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Pediatric Microbial Keratitis With Overnight Orthokeratology in Russia

Bullimore, Mark A. M.C.Optom., Ph.D.; Mirsayafov, Dmitry S. M.D.; Khurai, Aslan R. M.D., Ph.D.; Kononov, Leonid B. M.D., Ph.D.; Asatrian, Suzanna P. M.D.; Shmakov, Andrei N. M.D., Ph.D.; Richdale, Kathryn O.D., Ph.D.; Gorev, Valery V. M.D., Ph.D.

Author Information
Eye & Contact Lens: Science & Clinical Practice: July 2021 - Volume 47 - Issue 7 - p 420-425
doi: 10.1097/ICL.0000000000000801
  • Open

Abstract

Overnight orthokeratology is the planned, temporary reduction in myopia by the wearing of flat-fitting rigid contact lenses.1 These rigid gas permeable (RGP) contact lenses possess reverse geometry with the first peripheral curve steeper than the central base curve to improve centration.2–4 Modern high oxygen transmissible materials minimize hypoxic stress and corneal edema when worn on an overnight basis. Lenses are inserted before bedtime and removed the following morning, resulting in correction-free vision throughout the day.5 Patients are free to engage in sports and outdoor activities, which may otherwise be difficult to perform wearing spectacles or even daily wear contact lenses. The treatment is reversable and modifiable. Lenses are only handled at home, allowing for parental supervision of children.

In an international survey conducted between 2000 and 2008, overnight orthokeratology fits represented 28% of all RGP contact lenses prescribed to minors, including 47% among 6- to 12-year-olds.6 The use of overnight orthokeratology is increasing. The same authors recently reported their 2011 to 2018 survey data and estimated that 52% of children fitted for myopia control purposes were fitted with RGP lenses, presumably orthokeratology.7 Morgan et al.8 reported 14 years of survey data (2004–2017) from 45 countries, representing 295,044 contact lens fits. Overall, orthokeratology represented 1.2% of all contact lens fits with a range of 0% to 6% across countries. Furthermore, orthokeratology contact lens fitting has risen from 0.5% in 2004 to 1.3% in 2017. This may be because of the fact that eye care practitioners perceive orthokeratology to be the most effective method of myopia control.9

Practitioners began discussing the viability of overnight orthokeratology for myopia control around 20 years ago.10,11 The first peer-reviewed paper reported 35 children fitted by eight clinicians who completed 2 years of follow-up.12 A historical control group of 35 children wearing single-vision spectacles was used as a comparison. The increase in axial length was 0.29±0.27 and 0.54±0.27 mm in the orthokeratology and control groups, respectively. The difference of 0.25 mm corresponds to around 0.65 D.13,14 Refractive error measurements are, of course, confounded by the induced changes in corneal curvature. The first randomized clinical trial assigned 102 children, 6 to 10 years old, to either overnight orthokeratology or spectacles.15 For the 78 patients completing the 2-year study, the mean axial elongation was 0.36±0.24 and 0.63±0.26 mm in the orthokeratology and control groups, respectively. These results have been supported by multiple studies in at least six countries.16,17 In summary, overnight orthokeratology slows axial elongation by around 0.25 mm over two years. Longer-term studies have demonstrated slowing of axial elongation of around 0.4 mm, corresponding to a 1 D slowing of myopia progression.18–20

There have been long-held concerns regarding the safety of overnight orthokeratology.21–25 To date, there has been only one comprehensive study designed to estimate the incidence of microbial keratitis in overnight orthokeratology.26 In a retrospective sample of 1,317 patients (640 adults and 677 children) representing 2,599 patient-years of wear, 2 cases of microbial keratitis were identified resulting in an overall estimated incidence of 7.7 per 10,000 years of wear (95% confidence interval [CI]: 0.9–27.8). Both occurred in children but neither resulted in a loss of visual acuity, so in children, the estimated incidence is 13.9 per 10,000 years of wear (95% CI: 1.7–50.4).

With the ongoing interest in overnight orthokeratology for myopia control in children, further studies of its safety are needed.25 This paper describes a joint study between Doctor Lens, a group of ophthalmology and optometry practices in Moscow, and Morozovskaya City Children's Clinical Hospital (MCCCH), Moscow Healthcare Department to estimate the incidence of microbial keratitis in children wearing overnight orthokeratology lenses.

