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Hospital-based emergency department visits with herpetic gingivostomatitis in the United States
Vol. 113 No. 4 April 2012
Hospital-based emergency department visits with herpetic gingivostomatitis in the United States Satheesh Elangovan, BDS, DSc, DMSc,a Nadeem Y. Karimbux, DMD, MMSc,b Sreedevi Srinivasan, BDS, DSc,c Shankar R. Venugopalan, BDS, PhD,d Sridhar V.K. Eswaran, BDS, MS,e and Veerasathpurush Allareddy, BDS, MBA, MHA, MMSc, PhD,f Iowa City, Iowa, Boston, Massachusetts, and Houston, Texas UNIVERSITY OF IOWA, HARVARD SCHOOL OF DENTAL MEDICINE, TUFTS UNIVERSITY SCHOOL OF DENTAL MEDICINE, AND UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT HOUSTON
Objectives. The objectives of this study were to determine the number of hospital emergency department (ED) visits with a diagnosis of herpetic gingivostomatitis (HGS) for 2007 in the United States and to identify the possible comorbid conditions associated with HGS. Study Design. The Nationwide Emergency Department Sample for 2007 was used in this study. Patients who visited the ED with a diagnosis of HGS were selected. Estimates were projected to the national levels using the discharge weights. Presence of comorbid conditions in these patients was also analyzed. Results. A total of 23,124 patients had ED visits and received the diagnosis of HGS. Most of the patients were young females and those belonging to the lower socioeconomic strata. All patients with HGS also presented with comorbid conditions. Conclusions. Physicians should be trained to diagnose, manage, and refer common dental emergencies. In the long term, improving access to dental care for these patients is crucial to managing this problem. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:505-511)
The occurrence of human orofacial infections caused by herpes simplex virus (HSV) is extremely high and is prevalent worldwide.1,2 Type 1 HSV causes oral, facial, and ocular infections, whereas HSV type 2 typically causes genital lesions but is also implicated in some cases of oral infections.3 Herpetic gingivostomatits (HGS), the primary form of HSV-1 oral infection usually affects patients aged 6 months to 5 years and adolescents.4 Signs and symptoms of HGS include pain, fever, lymphadenopathy, irritability, malaise, and headache. Oral lesions present as vesicles on the tongue, buccal mucosa, and gingival that may rupture to become ulcers covered eventually by a yellowish-gray membrane.5,6 Because of the pain a
Assistant Professor, Department of Periodontics, University of Iowa. Assistant Dean for Dental Education and Director of Postdoctoral Periodontology Program, Harvard School of Dental Medicine. c Postdoctoral Orthodontics Resident, Tufts University School of Dental Medicine. d Postdoctoral Orthodontics Resident, Department of Developmental Biology, Harvard School of Dental Medicine. e Assistant Professor, Department of Periodontology, University of Texas Health Science Center at Houston. f Instructor and Director, Predoctoral Orthodontics Program, Department of Developmental Biology, Harvard School of Dental Medicine. Received for publication Aug 19, 2011; returned for revision Sep 21, 2011; accepted for publication Sep 23, 2011. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.oooo.2011.09.014 b
and discomfort associated with this condition, children tend to avoid eating or drinking, leading to severe dehydration.5 Apart from oral lesions, HSV-1 virus has also been cited as the causative agent for other diseases, such as viral encephalitis, lymphadenitis, and severe ocular lesions.7 Up to 90% of Americans exhibit serum antibodies (seropositive) to HSV-1.8 Although the exposure to HSV is extremely common, only a small percentage (⬃1%) of patients exhibit clinical manifestations.9 Epidemiologic studies further demonstrated that such factors as socioeconomic status had a significant effect on the seroprevalence of this condition. Patients in the lower socioeconomic strata were frequently found to be seropositive for HSV-1.10,11 Therefore, it is reasonable to state that owing to the high exposure of HSV in individuals having lower socioeconomic status, the prevalence of those individuals seeking hospital-based emergency department (ED) treatment could be significantly high. Several studies in the past investigated the seroprevalence of HSV-1 in various populations, but, to our knowledge, little is known about the emergency hospitalization of patients diagnosed with herpetic oral infections. The objectives of this study were twofold: to determine the number of hospital-based ED visits with a diagnosis of HGS for 2007, using a nationwide sample, and to identify the possible comorbid conditions associated with HGS.
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MATERIAL AND METHODS The Nationwide Emergency Department Sample (NEDS) for 2007 was used for the current study. The NEDS is one of the component databases of the Healthcare Cost and Utilization Project, which is under the purview of the Agency for Healthcare Research and Quality.12 The NEDS is drawn from a sample of 950 hospitals from 27 states in the United States and the unweighted sample provides emergency information on close to 25 million hospitalbased ED visits. The NEDS database has a weighting variable assigned to each visit that can be used to yield national estimates of all hospital-based ED visits occurring in the United States. It provides health care usage and outcomes information for both treatment and release ED visits, as well as information on hospital admissions that originate in the ED. The variables that are available in the NEDS database include age, gender, day of ED visit, diagnoses coded during ED visit and during hospitalization, procedures performed during ED visit and during hospitalization, disposition of patient following ED visit, median household income of patient’s residence based on the zip code income quartile, insurance status, ED charges, hospital region, and hospital location/teaching status. The NEDS database is available for public purchase from the Agency for Healthcare Research and Quality. The last author (V.A.) obtained the database following completion of a data user agreement. As per this agreement, any individual cell counts fewer than or equal to 10 visits cannot be reported so as to preserve patient confidentiality. Such low numbers are not reported in the current study in compliance with the data user agreement. For the current study, all hospital-based ED visits with International Classification of Diseases (ICD)9-CM diagnosis code for HGS (ICD-9-CM code of 054.2) in any of the diagnoses fields in the NEDS database were selected. The demographic and hospitalization characteristics of these visits were examined. The complex sampling frame design of the NEDS database was taken into consideration while calculating the national estimates. Each individual ED visit was used as the unit of analysis. The discharge weight variable assigned to each ED visit was used to project all estimates to nationwide levels. Descriptive statistics were used to summarize the data. Presence of comorbid conditions was identified by using the Clinical Classification Software codes, which group similar ICD9-CM diagnoses codes together. Clinical Classification Software codes in all the diagnoses fields were included. More than 200 comorbid conditions were examined. Only the most frequently prevalent comorbid
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conditions are reported in the current study. Estimates on all other comorbid conditions, including the Clinical Classification Software codes used, are available from the authors on request. All statistical analyses were conducted using SAS version 9.2 software (SAS Institute, Cary, NC).
