Martinez‑de‑la‑Casa et al. Eye and Vision (2022) 9:12 https://doi.org/10.1186/s40662-022-00284-4 RESEARCH Intense pulsed light‑based treatment for the improvement of symptoms in glaucoma patients treated with hypotensive eye drops Jose Maria Martinez‑de‑la‑Casa1,2*† , Carlos Oribio‑Quinto1†, Almudena Milans‑del‑Bosch1, Pilar Perez‑Garcia1, Laura Morales‑Fernandez1 , Javier Garcia‑Bella1, Jose Manuel Benitez‑del‑Castillo1,2, Julian Garcia‑Feijoo1,2 and David P. Piñero3 Abstract Background: Ocular surface disease in glaucoma patients is a signifcant ocular co-morbidity that can afect 40% to 59% of these patients worldwide. The current study was aimed at evaluating the potential clinical beneft of an intense pulsed light (IPL)-based treatment in glaucomatous patients with ocular surface disease due to prolonged hypotensive eyedrop treatments. To our knowledge, this is the frst series analyzing the therapeutic efect of this treat‑ ment option in this type of patients. Methods: This non-comparative prospective case series study enrolled a total of 30 glaucoma patients ranging in age from 57 to 94 years old and treated with hypotensive eyedrops for years with dry eye symptomatology. All patients received four sessions of IPL treatment using the Optima IPL system (Lumenis, Yokneam, Israel) adjusted to the ofcial optimized Lumenis setting. Changes in symptomatology, corneal staining, conjunctival hyperemia, non-invasive break-up time (NIBUT), tear osmolarity, tear meniscus height (TMH), meiboscore and meibomian gland expressibility was analyzed after treatment. Results: Statistically signifcant reductions were observed after IPL treatment in the symptomatology scores meas‑ ured with diferent questionnaires [ocular surface disease index (OSDI), standard patient evaluation of eye dryness (SPEED) and symptom assessment questionnaire in dry eye (SANDE)] as well as with the visual analogue scale (P<0.001). Mean change in OSDI was−15.0±11.3. A signifcant reduction was found after treatment in the corneal staining score (P<0.001). A signifcant reduction was found in tear flm meniscus height (P=0.012), as well as in tear flm osmolarity (P=0.001). A signifcant reduction was also found in meibomian gland expressibility (P=0.003), changing the percentage of grade 3 eyes from 44.4% before IPL to 17.2% after treatment. Conclusions: IPL therapy combined with meibomian gland expression (MGX) seems to be an efective option to improve symptomatology in glaucomatous patients with ocular surface disease due to prolonged hypotensive eye‑ drop treatments, with an additional improvement in clinical signs, such as tear osmolarity and corneal staining. © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativeco mmons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Open Access *Correspondence: jmmartinezcasa@gmail.com † Jose Maria Martinez-de-la-Casa and Carlos Oribio-Quinto contributed equally and thereby should be considered as frst authors 1 Ophthalmology Unit, Department of Ophthalmology and ORL, Faculty of Medicine, Hospital Clinico San-Carlos, Universidad Complutense de Madrid, Instituto de Investigación Sanitaria del Hospital Clinico San-Carlos (IdISSC), 28040 Madrid, Spain Full list of author information is available at the end of the article Martinez‑de‑la‑Casa et al. Eye and Vision (2022) 9:12 Page 2 of 10 Background Chronic glaucoma patients are routinely subjected to topical hypotensive treatments for years [1]. These treatments usually contain preservatives that may have a negative impact on the ocular surface, including alterations of the meibomian gland morphology and function [2, 3], increased subbasal nerve tortuosity and dendritic cell density [4], and affectation of the viability and functions of the conjunctival Goblet cells [5]. These pharmacologically-induced alterations of the ocular surface lead to a significant reduction of the tear film lipid layer [6], and consequently can lead to evaporative dry eye syndrome. This condition is associated to disturbing symptomatology [7] that can affect the patient’s quality of life significantly [8]. For this reason, it must be treated with some medical therapeutic approaches proposed, such as the topical use of a preservative-free ophthalmic solution containing