Introduction

The number of patients with glaucoma in Europe is predicted to increase considerably due to an aging population,^1,2 possibly leading to an increased burden on glaucoma services in the future. In Sweden, it is estimated that glaucoma accounts for every fourth patient seen within the eye care system,³ and the number of patients with intraocular pressure (IOP)-lowering treatment is expected to increase by 50% in 2040.⁴ Since health care resources are limited, glaucoma management strategies need to be adopted. Patients with glaucoma have a considerable risk of loss of vision-related quality of life (VRQoL),⁵ and up to 16% become bilaterally blind due to the disease.^6,7 However, the visual disability risk and loss of VRQoL varies among patients. Patients with elevated IOP and pseudoexfoliation syndrome (PEX) are at a higher risk of developing glaucoma^8–11 compared with patients with elevated IOP alone. In addition, patients with pseudoexfoliation glaucoma (PEXG) progress faster^12–14 and become visually disabled more often compared to patients with open-angle glaucoma.¹⁵ PEX is common in the Nordic Countries and PEXG constitutes a large proportion of all glaucoma cases found in Sweden.¹⁶ Therefore, it is of importance to detect and treat patients with PEX and PEXG at early stages to reduce the risk of glaucoma related visual disability and loss of vision-related quality of life.

In Sweden, patients with glaucoma are mainly identified based on opportunistic case findings because there is no systematic population screening for glaucoma. Since tonometers became more commonly used by Swedish optometrists around the end of the 1990s, an increasing number of patients with glaucoma have been identified because of referrals from optometrists.¹⁷ In Sweden, primary care optometrists can refer directly to secondary eye care units (Figure 1) in cases of suspected eye pathology; however, the conditions for optometrists to examine the eye have changed considerably during the past 30 years. Since 1994, the Swedish optometry education leads to a Bachelor of Science (BSc) in optometry. In 2009, the first class of optometrists with master’s degrees graduated, and these optometrists have been allowed to use diagnostic eye drops since 2016. However, optometrists in Sweden are not allowed to prescribe any therapeutic drugs and all patients with glaucoma are treated and followed by secondary eye care units (Figure 1). An increasing number of optometrists with a Master of Science (MSc) work in opticians’ offices outside of the hospital system (I-level; Figure 1) but those with a BSc still form the majority. In January 2024, the national regulations for the optometry profession were revised.¹⁸ One important change is that referrals from optometrists to physicians should now only be made in cases where further investigations are needed, and treatment is expected.

Figure 1 Organization and care levels of glaucoma care in Sweden. Eye care in Sweden is organized into three different levels. Optometrists and general practitioners deliver primary (I-level) eye care, while private ophthalmologists and public care units such as public hospitals and outpatient clinics provide secondary (II-level) eye care. Complex cases are managed, and surgical treatment is provided only in tertiary (III-level) eye care hospitals (mainly university hospitals). Usually, patients are referred from one care level to the next; however, individuals can request care without referral to a secondary eye care level. Tertiary eye care is only available through referrals from secondary care units. The image is the property of the authors.

The new Swedish national guidelines for open-angle glaucoma, published in Swedish in September 2022 and in English in 2024,¹⁹ emphasize the importance of determining the right level of eye care for patients with low risk of developing glaucoma, those with high-risk factors for glaucoma, and those with the manifest disease. In addition, specific requirements for glaucoma referrals from optometrists (I-level; Figure 1) to secondary glaucoma care facilities (II-level; Figure 1) were put in place to minimize the number of false-positive referrals and to use the limited health care resources more efficient. According to the new glaucoma guidelines, the required level of IOP for referrals from optometrists is lower (≥ 22 mmHg) when the optometrist detects PEX compared to referrals based solely on an elevated IOP (≥ 25 mmHg).⁹ Hence, PEX assessment by primary care optometrists has become more important in Sweden in order to reduce the risk of missing individuals with high risk for glaucoma. Still the frequency and accuracy of optometrists’ PEX assessments in Sweden are unknown.

In 2019, we conducted a prospective study evaluating all glaucoma referrals with elevated IOP from optometrists to the Skåne University Hospital Ophthalmology Department in Malmö, Sweden.²⁰ This study gave us the opportunity to evaluate PEX assessment in glaucoma referrals from optometrists before the new glaucoma guidelines were established. In addition, we evaluated an optometrist’s ability to identify PEX compared to an ophthalmologist specialized in glaucoma.

