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Review Article The eye and visual system in , what to expect? An in‑depth review

Khawla Abu Samra

Department of Ophthalmology, Ross Eye Institute, Buffalo, NY, USA

Pregnancy represents a real challenge to all body pregnancy can affect vision through systemic disease systems. Physiological changes can involve any of the that are either specific to the pregnant state itself such as body organs including the eye and visual system. The the pre‑/eclampsia and Sheehan’s syndrome, ocular effect of pregnancy involves a wide spectrum of or systemic diseases that occur more frequently in physiologic and pathologic changes. The latter might be relation to pregnancy such as Graves’ disease, idiopathic presenting for the first time during pregnancy such as intracranial , anti‑phospholipid syndrome, corneal melting and corneal ectasia, or an already existing and disseminated intravascular . ocular pathologies that are modified by pregnancy such as diabetic retinopathy and glaucoma. In addition, Keywords: Complications, eye, ocular effect, pregnancy

Introduction • Ocular complications of systemic diseases. These are either pregnancy specific diseases such as pre‑eclampsia/eclampsia Pregnancy represents a serious challenge to all body systems. The syndrome and Sheehan syndrome, or diseases that occur more progressive physiological changes that occur are essential to support frequently during pregnancy such as idiopathic intracranial and protect the developing in addition to prepare the mother hypertension (IIH), Graves’ disease, Antiphospholipid for parturition.[1] These physiologic changes involve cardiovascular, syndrome (APS) and disseminated intravascular coagulation [3] renal, pulmonary, hormonal, metabolic, hematologic, immunologic, (DIC). and visual systems.[1] In the presence of clinical or sub‑clinical pathology, the normal physiologic changes of pregnancy can place Although, most of pregnancy ocular complications are mild, significant strain on already compromised systems.[1,2] transient and require no treatment, some are occasionally serious, permanent and require prompt ophthalmic referral. In Ocular complications are common during pregnancy.[3] In general, addition, some ocular complications occurring during pregnancy the ocular effect of pregnancy can be divided in to physiologic and may provide a direct insight in to the pathophysiology of many pathologic changes. The pathologic changes are further divided in systemic diseases. to the following: • Ocular changes occurring for the first time during pregnancy This article provides a review of the physiologic changes of • An already existing ocular pathology that is modified pregnancy, the effect of pregnancy on pre‑existing ocular disease by pregnancy and the ocular manifestations of systemic diseases in pregnant women. The ocular complications of pre‑eclampsia/eclampsia syndrome will be discussed in part 2 of this review. Access this article online Quick Response Code: Website: Physiologic Changes www.ojoonline.org Eyelids DOI: One of the most common ocular physiologic changes includes 10.4103/0974-620X.116626 increased pigmentations around the eye.[4] These pigmentations, known as or chloasma, are reversible and fade slowly

Copyright:  2013 Samra K. A., et al. This is an open‑access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Correspondence: Dr. Khawla Abu Samra, 911 Harvest Lane, Apt 3, Lansing/MI, USA 48917. E‑mail: [email protected]

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Samra: Eye and visual system in pregnancy