hyaluronic acid 0.4% and taurine 0.5% [9], vitamin A palmitate eye gel 0.1% [10], carbomer eye gel 0.2% [10], cannabinomimetic palmitoylethanolamide [11], or oral supplementation with antioxidants and essential fatty acids [12]. In previous years, intense pulsed light (IPL) therapy has demonstrated its efectiveness for the treatment of the dry eye associated to meibomian gland dysfunction (MGD); a recent report from the American Academy of Ophthalmology stated that the existing scientifc literature on IPL treatment of MGD confrms the efcacy of this therapeutic option, with improvements in the signs and symptoms associated to this condition [13]. Specifcally, the efcacy of IPL for the treatment of dry eye associated to MGD without [14–21] and with the combined meibomian gland expression (MGX) [22–27] has been investigated and confrmed in a great variety of studies. Tis efcacy is the result of the various therapeutic efects of this irradiation of fltered polychromatic broad-bandwidth wavelengths with varying pulse duration, including the facilitation of the expressibility and release of the meibum inside, the improvement of the function of meibomian glands, the reduction of proinfammatory mediators contributing to dry eye, or the improvement of the cellular functions including fbroblasts regeneration, collagen synthesis, and motility in immunoregulatory cells [19, 28]. Tese changes induced by IPL facilitates an improvement of ocular surface anomalies or even their resolution, suggesting that the use of this therapeutic approach might be potentially useful in glaucoma patients with an altered ocular surface due to topical hypotensive treatments for years. Te aim of this study was to investigate the efect of an IPL-based treatment combined with MGX in glaucomatous patients with pharmacologicallyinduced moderate to severe ocular surface disease due to prolonged hypotensive eyedrop treatments. Methods Patients Tis non-comparative prospective case series study enrolled a total of 30 glaucoma patients treated with hypotensive eyedrops for at least two years with dry eye symptomatology. Te study was conducted at the Department of Ophthalmology of the Hospital Clínico San Carlos in Madrid (Spain) following the tenets of the Declaration of Helsinki. All patients were informed about the nature of the study and provided written informed consent before being included in the trial. Te study was approved by the Clinical Investigation Ethics Committee of the San Carlos Clinic Hospital in Madrid (20/588-E). Te following inclusion criteria were defned for this study: chronic glaucoma being treated with at least one hypotensive eye drops for at least two years without changes during the six months before patient’s enrolment, patient’s ability to read, understand and sign an informed consent form, patient’s ability and willingness to comply with the program and the requirements of the treatment, age>18 years, and two of the following conditions revealing the presence of ocular surface disease: • Ocular surface disease index (OSDI) questionnaire score≥23 (moderate to severe symptomatology) • TBUT (tear flm break-up time)≤7 s in the studied eye • MGD score≤12 (evidence of meibomian gland obstruction along the lower eyelid) in the studied eye [29] • At least 5 non-atrophied meibomian glands along the lower lid of the studied eye • Tear flm osmolarity≥310 mOsm/l in both eyes • Standard patient evaluation of eye dryness (SPEED) questionnaire score≥10. Patients with moderate or severe dry eye disease and MGD associated with chronic use of topical hypotensive drugs were included. In all cases, no other causative ophthalmological or systemic pathologies were present, such as Sjögren’s syndrome, infammatory Keywords: Glaucoma, Intense pulsed light, Dry eye, Meibomian glands Martinez‑de‑la‑Casa et al. Eye and Vision (2022) 9:12 Page 3 of 10 diseases (pemphigus and pemphigoid), infectious (Staphylococci, Demodex folliculorum) or other diseases of the ocular surface. Te exclusion criteria of the study included: skin type V or VI according to Fitzpatrick classifcation, contact lens wear in the month prior to the baseline evaluation of the current study, ocular or eyelid surgery within 6 months prior to the baseline evaluation