Materials and Methods

The Ethics Review Board of Lund University, Sweden, approved this study and the methods used adhered to the Declaration of Helsinki. All participants provided written informed consent. We conducted a prospective study to evaluate the outcomes of glaucoma referrals over a twelve-month study period between January 1st and December 31st, 2019 from optometrists in Sweden to the Skåne University Hospital, Department of Ophthalmology Malmö. We previously published results from this study concerning the effect of elevated IOP as the only referral criterion.²⁰ Only referrals from optometrists based on an IOP of ≥ 21 mmHg and concerning adult patients (≥ 18 years) without symptoms of acute angle closure were eligible. Patients already receiving treatment for glaucoma or ocular hypertension (OH) were not eligible. The study design has been presented in detail previously.²⁰ Briefly, study visits followed a standardized examination protocol including visual acuity, automated refraction, automated visual field measurement, PEX and anterior chamber depth assessments, IOP measurement with Goldman applanation tonometry, measurement of central corneal thickness, fundus photography and optical coherence tomography of the optic disc. The study optometrist (K.L)., holding an MSc, performed all the examinations.

In addition, the study optometrist assessed PEX in the slit lamp before and after pupil dilatation, with possible options of “PEX”, “no PEX” or “unsure”. The study ophthalmologist then assessed PEX in the slit lamp after dilatation. The ophthalmologist’s assessment of PEX was decisive. PEX was defined as the presence of small, grey-white fibrillar aggregates on the anterior lens capsule and tiny flakes of dandruff-like dustpans in the pupillary border. PEX assessment was performed with as little previous information as possible; the study optometrist did not have access to information from the referral letters before the study visit. In addition, all participants were requested not to reveal any eye-related information to the study optometrist until all assessments were completed. The study optometrist assessed PEX after visual acuity and visual field tests but before any other assessments. The eyes were dilated with 0.5% tropicamide and 2.5% phenylephrine, and the optometrist assessed PEX again 10 min after administration. The ophthalmologist was blinded to all the examination results obtained by the optometrist during the study visit until the PEX assessment was performed. Clinical examinations of the anterior and posterior segments of the slit lamp were performed by the study ophthalmologist (D.P).

The optometrist had no previous clinical experience with PEX assessment; however, some patients diagnosed with PEX had been examined by the optometrist over the course of a couple of months before the study began. During the study, the optometrist received direct feedback on the PEX assessments, as the ophthalmologist’s assessments were revealed to the study optometrist directly after each visit. This clinical study was conducted over 12 months.

Similar to the previous study,²⁰ glaucoma was defined either as repeatable glaucoma-specific visual field defects or glaucoma-specific visual field defects confirmed by the corresponding optic nerve head appearance. In addition, patients with PEX were diagnosed with PEXG, glaucoma suspect with PEX, PEX with OH, or PEX with normal IOP.

In this study, referrals based on an IOP of up to 24 mmHg were selected and then reviewed to identify any additional examinations included in the referral (such as visual field measurements or optic nerve head evaluation) which fall under the new guidelines for accepting referrals by secondary care. In addition, all referrals, regardless of the IOP level, were reviewed to establish the number of referrals that included PEX assessment. In the first step, referrals including information from a slit-lamp examination by the optometrist were identified. Results from slit-lamp examinations in these referrals were then reviewed for any information on PEX and other glaucoma-relevant findings. In addition, referrals were reviewed for all patients for whom PEX was identified during the study visit. We recorded the diagnoses as defined above and identified hypothetical missed cases (according to the new guidelines) for referrals with PEX assessment by the optometrists and those concerning patients found with PEX during the study visit. We also evaluated whether these referrals fell within or outside the new requirements for referrals in the national guidelines.

Results

In total, 95 referrals (95 patients; 189 eyes) were included in this study, 34% (32/95) of which included an IOP of 21–24 mmHg. Of those referrals, 19% (6/32) included the results of a slit-lamp examination, and 6% (2/32) included a PEX assessment. Five referrals included both an optic nerve head evaluation and visual field measurement (5/32, 16%) and two referrals included only optic nerve head evaluation (2/32, 6%). In total, 25 referrals were based solely on an IOP of 21–24 mmHg. We found neither glaucoma nor OH requiring IOP-lowering treatment in 80% of these referrals (20/25).