METHODS

Identification of Cases of Microbial Keratitis

The MCCCH institutional review board granted a waiver of informed consent for this study. MCCCH is a large facility with a full ophthalmology service that consists of 3 units: an outpatient clinic, an emergency department, and a hospital department of 40 beds. Each year they handle approximately 23,000 ophthalmology outpatient visits and 4,700 urgent ophthalmology outpatient visits. More importantly, it is the only hospital in the Moscow area providing urgent ophthalmological care for children. Thus, the probability that any child with microbial keratitis will be seen at MCCCH is very high. If a child with microbial keratitis is seen at other hospitals or outpatient facilities, he or she is referred to MCCCH according to the established practice and regulations.

To identify all potential cases of microbial keratitis, all cases with the diagnosis “keratitis” with corneal infiltrates at presentation were recorded in a database from January 1, 2018 to December 31, 2018. Three experienced ophthalmologists later reviewed and adjudicated the cases. The criteria for a diagnosis of keratitis included one or more dense white, grayish, or yellowish stromal infiltrates more than 1 mm in size, with uneven edges and an epithelial defect, accompanied by pronounced conjunctival injection, corneal edema, and pain more than mild. Additional criteria that were considered included a positive culture result, anterior chamber reaction, response to treatment, and a residual scar. A diagnosis of Acanthamoeba keratitis was based on a ring infiltrate, severe pain, and confirmation by confocal microscopy. Classification of a case as microbial keratitis required unanimous agreement among the three adjudicators.

Estimating the Number of Overnight Orthokeratology Wearers

The Doctor Lens ophthalmological clinic was established in 2002 and has 15 functional units in Moscow. The clinic specializes in overnight orthokeratology, which accounts for most lenses fitted, although conventional RGP lenses, for refractive and medical indications, and scleral lenses are also prescribed. ESA Ortho-6 designs (design by Prof. Antonio Calossi, Chertaldo, Italy; manufactured by Doctor Lens Technology, Moscow, Russia) in Boston XO material (Bausch+Lomb, Bridgewater, NJ) with a Dk of 100 cm.mL.O2/sec.ml.mm Hg account for 98% of the orthokeratology lenses fitted. All patients are instructed to use Boston Advance daily cleaner (Bausch+Lomb, Bridgewater, NJ). Around 70% store their lenses in BioTrue multipurpose solution (Bausch+Lomb, Bridgewater, NJ) while 30% use Refine One Step Hydrogen Peroxide Solution (CooperVision, Pleasanton, CA).

A database was originally created for marketing purposes, primarily to identify the number of patients referred to the practice and to observe changing referral patterns. Since the end of 2010, all new patients have been added to the database resulting in a total of more than 23,000 unique overnight orthokeratology fits by the end of 2018.

The database does not contain complete data on patient age, gender, and initial myopia, so around 100 patient records from each unit (13 at that time) were selected at random and the patient's age at fitting recorded. This resulted in a sample of 1,368 records. These distributions were extrapolated to the entire database to estimate the number of children wearing overnight orthokeratology in 2018.

Exposure to overnight orthokeratology wear during 2018 requires an estimate of the number of previous fitted patients still wearing lenses and younger than 18 years during 2018. The maximum possible number of patients younger than 18 years still wearing lenses was estimated based on the distribution of age at fitting and adjusted for confirmed discontinuations. Further adjustments were made to account for discontinuations and loss to follow-up. A previous study of Doctor Lens patients surveyed 826 patients fitted with overnight orthokeratology over a 5-year period.27 Of these, 89 had discontinued wear (10.8%). Most discontinuations occurred during the first year of wear (58 patents, 7.0%) During the 2020 COVID-19 lockdown, all medical records were reviewed in April and an attempt made to call every patient who had not visited the clinic in the previous 5 months. These data were used to further inform the number of discontinuations.

Statistical Methods

Descriptive statistics were calculated, and unpaired t-tests were used to compare groups of patients. Estimates of microbial keratitis were calculated based on the number of cased divided by the estimated number of wearers and converted to incidence per 10,000 years of wear. Finally, 95% CIs were estimated using the Wilson score interval.

RESULTS

Estimating the Number of Overnight Orthokeratology Wearers in 2018

Table 1 shows the total number of overnight orthokeratology patients fitted by year at all Doctor Lens practices since 2010 along with the number of confirmed discontinuations. The number of fits increased through 2013 and was relatively constant thereafter. Also shown are the number of fits by year in the random sample of 1,368 patients. The distribution of the 1,368 patients by year is very similar indicating that this sample can be generalized to the entire dataset. Of the 1,368 patients, 1,078 (79%) were younger than 18 years at initial fitting (mean=12.4±2.5 years). The age distribution for these 1,078 children is shown in Figure 1. The age distribution for patients fitted in each year are also shown, indicating a consistent distribution and further supporting the generalizability of this sample. The age distribution was combined with the total number of patients to estimate the number of children fitted in each year.

