|Year : 2022 | Volume
| Issue : 4 | Page : 270-274
Periapical lesions in patients with primary Sjögren syndrome: A cross-sectional retrospective study of medical charts platform
Ilan Rotstein1, Joseph Katz2
1 Department of Endodontics and Periodontics, University of Southern California, Los Angeles, California, USA
2 Department of Oral Diagnostic Sciences, University of Florida College of Dentistry, Gainesville, Florida, USA
|Date of Submission||19-Feb-2022|
|Date of Decision||25-May-2022|
|Date of Acceptance||31-May-2022|
|Date of Web Publication||28-Dec-2022|
Dr. Ilan Rotstein
Herman Ostrow School of Dentistry, University of Southern California, Los Angeles 90007, California
Source of Support: None, Conflict of Interest: None
Aim: The aim of this study was to assess the prevalence of acute periapical lesions in patients with pSS.
Methods: Integrated data of hospital patients was used. Data from the corresponding diagnosis codes for pSS and acute periapical abscess was retrieved by searching the appropriate query in the database. The patient population analyzed was mixed, presenting with different disease conditions including periapical abscesses without sinus. The different diagnoses were coded using the international coding systems ICD 10. Diagnosis was made by calibrated dentists in a hospital setting based on clinical examination and imaging data. Patients with ICD 10 diagnosis code of acute periapical abscess were recorded and the prevalence of acute periapical abscesses in patients with primary Sjögren syndrome were compared to the prevalence in the total hospital patient population. The odds ratio (OR) for the prevalence of acute periapical abscesses and its association with pSS were calculated with a 95% confidence interval and the statistical difference between the groups was assessed.
Results: The odds ratio (OR) for the prevalence of acute apical abscesses and its association with pSS were calculated and analyzed statistically. The prevalence of periapical abscesses in patients with pSS was 1.87% as compared to 0.58% in the general patient population of the hospital. The OR was 3.11 and the difference was statistically significant (p<0.0001).
Conclusions: Under the conditions of this study, it appears that the prevalence of acute periapical abscesses is significantly higher in patients with pSS.
Keywords: Apical abscess, periapical lesion, primary Sjögren syndrome
|How to cite this article:|
Rotstein I, Katz J. Periapical lesions in patients with primary Sjögren syndrome: A cross-sectional retrospective study of medical charts platform. Endodontology 2022;34:270-4
| Introduction|| |
Sjögren syndrome (SS) is an autoimmune disorder that affects mainly exocrine glands, resulting in low production of body fluids such as saliva and tears.,, Low production of fluids by salivary and lacrimal glands causes dry eyes and mouth syndrome that can lead to further health complications such as cornea damage, blurry vision, and dental caries., Females have a higher risk of developing SS compared to males, with a ratio of almost 9:1, and the risk increases after the age of 40 years.,,
There are two types of SS, primary SS (pSS) and secondary SS (sSS). pSS refers to patients without any other autoimmune disorders, and sSS refers to patients with an autoimmune disorder who was later also diagnosed with SS.,,
The etiology and certain aspects of the pathogenesis of SS are still not completely clear. It has been theorized that genetic predisposition and environmental factors are involved. Currently, there is no cure for SS and therapies are focused mainly on relieving the symptoms.
Reported oral manifestations of SS include xerostomia and a higher incidence of caries and periodontal disease.,,,,,,,, Normal saliva flow and its buffering capacity provide lubrication to the oral mucosa and maintain a favorable pH level within the oral cavity. In patients with SS, salivary gland hypofunction causes the connective tissues to be more prone to oral infections, mainly candidiasis.,
Several studies examined the association between SS and periodontal disease.,,, Antoniazzi et al. reported that SS can negatively affect the periodontal condition. An odds ratio (OR) analysis suggested that patients with SS are at 2.2 times higher risk of having adult periodontitis than healthy individuals. A large-scale, population-based study, found an association between SS and periodontal disease. However, another study did not find such an association.
To date, the association between SS and endodontic disease has not been comprehensively explored. Therefore, the aim of this cross-sectional study was to assess the prevalence of acute periapical lesions in patients with pSS.
| Materials and Methods|| |
The University of Florida (UF) Integrated Data i2b2, provided by the UF Health Office of the Chief Data Officer from June 2015 to June 2021, was used. When queried, the i2b2 search engine provides a totally de-identified data set. Research conducted using that de-identified data set has been determined by the UF Institutional Review Board (IRB) to not meet the definition of human research, and thus does not require IRB approval. The study was in compliance with the UF IRB and privacy rules for research on IRB-approved de-identified data sets (IRB letter referenced June 4, 2021).
