Ocular Manifestations in Colombian Patients with Systemic Rheumatologic Diseases

Figures & data

Table 1 Sociodemographic Data

Variable	Data n (%)
Female	670 (84.06%)
Age (mean, SD)	54.61 ± 15.64 years
Active smokers	49 (6.14%)
Past smokers	178 (22.33%)
Tattoos	16 (2%)
Silicon prosthesis	22 (2.76%)
Family history of autoimmune disease	211 (26.47%)
Mean age of autoimmune disease diagnosis	Female: 45.88 years Male: 50.656 years

Abbreviation: SD, Standard deviation.

Figure 1 Most common rheumatologic and ophthalmologic diagnoses.

Table 2 Ocular Symptoms and Ophthalmological Diagnosis for Each Rheumatologic Disease

		Sample n (%)	Ocular Symptoms	Ophthalmological Diagnosis
Connective tissue disease
Rheumatoid arthritis		266 (33.37%)	80 (30.08%) *	49 (18.42%)
Sjögren syndrome		157 (19.72%)	117 (74.72%) **	123 (78.34%) **
Systemic Lupus Erythematosus		79 (9.91%)	34 (43.03%)	19 (24.05%)
Polyautoimmunity		55 (6.9%)	24 (43.63%)	23 (41.82%) **
Systemic sclerosis		42 (5.27%)	19 (45.23%)	9 (21.43%)
Localized Scleroderma		13 (1.63%)	3 (23%)	1 (7.7%)
Undifferentiated Connective Tissue Disease		46 (5.78%)	17 (37%)	6 (13%)
Juvenile Idiopathic Arthritis		5 (0.62%)	0	0
Mixed Connective Tissue Disease		4 (0.5%)	1 (25%)	0
Sarcoidosis		3 (0.38%)	1 (33.33%)	0
Spondyloarthropathies
Ankylosing Spondylitis		25 (3.14%)	4 (16%)	3 (12%)
Psoriatic Arthritis		19 (2.38%)	1 (5.26%) *	1 (5.2%)
Axial undifferentiated spondylitis		18 (2.26%)	5 (27.78%)	3 (16.66%)
Undifferentiated peripheral spondylitis		5 (0.63%)	0	0
Reactive Arthritis		5 (0.63%)	1 (20%)	0
Reiter syndrome		2 (0.25%)	2 (100%)	1 (50%)
Enteropathic arthritis	Chron Disease	3 (0.38%)	1 (33.3%)	0
	Ulcerative Colitis	1 (0.125%)	0	0
	Celiac disease	1 (0.125%)	1 (100%)	1 (100%)
Myositis
Polymyalgia rheumatica		35 (4.39%)	10 (28.57%)	5 (14.29%)
Dermatomyositis		7 (0.88%)	3 (42.85%)	3 (42.86%)
Polymyositis		2 (0.25%)	0	1 (50%)
Autoimmune glandular disease
Hashimoto thyroiditis		20 (2.51%)	11 (55%)	6 (30%)
Graves’ disease		10 (1.25%)	1 (10%)	1 (10%)
Type 1 Diabetes		1 (0.13%)	1 (100%)	0
Autoimmune hematologic diseases
Antiphospholipid Syndrome		43 (5.4%)	14 (32.55%)	8 (18.6%)
Autoimmune thrombocytopenic purpura		4 (0.50%)	0	0
Pernicious anemia		2 (0.25%)	2 (100%)	0
Autoimmune hemolytic anemia		1 (0.13%)	0	0
Vasculitis
Vasculitis associated with probable etiology		10 (1.25%)	3 (30%)	2 (20%)
Vasculitis associated with a systemic disease		3 (0.38%)	2 (66.67%)	2 (66.67%)
Medium size vessel vasculitis		3 (0.38%)	1 (33.33%)	1 (33.33%)
Small size vessel vasculitis associated with ANCA		3 (0.38%)	1 (33.33%)	2 (66.67%)
Behcet Disease		3 (0.38%)	1 (33.33%)	1 (33.33%)
Large size vessel vasculitis		2 (0.25%)	2 (100%)	1 (50%)
Henoch-Schönlein purpura		1 (0.13%)	0	0
Autoimmune dermatologic diseases
Psoriasis		18 (2.26%)	1 (5.55%) **	2 (11.1%)
Vitiligo		3 (0.38%)	1 (33.3%)	1 (33.3%)
Pemphigoid		1 (0.13%)	1 (100%)	0
Autoimmune liver diseases
Primary biliary cholangitis		1 (0.25%)	0	1 (50%)
Autoimmune hepatitis		8 (1%)	5 (62.5%)	2 (25%)
Sclerosing cholangitis		1 (0.13%)	1 (100%)	0
Autoimmune neurological diseases
Multiple Sclerosis		5 (0.63%)	3 (60%)	3 (60%)
Neuromyelitis Optica		2 (0.25%)	2 (100%)	2 (100%)
Myasthenia gravis		2 (0.25%)	1 (50%)	0
Other rheumatologic diseases
Fibromyalgia		181 (22.71%)	63 (34.8%)	36 (19.88%)