TABLE 1. - Number of New Overnight Orthokeratology Lens Fits at All Doctor Lens Locations by Year With Confirmed Discontinuations
Year All Patients in Database Random Sample
New Fits Percentage of Total Confirmed Discontinuations New Fits in Sample Percentage in Sample
2010 240 1% 29 (12%) 15 1%
2011 1,158 5% 109 (9%) 57 4%
2012 2,559 11% 211 (8%) 146 11%
2013 3,311 14% 297 (9%) 192 14%
2014 3,119 14% 271 (9%) 181 13%
2015 3,178 14% 262 (8%) 190 14%
2016 2,906 13% 281 (9%) 177 13%
2017 3,261 14% 276 (8%) 168 12%
2018 3,317 14% 285 (9%) 242 18%
Total 23,049 100% 2,021 (9%) 1,368 100%
Also shown are the number of fits by year in the random sample of 1,368 patients.

FIG. 1.
FIG. 1.:
Age distribution of patients fitted with orthokeratology in each year in the random sample of 1,078 patients younger than 18 years at fitting.

On average, 9% of patients were known to have discontinued lens wear (patients were entitled to a full refund within two months of the initial fitting). Of the 40,681 active patients in April 2020, 20,709 (50.9%) had not been examined within the previous 5 months and attempts were made to contact them all by phone. Discontinuation of contact lens wear was confirmed in 2,646 (6.5% of all current patients), whereas 2,932 (7.2%) did not respond to multiple calls. Thus, the maximum cumulative discontinuation rate was 13.7%. Note that this represents all contact lens wearers, not just overnight orthokeratology, and includes discontinuation at any time. Years since fitting was not recorded, but if the mean was 3 years, then the annual discontinuation rate would be less than 5%.

Based on the distribution of age at fitting, the number of patients younger than 18 years in 2018 was first calculated and adjusted for confirmed discontinuations (Table 2). Thereafter, a conservative approach was used, two different annual rates of discontinuation were used: 7% and 10%. The former is the previously estimated rate for the first year of wear,27 and similar to the confirmed discontinuation rate, whereas the latter is more conservative. Table 2 shows the number of patients younger than 18 years estimated to be wearing lenses based on fitting year. For those fitted in 2018, discontinuation rates of 7% and 10%. are used, but given that these patients commenced wear throughout the year, the number is halved to calculate the patient years of wear. Thus, based on a 7% annual discontinuation rate, the estimated number of children wearing overnight orthokeratology lenses in 2018 was 10,307. Likewise, based on a 10% annual discontinuation rate, the number of children wearing lenses in 2018 was 9,422. Children fitted before 2014 represent fewer than 20% of these totals.

TABLE 2. - Estimated Number of Patients Younger Than the Age of 18 Years at the Time of Fitting and at the Beginning of 2018
Initial Fitting Year Under 18 Years at Fitting Under 18 Years in 2018 Assuming 7% Discontinuation per Year Assuming 10% Discontinuation per Year
2010 181 21 11 9
2011 906 219 131 104
2012 2,010 1,059 685 562
2013 2,603 1,690 1,175 997
2014 2,449 1,874 1,401 1,229
2015 2,499 2,160 1,737 1,574
2016 2,283 1,974 1,707 1,598
2017 2,564 2,417 2,247 2,175
2018 2,609 2,609 1,213a 1,174a
Total 18,104 14,023 10,307 9,422
aThe number of fits in 2018 was halved as, on average, patients wore lenses for only 6 months of the year.
Also shown are the estimated number wearing their lenses at the beginning of 2018 assuming discontinuation rates of 7% and 10% per year.

Cases of Microbial Keratitis in Children in 2018

During 2018, 139 cases of corneal infiltrative keratitis in children (younger than 18 years) presenting at MCCCH were recorded and 45 were adjudicated as microbial keratitis (32%). Of these 20 cases were associated with contact lens wear (44%): 15 soft lens wearers (33%) and five overnight orthokeratology wearers (11%). The remaining cases comprised 12 secondary to other ocular conditions, two secondary to systemic conditions, five traumatic, one postcataract surgery, and five unattributed (but all non–contact lens wearers). The contact lens wearers were older than the non–contact lens patients (15.7±1.1 vs. 9.2±5.4 years, unpaired t test, P<0.001), but the orthokeratology patients were not different from the soft lens patients (15.2±1.1 vs. 15.9±1.1 years, unpaired t test, P>0.05).