of the study and other uncontrolled eye disorders afecting the ocular surface (i.e., active allergies), precancerous lesions, skin cancer or pigmented lesions in the planned treatment area, uncontrolled infections or uncontrolled immunosuppressive diseases, subjects with ocular infections within 6 months prior to baseline examination of the study, previous history of herpes simplex virus 1 and 2, systemic lupus erythematosus, and porphyria, use of photosensitive medications and/or herbs that may cause sensitivity to 560–1200 nm light exposure within 3 months of baseline examination, such as isotretinoin, tetracycline, doxycycline, or St. John’s wort, previous facial treatment with IPL within 12 months of evaluation, and not wanting or being able to refrain from the use of medications known to cause dryness (e.g., isotretinoin, antihistamines) for the duration of the study. Clinical protocol Once the informed consent was signed and a patient’s auto-evaluation of symptomatology using the OSDI, symptom assessment questionnaire in dry eye (SANDE) and SPEED questionnaires as well as a visual analogue scale (VAS; scale: 0 to 10), and a complete baseline examination was performed in all patients by a masked examiner including the following tests or clinical evaluations: three consecutive measures of NIBUT (Keratograph 5 M, Oculus Optikgerate, Wetzlar, Germany), slit lamp biomicroscopy (corneal and conjunctival staining evaluated with the Oxford scoring system, 0 to 15; limbar and bulbar conjunctival hyperemia grading), manifest refraction, corrected distance visual acuity measurement using an ETDRS chart, Goldmann tonometry, and infrared meibography (Keratograph 5 M, Oculus Optikgerate, Wetzlar, Germany), grading the meibomian gland dropout degree for each eyelid as meiboscore [30]: grade 0 (no loss of meibomian glands), grade 1 (loss of<33% of the whole glands area), grade 2 (loss area between 33% and 67%), and grade 3 (loss of>67% of the whole area). Te meiboscore of each eye was calculated as the sum of the scores from both upper and lower eyelids. Likewise, the ability of fve meibomian glands in the central area of the lower eyelid was tested for meibum secretion after applying frm digital pressure. Te results were scored from 0 to 3 depending on the number of expressible glands found among the 5 central glands, where 0=all glands expressible; 1=3–4 glands expressible; 2=1–2 glands expressible; and 3=no glands expressible. Immediately after the baseline measurement, the studied eye was determined as the eye with the most severe TBUT (lowest value). If both eyes of the subject had identical TBUT values, the studied eye was determined randomly. Each subject underwent 4 treatment sessions at 2-week intervals and a follow-up session at 4 weeks after the fnal treatment session. Te frst treatment session took place within one week of selection. In addition to this frst treatment session, there were three additional treatment sessions at 2-week intervals. Te subject could advance a treatment session up to 3 days or delay it up to 7 days. Each treatment session included the following procedures in a sequential order: 1. Slit lamp biomicroscopy (observation of eyelid margins, conjunctiva, and eyelashes). 2. IPL active treatment. 3. MGX of the upper and lower eyelids in both eyes. 4. Slit lamp biomicroscopic evaluation after treatment. 5. Assessment of skin reaction between 5 and 10 min after IPL Tere was a single follow-up visit 4 weeks after the last treatment session. Te subject could advance the follow-up visit session by up to 3 days or delay it by up to 7 days. At the beginning of the follow-up visit, the subject self-assessed their symptoms using two tools, the OSDI questionnaire and the ocular dryness score using a VAS. A masked examiner conducted the same clinical evaluations that were performed in the baseline examination. Treatment sessions All patients received four sessions of IPL treatment using the Optima IPL system (Lumenis, Yokneam, Israel) adjusted to the ofcial optimized Lumenis setting (590 nm cutof flter, triple pulses of 6 ms with an interval of 50 ms, and total fuence ranging 11 to 14 J/cm2 ). Before initiating the treatment, each patient underwent a Fitzpatrick skin typing test [31] to