Notes: p-value is based in Chi-square proof with a 95% (*) and 99% (**) confidence level.

Table 3 Ophthalmological Diagnoses Associated to the Main Rheumatologic Diseases

Rheumatologic/Ophthalmological Diagnoses	Rheumatoid Arthritis		Sjögren Syndrome		SLE		Fibromyalgia		Total Per Symptom
	Ocurrence	p-value	Ocurrence	p-value	Ocurrence	p-value	Ocurrence	p-value	Ocurrence	%
Keratoconjunctivitis sicca	34 (12.78%)	0.1	121 (77.07%)	0.0001**	16 (20.25%)	0.34	28 (15.46%)	0.93	127	15.93%
Uveitis	3 (1.13%)	0.91	2 (1.27%)	1	0		1 (0.55%)	0.93	11	1.38%
Cataract	4 (1.5%)	1	1 (0.63%)	0.6	1 (1.26%)		1 (0.55%)	0.46	11	1.38%
Scleritis	6 (2.25%)	0.14	3 (1.91%)	0.67	0		0	0.17	10	1.25%
Keratitis	2 (0.75%)	0.89	6 (3.82%)	0.0004**	2 (2.5%)	0.4	2 (1.1%)	1	8	1.0%
Glaucoma	2 (0.75%)	1	2 (1.27%)	0.9	0	0.8	2 (1.1%)	1	7	0.88%
Anterior uveitis	1 (0.37%)	0.49	2 (1.27%)	0.9	0		0		7	0.88%
Optic neuritis	0		2 (1.27%)	0.56	2 (2.5%)	0.13	1 (0.55%)	1	5	0.63%
Maculopathy	3 (1.13%)	0.21	1 (0.63%)	1	0		2 (1.1%)	0.47	4	0.5%
Conjunctivitis	1 (0.37%)	1	1 (0.63%)	1	1 (1.26%)	0.86	0		4	0.5%
Episcleritis	1 (0.37%)	1	1 (0.63%)	1	0		0		3	0.38%
Exoftalmos	0		0		0		0		2	0.25%
Peripheral ulcerative keratitis	1 (0.37%)	1	1 (0.63%)	0.85	0		0		2	0.25%
Ocular Surface Squamous Neoplasia	2 (0.75%)	0.21	0		0		0		2	0.25%
Retinal vasculitis	0		0		0		0		1	0.13%
Panuveitis	0		0		0		0		1	0.13%
Posterior uveitis	0		0		0		0		1	0.13%
Corneal perforation	1 (0.37%)	0.72	1 (0.63%)	0.44	0		0		1	0.13%
Macular edema	1 (0.37%)	0.72	0		0		0		1	0.13%
Central retinal artery ocussion	0		1 (0.63%)	0.44	0		1 (0.63%)	0.44	1	0.13%
Blind eye	0		0		0		0		1	0.13%
Retinal detachment	1 (0.37%)	0.72	1 (0.63%)	0.44	0		1 (0.63%)	0.44	1	0.13%

Notes: **p-value is based in chi squared proof with a 99% confidence level.