after pregnancy. It is postulated that hormonal variations of changes. In one study that was conducted in healthy pregnant pregnancy increase melanin as a result of an increase in both women, Akar et al.[17] found that the VF mean threshold sensitivity melanogenesis and melanocytosis.[4] increased significantly in the third trimester. These asymptomatic VF changes were shown to be completely reversible postpartum.[17] Tear Pregnancy affects the physiology of the tear film resulting in Ocular Diseases Modified by Pregnancy dry eye syndrome.[5] This may occur as a result of the direct disruption of lacrimal acinar cells through pregnancy enhanced Diabetic retinopathy immune‑reactivity of prolactin, transforming growth factor beta 1, The number of women with in pregnancy is increasing, and epidermal growth factor in ductal cells.[5,6] partly as a reflection of increasing obesity in women of child‑bearing age.[18] DR is the most common ocular condition modified by Cornea pregnancy and pregnancy is associated with an increased risk of Cornea may show changes in sensitivity, thickness or curvature. development and progression of DR.[18‑21] Corneal sensitivity tends to decrease, with most changes occur late in pregnancy.[7] A measurable increase in corneal thickness DR developing during pregnancy may show a high‑rate of due to has been reported to occur during pregnancy.[8] An spontaneous regression after delivery. In a study of patients increase in corneal curvature also has been reported.[9] Park et al. with no DR at onset who then developed mild non‑proliferative showed that there was a statistically significant increase in corneal DR (NPDR) during pregnancy, 50% had complete regression, and curvature during the second and third trimesters which resolved 30% had partial regression of DR after delivery.[22] completely after delivery or after the cessation of breast feeding.[9] Factors that have been shown to influence the progression of DR in Changes in thickness may alter the refractive index of the cornea; pregnancy include, the pregnant state itself, duration of diabetes, thereby changing refraction.[10] Many women develop contact degree of retinopathy at time of conception, metabolic control of lens intolerance while pregnant despite a previous success. This diabetes, and the presence of co‑existing hypertension.[23] intolerance may be due to the increase in either corneal curvature or thickness.[10,11] It is advisable that pregnant women wait until at The exact pathogenesis for the progression of DR during pregnancy least several weeks postpartum before obtaining a new spectacle remains controversial. Some studies demonstrated a decrease in prescription or new contact lens fitting.[10,11] retinal venous diameter and volumetric flow in diabetic patients during pregnancy and hypothesized that this may exacerbate Lens retinal and .[24,25] On the other hand, several Transient loss of accommodation has been reported previously studies have reported an increase in retinal blood flow in diabetic both with pregnancy and lactation.[3] The timing for refractive patients during pregnancy and suggested that this hyper‑ surgery in a pregnant or in a woman planning to become causes an added stress to an already compromised retinal circulation pregnant can be a difficult decision. It is better to delay refractive leading to the progression of Diabetic retinopathy (DR).[26] surgery during pregnancy and wait until stability of refraction is clear postpartum.[11] Several studies have shown that higher glycosylated hemoglobin (HbA1C) levels at conception and the rapid tightening of glycemic Intraocular pressure control during pregnancy have been associated with a higher risk IOP decreases during pregnancy.[12,13] Studies in healthy women of DR progression. The diabetes in early pregnancy study showed have shown a statistically significant decrease in IOP during all that elevated HbA1C at baseline was associated with a higher risk trimesters of pregnancy compared with non‑pregnant women.[14] of retinopathy progression and the rates of progression almost IOP declines as pregnancy advances, with statistically significant doubled in women with HbA1C levels greater than 6 standard decrease in IOP from the first to the third trimesters.[13] deviation above the control mean.[19,26]

Immunity Diabetic women in child‑bearing age should be counseled Pregnancy is associated with immune suppression, an essential regarding the risk of development and progression of DR. The risk physiologic element for the implantation of the embryo.[15] It of retinopathy progression during pregnancy is higher in patients is associated with lower rates of flare‑ups of non‑infectious with inadequate glycemic control, thus, whenever possible, tight uveitis compared to the non‑pregnant state.[14] Pregnancy has glycemic control should be attained before conception.[27] a beneficial effect on number of uveitis syndromes including Vogt‑Koyanagi‑harada syndrome, Behcet disease and the Patients with severe NPDR or proliferative DR (PDR) are at a idiopathic uveitis syndrome.[14,16] higher risk of progression during pregnancy thus, it is advisable to postpone conception until stabilization of their ocular disease.[27] Visual field VF changes have been reported in pregnant women.[17] Wide Diabetic patients with PDR during pregnancy should be managed speculation exists about the degree and mechanism of these the same way as non‑pregnant patient. However, retinopathy level

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Samra: Eye and visual system in pregnancy