RESULTS During 2007 in the United States, HGS was given as a diagnosis in a total of 23,124 ED visits. The demographic characteristics of these ED visits are summarized in Table I. The average age of the patients who visited the ED was 16 years. Close to 69.5% of all ED visits occurred in those 19 years and younger. Females accounted for 55.7% of all ED visits. Most of the ED visits (82.2%) were discharged routinely. Admission into the same hospital was required for 3575 (15.5%) ED visits. Discharge to a home health care facility was required for 261 ED visits (1.1%). Close to 38.5% of all ED visits occurred in those residing in geographic areas with median household income levels of less than $39,000, whereas 25.8% of all ED visits occurred in those residing in areas with household levels between $39,000 and $47,999. The primary payers for the ED visits were Medicaid (41.4% of all ED visits), Medicare (7.1%), private insurance plans (31.3%), and other insurance plans (3.6%). Uninsured comprised 16.5% of all ED visits. Most of the ED visits occurred in the South (39.5% of ED visits). The Midwest, Northeast, and Western regions accounted for 21.6%, 17.0%, and 21.9% of all ED visits, respectively. Metropolitan teaching hospitals treated 50.5% of all the ED visits, whereas metropolitan nonteaching and nonmetropolitan hospitals treated 35.1% and 14.3% of the ED visits, respectively. The presence of more than 200 comorbid conditions was examined in these ED visits. All patients had at least one comorbid condition. Only those conditions that were prevalent in at least 1% of those with HGS are reported in Table II. The prevalence estimates of comorbid conditions among those admitted into the same hospital following the ED visit are also provided in Table II. In summary, the 20 most frequently prevalent comorbid conditions in patients with HGS include fever of unknown origin (10.58% of all ED visits), fluid and electrolyte disorders (10.38%), upper respiratory infections (9.37%), otitis media and related conditions (4.32%), deficiency and other anemia (4.10%), screening and or history of mental health and substance abuse (3.90%), essential hypertension (3.90%), mycoses (3.82%), diseases of mouth (3.76%), gastrointestinal disorders (3.70%), asthma (3.50%), pneumonia (2.95%), urinary
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Table I. Characteristics of hospital-based emergency department visits with herpetic gingivostomatitis (n ⫽ 23,124) Characteristic Admission timing Disposition of patient from the ED
Gender Age, y
Median household income quartiles for patient’s ZIP code
Response Admission on Monday-Friday Admission on Saturday-Sunday Routine discharge Transfer to short-term facility Other transfers, including skilled nursing facility, intermediate care, and another type of facility Home health care Against medical advice Admitted as an inpatient to this hospital Died in ED Not admitted, destination unknown Male Female ⬍10 10-19 20-29 30-39 40-49 50-59 60-69 70-79 ⬎79 $1-$38,999 $39,000-$47,999 $48,000-$62,999
Insurance status
Hospital region
Hospital location and teaching status
$63,000 or more Medicare Medicaid Private, including HMO Uninsured Other Northeast Midwest South West Metropolitan nonteaching Metropolitan teaching Nonmetropolitan
Frequency* (%) 15,260 (66.0) 7846 (34.0) 18,998 (82.2) DS DS 261 (1.1) 26 (0.1) 3575 (15.5) DS 244 (1.1) 10,240 (44.3) 12,879 (55.7) 13,287 (57.5) 2774 (12) 2448 (10.6) 1305 (5.6) 1086 (4.7) 791 (3.4) 574 (2.5) 499 (2.2) 354 (1.5) 8579 (38.5) 5864 (25.8) 4912 (21.5) 3221 (14.1) 1638 (7.1) 9552 (41.4) 7224 (31.3) 3809 (16.5) 823 (3.6) 3922 (17) 5003 (21.6) 9132 (39.5) 5067 (21.9) 8123 (35.1) 11,684 (50.5) 3317 (14.3)
DS, discharge information suppressed because individual cell counts are ⱕ 10, as per the data user agreement with Agency for Healthcare Research and Quality, such low numbers cannot be reported; ED, emergency department; HMO, health maintenance organization. *All percentages are based on the total admission for respective category (i.e., all discharged and age groups). Individual cell counts may not add up to the global cell counts because of missing values.
tract infections (2.68%), skin and subcutaneous tissue infections (2.61%), allergic reactions (2.50%), septicemia (2.34%), esophageal disorders (2.18%), lower respiratory diseases (2.02%), diabetes mellitus without complications (1.92%), and bacterial infections (1.86%).
DISCUSSION The data presented in the current study include all patients presenting to the ED with HGS regardless if they were treated and released from the ED or admitted into the same hospital. Among these patients visiting the ED with HGS, 15.5% were admitted as inpatients into the same hospital.
