Sjogren's Syndrome an Update on Disease Pathogenesis, Clinical

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Sjogren's Syndrome an Update on Disease Pathogenesis, Clinical Clinical Immunology 203 (2019) 81–121 Contents lists available at ScienceDirect Clinical Immunology journal homepage: www.elsevier.com/locate/yclim Review Article Sjogren’s syndrome: An update on disease pathogenesis, clinical T manifestations and treatment ⁎ Frederick B. Vivinoa, , Vatinee Y. Bunyab, Giacomina Massaro-Giordanob, Chadwick R. Johra, Stephanie L. Giattinoa, Annemarie Schorpiona, Brian Shaferb, Ammon Peckc, Kathy Sivilsd, ⁎ Astrid Rasmussend, John A. Chiorinie, Jing Hef, Julian L. Ambrus Jrg, a Penn Sjögren's Center, Penn Presbyterian Medical Center, University of Pennsylvania Perelman School of Medicine, 3737 Market Street, Philadelphia, PA 19104, USA b Scheie Eye Institute, University of Pennsylvania Perelman School of Medicine, 51 N. 39th Street, Philadelphia, PA 19104, USA c Department of Infectious Diseases and Immunology, University of Florida College of Veterinary Medicine, PO Box 100125, Gainesville, FL 32610, USA d Oklahoma Medical Research Foundation, Arthritis and Clinical Immunology Program, 825 NE 13th Street, OK 73104, USA e NIH, Adeno-Associated Virus Biology Section, National Institute of Dental and Craniofacial Research, Building 10, Room 1n113, 10 Center DR Msc 1190, Bethesda, MD 20892-1190, USA f Department of Rheumatology and Immunology, Peking University People’s Hospital, Beijing 100044, China g Division of Allergy, Immunology and Rheumatology, SUNY at Buffalo School of Medicine, 100 High Street, Buffalo, NY 14203, USA 1. Introduction/History and lacrimal glands [4,11]. The syndrome is named, however, after an Ophthalmologist from Jonkoping, Sweden, Dr Henrik Sjogren, who in Sjogren’s syndrome (SS) is one of the most common autoimmune 1930 noted a patient with low secretions from the salivary and lacrimal diseases. It may exist as either a primary syndrome or as a secondary glands. He subsequently published on a series of patients with “kera- syndrome when associated with other autoimmune diseases, such as toconjunctivitis sicca” in 1933 and 1951 that brought the syndrome to rheumatoid arthritis, systemic lupus erythematosus, systemic sclerosis worldwide medical attention [11,12]. He distinguished the primary and primary biliary cirrhosis [1–4]. The true prevalence of SS is very disease from other causes of keratoconjunctivitis sicca, such as vitamin hard to determine because of frequent changes in diagnostic criteria, A deficiency and tuberculosis. In the 1950’s and 1960’s Sjogren’s syn- variation in the method of diagnosis based on the training of the clin- drome was felt to be a relatively rare disorder and the appreciation of ician making the diagnosis (i.e. Ophthalmologist vs. Oral surgeon v its association with other autoimmune diseases was just starting [13]. Rheumatologist vs. Internist, etc.) and inclusion of novel diagnostic In the 1970’s, immunological abnormalities associated with Sjogren’s markers that are potentially more sensitive. While SS was once con- syndrome, especially hypergammaglobulinemia, monoclonal gammo- sidered a rare disease, it is now considered the second most common pathiy and various lymphoid abnormalities were just being elucidated. autoimmune disease, after rheumatoid arthritis. Its prevalence is esti- The association between SS and lymphomas was noted, minor salivary mated at 1% (0.1 – 4.8%) with an incidence of 7 per 100,000 in the gland biopsies were used for diagnosis, immunological therapies, such United States. It is felt that roughly 4 million Americans have SS with as the use of corticosteroids were attempted, the association of SS with 90% of them being women and 50% of them having SS in association HLA-B8 and DR3 was made, and animal models for SS were first ex- with another autoimmune disease [5–7]. The incidence of SS is felt to amined [14–16]. In the 1980’s came the association of SS with anti-SSA be lower in China and higher in Japan [8]. While SS is felt to be a and anti-SSB antibodies [17]. In addition, SS was noted to have a strong disease predominantly of women, with a female to male ratio of 9:1, the correlation with chronic fatigue, cholinergic agents were used to in- incidence of SS is likely higher in males than is currently estimated, crease salivary gland flow [18], immunological studies focused on the since males tend to make a different pattern of autoantibodies than hypothesis that SS involves abnormal B cells and T cells of the adaptive females and are often missed with the current diagnostic criteria [9,10]. immune system producing autoreactive antibodies and direct cyto- Dr Johann von Mikulicz-Rdeck, a surgeon from Cernowitz, Austria, toxicity [19], and genetic studies identified