Among the five orthokeratology cases, two were culture positive (one each Staphylococcus aureus and Enterococcus faecalis), whereas seven of the 15 soft lens cases were positive (three Staphylococcus epidermidis, and one each S. aureus, E. faecalis, Streptococcus mitis, and Acanthamoeba). All cases were monocular except one soft lens wearer who was diagnosed with bilateral Acanthamoeba keratitis. The mean size of the largest infiltrate at presentation was not different between orthokeratology and soft lens patients (3.0±0.7 vs. 3.1±0.9 mm, P>0.05). All of the orthokeratology eyes demonstrated best-corrected 20/20 visual acuity at discharge, but 5 of the 16 soft lens wearing eyes, including both eyes in the bilateral case, presented with visual acuity worse than 20/20, with a range from 20/25 to 20/40.

Four of the five orthokeratology-related cases of microbial keratitis were confirmed to be patients of Doctor Lens. Thus, estimation of incidence were performed for both four and five cases.

Incidence of Microbial Keratitis in Overnight Orthokeratology

The incidence of microbial keratitis in children wearing overnight orthokeratology may be estimated from the above data. For all five cases at MCCCH and assuming a 7% discontinuation rate, the incidence is 4.9 per 10,000 patient years (95% CI: 2.1–11.4). For a 10% discontinuation rate, the incidence is 5.3 per 10,000 patient years (95% CI: 2.3–12.4). Only four cases were patients of Doctor Lens, thus for the 7% discontinuation rate, the incidence is 3.9 per 10,000 patient years (95% CI: 1.5–10.0). Likewise, for a 10% discontinuation rate, the incidence is 4.2 per 10,000 patient years (95% CI: 1.7–10.9).

DISCUSSION

Causes of Microbial Keratitis in Children

This is the first study describing a case series of microbial keratitis in children outside of east Asia. The data are compared with three previous studies in Table 3.28–30 Interestingly, the proportion of cases of microbial keratitis attributed to contact lenses in the current study is similar to the two studies in Taiwan. Furthermore, the proportion of cases attributed to overnight orthokeratology was between 10% and 19% in all three case series. The Hong Kong study is different in that more than 80% of cases were associated with contact lenses—divided evenly between soft contact lenses and overnight orthokeratology. This probably represents differences in practice patterns. Hong Kong has one of the highest rates of orthokeratology fitting (5.9%) in the world.8 As well, the tropical climate and contamination of water sources may be potential reasons for higher rate of contact lens-related microbial keratitis in Hong Kong.31

TABLE 3. - Comparison of the Current Study With Previous Studies of Pediatric Microbial Keratitis
Authors Location Years No. of Cases Age (years) Attributed Cause
Contact Lenses Soft Ortho-k
Hsiao et al.28 Taiwan 1998–2002 78 ≤16 41% 31% 10%
Young et al.29 Hong Kong 2001–2010 18 ≤18 83% 44% 39%
Lee et al.30 Taiwan 2008–2012 67 ≤16 53% 34% 19%
Current study Russia 2018 45 ≤17 44% 33% 11%

Age Distribution of Overnight Orthokeratology Patients

The only previous comprehensive study of the safety of overnight orthokeratology reported data on 1,317 patients fitted in 2005 and 2006.26 That was a postmarket surveillance study (PMS) mandated by the US Food and Drug Administration (FDA) and is hereafter referred to as the FDA-PMS study. Figure 2, compares their age distribution with that of the present study, including adults. The FDA-PMS study included 48.6% adults compared with only 21.2% in the Doctor Lens patient population. Although conducted in different countries, this presumably reflects the increased use of overnight orthokeratology for myopia control in children in the past decade. Comparing only patients younger than 18 years in the two studies, shows nearly identical distributions (Fig. 2).

FIG. 2.
FIG. 2.:
Age distribution of patients fitted in a previous study of overnight orthokeratology compared with the present study. The upper panel shows all patients, whereas the lower panel represents only children.

Incidence of Microbial Keratitis in Children Wearing Overnight Orthokeratology

This is only the second study to estimate the incidence of microbial keratitis in overnight orthokeratology. The estimates based on different assumptions range from 3.9 to 5.3 per 10,000 patient years with an upper 95% CI as high as 12.4 per 10,000 patient years. The parameter estimates in these analyses are lower than the estimate in children of 13.9 per 10,000 patient years (95% CI: 1.7–50.4) in the FDA-PMS study, although the confidence intervals show considerable overlap.26 There are a number of potential reasons for the difference. For example, the present study includes only data from a single group of practices with standardized training and methodology (see below), whereas the previous study obtained data from 87 different practices. Nevertheless, the new estimate of the incidence of microbial keratitis in overnight orthokeratology appears similar to that of daily wear soft lenses, the most common modality used in children and teenagers.32,33