Recent ED visit studies have concluded that patients belonging to the lower socioeconomic strata and those lacking insurance rely heavily on EDs for their dental needs.13 Earlier, using a nationwide sample, we identified that a substantial number of patients visited the ED with common dental ailments, such as dental caries14 and periodontal disease,15 as well as with acute dental conditions, such as pulpal and/or periapical pathologies.16 Hospitalization of a patient visiting an ED for dental needs was a common occurrence, resulting in the use of a significant amount of resources.14-16 Based on the prevalence of HSV-1 and HSV-2 infections, we hypothesize that there may be a higher incidence of ED visits by patients with herpetic infections belonging to
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Table II. Presence of concomitant comorbid conditions in patients visiting the emergency department with herpetic gingivostomatitis ED visits
Admitted into same hospital after ED visit
Comorbid condition
Frequency
Percentage of all ED visits (n ⫽ 23,124)
Frequency
Percentage of all ED visits that resulted in hospitalization (n ⫽ 3575)
Fever of unknown origin Fluid and electrolyte disorders Upper respiratory infections, including ● Acute sinusitis ● Acute pharyngitis ● Acute laryngitis and tracheitis ● Acute upper respiratory infections of multiple sites ● Chronic sinusitis Otitis media and related conditions Deficiency and other anemia Screening and history of mental health and substance abuse Essential hypertension Mycoses Diseases of mouth, excluding dental Gastrointestinal disorders, including ● Gastrointestinal mucositis ● Gastroenteritis and colitis caused by radiation ● Toxic gastroenteritis and colitis ● Functional digestive disorders ● Disorders of peritoneum ● Disorders of intestine ● Intestinal malabsorption ● Symptoms involving digestive system ● Symptoms involving abdomen and pelvis Asthma Pneumonia (except that caused by tuberculosis or sexually transmitted disease) Urinary tract infections Skin and subcutaneous tissue infections Allergic reactions Septicemia (except in labor) Esophageal disorders Lower respiratory disease ● Abscess of mediastinum ● Pulmonary congestion and hypostasis ● Postinflammatory pulmonary fibrosis ● Alveolar and parietoalveolar pneumonopathy ● Lung involvement in systemic sclerosis ● Lung involvement in other diseases ● Pulmonary eosinophilia ● Acute edema of lung ● Disorders of diaphragm ● Cyanosis ● Dyspnea and respiratory abnormalities ● Symptoms involving respiratory system Diabetes mellitus without complication Bacterial infection, unspecified site Mood disorders Diseases of white blood cells Chronic obstructive pulmonary disease and bronchiectasis Cardiac dysrhythmias Disorders of lipid metabolism Nutritional, endocrine, and metabolic disorders, including
2447 2400
10.8 10.4
286 1749
8.0 48.9
2166 999 948 902
9.4 4.3 4.1 3.9
314 116 919 419
8.8 3.2 25.7 11.7
901 884 869
3.9 3.8 3.8
582 622 181
16.3 17.4 5.1
855 810 683
3.7 3.5 3.0
610 309 638
17.1 8.6 17.8
619 604 577 540 504
2.7 2.6 2.5 2.3 2.2
494 239 195 540 406
13.8 6.7 5.4 15.1 11.4
467 444 429 415 408 393 391 389 378
2.0 1.9 1.9 1.8 1.8 1.7 1.7 1.7 1.6
206 297 369 325 397 307 356 333 325
5.8 8.3 10.3 9.1 11.1 8.6 9.9 9.3 9.1
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Table II. Continued ED visits
Comorbid condition Upper respiratory disease, including ● Nasal polyps ● Chronic pharyngitis and nasopharyngitis ● Chronic laryngitis and laryngotracheitis ● Allergic rhinitis ● Diseases of upper respiratory tract ● Diseases of trachea and bronchus—not classified ● Mediastinitis ● Diseases of mediastinum, not elsewhere classified ● Symptoms, such as voice disturbance Nervous system disorders Disorders of teeth and jaw Aftercare HIV infection Skin disorders Coagulation and hemorrhagic disorders Respiratory failure, insufficiency, arrest (adult) Acute and unspecified renal failure Coronary atherosclerosis and other heart disease Thyroid disorders Nausea and vomiting Lymphadenitis Connective tissue disease Leukemias Circulatory disease, including ● Peripheral vascular disease ● Polyarteritis nodosa and allied conditions ● Disorders of arteries and arterioles ● Disease of capillaries ● Hypotension Congestive heart failure, nonhypertensive Chronic renal failure Epilepsy, convulsions Headache, including migraine Nutritional deficiencies
Admitted into same hospital after ED visit
Frequency
Percentage of all ED visits (n ⫽ 23,124)
Frequency
Percentage of all ED visits that resulted in hospitalization (n ⫽ 3575)
350 344 325 325 320 308 295 288 286 284 282 270 259 258 256
1.5 1.5 1.4 1.4 1.4 1.3 1.3 1.3 1.2 1.2 1.2 1.2 1.1 1.1 1.1
61 266 70 142 248 99 272 283 281 231 230 87 40 141 235
1.7 7.4 1.9 4 6.9 2.8 7.6 7.9 7.9 6.5 6.4 2.4 1.1 3.9 6.6
256 253 248 246 239 234
1.1 1.0 1.0 1.0 1.0 1.0
200 240 248 131 80 234
5.6 6.7 6.9 3.7 2.2 6.5
the lower socioeconomic strata and by those lacking good insurance coverage; however, this needs further empiric support by future studies. The prevalence estimates presented in our study regarding the socioeconomic levels are too close to draw clinically meaningful conclusions regarding the definitive role of socioeconomic status on HSV infections. To our knowledge, this is the first descriptive study using the NEDS database to provide a nationwide estimate of ED visits with HGS in the United States. We found a total of 23,124 ED visits with a diagnosis of HGS, composed predominantly of young patients (19 years and younger). Most visits were made during weekdays. Our results indicate that slightly more females visited EDs with HGS. The authors were unable to obtain information regarding the type of drugs administered to these patients in an ED from the NEDS database but it was reported in a previous study that
children and adults with HGS visiting the ED were commonly prescribed acyclovir 15 mg/kg (5 times a day) and valacyclovir 1 g (twice a day for 5-7 days), respectively.17 Because of the rising number of patients with this condition visiting the ED, the same study also underscored the importance of training physicians to diagnose and treat this dental condition on an emergency basis.17 With respect to patients’ disposition from the ED following their visit, we found that most patients were routinely discharged. This study found that a subset of the population (n ⫽ 3575; 15.5%) who visited the ED with HGS were hospitalized. We also observed this trend with regard to other dental conditions.14-16 It is known from the literature that dehydration, a common symptom in patients with HGS (especially in younger patients), seemed to be the major factor favoring hospitalization, although we were unable to validate this
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information from our dataset.18 Approximately 10.4% of patients diagnosed with HGS had fluid and electrolyte disorders (Table II), possibly influencing the physician to hospitalize. From a recent report, it is clear that patients admitted for dehydration following HSV infection received intravenous fluids (20 mg/kg bolus).18 The presence of other comorbid conditions, such as fever, the severity of the HSV lesions, and the extraoral complications arising from HSV infection could have influenced the decision to hospitalize these patients. Our study shows that patients with an annual income of less than $39,000 visited the ED more frequently (⬃39%), a finding that is consistent with our previous studies.14-16 This observation is in agreement with the current evidence that the seroprevalence of HSV is higher in the population with lower socioeconomic status.10 Most patients who visited the ED were enrolled in the Medicaid program (41.1%), similar to our previously published studies, and agrees with a recent study that indicated that individuals with governmentsponsored insurance programs, such as Medicaid, visit the ED more often than others.14-16,19 Interestingly, a significant percentage of patients with private insurance coverage (31.3%) also visited the ED with HGS. Geographically, we found that patients from the South visited the ED more than those from the other parts of the country. Socioeconomic variations of the patient population and changes in the health care delivery system have been cited as causing drastic geographic variations in ED visits.20 The type of insurance available in a locality, and the number and size of hospitals are other potential factors that could influence the geographic variation in the prevalence of ED visits. It should be noted that NEDS, although a nationally representative database, includes ED visit sample data from only 27 states, which could affect the geographic distribution of the ED visits.12 A patient’s underlying systemic conditions can have a significant impact on the oral cavity and considerably influence the patient’s response to treatment.21 Immunocompromised individuals tend to develop HGS lesions that are more severe in nature and also exhibit poor healing response.22 It was also shown that these individuals tend to demonstrate lower response to the prescribed antiviral medications and also exhibit a higher chance of developing serious systemic complications.23 We looked for the presence of comorbid conditions in these patients. Our analysis revealed that in patients visiting the ED with HGS, most presented with fever of unknown origin (10.58%), fluid imbalance (10.38%), and upper respiratory infections (9.37%). We also observed that approximately 4.1% and 3.8% of patients were diagnosed with some form of anemia and mycosis, respectively.