Data aggregated from inpatients and outpatients visiting the UF Health Center were recorded using the electronic patient record Epic Systems (epic.com). Epic is the preferred electronic medical record system used by more than 250 health-care organizations nationwide. More than 50% of the United States (US) population have their medical records in an Epic System.
The different diagnoses were coded using the international coding system International Classification of Diseases (ICDs) 10. The ICD classification has been introduced following a mandate from the Centers for Medicare and Medicaid Services effective October 1, 2015. Medicare and Medicaid are the Government National Health Insurance and Health Cost Assistance Programs in the US. It requires that all Health Insurance Portability and Accountability Act (HIPAA)-covered entities implement the ICD-10-CM diagnosis code set. Medicaid is a HIPAA entity, as are medical and dental clinics. The ICD classification has been adopted by the American Dental Association.
The patient population analyzed was mixed, presenting with different disease conditions including periapical abscesses (PAs) without sinus (ICD-10-K04.7). Individual data were not analyzed; however, all cases were diagnosed by three calibrated dentists that reached an agreement of 0.8 when calibrated before the study. The diagnosis was made in a hospital setting, for patients admitted to urgent care with symptoms of acute PAs.
The diagnosis was made based on clinical examination and imaging data confirming the presence of acute periapical abscess without a sinus tract.
Inclusion criteria encompassed all patients with the corresponding diagnostic code for PAs without sinus (ICD-10-K04.7). There were no exclusion criteria since all codes were computerized and specific diagnoses of acute periapical abscesses in the total hospital patient population, were searched using the appropriate ICD-10 code. The history of pSS was retrieved by searching the appropriate query in the database.
Patients with ICD-10 diagnosis code of acute periapical abscess were recorded and the prevalence of acute PAs in patients with pSS was compared to the prevalence in the total hospital patient population.
The OR for the prevalence of acute PAs and its association with pSS were calculated with a 95% confidence interval and the statistical difference between the study groups was assessed using MedCalc software. MedCalc is statistical software that includes more than 200 statistical tests. A standard normal deviation (z-value) was calculated as follows: ln (OR)/SE (ln [OR]). The P value was the area of the normal distribution that falls outside ± z. A value of P < 0.05 was considered statistically significant.
| Results|| |
The total hospital patient population studied was 1,149,653, of which 46.2% were males and 53.8% females [Table 1]. Out of the total patient population, 2675 patients were diagnosed with pSS, of which 12.56% were males and 87.46% females; 73.9% white and 16.41% African Americans (9.69% were of other ethnicities); and 97.27% were adults and 2.72% children (younger than 18 years old) [Table 1].
Out of the patients with pSS who presented with acute PAs, 20% were males and 80% females; 76% were white and 24% African Americans; and 100% were adults [Table 1].
The prevalence of acute PAs in patients with pSS was 1.87% as compared to 0.58% in the general patient population of the hospital. The OR for PAs in pSS patients, including males and females, was 3.11 and the difference was statistically significant (P < 0.0001) [Table 2].
|Table 2: Prevalence of acute periapical abscesses in patients with primary Sjögren syndrome and total hospital patient population|
Click here to view
| Discussion|| |
The results of this cross-sectional hospital-based study indicate that, overall, the OR for the prevalence of acute PAs is significantly higher in patients with pSS than in patients without this condition. As expected, females have dominated the pSS's patient population. Although the prevalence of acute PAs in the general hospital population was relatively low, the prevalence of acute PAs in pSS patients was 3-fold higher than in non-pSS patients.
The most common oral manifestation of pSS is severe hyposalivation and as a result, a higher incidence of dental caries. Patients with salivary hypofunction secondary to pSS present a greater risk to develop dental caries compared to healthy individuals. It has been recognized that dental caries is a significant etiologic factor, probably the most significant one, in the development of pulpal and periapical disease. Although the increased rate of dental caries due to hyposalivation is associated with an increased rate of corresponding pulp pathosis and PAs, to date, we could not find any studies demonstrating a direct connection between dental caries and a higher prevalence of PAs in pSS patients. However, it is plausible that since bone metabolism in pSS patients may be compromised, it reduces bone tissue capacity to combat infection. This condition can be further aggravated by external factors such as tobacco smoking. Therefore, regular prophylactic treatments, good oral hygiene, and elimination of unsound habits such as smoking, can prevent complications.