Table 4 Ophthalmological Symptoms Associated to the Main Rheumatologic Diseases

Disease/Symptom	Rheumatoid Arthritis		Sjögren Syndrome		SLE		Fibromyalgia		Total Per Symptom
	Ocurrence	p-value	Ocurrence	p-value	Ocurrence	p-value	Ocurrence	p-value	Ocurrence	%
Dry eye	72 (27%)	0.106	113 (72.43%)	0.000**	28 (35.9%)	0.385	57 (31.49%)	0.928	246	30.86%
Ocular pain	9 (3.4%)	0.595	4 (2.56%)	1,00	1 (1.27%)	0.616	3 (1.67%)	0.446	22	2.76%
Red eye	10 (3.77%)	0.244	6 (3.82%)	0.456	2 (2.5%)	1,00	3 (1.66%)	0.497	21	2.63%
Decreased VA	4 (1.5%)	0.236	6 (3.82%)	0.452	2 (2.5%)	1,00	2 (1.10%)	0.229	21	2.63%
Photophobia	2 (0.75%)	0. 213	3 (1.91%)	1,00	6 (7.6%)	0.000**	1 (0.55%)	0.276	14	1.76%
Floaters	3 (1.13%)	1,00	1 (0.63%)	0.815	0		3 (1.66%)	0.716	9	1.13%
Burning	3 (1.12%)	0.668	2 (1.27%)	0.745	0				6	0.75%
Foreign body sensation	1 (0.37%)	0.872	2 (1.27%)	0.564	0		0		5	0.63%
Tearing	3 (1.12%)	0.431	2 (1.27%)	0.563	0		2 (1.10%)	0.697	5	0.63%
Pruritus	2 (0.75%)	0.863	1 (0.63%)	1,00	0		3 (1.66%)	0.057*	4	0.5%
Diplopia	0		0		1 (1.27%)	0.475	0		2	0.25%

Notes: ** p-value is based in chi squared proof with a 95% confidence level. * p-value asymptotically significant for a 95% confidence level.

Table 5 Literature Reported Ophthalmological Symptoms and Diseases Associated to Rheumatologic Diseases