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The findings of this study should be interpreted keeping the following issues in perspective. The ED visits reported in this study include visits in which a patient was given a primary or secondary diagnosis of HGS. Therefore, it is possible that some of the patients visited the ED primarily for a comorbid condition but HGS could have been an additional (secondary) diagnosis given after the clinical examination. It is also important to remember that we have no direct evidence to associate the comorbid conditions reported in these patients with HGS. Also, information is not available regarding the type of diagnostic tests used or treatment rendered during the visits as well during the follow-up care after an ED visit. Another inherent limitation with the data set is the possible misdiagnoses rendered by physicians who were seeing these patients during the ED visits. Furthermore, comorbid conditions are identified using ICD-9-CM diagnoses codes. It is not clear who coded the data into the hospital discharge databases. Consequently, the estimates presented in the current study could be subject to biases associated with inconsistencies in coding practices within and across hospitals in the United States. The results from this study, along with our previous studies focusing on other dental conditions, clearly demonstrate that a significant number of patients visited hospitals for their dental needs in 2007 and, as a result, significant resources were used. The results of this study are consistent with our previous observations that these patients usually have lower socioeconomic status; however, further empiric support is needed to draw definitive conclusions regarding the same. It is clear that physicians and other ED personnel should be trained to diagnose, manage, and refer common dental emergencies. On a long-term basis, improving access to dental care for these patients is crucial to overcome this problem. This study also emphasizes the importance of preventive programs, such as a “dental home” for children, which will allow for early intervention and prevention of common childhood oral infections, including herpes.24 REFERENCES 1. Whitley RJ, Roizman B. Herpes simplex virus infections. Lancet 2001;357:1513-8. 2. Siegel D, Golden E, Washington AE, Morse SA, Fullilove MT, Catania JA, et al. Prevalence and correlates of herpes simplex infections. The population-based AIDS in Multiethnic Neighborhoods Study. JAMA 1992;268:1702-8. 3. Miller CS, Redding SW. Diagnosis and management of orofacial herpes simplex virus infections. Dent Clin North Am 1992; 36:879-95. 4. Scully C. Orofacial herpes simplex virus infections: current concepts in the epidemiology, pathogenesis and treatment, and disorders in which the virus may be implicated. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1989;68:701-10.
OOOO Volume 113, Number 4 5. Huber MA. Herpes simplex type-1 virus infections. Quintessence Int 2003;34:453-67. 6. Eisen D. The clinical characteristics of intraoral herpes simplex virus infection in 52 immunocompetent patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:432-37. 7. Arduino PG, Porter SR. Herpes simplex virus type 1 infection: overview on relevant clinico-pathological features. J Oral Pathol Med 2008;37:107-21. 8. Regezi JA, Sciubba JJ. Vesiculo-bullous diseases. In: Oral pathology: clinical pathologic correlations. 2nd ed. Philadelphia: W. B. Saunders; 1993. p. 1–33. 9. Siegel MA. Diagnosis and management of recurrent herpes simplex infections. J Am Dent Assoc 2002;133:1245-49. 10. Corey L, Spear PG. Infections with herpes simplex viruses (1). N Engl J Med 1986;314:686-91. 11. Stock C, Guillén-Grima F, de Mendoza JH, Marin-Fernandez B, Aguinaga-Ontoso I, Krämer A. Risk factors of herpes simplex type 1 (HSV-1) infection and lifestyle factors associated with HSV-1 manifestations. Eur J Epidemiol 2001;17:885-90. 12. Agency for Healthcare Research and Quality. National ED sample database documentation. Available at: http://www.hcupus.ahrq.gov/nedsoverview.jsp. Accessed July 26, 2011. 13. Lewis C, Lynch H, Johnston B. Dental complaints in emergency departments: A national perspective. Ann Emerg Med 2003; 42:93-9. 14. Nalliah RP, Allareddy V, Elangovan S, Karimbux N, Allareddy V. Hospital-based emergency department visits attributed to dental caries in the United States in 2006. J Evid Based Dent Pract 2010;10:212-22. 15. Elangovan S, Nalliah R, Allareddy V, Karimbux NY, Allareddy V. Outcomes in patients visiting hospital emergency departments in the United States because of periodontal conditions. J Periodontol 2011;82:809-19.