Of all the referrals, 17% (16/95) included a slit-lamp examination, but only 7% (7/95) of the referrals assessed PEX. Of these, three were positive, and four were negative for PEX (Table 1). Other glaucoma-related assessments described in the referral text were anterior chamber depth evaluation (seven referrals) and pigment dispersion syndrome assessment (two referrals, one with a positive finding later confirmed by the ophthalmologist). In total, 23% of all referrals (22/95) included either visual field measurement, optic nerve head assessment, or both.

Table 1 Clinical Characteristics and Hypothetical Referral Acceptance, According to the New Glaucoma Guidelines,10 in Patients with PEX Assessment by the Referring Optometrists and All Patients Diagnosed with PEX at the Study Visit. IOP Presented in mmHg

Of all patients referred, 17% (16/95) were identified with PEX during the study visit but PEX assessment was lacking in the referral text for 13 cases (Table 1). Of the 13 referrals, three would not have been accepted according to the new national guidelines (ie, an IOP of at least 25 mmHg is needed for referrals solely based on elevated IOP), and thus two patients in need of treatment would have been missed (Table 1), which means that one patient with PEXG and another with PEX and OH requiring treatment would not have been detected.

Of the 189 eyes included in the study, the ophthalmologist diagnosed 19 with PEX during the study visit. The study optometrist positively assessed PEX in 12 of 19 eyes (63%) before dilatation and in 14 of 19 eyes (74%) after dilatation (Figure 2). In one eye, later confirmed with PEX, the optometrist noted “unsure” before dilatation but changed the assessment to “PEX” after dilatation. Only one pseudophakic patient presented with PEX (Table 1); the study optometrist did not find this case. The study optometrist never assessed that PEX was present when the ophthalmologist assessed as “no PEX” (that is, there were no false positives). Still, in 13 of 189 eyes (7%) the optometrist noted “unsure” either before or after dilatation or both. Of these cases, 12 involved eyes in which PEX was not confirmed; among those, one case had PEX in the other eye (both detected by the optometrist and confirmed by the ophthalmologist).

Figure 2 The study optometrist’s assessment of PEX before and after dilation. The study optometrist’s assessment of PEX is shown as correct, unsure, or wrong before dilation (upper section) and after dilation (lower section) in chronological order. Most “unsure” assessments took place in the first half of the study, while most patients with PEX presented in the second half of the study. None of the eyes without PEX were assessed as having PEX. The study optometrist incorrectly classified five eyes with PEX before and after dilation. Of the first six eyes with PEX, 67% (4 of 6 eyes) were missed by the study’s optometrist even after dilation, but only 8% (1 of 13 eyes) of the remaining PEX-eyes were not found by the optometrist. The image is the property of the authors. Abbreviation: PEX, pseudoexfoliation syndrome.

Discussion

Every fourth referral sent to our hospital during 2019 was based solely on an IOP of 21–24 mmHg. None of these referrals would have been accepted today according to the new Swedish glaucoma guidelines. Hence, 20 unnecessary referrals (21%, 20/95) would have been avoided. According to the new guidelines, additional examinations by optometrists are now required before referring individuals with only modestly elevated IOP (up to 24 mmHg) to secondary eye care (II-level). In this study, one-third of the referrals included IOP measurements ≤ 24 mmHg. However, findings from a slit-lamp examination were included in fewer than one-fifth of referrals with IOP ≤ 24 mmHg and even fewer comprised a PEX assessment. In contrast, the study optometrist detected PEX in a majority of the cases before dilatation and in three-quarters of the cases after dilation.

Most patients with PEX in our study had IOP > 25 mmHg, and referrals from optometrists concerning these patients would have been accepted based on the IOP level alone, according to the new glaucoma guidelines. However, one patient with PEXG and one with PEX and OH requiring IOP-lowering therapy would have been missed because the referring optometrist did not assess PEX. This finding is in line with previous studies showing that PEX is a relevant risk factor for glaucoma, even in eyes with modestly elevated IOP.^9–11,16 In addition, PEX increases the risk for disease progression and disease related loss of quality of life. Therefore, it is of importance to detect these high-risk patients early in the course of the disease. As the prevalence of PEX is high in Sweden,¹⁶ it is relevant for primary care optometrists to address this specific risk factor for glaucoma. Accurate referrals from optometrist are essential to use the health care resources efficient and at the same time increase the chances to find high-risk patients early on.