particular human leukocyte is credited with identifying the first patient with Sjogren’s syndrome in antigen (HLA) associations with SS [20]. The 21st century has seen a 1892 based on round-cell infiltrate and acinar atrophy of the parotid blossoming of research in SS that has led to improved understanding of ⁎ Corresponding author. E-mail addresses: [email protected] (F.B. Vivino), [email protected] (V.Y. Bunya), [email protected] (G. Massaro-Giordano), [email protected] (C.R. Johr), [email protected] (S.L. Giattino), [email protected] (A. Schorpion), [email protected] (B. Shafer), [email protected] (A. Peck), [email protected] (K. Sivils), [email protected] (A. Rasmussen), [email protected] (J.A. Chiorini), [email protected] (J.L. Ambrus). https://doi.org/10.1016/j.clim.2019.04.009 Received 19 April 2019; Accepted 19 April 2019 Available online 29 April 2019 1521-6616/ © 2019 Published by Elsevier Inc. F.B. Vivino, et al. Clinical Immunology 203 (2019) 81–121 clinical manifestations, greater appreciation of disease pathophysiology submandibular glands may be unilateral or bilateral and observed in up including the involvement of the innate immune system, role of epi- to 30% of SS patients. This swelling can be the presenting manifestation thelial cells and other cell types, determination of contributory genetic of the disease or occur at any point during the course. Patients who factors, development of improved animal models and therapeutic trials present with acute glandular swelling associated with fevers and facial with encouraging outcomes. These are discussed in the remainder of erythema are presumed to have acute bacterial sialadenitis until proven this review. otherwise. An attempt should be made to milk the involved gland and culture the exudate from Stenson's or Wharton's duct. An individual 2. Clinical manifestations who develops salivary gland swelling after eating or chewing most likely has obstructive symptoms due to sialolithiasis or sialostenosis 2.1. Oral manifestations and complications with mucus plugs. When the swelling begins to subside patients may be aware of passing stones or gravel in the mouth or experiencing a sour 2.1.1. Dry mouth taste from a mucus plug. Intermittent or persistent salivary gland Sjögren's is often referred to as the "sicca syndrome" (from the Latin swelling may also be due to inflammatory sialadenitis from lympho- siccus meaning dry or thirsty) and xerostomia is one of its most pre- cytic infiltration of the major salivary glands and is typically responsive valent symptoms. to steroids and other immunosuppressives. Sjögren's patients on chronic Saliva is a chemically complex fluid containing over 2000 proteins or frequent intermittent corticosteroids or with metabolic disorders and various glycoproteins, lipids, electrolytes, small molecules, specific sometimes develop sialadenosis or fatty infiltration of the glands. Any salivary IgA’s, hormones and buffers that all play a vital role inoral individual with persistent glandular swelling despite prolonged therapy health [21]. It preserves the dentition and inhibits the growth of mi- (e.g. > 12 weeks) or whose salivary glands feel indurated or nodular croorganisms; lubricates and protects the tongue and oral mucosa from should undergo imaging and/or a major salivary gland biopsy to rule trauma; facilitates taste, mastication, deglutition, speech and initiates out non-Hodgkin’s B-cell lymphoma. carbohydrate digestion in the mouth [22,23]. Consequently, the oral signs and symptoms of SS extend far beyond those of simple dryness. 2.2. Spectrum of ocular disease Patients may initially notice intermittent daily or nocturnal dryness or cotton mouth sensation that gradually becomes more prominent Dry eye, or keratoconjunctivitis sicca (KCS) is the most common during the day. As the condition progresses Sjögren's sufferers even- ocular manifestation of SS [30]. As such, management of Sjögren's is tually find themselves constantly drinking water. The mucosa becomes heavily focused on ocular surface rehabilitation. However, SS can also traumatized and mouth sores and/or oral discomfort develop. This may lead to other serious vision-threatening ocular complications including eventually lead to glossodynia or stomatopyrosis. The patient may de- corneal melts [31], uveitis [32], scleritis [33], and optic neuritis scribe an unpleasant taste in the mouth or dysgeusia with familiar [34,35] as detailed below. foods. Food particles may stick to the gums and mucosa and, it may be difficult to chew and swallow dry foods without water. Eating becomes 2.2.1. Tear film unpleasant and weight loss ensues. Cheilosis is present. Dry throat, The tear film is critical for maintaining the health of the ocular hoarseness and dysphonia can also occur.
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