ORIGINAL ARTICLE Elangovan et al. 511 16. Nalliah RP, Allareddy V, Elangovan S, Karimbux N, Lee MK, Gajendrareddy P, et al. Hospital emergency department visits attributed to pulpal and periapical disease in the United States in 2006. J Endod 2011;37:6-9. 17. Mell HK. Management of oral and genital herpes in the emergency department. Emerg Med Clin North Am 2008;26:457-73. 18. Amir J, Harel L, Smetana Z, Varsano I. The natural history of primary herpes simplex type 1 gingivostomatitis in children. Pediatr Dermatol 1999;16:259-63. 19. LaCalle E, Rabin E. Frequent users of emergency departments: the myths, the data, and the policy implications. Ann Emerg Med 2010;56:42-8. 20. Liu T, Sayre MR, Carleton SC. Emergency medical care: types, trends, and factors related to nonurgent visits. Acad Emerg Med 1999;6:1147-52. 21. Williams RC, Offenbacher S. Periodontal medicine: the emergence of a new branch of periodontology. Periodontol 2000 2000;23:9-12. 22. Cohen SG, Greenberg MS. Chronic oral herpes simplex virus infection in immunocompromised patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1985;59:465-71. 23. Woo SB, Challacombe SJ. Management of recurrent oral herpes simplex infections. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103:S12-8. 24. Nowak AJ, Casamassimo PS. The dental home: a primary care oral health concept. J Am Dent Assoc 2002;133:93-8. Reprint requests: Satheesh Elangovan, BDS, ScD, DMSc Department of Periodontics University of Iowa College of Dentistry Iowa City, IA 52241 [email protected]
Hospital-based emergency department visits with herpetic gingivostomatitis in the United States Satheesh Elangovan, BDS, DSc, DMSc,a Nadeem Y. Karimbux, DMD, MMSc,b Sreedevi Srinivasan, BDS, DSc,c Shankar R. Venugopalan, BDS, PhD,d Sridhar V.K. Eswaran, BDS, MS,e and Veerasathpurush Allareddy, BDS, MBA, MHA, MMSc, PhD,f Iowa City, Iowa, Boston, Massachusetts, and Houston, Texas UNIVERSITY OF IOWA, HARVARD SCHOOL OF DENTAL MEDICINE, TUFTS UNIVERSITY SCHOOL OF DENTAL MEDICINE, AND UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT HOUSTON
Objectives. The objectives of this study were to determine the number of hospital emergency department (ED) visits with a diagnosis of herpetic gingivostomatitis (HGS) for 2007 in the United States and to identify the possible comorbid conditions associated with HGS. Study Design. The Nationwide Emergency Department Sample for 2007 was used in this study. Patients who visited the ED with a diagnosis of HGS were selected. Estimates were projected to the national levels using the discharge weights. Presence of comorbid conditions in these patients was also analyzed. Results. A total of 23,124 patients had ED visits and received the diagnosis of HGS. Most of the patients were young females and those belonging to the lower socioeconomic strata. All patients with HGS also presented with comorbid conditions. Conclusions. Physicians should be trained to diagnose, manage, and refer common dental emergencies. In the long term, improving access to dental care for these patients is crucial to managing this problem. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:505-511)
The occurrence of human orofacial infections caused by herpes simplex virus (HSV) is extremely high and is prevalent worldwide.1,2 Type 1 HSV causes oral, facial, and ocular infections, whereas HSV type 2 typically causes genital lesions but is also implicated in some cases of oral infections.3 Herpetic gingivostomatits (HGS), the primary form of HSV-1 oral infection usually affects patients aged 6 months to 5 years and adolescents.4 Signs and symptoms of HGS include pain, fever, lymphadenopathy, irritability, malaise, and headache. Oral lesions present as vesicles on the tongue, buccal mucosa, and gingival that may rupture to become ulcers covered eventually by a yellowish-gray membrane.5,6 Because of the pain a
Assistant Professor, Department of Periodontics, University of Iowa. Assistant Dean for Dental Education and Director of Postdoctoral Periodontology Program, Harvard School of Dental Medicine. c Postdoctoral Orthodontics Resident, Tufts University School of Dental Medicine. d Postdoctoral Orthodontics Resident, Department of Developmental Biology, Harvard School of Dental Medicine. e Assistant Professor, Department of Periodontology, University of Texas Health Science Center at Houston. f Instructor and Director, Predoctoral Orthodontics Program, Department of Developmental Biology, Harvard School of Dental Medicine. Received for publication Aug 19, 2011; returned for revision Sep 21, 2011; accepted for publication Sep 23, 2011. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.oooo.2011.09.014 b
and discomfort associated with this condition, children tend to avoid eating or drinking, leading to severe dehydration.5 Apart from oral lesions, HSV-1 virus has also been cited as the causative agent for other diseases, such as viral encephalitis, lymphadenitis, and severe ocular lesions.7 Up to 90% of Americans exhibit serum antibodies (seropositive) to HSV-1.8 Although the exposure to HSV is extremely common, only a small percentage (⬃1%) of patients exhibit clinical manifestations.9 Epidemiologic studies further demonstrated that such factors as socioeconomic status had a significant effect on the seroprevalence of this condition. Patients in the lower socioeconomic strata were frequently found to be seropositive for HSV-1.10,11 Therefore, it is reasonable to state that owing to the high exposure of HSV in individuals having lower socioeconomic status, the prevalence of those individuals seeking hospital-based emergency department (ED) treatment could be significantly high. Several studies in the past investigated the seroprevalence of HSV-1 in various populations, but, to our knowledge, little is known about the emergency hospitalization of patients diagnosed with herpetic oral infections. The objectives of this study were twofold: to determine the number of hospital-based ED visits with a diagnosis of HGS for 2007, using a nationwide sample, and to identify the possible comorbid conditions associated with HGS.
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MATERIAL AND METHODS The Nationwide Emergency Department Sample (NEDS) for 2007 was used for the current study. The NEDS is one of the component databases of the Healthcare Cost and Utilization Project, which is under the purview of the Agency for Healthcare Research and Quality.12 The NEDS is drawn from a sample of 950 hospitals from 27 states in the United States and the unweighted sample provides emergency information on close to 25 million hospitalbased ED visits. The NEDS database has a weighting variable assigned to each visit that can be used to yield national estimates of all hospital-based ED visits occurring in the United States. It provides health care usage and outcomes information for both treatment and release ED visits, as well as information on hospital admissions that originate in the ED. The variables that are available in the NEDS database include age, gender, day of ED visit, diagnoses coded during ED visit and during hospitalization, procedures performed during ED visit and during hospitalization, disposition of patient following ED visit, median household income of patient’s residence based on the zip code income quartile, insurance status, ED charges, hospital region, and hospital location/teaching status. The NEDS database is available for public purchase from the Agency for Healthcare Research and Quality. The last author (V.A.) obtained the database following completion of a data user agreement. As per this agreement, any individual cell counts fewer than or equal to 10 visits cannot be reported so as to preserve patient confidentiality. Such low numbers are not reported in the current study in compliance with the data user agreement. For the current study, all hospital-based ED visits with International Classification of Diseases (ICD)9-CM diagnosis code for HGS (ICD-9-CM code of 054.2) in any of the diagnoses fields in the NEDS database were selected. The demographic and hospitalization characteristics of these visits were examined. The complex sampling frame design of the NEDS database was taken into consideration while calculating the national estimates. Each individual ED visit was used as the unit of analysis. The discharge weight variable assigned to each ED visit was used to project all estimates to nationwide levels. Descriptive statistics were used to summarize the data. Presence of comorbid conditions was identified by using the Clinical Classification Software codes, which group similar ICD9-CM diagnoses codes together. Clinical Classification Software codes in all the diagnoses fields were included. More than 200 comorbid conditions were examined. Only the most frequently prevalent comorbid
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conditions are reported in the current study. Estimates on all other comorbid conditions, including the Clinical Classification Software codes used, are available from the authors on request. All statistical analyses were conducted using SAS version 9.2 software (SAS Institute, Cary, NC).