The strengths of this study include its prospective design with the same double-blinded examiners, the use of a standard study protocol at all study visits, the relatively high number of eyes evaluated for PEX, and the fact that one-third of the referrals concerned eyes with only modestly elevated IOP. In addition, nearly all eligible referrals to our hospital were included in the study period, and all referrals were sent to our hospital before the new glaucoma guidelines were published.

Our study had some limitations. First, the proportion of eyes with PEX is relatively small. The proportion of eyes with PEX was lower than expected in our study; another study from the same catchment area found that 25% of clinically detected patients with glaucoma had PEXG.⁸ In this study, most patients with PEX were discovered in the second half of the study (Figure 2). We assume that this unexpected skewness could partly explain the higher number of uncertain assessments by the study optometrist during the first half of the study. After six eyes with confirmed PEX had run through the study, the study optometrist missed only one more eye with PEX after dilatation. Second, our hospital is not the only referral unit for secondary (II-level) glaucoma care in the catchment area. Primary care optometrists can choose to refer suspected glaucoma cases to either our hospital or several private ophthalmologists working in the same region. However, the main motivation for referral to our hospital was either geographical or because the patient wanted to be referred to the hospital.²⁰ Therefore, we assume it is unlikely that referrals to private practitioners differed significantly from those included in this study concerning PEX assessment by optometrists. Third, as previously reported,²⁰ 16% of referrals did not specify the method used for IOP measurement. Most referring optometrists used non-contact tonometry and a few used applanation tonometry. Thus, there is a variance in the data for IOP measurements from referring optometrist that we cannot control. Forth, most referrals did not specify whether the referring optometrist held a BSc or an MSc.

Recently, Carmichael et al reported the accuracy of glaucoma referrals from primary care optometrists to secondary eye care facilities in a meta-analysis of eleven studies mainly from the UK.²¹ However, only one of the studies evaluated reported PEX assessment by an optometrist before referral with a rather low confirmation rate at the hospital of between 0–50% correct assessments.²² In comparison to that study, the confirmation rate of the few PEX assessments performed by optometrists before referral in our study was much higher (100% correct assessments). A retrospective study conducted at our hospital reported that none of the referrals from optometrists sent to the same hospital based on elevated IOP during 2012 and 2013 included any PEX assessment before referral.²³ To the best of our knowledge, no other previous data is available on the frequency of PEX assessments by optometrists before referral in Sweden. Further studies are necessary to evaluate whether the rate of PEX assessment by optometrists has increased since the new glaucoma guidelines were published and to identify the need for additional education of optometrists in primary (I-level) eye care to accomplish relevant glaucoma referrals.

Conclusion

One group in great risk of visual disability is patients with PEXG. Thus, it is important to identify these patients early on. A majority of patients with glaucoma is detected through referrals from first care eye practitioners to secondary eye care units (Figure 1), but an increasing number of unnecessary referrals burdens glaucoma care units. Therefore, accurate referrals and an assessment of PEX at a primary care level is essential to use the limited health care resources wisely. In our study, PEX assessment was relatively easy to learn for an optometrist holding a Master’s degree and working at the hospital. Evaluating PEX status was even successful in many undilated eyes. However, only a handful of referrals from primary care optometrists included any PEX assessment. Our results suggest that primary care optometrists should assess PEX before referral, at least in patients with a modestly elevated IOP. Otherwise, there is a risk that relevant cases of glaucoma will be missed if referrals from optometrists to secondary eye care facilities are judged according to the new Swedish glaucoma guidelines. In Sweden, stricter referral guidelines for IOP-only referrals from primary care optometrists to ophthalmologists have been established to use the health care resources more wisely. Assessment of PEX by primary care optometrists should be considered if similar requirements for IOP-only referrals are to be introduced in other countries, especially in populations with a high prevalence of PEX.