Human Platelets and Derived Products in Treating Ocular Surface Diseases – A Systematic Review

Figures & data

Table 1 Summary of Different Types of PRP Used in Ophthalmic Clinics

Single Centrifuge Preparation
Name	Starting Material	Preparation Method	Average Platelet Counts^a	Leukocyte Presence	Growth Factors and Other Proteins Measured^b	References
E-PRP	Autologous blood	Mix with anti-coagulant sodium citrate as anti-coagulant; centrifuge at 1600 rpm, 10 min at 5°C;	3x10^8/mL	Yes	Not available	Alio et al 2017^Citation58
PRGF/PRGF-Endoret	Autologous blood	Mix with sodium citrate, centrifuge at 460 to 580 g for 8 min	5x10^8/mL	No	PDGF: 12,645 pg/mL EGF: 468.0 pg/mL HGF: 149 pg/mL VEGF: 204.5 pg/mL FGF: 82.6 pg/mL NGF: 37.7 pg/mL	Anitua et al 2018;^Citation59 Lopez-Cotarelo et al 2017^Citation60
Wu et al autologous PRP	Autologous blood	Mix with citrate phosphate dextrose adenine, centrifuge at 800 rpm for 10 min	6x10^8/mL	Unknown	Not available	Wu et al 2015^Citation25
Kim et al autologous PRP	Autologous blood	Mix with citrate dextrose, centrifuge at 200 g for 11 min	4x10^8/mL	Unknown	EGF: 860 pg/mL TFG-β1: 67.34X10^3 pg/mL TGF-β2: 654.92 pg/mL Fibronectin: 301.3x10^6 pg/mL Vitamin A: 0.558x10^6 pg/mL	Kim et al 2012^Citation44
Autologous PRP prepared commercially	Autologous blood	Prepared using RegenKit BCT tubes (REGENLABCH–1052Mont-sur-Lausanne Switzerland), centrifuge at 1500 g for 5 min at room temperature	3x10^8/mL	Unknown	PDGF-AA: 296 pg/mL PDGF-BB: 201.8 pg/mL VEGF: 53 pg/mL EGF: 8.9 pg/mL	Ronci et al 2012^Citation43
Two Step Centrifugation
Whole blood plasma -PRP (WBP-PRP; WB-PRP)	Pooled blood	Soft spin, then hard spin which leads to formation of platelet pellet, followed by suspension into small plasma	1.5x10^9/mL	Yes	Not available	Weibrich et al 2003^Citation61
Buffer coat- PRP (BC-PRP)	Pooled buffer coat	Hard spin, then soft spin; platelet isolated from the buffer coat, no platelet pellet formed during the process	1 x10^9/mL	Yes	Not available	Dhurat and Sukesh 2014^Citation62
Apheresis-PRP (AP-PRP)	Autologous	Apheresis machine	1.7 x10^9/mL	Yes	PDGF-AA: 769 pg/mL PDGF-BB: 665 pg/mL VEGF: 32 pg/mL EGF: 15 pg/mL	Ronci et al 2015^Citation43

Notes: ^aThe base of number in this column is calculated based on the study and acts as an indicator. It should not be used for comparison. However, the exponent of the number truly reflects the scale of the platelet counts. Platelets in PRP generated from two step centrifugation are one exponent higher than one step centrifugation preparation. ^bThe data specifically refer to PRP samples used in the clinical studies reviewed in this paper.