RESULTS During 2007 in the United States, HGS was given as a diagnosis in a total of 23,124 ED visits. The demographic characteristics of these ED visits are summarized in Table I. The average age of the patients who visited the ED was 16 years. Close to 69.5% of all ED visits occurred in those 19 years and younger. Females accounted for 55.7% of all ED visits. Most of the ED visits (82.2%) were discharged routinely. Admission into the same hospital was required for 3575 (15.5%) ED visits. Discharge to a home health care facility was required for 261 ED visits (1.1%). Close to 38.5% of all ED visits occurred in those residing in geographic areas with median household income levels of less than $39,000, whereas 25.8% of all ED visits occurred in those residing in areas with household levels between $39,000 and $47,999. The primary payers for the ED visits were Medicaid (41.4% of all ED visits), Medicare (7.1%), private insurance plans (31.3%), and other insurance plans (3.6%). Uninsured comprised 16.5% of all ED visits. Most of the ED visits occurred in the South (39.5% of ED visits). The Midwest, Northeast, and Western regions accounted for 21.6%, 17.0%, and 21.9% of all ED visits, respectively. Metropolitan teaching hospitals treated 50.5% of all the ED visits, whereas metropolitan nonteaching and nonmetropolitan hospitals treated 35.1% and 14.3% of the ED visits, respectively. The presence of more than 200 comorbid conditions was examined in these ED visits. All patients had at least one comorbid condition. Only those conditions that were prevalent in at least 1% of those with HGS are reported in Table II. The prevalence estimates of comorbid conditions among those admitted into the same hospital following the ED visit are also provided in Table II. In summary, the 20 most frequently prevalent comorbid conditions in patients with HGS include fever of unknown origin (10.58% of all ED visits), fluid and electrolyte disorders (10.38%), upper respiratory infections (9.37%), otitis media and related conditions (4.32%), deficiency and other anemia (4.10%), screening and or history of mental health and substance abuse (3.90%), essential hypertension (3.90%), mycoses (3.82%), diseases of mouth (3.76%), gastrointestinal disorders (3.70%), asthma (3.50%), pneumonia (2.95%), urinary
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Table I. Characteristics of hospital-based emergency department visits with herpetic gingivostomatitis (n ⫽ 23,124) Characteristic Admission timing Disposition of patient from the ED
Gender Age, y
Median household income quartiles for patient’s ZIP code
Response Admission on Monday-Friday Admission on Saturday-Sunday Routine discharge Transfer to short-term facility Other transfers, including skilled nursing facility, intermediate care, and another type of facility Home health care Against medical advice Admitted as an inpatient to this hospital Died in ED Not admitted, destination unknown Male Female ⬍10 10-19 20-29 30-39 40-49 50-59 60-69 70-79 ⬎79 $1-$38,999 $39,000-$47,999 $48,000-$62,999
Insurance status
Hospital region
Hospital location and teaching status
$63,000 or more Medicare Medicaid Private, including HMO Uninsured Other Northeast Midwest South West Metropolitan nonteaching Metropolitan teaching Nonmetropolitan
Frequency* (%) 15,260 (66.0) 7846 (34.0) 18,998 (82.2) DS DS 261 (1.1) 26 (0.1) 3575 (15.5) DS 244 (1.1) 10,240 (44.3) 12,879 (55.7) 13,287 (57.5) 2774 (12) 2448 (10.6) 1305 (5.6) 1086 (4.7) 791 (3.4) 574 (2.5) 499 (2.2) 354 (1.5) 8579 (38.5) 5864 (25.8) 4912 (21.5) 3221 (14.1) 1638 (7.1) 9552 (41.4) 7224 (31.3) 3809 (16.5) 823 (3.6) 3922 (17) 5003 (21.6) 9132 (39.5) 5067 (21.9) 8123 (35.1) 11,684 (50.5) 3317 (14.3)
DS, discharge information suppressed because individual cell counts are ⱕ 10, as per the data user agreement with Agency for Healthcare Research and Quality, such low numbers cannot be reported; ED, emergency department; HMO, health maintenance organization. *All percentages are based on the total admission for respective category (i.e., all discharged and age groups). Individual cell counts may not add up to the global cell counts because of missing values.
tract infections (2.68%), skin and subcutaneous tissue infections (2.61%), allergic reactions (2.50%), septicemia (2.34%), esophageal disorders (2.18%), lower respiratory diseases (2.02%), diabetes mellitus without complications (1.92%), and bacterial infections (1.86%).
DISCUSSION The data presented in the current study include all patients presenting to the ED with HGS regardless if they were treated and released from the ED or admitted into the same hospital. Among these patients visiting the ED with HGS, 15.5% were admitted as inpatients into the same hospital.