The incidence of microbial keratitis among Doctor Lens patients were reported in an earlier study.27 The study included 826 patients fitted between November 2002 and April 2008. The incidence of microbial keratitis was 32 per 10,000 patient years for all patients and 40 per 10,000 patient years in patients 20 years or younger. Another case series was presented at the EurOK conference in 2012 (D.S. Mirsayafov, E.A. Dyakonova, A.R. Khuray, P.V. Astinskaya, T.Yu. Verzhanskaya, E.P. Tarutta. The incidence of corneal pathology in myopic Ortho-K. 1st Meeting of European Academy of Orthokeratology, Madrid, June 9–10, 2012). This report included 1,390 patients fitted between January 2007 and June 2009. The incidence of microbial keratitis was 9.4 per 10,000 patient years, 10.4 per 10,000 patient years in patients 20 years or younger. Taken together with data from the current study, these results suggest that methodical and systematic efforts to improve patient compliance, along with standardization of care systems, may have lowered the incidence of microbial keratitis.

Study Limitations

Although data on children presenting with microbial keratitis were collected for a full year, there is some uncertainty regarding the number of children wearing overnight orthokeratology during this year. We have used conservative estimates of discontinuation of wear based on confirmed discontinuations and supported by earlier work. In the FDA-PMS study of the incidence of microbial keratitis with overnight orthokeratology,26 748 pediatric patients were identified, although only 677 (90.5%) contributed to the estimates. Among the remainder, 27 (3.6%) had worn their lenses for less than 3 months within the study window, 15 (2.0%) had documented discontinuation, and 29 (3.9%) had been lost to follow-up. The remaining eligible patients contributed an average of 2.1 years of wear to the estimates and continued to wear their lenses at the last documented visit.

A constant discontinuation rate was used, but patients might discontinue wear at higher rates in their teens as their myopia stabilizes. The mean age for stabilization of myopia has been estimated as 15.6 years, although a quarter of patients progress beyond 18 years.34 Nonetheless, patients may enjoy the convenience of overnight orthokeratology and continue to wear them after their refractive error has stabilized. Of note, 24% of the pediatric patients were fitted at age 15 years or older (Fig. 1), so older children still choose this modality. It is also interesting to note that the mean age at fitting is 12.4 years, but that mean age of the microbial keratitis cases in orthokeratology patients is 15.2 years (range 14–16 years). This three-year difference further suggests that children continue to wear their lenses well into their teens.

The combined influence of discontinuation of lens wear and patients reaching their 18th birthday, means that the distribution of patients is skewed toward recent fittings. Indeed, Table 2 shows that more than 80% of the estimated wearers in 2018 were fitted in 2014 or later. Because of this, increasing the assumed discontinuation rate has a modest effect on the estimated incidence. For example, assuming a 20% annual discontinuation rate would lead to 6,989 patient years of wear during 2018 and an incidence of 7.2 per 10,000 patient years (95% CI: 3.1–16.7), not markedly higher than the incidence for a 10% annual discontinuation rate: 5.3 per 10,000 patient years (95% CI: 2.3–12.4).

It is possible that other cases of microbial keratitis could have occurred in children fit with overnight orthokeratology and not presented at MCCCH, but this is unlikely given the established practices in the treatment of pediatric patients. Only nonurgent cases would have been seen elsewhere. All hospitals including MCCCH share statistical records with the Moscow Ministry of Public Health and these data are available to all participating hospitals. According to these data, no other cases of microbial keratitis in children were identified. Nonetheless, no data are available on the total number of patients fit with overnight orthokeratology in Moscow, although clinics in the city other than Doctor Lens do fit orthokeratology lenses.

A 2016 case-control study of Acanthamoeba keratitis in US RGP contact lens wearers and a more recent case series, both showed that overnight orthokeratology wearers were overrepresented.35,36 The recent case series documented 47 cases of Acanthamoeba keratitis in contact lens users younger than 18 years between 2003 and 2016.36 Six (13%) were orthokeratology wearers, exceeding the expected proportion based on the previously described market data.7,8 This is consistent with the present study, where about 25% of the contact lens-related microbial keratitis cases were associated with orthokeratology lens wear.

SUMMARY

This study identified cases of microbial keratitis associated with overnight orthokeratology wear in children in a large urban area in Russia in 2018. We used conservative estimates of patients wearing these lenses to provide a contemporary estimate of the incidence of microbial keratitis. Our estimates are largely consistent with the FDA-PMS study conducted in the United States.

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Keywords:

Microbial keratitis; Overnight orthokeratology; Children; Contact lenses

Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the Contact Lens Association of Opthalmologists.