Table 2 Clinical Studies Using Platelet Products for Ocular Surface Diseases Treatment

First Author/Year	Study Design (Level of Evidence I–VII)	Patient Condition	Sample Size (Control)	Comparison Arm	Product	Treatment	Follow-Up	Outcome
Dry eye
Garcia-Conca et al 2019^Citation28	Prospective, randomized, blind intervention study (Level III)	Hypo-secretory dry eye	44 (39)	Artificial tears	Autologous PRP eye drops	6/day	1 month	Both treatments improved OSDI score PRP group showed more significant and earlier improvement in symptoms.
Alio et al 2007^Citation40	Prospective, non-randomized, consecutive observational study (Level IV)	Moderate to Severe Dry Eye Disease	18	No	E-PRP eye drops;	4–6/day	2 months	89% patients showed improvement in symptoms
Alio et al 2017^Citation58	Prospective, interventional, non-randomized study (Level IV)	Moderate to severe dry eye patients	368	No	E-PRP eye drops	6/day	6 weeks	87.5% patients showed improvement in patient symptoms. 28.8% improved ≥ 1 line CDVA. Significant decrease in clinical signs in 76.1% eyes
Avila et al 2019^Citation50	Prospective, randomized, consecutive intervention study (Level II)	Sjogren syndrome	15 (15)	Hyaluronic acid drops	Autologous PRP injection	Monthly injection	3 months	No adverse effects. PRG injection group showed improvements in all symptoms compared to control cohort. Less corneal staining in PRP group
Fea et al 2016^Citation30	Prospective, randomized, case-control trial (Level III)	Sjogren syndrome	20 (10)	Artificial tears	Autologous PL eye drops	4/day	3 months	Significant improvement in symptoms Basal epithelial cell density and sub-basal nerve plexus density significantly increased Inflammatory cells significantly decreased in APL cohort
Avila 2014^Citation63	Prospective, non-randomized, non-comparative, interventional case series (Level IV)	Sjogren syndrome	4	No	Autologous PRP injection	Monthly injection	3 months	Significant increase in tear film break up time and lacrimal volume following treatment. Significant reduction of corneal and conjunctival staining.
Sanchez-Avila et al 2017^Citation35	Retrospective, non-comparative, consecutive study (Level IV)	Sjogren syndrome	26	No	Immunosafe PRGF: PRGF-Endoret eye drops	4/day	12 months	Significant improvement in OSDI and CDVA Adverse events (n = 2)
Pezzotta et al 2012^Citation64	Prospective, non-randomized, intervention (Phase II clinical trial) (Level IV)	GVHD	23	No	Plasma rich in PDGF eye drops (PRGD)	4/day	6 months	73.9% patients showed improvement of symptoms.
Zallio et al 2016^Citation32	Single-center, prospective pilot study (Level IV)	GVHD	26	No	Autologous PL	6/day	12 months	91% patients reported improvement. Remission of clinical signs in 86% eyes.
Valentini et al 2016^Citation36	Prospective, non-randomized, consecutive case series (Level IV)	GVHD	6	No	Platelet-derived eye drops	4/day	4–14 months	4 patients had significant attenuation of symptoms. 2 patients had exacerbation of burning and ocular discomfort
Pezzotta et al 2017^Citation31	Prospective, non-randomized, non-comparative cohort study (Level IV)	GVHD	31	No	Autologous PL	4/day	Median 36 months	At 6M all patients improved TBUT improved by 6M and maintained 2 patients showed relapse of symptoms across study.
Alio, Pastor et al 2007^Citation34	Prospective, no-randomized, non-comparative case series (Level IV)	Corneal laser refractive surgery	13	No	Autologous E-PRP eye drops	6/day	2 months	85% patients experienced significant improvement of symptoms No worsening of symptoms Adverse event (n = 1)
Javaloy et al 2013^Citation56	Prospective, randomized, consecutive, controlled masked study (Level II)	Corneal laser refractive surgery for myopia	54 (54)	Balanced salt solution eye drops	E-PRP eye drops	3/day	3 months	No significant difference in corneal sensitivity between groups Staining reduced in E-PRP group to comparison