determine the intensity of the pulsed light that would be administered. At each treatment session, the patient was placed in a special chair to perform the treatment, allowing to maintain a comfortable position. Te skin was cleaned with micellar water and both eyes of the patient were closed and sealed with special adhesive patches (IPL-aid disposable eye shields, Honeywell Safety Products, Smithfeld, USA). A layer of conductive gel for IPL was placed afterwards following the path of the skin on the lower eyelids from temple to temple, including the nose. A total of 5 impacts were then made in each region (right and left), Martinez‑de‑la‑Casa et al. Eye and Vision (2022) 9:12 Page 4 of 10 with a total of 10 impacts in each application without overlapping them. After this, another series of a total of 10 impacts was applied again. Finally, MGX was performed using sterile forceps in the slit lamp after instilling anesthetic drops (0.4% oxybruprocaine hydrochloride). Statistical analysis Te SPSS software package (SPSS Version 20.0; IBM Corporation, Armonk, NY, USA) was used to analyze the data obtained in this study. Normality of data was frst evaluated using the Kolmogorov-Smirnov test. Te paired Student t-test and Wilcoxon tests were used for analyzing the statistical signifcance of the diferences between pre-treatment and post-treatment visits when the data samples were normally and not normally distributed, respectively. Te Pearson or Spearman correlation coefcients were calculated to assess the degree of association between the change obtained in diferent variables and the magnitude of baseline parameters depending on whether the data samples were or not normally distributed, respectively. A P value<0.05 was considered as representative of statistical signifcance. Results Demographics A total of 30 eyes of 30 patients with ages ranging from 57 to 94 years old [mean±standard deviation (SD): 74.6±9.0 years; median: 75.0 years] were analyzed in our study. Te sample included 22 females (73.3%) and 8 males (26.7%). Likewise, a total of 16 and 14 right and left eyes were included, respectively. A total of 1, 2 and 3 diferent types of hypotensive drops were prescribed in 21 (70.0%), 7 (23.3%) and 2 eyes (6.7%), respectively. Te Fitzpatrick test confrmed the following distribution of the types of skin: 1 patient (3.3%) skin type I, 5 patients (16.7%) type II, 23 patients (76.7%) type III and 1 patient (3.3%) type IV. Table 1 shows the pre- and post-treatment data for all the variables evaluated in the current sample. Regarding the type of hypotensive drug used, the following distribution was found in the sample evaluated: Table 1 Summary of the pre- and post-treatment clinical data OSDI=ocular surface disease index; VAS=visual analogue scale; NIBUT=non-invasive break-up time Parameters Pre-treatment Mean (SD) Median (Range) Post-treatment Mean (SD) Median (Range) P value OSDI 37.6 (16.6) 34.7 (5.0 to 78.0) 22.6 (14.6) 18.3 (0.0 to 50.0) <0.001 SPEED score 13.0 (4.9) 12.5 (6.0 to 25.0) 7.3 (4.8) 6.0 (0.0 to 22.0) <0.001 SANDE frequency score 63.8 (22.5) 72.5 (10.0 to 100.0) 37.8 (24.2) 34.2 (0.0 to 95.0) <0.001 SANDE severity score 58.6 (22.9) 59.2 (10.0 to 94.1) 35.3 (21.7) 30.0 (0.0 to 85.0) <0.001 Symptomatology VAS 5.9 (2.1) 5.5 (1.0 to 10.0) 4.1 (1.7) 4.0 (1.0 to 7.0) <0.001 Bulbar hyperemia grading 1.6 (0.5) 1.5 (0.9 to 3.4) 1.4 (0.5) 1.3 (0.5 to 2.3) 0.101 Nasal limbar hyperemia grading 1.2 (0.6) 1.1 (0.4 to 2.7) 1.1 (0.5) 0.9 (0.3 to 2.2) 0.316 Temporal limbar hyperemia grading 1.3 (0.4) 1.3 (0.4 to 1.9) 1.1 (0.6) 1.0 (0.4 to 2.9) 0.123 Oxford staining score 8.9 (2.7) 9.0 (5.0 to 15.0) 6.9 (2.3) 7.0 (3.0 to 12.0) <0.001 Tear flm osmolarity (mOsm/l) 330.1 (21.1) 328.5 (279.0 to 378.0) 313.8 (21.6) 317.0 (249.0 to 353.0) 0.001 Meiboscore 2.4 (0.6) 2.0 (1.0 to 4.0) 2.2 (0.7) 2.0 (1.0 to 4.0) 0.185 Meibomian gland expressibility 2.4 (0.5) 2.0 (2.0 to 3.0) 2.1 (0.4) 2.0 (1.0 to 3.0) 0.003 Tear flm meniscus (μm) 288.5 (169.4) 242.5 (100.0 to 781.0) 229.9 (112.0) 208.5 (129.0 to 710.0) 0.012 First break NIBUT 6.0 (3.7) 5.3 (2.1 to 17.4) 7.4 (3.8) 6.7 (1.9 to 15.1) 0.091 Average NIBUT 13.2 (4.6) 14.2 (4.2 to 21.6) 14.0 (5.1) 15.3 (2.0 to 21.5) 0.348

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