cluster infestations, history of scabies exposure, socioeconomic status, and likelihood of transmission to hospital personnel. The limited records for diagnostic factors associated with scabies suggest that medical staff did not initially suspect scabies when seeing patients. The number of cases with occupational exposure to scabies obtained from hospital-based investigations may be underestimated. Staff who went to outpatient clinics or even other hospitals to receive treatment for scabies were not included in the investigation. The potential implications of missing incidental scabies that we have identied here may be just the tip of the iceberg. CONCLUSIONS This study emphasizes the pivotal role of ED evaluation to make a common diagnosis and the potential implications of missing the diagnosis. Missed diagnosis of incidental scabies infestations in patients admitted via the ED to inpatient services was not uncommon, and overcrowding and time constraints in the ED were associated with missed diagnoses. Lower illness severity scores were also associated with failure to diagnose and treat scabies prior to hospital admission. These ndings suggest that health care workers should be particularly vigilant in similar situations and that early scabies screening in high-risk patients may be appropriate.
The authors thank Shang-Chi Lee, MSc, Research Center of Clinical Medicine, National Cheng Kung University Hospital, for her valuable comments on the statistical analysis in the manuscript.

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