Alio, Rodriguez et al 2017^Citation29	Prospective interventional non-comparative, consecutive clinical study (Level IV)	Corneal laser refractive surgery	80	No	E-PRP	6/day	6 weeks	Dry eye symptoms improved in 85% of patients Decrease in staining in at least one quadrant evident in 89.6% of patients. Conjunctival hyperemia improved in 93.3% of patients.
Corneal ulcers
Alizadeh et al 2019^Citation26	Prospective, non-randomized, consecutive case series (Level IV)	Persistent corneal epithelial defects (Post keratoplasty)	34	No	Autologous PRP eye drops	6/day	Resolution	No adverse events. Significant decrease in time to re-epithelialization with PRP treatment.
Alio et al 2018^Citation41	Prospective, non-comparative observational consecutive study (Level IV)	Dormant corneal ulcers related to surgical procedures	28	No	Autologous E-PRP	4/day	6 weeks	90.9% improvement of symptoms. 65.9% had an improvement ≥ 1 line CDVA 59.1% decrease in corneal staining
Sanchez-Avila et al 2018^Citation65	Retrospective, consecutive, non-controlled study (Level IV)	Neurotrophic keratitis	31	No	PRGF-Endoret eye drop	4/day	Resolution	Complete resolution of corneal ulcer in 97.4% of eyes. Mean time to complete closure of ulcer was 11.4 weeks.
Wrobel-Dudzinska et al 2018^Citation42	Prospective, non-randomized, observational consecutive pilot study (Level IV)	Neurotrophic corneal ulcer	25	No	E-PRP eye drops	5/day	3 months.	Improved symptoms in all patients, 80% complete healing of ulcerations, 16% experienced reduction of ulceration and inflammatory state.
Can et al 2016^Citation66	Prospective, consecutive case series (Level VI)	Descemetocele	3	No	Autologous PRF	Single	12 Months	Stabilization achieved in all cases. Adverse event (n = 1)
Wu et al 2015^Citation22	Prospective, non-randomized, observational consecutive case series (Level VI)	Refractory corneal ulcer	3	No	PRP eye drop	8/day	1 month	All cases improved Corneal ulcer/scarring and stromal infiltration least responsive of cases
Ronci et al 2015^Citation43	Prospective, non-randomized, consecutive case series (Level IV)	Persistent corneal epithelial defect	9 (1)	Homologous PRP-f	Autologous PRP	3/day	1 month	Visual acuity and lesions improved in all cases
Alio et al 2013^Citation49	Prospective, non-randomized, non-controlled, intervention case series (Level IV)	Perforated corneal ulcer	11	No	E-PRP clot: E-PRP activated by addition of CaCl2.	Single	3 Months	All perforations sealed No relapses or perforation during follow-up period. Fibrin membrane disappeared in all cases.
Alio, Rodriguez and Martinez 2013^Citation48	Prospective, non-randomized, non-comparative intervention (Level IV)	Perforated corneal ulcer	6	No	E-PRP clot	Single	3 months	All perforation sealed No infection or inflammation No adverse effect or relapse in 5 patients. 1 relapse exhibited history of limbal stem cell deficiency
Panda et al 2012^Citation47	Prospective, randomized, comparative, double-blind clinical intervention (Level II)	Chemical injuries (grades III, IV and V)	10 (10)	Yes	E-PRP eye drops	10/day	3 months	All eyes healed Significantly faster healing of epithelial defects and improved corneal clarity in PRP treated group
Kim et al 2012^Citation44	Retrospective, non-randomized, consecutive case-control series (Level IV)	Post infectious keratitis epithelial defects	11 (17)	Yes	Autologous PRP eye drops	Not described	Resolution	Healing rate significantly higher in PRP group than autologous serum (AS) group. All PRP treated patients had complete re-epithelialization (5/17 patients treated with AS had no response)
Lopez-Plandolit et al 2010^Citation45	Prospective, non-randomized, non-comparative case series (Level IV)	Persistent epithelial defect (various aetiologies)	18	No	Autologous PRGF eye drops	8/day (then as needed)	Resolution (1–104 weeks)	Significantly shorter healing rate after PRGF treatment , 85% of epithelial defect restored, 3 cases that did not heal identified as neurotrophic origin. Adverse event (n = 1)