Recent ED visit studies have concluded that patients belonging to the lower socioeconomic strata and those lacking insurance rely heavily on EDs for their dental needs.13 Earlier, using a nationwide sample, we identified that a substantial number of patients visited the ED with common dental ailments, such as dental caries14 and periodontal disease,15 as well as with acute dental conditions, such as pulpal and/or periapical pathologies.16 Hospitalization of a patient visiting an ED for dental needs was a common occurrence, resulting in the use of a significant amount of resources.14-16 Based on the prevalence of HSV-1 and HSV-2 infections, we hypothesize that there may be a higher incidence of ED visits by patients with herpetic infections belonging to
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Table II. Presence of concomitant comorbid conditions in patients visiting the emergency department with herpetic gingivostomatitis ED visits
Admitted into same hospital after ED visit
Comorbid condition
Frequency
Percentage of all ED visits (n ⫽ 23,124)
Frequency
Percentage of all ED visits that resulted in hospitalization (n ⫽ 3575)
Fever of unknown origin Fluid and electrolyte disorders Upper respiratory infections, including ● Acute sinusitis ● Acute pharyngitis ● Acute laryngitis and tracheitis ● Acute upper respiratory infections of multiple sites ● Chronic sinusitis Otitis media and related conditions Deficiency and other anemia Screening and history of mental health and substance abuse Essential hypertension Mycoses Diseases of mouth, excluding dental Gastrointestinal disorders, including ● Gastrointestinal mucositis ● Gastroenteritis and colitis caused by radiation ● Toxic gastroenteritis and colitis ● Functional digestive disorders ● Disorders of peritoneum ● Disorders of intestine ● Intestinal malabsorption ● Symptoms involving digestive system ● Symptoms involving abdomen and pelvis Asthma Pneumonia (except that caused by tuberculosis or sexually transmitted disease) Urinary tract infections Skin and subcutaneous tissue infections Allergic reactions Septicemia (except in labor) Esophageal disorders Lower respiratory disease ● Abscess of mediastinum ● Pulmonary congestion and hypostasis ● Postinflammatory pulmonary fibrosis ● Alveolar and parietoalveolar pneumonopathy ● Lung involvement in systemic sclerosis ● Lung involvement in other diseases ● Pulmonary eosinophilia ● Acute edema of lung ● Disorders of diaphragm ● Cyanosis ● Dyspnea and respiratory abnormalities ● Symptoms involving respiratory system Diabetes mellitus without complication Bacterial infection, unspecified site Mood disorders Diseases of white blood cells Chronic obstructive pulmonary disease and bronchiectasis Cardiac dysrhythmias Disorders of lipid metabolism Nutritional, endocrine, and metabolic disorders, including
2447 2400
10.8 10.4
286 1749
8.0 48.9
2166 999 948 902
9.4 4.3 4.1 3.9
314 116 919 419
8.8 3.2 25.7 11.7
901 884 869
3.9 3.8 3.8
582 622 181
16.3 17.4 5.1
855 810 683
3.7 3.5 3.0
610 309 638
17.1 8.6 17.8
619 604 577 540 504
2.7 2.6 2.5 2.3 2.2
494 239 195 540 406
13.8 6.7 5.4 15.1 11.4
467 444 429 415 408 393 391 389 378
2.0 1.9 1.9 1.8 1.8 1.7 1.7 1.7 1.6
206 297 369 325 397 307 356 333 325
5.8 8.3 10.3 9.1 11.1 8.6 9.9 9.3 9.1
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Table II. Continued ED visits
Comorbid condition Upper respiratory disease, including ● Nasal polyps ● Chronic pharyngitis and nasopharyngitis ● Chronic laryngitis and laryngotracheitis ● Allergic rhinitis ● Diseases of upper respiratory tract ● Diseases of trachea and bronchus—not classified ● Mediastinitis ● Diseases of mediastinum, not elsewhere classified ● Symptoms, such as voice disturbance Nervous system disorders Disorders of teeth and jaw Aftercare HIV infection Skin disorders Coagulation and hemorrhagic disorders Respiratory failure, insufficiency, arrest (adult) Acute and unspecified renal failure Coronary atherosclerosis and other heart disease Thyroid disorders Nausea and vomiting Lymphadenitis Connective tissue disease Leukemias Circulatory disease, including ● Peripheral vascular disease ● Polyarteritis nodosa and allied conditions ● Disorders of arteries and arterioles ● Disease of capillaries ● Hypotension Congestive heart failure, nonhypertensive Chronic renal failure Epilepsy, convulsions Headache, including migraine Nutritional deficiencies
Admitted into same hospital after ED visit
Frequency
Percentage of all ED visits (n ⫽ 23,124)
Frequency
Percentage of all ED visits that resulted in hospitalization (n ⫽ 3575)
350 344 325 325 320 308 295 288 286 284 282 270 259 258 256
1.5 1.5 1.4 1.4 1.4 1.3 1.3 1.3 1.2 1.2 1.2 1.2 1.1 1.1 1.1
61 266 70 142 248 99 272 283 281 231 230 87 40 141 235
1.7 7.4 1.9 4 6.9 2.8 7.6 7.9 7.9 6.5 6.4 2.4 1.1 3.9 6.6
256 253 248 246 239 234
1.1 1.0 1.0 1.0 1.0 1.0
200 240 248 131 80 234
5.6 6.7 6.9 3.7 2.2 6.5
the lower socioeconomic strata and by those lacking good insurance coverage; however, this needs further empiric support by future studies. The prevalence estimates presented in our study regarding the socioeconomic levels are too close to draw clinically meaningful conclusions regarding the definitive role of socioeconomic status on HSV infections. To our knowledge, this is the first descriptive study using the NEDS database to provide a nationwide estimate of ED visits with HGS in the United States. We found a total of 23,124 ED visits with a diagnosis of HGS, composed predominantly of young patients (19 years and younger). Most visits were made during weekdays. Our results indicate that slightly more females visited EDs with HGS. The authors were unable to obtain information regarding the type of drugs administered to these patients in an ED from the NEDS database but it was reported in a previous study that
children and adults with HGS visiting the ED were commonly prescribed acyclovir 15 mg/kg (5 times a day) and valacyclovir 1 g (twice a day for 5-7 days), respectively.17 Because of the rising number of patients with this condition visiting the ED, the same study also underscored the importance of training physicians to diagnose and treat this dental condition on an emergency basis.17 With respect to patients’ disposition from the ED following their visit, we found that most patients were routinely discharged. This study found that a subset of the population (n ⫽ 3575; 15.5%) who visited the ED with HGS were hospitalized. We also observed this trend with regard to other dental conditions.14-16 It is known from the literature that dehydration, a common symptom in patients with HGS (especially in younger patients), seemed to be the major factor favoring hospitalization, although we were unable to validate this
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information from our dataset.18 Approximately 10.4% of patients diagnosed with HGS had fluid and electrolyte disorders (Table II), possibly influencing the physician to hospitalize. From a recent report, it is clear that patients admitted for dehydration following HSV infection received intravenous fluids (20 mg/kg bolus).18 The presence of other comorbid conditions, such as fever, the severity of the HSV lesions, and the extraoral complications arising from HSV infection could have influenced the decision to hospitalize these patients. Our study shows that patients with an annual income of less than $39,000 visited the ED more frequently (⬃39%), a finding that is consistent with our previous studies.14-16 This observation is in agreement with the current evidence that the seroprevalence of HSV is higher in the population with lower socioeconomic status.10 Most patients who visited the ED were enrolled in the Medicaid program (41.1%), similar to our previously published studies, and agrees with a recent study that indicated that individuals with governmentsponsored insurance programs, such as Medicaid, visit the ED more often than others.14-16,19 Interestingly, a significant percentage of patients with private insurance coverage (31.3%) also visited the ED with HGS. Geographically, we found that patients from the South visited the ED more than those from the other parts of the country. Socioeconomic variations of the patient population and changes in the health care delivery system have been cited as causing drastic geographic variations in ED visits.20 The type of insurance available in a locality, and the number and size of hospitals are other potential factors that could influence the geographic variation in the prevalence of ED visits. It should be noted that NEDS, although a nationally representative database, includes ED visit sample data from only 27 states, which could affect the geographic distribution of the ED visits.12 A patient’s underlying systemic conditions can have a significant impact on the oral cavity and considerably influence the patient’s response to treatment.21 Immunocompromised individuals tend to develop HGS lesions that are more severe in nature and also exhibit poor healing response.22 It was also shown that these individuals tend to demonstrate lower response to the prescribed antiviral medications and also exhibit a higher chance of developing serious systemic complications.23 We looked for the presence of comorbid conditions in these patients. Our analysis revealed that in patients visiting the ED with HGS, most presented with fever of unknown origin (10.58%), fluid imbalance (10.38%), and upper respiratory infections (9.37%). We also observed that approximately 4.1% and 3.8% of patients were diagnosed with some form of anemia and mycosis, respectively.