should be monitored closely and treatment initiated early once infarcted or hemorrhagic pituitary adenoma.[34] VF defect presents indicated. Guidelines for screening of diabetic women include, in 64% of cases and visual acuity (VA) abnormalities present in an ophthalmic evaluation before conception and then again in 52% of cases. VF defect results from upward expansion of the the first trimester. Subsequent examination depends on the level tumor, which compresses the optic chiasm, optic tracts, or optic of retinopathy. Women with are not at an nerve. The classic VF defect is a bitemporal superior quadrantic increased risk of DR and thus, don’t need to be examined under defect.[3,34] these guidelines.[19,25‑27] Ophthalmoplegia occurs in 78% of cases. It results from Glaucoma compression of the cavernous sinus, which makes cranial nerves It was mentioned earlier that IOP decreases during pregnancy III, IV, and VI vulnerable to injury. Oculomotor nerve is involved as part of normal physiologic changes.[12,13] During pregnancy the most commonly, resulting in a unilateral dilated pupil, ptosis, women with ocular hypertension demonstrate a similar decrease with inferiorly and laterally deviated globe.[33,34] in IOP that becomes notable during the second trimester and decreases further with advancing pregnancy.[28] The decrease in Cranial nerve IV is also involved resulting in vertical diplopia. The IOP during pregnancy is likely multifactorial. Theories to explain sixth cranial nerve is least commonly involved, perhaps because the mechanisms of IOP drop include, special consideration to of its sheltered in the cavernous sinus. Its involvement hormonal levels that fluctuate during pregnancy such as estrogen, produces horizontal diplopia. Horner syndrome may develop relaxin, progesterone, and human chorionic gonadotrophin‑ and from damage to the sympathetic fibers. second messenger systems that result in increased outflow facility and in decreased episcleral venous pressure.[29] Following pituitary apoplexy, resolution of ophthalmoplegia is more likely to occur than recovery of vision.[34] In general, pre‑existing glaucoma improves and few cases of glaucoma are diagnosed during pregnancy.[30] However, there are Graves’s disease few case reports described women with glaucoma whose IOP was Thyroid disorders are prevalent in women of child‑bearing difficult to control during pregnancy, despite medical and surgical age thus it is commonly present in pregnancy and the intervention.[31,32] puerperium.[35] Hyperthyroidism occurs in 2/1000 , the most common cause (85%) being Graves’ disease.[35] It is common for patients to be hesitant to take during pregnancy because of the potential teratogenic adverse Recognition of hyperthyroidism during pregnancy can be elusive effects. Whenever possible, physicians should address glaucoma because signs overlap with pregnancy symptoms such as nausea management options in all women of child‑bearing age before and vomiting, increased appetite, heat intolerance, fatigue, and conception. With proper planning, surgical treatments such as irritable or anxious mood. Symptoms uncommon in normal laser trabeculoplasty can be offered in anticipation of decreasing pregnancy, but found in hyperthyroidism, are weight loss or failed or stopping medication use during pregnancy when choosing weight gain despite increased dietary intake, resting tachycardia, IOP‑lowering for use during pregnancy, it is wise to hypertension, tremor, thyroid enlargement or nodule, and ocular consider the pregnancy safety categories and to work closely with manifestations.[35,36] Abnormal eye findings in Grave’s diseases the patient’s obstetrician.[31,32] are common. These include, eye stare, eyelid lag, proptosis, and extraocular muscle palsy.[35] Systemic Disease with Ocular Complications Graves’s disease is known to exacerbate in the first trimester and Systemic diseases with ocular complications occurring during to improve in the second and third trimesters of pregnancy. Close pregnancy are either specific to the pregnancy itself such as the monitoring in the is important, as disease eclampsia/pre‑eclampsia complex, and Sheehan syndrome, or flares have been reported. Care of women with Graves’s disease in occur more in relation to pregnancy such as Graves’ disease, IIH, pregnancy should be multidisciplinary and involve an obstetrician APS, and DIC. familiar with the management of maternal medical conditions, an endocrinologist, and an ophthalmologist. Women with proptosis Sheehan syndrome or other eye findings should be referred to an ophthalmologist One of the most common causes of hypopituitarism in the developing for evaluation and management of ophthalmopathy, which countries is an ischemic necrosis of the pituitary gland due to may be present in as many as half the cases of Graves’s disease. severe postpartum hemorrhage.[33] It is considered a potentially Management with anti‑thyroid medications is standard during visually‑threatening disorder as a result of sudden increase in pregnancy, reserving surgery for complicated cases.[35,36] pituitary size from infarction or hemorrhage. It may present as a sudden onset of headache, visual loss, and/or ophthalmoplegia.[34] IIH IIH is a disease of unknown etiology associated with increased The symptomatology of pituitary apoplexy is dependent on intracranial pressure. The disease predominantly affects compression of the neighboring structures by the expanding obese females of child‑bearing age, thus occurring frequently

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Samra: Eye and visual system in pregnancy

in pregnancy.[37] The annual incidence of IIH is 1‑2 per of the overlying retinal pigment epithelium causing serous retinal 100,000 populations, with at least a three‑fold higher incidence detachment (SRD).[42] in obese females between the ages of 15 and 44.[37] Headache is the most common symptom, presenting in 92% of patients and is Conclusion frequently associated with nausea and vomiting.[37,38] Visual disturbances are very common during pregnancy. Ocular manifestations of IIH include, obscuration of vision, Physicians should have a firm understanding of the various blurring, scotomata, photopsias, diplopia, and retrobulbar ocular conditions that might appear pregnancy or get modified by [37,38] pain. On physical examination, most patients exhibit pregnancy. In addition, it is very important to be vigilant about the papilledema as the only objective finding. Papilledema is typically rare and serious conditions that may occur in pregnant women bilateral, but may be markedly asymmetric, unilateral, or even with visual complaints. Prompt evaluation may be required and absent in some cases. The degree of optic nerve head swelling the immediate transfer of care of the patient may help saving the does not always correlate well with intracranial pressure, but lives of both the mother and the baby. may correlate with higher risk of permanent visual loss.[37,38] Up to 20% of IIH patients may also exhibit abducens nerve palsy, a false localizing sign secondary to elevated intracranial pressure. References Patients may less commonly exhibit other signs that can affect 1. Carlin A, Alfirevic Z. Physiological changes of pregnancy and monitoring. visual function such as coulometer and trochlear cranial nerve Best Pract Res Clin Obstet Gynaecol 2008;22:801‑23. deficits.[37,38] 2. Thornburg KL, Jacobson SL, Giraud GD, Morton MJ. 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