Rheumatologic Disease	Literature
Connective tissue disease
Rheumatoid arthritis	Ocular involvement 10–58%,^Citation21^–^Citation25 Dry eye 10–58%,^Citation21^–^Citation25 Scleritis 1–5%,^Citation21^–^Citation30 Anterior uveitis 4%,^Citation31 Keratitis 3%,^Citation23 PUK <1%^Citation24
Sjögren syndrome	Ocular involvement 89–96%,^Citation21,Citation33,Citation34 Dry eye and KCS the most common 90–97%,^Citation21,Citation32,Citation34^–^Citation37 Corneal scarring 4.3%,^Citation14 Corneal perforation 3.1%,^Citation14 ON 1.8%,^Citation14 Uveitis 1.2%,^Citation14 Corneal ulcer 0.6%,^Citation14 Scleritis/episcleritis 0.6%^Citation14
Systemic Lupus Erythematosus	Ocular involvement in one third of the patients,^Citation21,Citation38^–^Citation42 KCS most common ocular manifestation 25%,^Citation41,Citation43,Citation44 Retinal Vasculitis 7%,^Citation45 ON 1%,^Citation45 Uncommon, PUK,^Citation39 Scleritis,^Citation39 Epiescleritis,^Citation39 Choroidopathy with serous detachments,^Citation39 Orbit myositis,^Citation39 Internuclear Ophthalmoplegia,^Citation39 Blepharospasm,^Citation39 Retinal Necrosis,^Citation39 Uveitis^Citation40
Polyautoimmunity	Dry eye Secondary Sjögren Syndrome and rheumatoid arthritis 4–18%,^Citation51,Citation52 Dry eye Secondary Sjögren Syndrome and Systemic Lupus Erythematosus 11%,^Citation51 Thyroid-associated orbitopathy Celiac disease and HT or GD,^Citation53 Dry eye Secondary Sjögren Syndrome and Primary Biliary Cirrhosis^Citation54
Systemic sclerosis	Pinguecula 82.2%,^Citation55 KCS 14.2–79%,^Citation17,Citation56,Citation57 Eyelid stiffness 29–65%,^Citation57^–^Citation59 Astigmatism 55%,^Citation60 Glaucoma 23%,^Citation55 Loss of sackcloth 15.6%,^Citation55 Uveitis 3%^Citation60
Localized Scleroderma	Ocular manifestations 2.1–6,7%,^Citation61,Citation62 Glaucoma,^Citation63 Uveitis,^Citation61,Citation62 Eyelid/eyelash involvement,^Citation62 Epiescleritis,^Citation61,Citation62 Dry eye,^Citation61 Keratitis,^Citation61 Papiledema^Citation61
Undifferentiated Connective Tissue Disease	Scleritis,^Citation64 ON,^Citation65 Corneal thinning^Citation66
Juvenile Idiopathic Arthritis	Uveitis 17%-12%,^Citation67,Citation68 Band keratopathy 7–70%,^Citation69,Citation70 Ocular hypotony 19%,^Citation70 KCS 8.5%^Citation70
Mixed Connective Tissue Disease	KCS (48%),^Citation71 Maculopathy (5%),^Citation72 Retinal vasculitis,^Citation73,Citation74 NO^Citation75
Sarcoidosis	Ocular involvement 13–79%,^Citation21,Citation76^–^Citation78 Uveitis,^Citation79 Scleritis,^Citation80 Dry eye,^Citation79,Citation80 Conjunctival nodules^Citation79
Spondyloarthropathies
Ankylosing Spondylitis	Uveitis 10–50%,^Citation17,Citation81^–^Citation83 Dry eye^Citation84
Psoriatic Arthritis	Ocular involvement 22.5–31.25%,^Citation85,Citation86 KCS 15%,^Citation86 Glaucoma 10%,^Citation86 Cataract 10%,^Citation86 Pinguecula 20.0%,^Citation86 Pterygium 5%,^Citation86 Uveitis 5%^Citation85,Citation86
Axial undifferentiated spondylitis	Uveitis 17%,^Citation87 Dry eye,^Citation84
Undifferentiated peripheral spondylitis	Uveitis 8%^Citation88
Reactive Arthritis	Conjunctivitis 10.52%,^Citation17 Uveitis 5.26%^Citation17
Reiter syndrome
Enteropathic arthritis	Chron Disease	Ocular involvement 10–43%,^Citation89,Citation90 Ocular inflammatory disorders 0.3–13%,^Citation8 Episcleritis (2–5%),^Citation8 Uveitis(0.5%-3.5%),^Citation8 Scleritis;^Citation8 KCS^Citation8
	Ulcerative Colitis
	Celiac disease	Dry eye,^Citation53 Cataract,^Citation53 Uveitis,^Citation53 NO,^Citation53 Orbital myositis,^Citation53 CRVO,^Citation53 nyctalopia^Citation53
Myositis
Polymyalgia rheumatica	Uveitis,^Citation11,Citation91 Scleritis and necrotizing scleritis,^Citation11,Citation91,Citation92 Episcleritis^Citation11,Citation92,Citation93
Dermatomyositis	Dry eye,^Citation94 Macular edema,^Citation94 Retinitis,^Citation94 CRAO^Citation94
Polymyositis	Dry eye^Citation18
Autoimmune glandular disease
Hashimoto thyroiditis	Thyroid-associated ophthalmopathy 22%,^Citation95^–^Citation97 Dry eye,^Citation96,Citation97 Proptosis,^Citation95^–^Citation97 Ocular myopathy^Citation95^–^Citation97
Graves’ disease	Ocular involvement 67%,^Citation98 Thyroid-associated ophthalmopathy 25%,^Citation99 Dry eye 11%,^Citation98 Proptosis,^Citation98 Lid lag^Citation98
Type 1 Diabetes	Macular edema,^Citation100 Glaucoma,^Citation100 RD;^Citation100 Cataract,^Citation100 Dry eye^Citation101,Citation102
Autoimmune hematologic diseases