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The findings of this study should be interpreted keeping the following issues in perspective. The ED visits reported in this study include visits in which a patient was given a primary or secondary diagnosis of HGS. Therefore, it is possible that some of the patients visited the ED primarily for a comorbid condition but HGS could have been an additional (secondary) diagnosis given after the clinical examination. It is also important to remember that we have no direct evidence to associate the comorbid conditions reported in these patients with HGS. Also, information is not available regarding the type of diagnostic tests used or treatment rendered during the visits as well during the follow-up care after an ED visit. Another inherent limitation with the data set is the possible misdiagnoses rendered by physicians who were seeing these patients during the ED visits. Furthermore, comorbid conditions are identified using ICD-9-CM diagnoses codes. It is not clear who coded the data into the hospital discharge databases. Consequently, the estimates presented in the current study could be subject to biases associated with inconsistencies in coding practices within and across hospitals in the United States. The results from this study, along with our previous studies focusing on other dental conditions, clearly demonstrate that a significant number of patients visited hospitals for their dental needs in 2007 and, as a result, significant resources were used. The results of this study are consistent with our previous observations that these patients usually have lower socioeconomic status; however, further empiric support is needed to draw definitive conclusions regarding the same. It is clear that physicians and other ED personnel should be trained to diagnose, manage, and refer common dental emergencies. On a long-term basis, improving access to dental care for these patients is crucial to overcome this problem. This study also emphasizes the importance of preventive programs, such as a “dental home” for children, which will allow for early intervention and prevention of common childhood oral infections, including herpes.24 REFERENCES 1. Whitley RJ, Roizman B. Herpes simplex virus infections. Lancet 2001;357:1513-8. 2. Siegel D, Golden E, Washington AE, Morse SA, Fullilove MT, Catania JA, et al. Prevalence and correlates of herpes simplex infections. The population-based AIDS in Multiethnic Neighborhoods Study. JAMA 1992;268:1702-8. 3. Miller CS, Redding SW. Diagnosis and management of orofacial herpes simplex virus infections. Dent Clin North Am 1992; 36:879-95. 4. Scully C. Orofacial herpes simplex virus infections: current concepts in the epidemiology, pathogenesis and treatment, and disorders in which the virus may be implicated. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1989;68:701-10.
OOOO Volume 113, Number 4 5. Huber MA. Herpes simplex type-1 virus infections. Quintessence Int 2003;34:453-67. 6. Eisen D. The clinical characteristics of intraoral herpes simplex virus infection in 52 immunocompetent patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:432-37. 7. Arduino PG, Porter SR. Herpes simplex virus type 1 infection: overview on relevant clinico-pathological features. J Oral Pathol Med 2008;37:107-21. 8. Regezi JA, Sciubba JJ. Vesiculo-bullous diseases. In: Oral pathology: clinical pathologic correlations. 2nd ed. Philadelphia: W. B. Saunders; 1993. p. 1–33. 9. Siegel MA. Diagnosis and management of recurrent herpes simplex infections. J Am Dent Assoc 2002;133:1245-49. 10. Corey L, Spear PG. Infections with herpes simplex viruses (1). N Engl J Med 1986;314:686-91. 11. Stock C, Guillén-Grima F, de Mendoza JH, Marin-Fernandez B, Aguinaga-Ontoso I, Krämer A. Risk factors of herpes simplex type 1 (HSV-1) infection and lifestyle factors associated with HSV-1 manifestations. Eur J Epidemiol 2001;17:885-90. 12. Agency for Healthcare Research and Quality. National ED sample database documentation. Available at: http://www.hcupus.ahrq.gov/nedsoverview.jsp. Accessed July 26, 2011. 13. Lewis C, Lynch H, Johnston B. Dental complaints in emergency departments: A national perspective. Ann Emerg Med 2003; 42:93-9. 14. Nalliah RP, Allareddy V, Elangovan S, Karimbux N, Allareddy V. Hospital-based emergency department visits attributed to dental caries in the United States in 2006. J Evid Based Dent Pract 2010;10:212-22. 15. Elangovan S, Nalliah R, Allareddy V, Karimbux NY, Allareddy V. Outcomes in patients visiting hospital emergency departments in the United States because of periodontal conditions. J Periodontol 2011;82:809-19.
ORIGINAL ARTICLE Elangovan et al. 511 16. Nalliah RP, Allareddy V, Elangovan S, Karimbux N, Lee MK, Gajendrareddy P, et al. Hospital emergency department visits attributed to pulpal and periapical disease in the United States in 2006. J Endod 2011;37:6-9. 17. Mell HK. Management of oral and genital herpes in the emergency department. Emerg Med Clin North Am 2008;26:457-73. 18. Amir J, Harel L, Smetana Z, Varsano I. The natural history of primary herpes simplex type 1 gingivostomatitis in children. Pediatr Dermatol 1999;16:259-63. 19. LaCalle E, Rabin E. Frequent users of emergency departments: the myths, the data, and the policy implications. Ann Emerg Med 2010;56:42-8. 20. Liu T, Sayre MR, Carleton SC. Emergency medical care: types, trends, and factors related to nonurgent visits. Acad Emerg Med 1999;6:1147-52. 21. Williams RC, Offenbacher S. Periodontal medicine: the emergence of a new branch of periodontology. Periodontol 2000 2000;23:9-12. 22. Cohen SG, Greenberg MS. Chronic oral herpes simplex virus infection in immunocompromised patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1985;59:465-71. 23. Woo SB, Challacombe SJ. Management of recurrent oral herpes simplex infections. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103:S12-8. 24. Nowak AJ, Casamassimo PS. The dental home: a primary care oral health concept. J Am Dent Assoc 2002;133:93-8. Reprint requests: Satheesh Elangovan, BDS, ScD, DMSc Department of Periodontics University of Iowa College of Dentistry Iowa City, IA 52241 [email protected]