Several mediators of inflammation may be associated with the development and progression of periapical disease. They include certain chemokines and cytokines, factors regulating resorption of bone, metabolites of arachidonic acid, and oxygen-generated free radicals., The interactions among these mediators depend on the etiology of the insult and may differ from one person to another.,
Patients with pSS can develop osteoporosis over the course of the disease, characterized by decreased bone mass and increased risk of bone fracture. In addition to their systemic inflammatory condition, patients with pSS have additional risk factors that can result in loss of bone mass and susceptibility to bone pathoses. In a large cross-sectional study, it was found that the prevalence of periapical lesions was significantly higher in osteoporotic patients and that women were significantly more affected than men.
It has been reported that regulators of bone resorption, such as receptor activator of NF-κB ligand (RANKL), its cellular receptor (RANK), and osteoprotegerin (OPG) play a significant role in the pathogenesis of alveolar bone loss. Changes in the ratio between RANKL and OPG have been associated with the progression of alveolar bone resorption in cases of apical periodontitis.,, It is, therefore, plausible that pSS patients will demonstrate more susceptibility to such condition.
Renal involvement is a well-recognized extraglandular complication in pSS. Long-standing untreated metabolic acidosis and hypophosphatemia due to pSS-related renal tubular dysfunction can lead to metabolic bone disease in the form of rickets and osteomalacia. Other pSS-associated factors that have a direct effect on bone include increased osteoclastic activity, increased parathyroid mediated bone resorption, and abnormal renal phosphate levels, leading to hypophosphatemia and acidosis-induced impairment of Vitamin D metabolism. Recently, it has been shown that the prevalence of PAs is higher in individuals with Vitamin D deficiency.
It should be noted that the association between pSS and periapical abscess does not necessarily imply causality. It has been established that SS can be secondary to several connective tissue diseases. However, in comparison to the total number of patients that were admitted to the hospital, it is plausible that this fact would not significantly skew the results.
Some limiting factors should be considered when extrapolating the data of this cross-sectional study. First, the patient population examined may have had additional underlying systemic or dental conditions. However, those conditions were not included in the present analysis. Second, whether the periapical pathoses were active or in a process of healing is unknown. Third, socioeconomic factors may affect the decision of certain patients to seek medical and dental care in a specific location. Therefore, the prevalence of PAs in this study may also reflect social-economic disparities.
| Conclusion|| |
The results of this cross-sectional study indicate that the prevalence of acute PAs is significantly higher in patients with pSS, mainly women. Additional studies are warranted to assess the exact cause-and-effect phenomenon.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Wang J, Zhou L, Liu B. Update on disease pathogenesis, diagnosis, and management of primary Sjögren's syndrome. Int J Rheum Dis 2020;23:723-7.
Manoussakis MN, Moutsopoulos HM. Sjögren's syndrome. Otolaryngol Clin North Am 1999;32:843-60.
Kruszka P, O'Brian RJ. Diagnosis and management of Sjögren syndrome. Am Fam Physician 2009;79:465-70.
Somani R, Sunil M, Khaira J, Kumar D. Sjögren's syndrome: A review. J Indian Acad Oral Med Radiol 2011;23:61-4. [Full text]
Baer AN, Walitt B. Sjögren syndrome and other causes of sicca in older adults. Clin Geriatr Med 2017;33:87-103.
Fox PC. Autoimmune diseases and Sjogren's syndrome: An autoimmune exocrinopathy. Ann N Y Acad Sci 2007;1098:15-21.
Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, et al.
Classification criteria for Sjögren's syndrome: A revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002;61:554-8.
Tsuboi H, Asashima H, Takai C, Hagiwara S, Hagiya C, Yokosawa M, et al
. Primary and secondary surveys on epidemiology of Sjögren's syndrome in Japan. Mod Rheumatol 2014;24:464-70.
Jonsson R, Vogelsang P, Volchenkov R, Espinosa A, Wahren-Herlenius M, Appel S. The complexity of Sjögren's syndrome: novel aspects on pathogenesis. Immunol Lett 2011;141:1-9.
Likar-Manookin K, Stewart C, Al-Hashimi I, Curtis W, Berg K, Cherian K, et al
. Prevalence of oral lesions of autoimmune etiology in patients with primary Sjogren's syndrome. Oral Dis 2013;19:598-603.
Soto-Rojas AE, Kraus A. The oral side of Sjögren syndrome. Diagnosis and treatment. A review. Arch Med Res 2002;33:95-106.
Chuang CJ, Hsu CW, Lu MC, Koo M. Increased risk of developing dental diseases in patients with primary Sjögren's syndrome – A secondary cohort analysis of population-based claims data. PLoS One 2020;15:e0239442.
Torres SR, Peixoto CB, Caldas DM, Silva EB, Akiti T, Nucci M, et al
. Relationship between salivary flow rates and Candida
counts in subjects with xerostomia. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;93:149-54.