Antiphospholipid Syndrome	Ocular involvement 8–88%,^Citation21,Citation103^–^Citation106 CRVO,^Citation104,Citation107^–^Citation109 CRAO,^Citation104,Citation107^–^Citation109 Branch retinal vein occlusion,^Citation104,Citation107^–^Citation109 Branch retinal artery occlusion,^Citation104,Citation107^–^Citation109 KCS,^Citation104 Anterior uveitis,^Citation110 Retinal vasculitis,^Citation110 Scleritis and necrotizing scleritis^Citation106,Citation111
Autoimmune thrombocytopenic purpura	Spontaneous bilateral peripapillary,^Citation112 subhyaloid and vitreous hemorrhage,^Citation112 Massive subretinal hemorrhage,^Citation113 Purtscher’s retinopathy;^Citation114 Progressive retinopathy,^Citation115 Valsalva retinopathy,^Citation116 Suprachoroidal hemorrhage simulating melanoma^Citation117
Pernicious anemia	ON,^Citation118,Citation119 Delayed visual evoked potential,^Citation120 Retrobulbar neuritis^Citation121,Citation122
Autoimmune hemolytic anemia	Retinal phlebitis,^Citation123 Bilateral macular hemorrhage^Citation124
Vasculitis
Vasculitis associated with probable etiology	No prevalence data
Vasculitis associated with a systemic disease	Episcleritis,^Citation125 Scleritis,^Citation125 PUK,^Citation125 Uveitis,^Citation125 Retinopathy^Citation125
Medium size vessel vasculitis	CRAO,^Citation126,Citation127 ON,^Citation126 Scleritis,^Citation127 Non granulomatous uveitis,^Citation127 Retinal vasculitis,^Citation127 PUK,^Citation127 Pseudotumor of the orbit^Citation127
Small size vessel vasculitis associated with ANCA	Ocular involvement 12.5–15.62%,^Citation16,Citation128 ON 50%,^Citation128 Scleritis 28%,^Citation128 Iritis 28%,^Citation128 Retinal vasculitis 17%,^Citation128 Oculomotor disorder 17%,^Citation128 PUK 11%^Citation128
Behcet Disease	Cataract 30.3%,^Citation129 Panuveitis 20%,^Citation129 Posterir uveitis 15.1%,^Citation129 Anterior uveitis 63.2%,^Citation130 Periphebitis 65%,^Citation130 Optic atrophy,^Citation129 RD,^Citation129 Macular edemar,^Citation129 Papillary edema,^Citation129 Ocular hypertonia,^Citation129 retinal ischemia^Citation129
Large size vessel vasculitis	Anterior ischemic optic neuropathy 81%,^Citation131 Ocular involvement 40–80%,^Citation132 Amaurosis fugax 25.6–30.6%,^Citation131,Citation133 Cilioretinal artery occlusion 22%,^Citation131 CRAO 14%,^Citation131 Posterior ischemic optic neuropathy 7%^Citation131
Henoch-Schönlein purpura	Anterior uveitis,^Citation134 Anterior ischemic neuropthy,^Citation135 Cystoid macular edema,^Citation136 Retinal hemorrhages,^Citation136 Cotton wool spots,^Citation136 Episcleritis^Citation137
Autoimmune dermatologic diseases
Psoriasis	Ocular involvement 10–67%,^Citation138^–^Citation140 Anterior uveitis 82%,^Citation85 Bilateral uveitis 64%,^Citation85 Cataract 28–30.2%,^Citation85,Citation141 KCS 16.28%,^Citation141 Posterior uveitis 9.9%,^Citation85 Macular edema 7.2%,^Citation85 Intermediate uveitis 3.3%,^Citation85 Central serous chorioretinopathy 2.4%,^Citation85 Episcleritis 2.4%,^Citation85 Glaucoma 2.3%,^Citation141 Retinal vasculitis 1.6%^Citation85
Vitiligo	Ocular involvement 22.2–66.6%,^Citation142,Citation143 Pigmentation on anterior chamber 18%,^Citation143 Retinal pigment epithelium hypopigmentation 9%,^Citation143 Uveitis 5%,^Citation143 Hypopigmented spots on the iris 3%,^Citation143 KCS^Citation143,Citation144
Pemphigoid	Conjunctival erosions 33.3%,^Citation145,Citation146 Epiphora 23.9%,^Citation145 Eyelid and medial epicanthus erosion 20.8–41.6%,^Citation145,Citation146 Dry eye;^Citation146 Conjunctival fibrosis,^Citation145,Citation146 Symblepharon,^Citation146 Ankyloblepharon,^Citation146 Frozen eye^Citation146
Autoimmune liver diseases
Primary biliary cholangitis	Refractive issues 27.8%,^Citation147 Cataract 12.5%,^Citation147 Dry eye and KCS,^Citation54,Citation147 Panuveitis,^Citation148 Persistent subretinal, Fluid due to central serous chorioretinopathy^Citation147,Citation148
Autoimmune hepatitis
Sclerosing cholangitis
Autoimmune neurological diseases
Multiple Sclerosis	Ocular pain 92%,^Citation149 Dyschromatopsia 88%,^Citation149 ON 25–75%,^Citation150^–^Citation152 Intranuclear ophthalmoplegia 30%,^Citation153 Intermediate uveitis 28.3%,^Citation154 Marcus Gunn pupil,^Citation155 Retinal periphlebitis^Citation154
Neuromyelitis Optica	Decreased VA 80%,^Citation156,Citation157 Anterior ON 40%,^Citation156 Retrobulbar ON 36%,^Citation156 Oculomotor abnormalities,^Citation158 Intranuclear ophthalmoplegia^Citation158
Myasthenia gravis	Ophthalmoparesis in eyelid elevators and extraocular muscles,^Citation159,Citation160 Decreased VA,^Citation161 Dry eye.^Citation162
Other rheumatologic diseases
Fibromyalgia	Dry eye,^Citation49 Scleritis,^Citation163^–^Citation165 Decreased retinal nerve fiber layer^Citation166

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