Geremiccaet al 2010^Citation67	Prospective, consecutive, non-blinded case series (Level IV)	Neurotrophic keratopathy or keratopathy due to chemical/physical trauma	103	No	Autologous PRP eye drops	5/day	1 month	Epithelial defects healed in all eyes 3 cases recurred 1 week post cessation of treatment.
Marquez De Aracena Del Cid and Montero De Espinosa Escoriaza 2009^Citation46	Prospective, consecutive, non-randomized, comparison study (Level III)	Ocular alkali burns	35	Yes	Regenerative factor-rich plasma (RFRP) injection	Single	40 days	RFRP was not used as a monotherapy. Significant improvement in signs and symptoms Significant scarring formation in treated group compared to control Less side effects than serum treatment
Alio, Abad et al 2007^Citation40	Prospective, non-randomized, non-comparative, consecutive interventional case series (Level IV)	Dormant corneal ulcers	24 (14)	Autologous PRP clot	Autologous PRP eye drops	6/day (vs single application)	Variable (3–18 months)	All patients showed improvement in pain, inflammation and healing scales by 1–2 weeks. 31% of drop and 36% of clot eyes improved between 1–3 lines CDVA
Lee et al 2016^Citation68	Retrospective, non-randomized, comparative, case-control series (Level IV)	Recurrent corneal erosions	27 (14)	Artificial tears	Autologous PRP eye drops	8/day	6 months	PRP treated group had 22.2% of major recurrences and 25.9% minor recurrences; control group 80% major recurrences and 100% minor recurrences
Other indications
Chen et al 2013^Citation52	Prospective, non-randomized, consecutive intervention study (Level IV)	Orbital floor fracture Reconstruction	10	No	PRP (biomaterial)	Single insertion	24 months	Easy to mold and apply Good restoration of orbital floor defect in all patients No ocular motility effects at final visit
Kalyam et al 2017^Citation55	Case report (Level VI)	Skin rejuvenation treatment of peri-ocular area	1	No	Not confirmed	Single injection	NA	Adverse event (n = 1) Ophthalmic artery occlusion, optic nerve infarction and extraocular muscle ischemia leading to restricted ocular motility. Skin necrosis described at injection site.
Sanchez-Avila, Merayo-Lloves, Fernandez et al 2018^Citation69	Retrospective non-comparison, consecutive, case-series (Level IV)	Glaucoma with secondary ocular surface disease	6	No	Immuno-safe PRGF-Endoret eye drops.	4/day	3 months	Significant reduction in OSDI scale; improvement in CDVA at follow up Adverse event (n = 1) One patient reported itching but continued to resolution.
Sanchez-Avila, Merayo-Lloves, Riestra et al 2018^Citation70	Retrospective, non-comparative, consecutive study (Level IV)	Various corneal and conjunctival conditions	15	No	PRGF fibrin membrane (mPRGF)	4/day	11 months	All patients treated with mPRGF improved CDVA Epithelial defects significantly reduced in patients treated only with mPRGF vs mPRGF with amniotic membrane
Arslan et al 2018^Citation53	Prospective open-label clinical trial (Level IV)	Retinitis pigmentosa	37 (11)	Autologous platelet-poor plasma	Autologous PRP injection	3 week injection	3 months	No serious adverse events related to injection. Significant improvement in visual field, multifocal electroretinography and microperimetry values at follow-up.
Rodriguez-Agirretxe et al 2018^Citation54	Prospective, non-randomized, non-comparative, interventional case series (Level IV)	Primary open angle glaucoma	10	No	mPRGF	Single application	24 months	Statistically significant reduction in IOP Ocular surface regeneration following glaucoma surgery.
Abdalrahman et al 2019^Citation51	Case report (Level VI)	Ocular hypotension post glaucoma surgery non-responsive to treatment	1	No	E-PRP injection	Single injection	6 months	Improved intraocular pressure Stable clinical signs at final follow up
Alio et al 2019^Citation50	Case report (Level VI)	Keratoconus hydrops	1	No	Autologous E-PRP injection	Single injection	6 months	Clinical signs resolved by 1 week Stability through 6 months.

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