Serrano J, López-Pintor RM, Ramírez L, Fernández-Castro M, Sanz M, Melchor S, et al
. Risk factors related to oral candidiasis in patients with primary Sjögren's syndrome. Med Oral Patol Oral Cir Bucal 2020;25:e700-5.
Antoniazzi RP, Miranda LA, Zanatta FB, Islabão AG, Gustafsson A, Chiapinotto GA, et al.
Periodontal conditions of individuals with Sjögren's syndrome. J Periodontol 2009;80:429-35.
Najera MP, al-Hashimi I, Plemons JM, Rivera-Hidalgo F, Rees TD, Haghighat N, et al
. Prevalence of periodontal disease in patients with Sjögren's syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;83:453-7.
Lin CY, Tseng CF, Liu JM, Chuang HC, Lei WT, Liu LY, et al
. Association between periodontal disease and subsequent Sjögren's syndrome: A nationwide population-based cohort study. Int J Environ Res Public Health 2019;16:E771.
Maarse F, Jager DH, Alterch S, Korfage A, Forouzanfar T, Vissink A, et al
. Sjögren's syndrome is not a risk factor for periodontal disease: A systematic review. Clin Exp Rheumatol 2019;37 Suppl 118:225-33.
Le Gall M, Cornec D, Pers JO, Saraux A, Jousse-Joulin S, Cochener B, et al
. A prospective evaluation of dental and periodontal status in patients with suspected Sjögren's syndrome. Joint Bone Spine 2016;83:235-6.
Berman N, Vivino F, Baker J, Dunham J, Pinto A. Risk factors for caries development in primary Sjogren syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol 2019;128:117-22.
Zero DT, Zandona AF, Vail MM, Spolnik KJ. Dental caries and pulpal disease. Dent Clin North Am 2011;55:29-46.
Rotstein I, Katz J. Prevalence of periapical pathosis in smokers versus nonsmokers: A cross-sectional study. Calif Dent Assoc J 2021;49:487-92.
Márton IJ, Kiss C. Overlapping protective and destructive regulatory pathways in apical periodontitis. J Endod 2014;40:155-63.
Jakovljevic A, Miletic M, Nikolic N, Beljic-Ivanovic K, Andric M, Milasin J. Notch signaling pathway mediates alveolar bone resorption in apical periodontitis. Med Hypotheses 2019;124:87-90.
Martin TJ, Sims NA, Quinn JM. Interactions among osteoblasts, osteoclasts, and other cells in bone. In: Lorenzo J, Choi Y, Horowitz M, Takayanagi H, editors. Osteoimmunology: Interactions of the Immune and Skeletal Systems. Cambridge: Academic Press; 2011. p. 227-67.
Menezes R, Garlet TP, Letra A, Bramante CM, Campanelli AP, Figueira Rde C, et al
. Differential patterns of receptor activator of nuclear factor kappa B ligand/osteoprotegerin expression in human periapical granulomas: possible association with progressive or stable nature of the lesions. J Endod 2008;34:932-8.
Salman-Monte TC, Sanchez-Piedra C, Fernandez Castro M, Andreu JL, Martinez Taboada V, Olivé A, et al
. Prevalence and factors associated with osteoporosis and fragility fractures in patients with primary Sjögren syndrome. Rheumatol Int 2020;40:1259-65.
Katz J, Rotstein I. Prevalence of periapical lesions in patients with osteoporosis. J Endod 2021;47:234-8.
Carneiro E, Parolin AB, Wichnieski C, Rosa EA, Silva Neto UX, Westphalen VP, et al
. Expression levels of the receptor activator of NF-κB ligand and osteoprotegerin and the number of gram-negative bacteria in symptomatic and asymptomatic periapical lesions. Arch Oral Biol 2017;73:166-71.
Salinas-Muñoz M, Garrido-Flores M, Baeza M, Huamán-Chipana P, García-Sesnich J, Bologna R, et al
. Bone resorptive activity in symptomatic and asymptomatic apical lesions of endodontic origin. Clin Oral Investig 2017;21:2613-8.
Bagga A, Bajpai A, Gulati S, Singh A. Distal renal tubular acidosis with severe bony deformities and multiple fractures. Indian Pediatr 2001;38:1301-5.
Krieger NS, Frick KK, Bushinsky DA. Mechanism of acid-induced bone resorption. Curr Opin Nephrol Hypertens 2004;13:423-36.
Rotstein I, Katz J. Prevalence of periapical abscesses in vitamin D deficient patients. Am J Dent 2021;34:163-5.
[Table 1], [Table 2]