Title Page

Gender inequalities in surgery for bilateral cataract among children in low income countries: a systematic review

Clare E Gilbert FRCOphth., MD.,1 and Nathalie Lepvrier-Chomette MD., DES1

Affiliations1 International Centre for Eye Health, Department of Clinical Research, London School of Hygiene & Tropical Medicine, London, UK

Corresponding author and address for reprintsClare GilbertDepartment of Clinical Research,London School of Hygiene & Tropical MedicineKeppel StreetLondon EC1V 7HTclare.gilbert@Lshtm.ac.uk+44 207 958 8332

Financial Support: None

Meeting presentationThe findings were briefly presented at a course of pediatric ophthalmologists, Institute of Child Health, November 23 2015

Conflict of interest No conflicting relationship exists for either author

Running head Gender and access to pediatric cataract surgery

Protocol registration Not registered

Abbreviations None

Key words: Pediatric cataract; childhood cataract, gender, cataract surgery

Word count 2717

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ABSTRACT

Topic

Gender differences in service access among children are reported for several conditions, but not for

surgery for bilateral cataract. In this review we compare the proportion of children undergoing surgery

for bilateral, non-traumatic cataract who were girls, using data from high-income, “gender-neutral”

countries as the reference.

Clinical relevance

Cataract is a common cause of avoidable blindness in children globally.

Methods

A systematic review of MEDLINE was undertaken in November 2014. Studies published from 2000

onwards were included as techniques and services have improved over time. A wide range of study

designs was included, i.e., population-based data, registers, studies of surgical techniques, clinical

trials etc. Papers with 20 or fewer cases were excluded or were of long-term follow up only, as this

may reflect gender differences in follow up. A meta-analysis was not planned.

Results

38 studies (6,854 children) were included from 1342 titles, 10 from high-income countries. Many did

not present data disaggregated by gender. Overall, 36.5% children were girls. In gender neutral

countries 47.5% (777/1,636) were girls, being similar in the Middle East, North Africa and Central

Asia region 48.6% (87/179) and in Latin America and Caribbean (43.7%, 188/430). Proportions were

significantly lower in Sub-Saharan Africa (41.1%, 225/547), East Asia and Pacific (36.0%, 237/658)

and South Asia (28.6%, 991/3,404).

Conclusions

Access to surgery by girls with bilateral cataract is lower in some regions than by boys. Barriers to

access specific to girls need to be identified, particularly in Asia, in order to assess interventions to

improve uptake.

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The epidemiology of blindness in children is dynamic, responding to socio-economic

development, demographic change, coverage of public health interventions for child survival (e.g.,

measles immunization, vitamin A supplementation) as well as the availability of and access to eye

care services.(1) In the mid-1990s there were estimated to be 1.4 million children who were blind, the

estimate being derived from prevalence estimates using under 5 mortality rates as a proxy, and the

child population aged 0-15 years in each country. In 2005 the estimate was revised, suggesting that

there had been a 10% decline in the number of blind children, to 1.26 million.(2) A further estimate,

using under 5 mortality data from 2008 and the child population for 2014 suggests a further decline, to

1.14 million.(3)

The causes of blindness in children can also change fairly rapidly over time, with a marked

reduction in corneal scarring being reported over the last two decades in the poorest countries, and

retinopathy of prematurity emerging as the commonest avoidable cause in many middle-income

countries. As corneal scarring from keratomalacia has declined, cataract is now the commonest cause

of avoidable blindness in children in many low-income settings.(1, 4)

Childhood cataract may be unilateral or bilateral, congenital or developmental and primary or

secondary. Bilateral congenital or developmental cataracts may be inherited, with autosomal

dominance being the most frequently reported mode of inheritance, or be due to intrauterine infection,

or associated with syndromes. However, in a high proportion of cases the underlying cause cannot be

determined.(5-7) No cause is likely to affect boys or girls differently, and one would, therefore, expect

an equal incidence by gender. Indeed, a study of all newly diagnosed children presenting with cataract

to health services in the UK over a 12 month period in 1995/6, reported that the proportion who were

girls almost equalled that of boys.(5)

Early presentation followed by high quality cataract surgery, with long term follow up are all

factors which influence visual acuity outcomes. However, in many low income settings children

present late for surgery, which compromises outcomes(8) and in Tanzania, girls were likely to present

later than boys.(9) In a study in Malawi, which included families of children with cataract who had or

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had not accessed surgery, poorer families and those living further from facilities were less likely to

have accessed services, but in this relatively small study gender was not associated with acceptance.

(10)

Gender differences have been reported for a wide range of health outcomes and conditions

affecting children, including under 5 mortality rates. For example, a study in almost 600 districts in

India estimated that there were 74,000 more deaths amongst girls than boys.(11) In another large scale

study, gender differences in under 5 mortality rates were compared between high income countries

that were considered “gender-neutral” (e.g., European countries and those in north America) with 31

Sub-Saharan countries and four countries in Asia. This study, along with many others, concluded that

maternal education reduces under-five mortality overall, and reduces gender inequality.(12)

The purpose of this study was to assess whether there are gender differences in children who

have accessed surgery for bilateral cataract and whether there was regional variation, using data from

high income countries, as defined by the World Bank(13) which could be considered “gender-neutral”

as a comparator. The objective of the review was to compare the proportion of boys and girls

identified by health service providers with bilateral cataract who had undergone cataract surgery in

one or both eyes, using data from a range of study designs, including surveillance, case series, and

clinical trials of different aspects of surgery.

METHODS

The study was limited to children with bilateral cataract. Children with unilateral cataract were

excluded for several reasons. Firstly, traumatic cataract is much more frequent in boys than girls.

Second, in settings where children often present very late, congenital/developmental cataract may be

misclassified as traumatic and visa versa, and lastly, unilateral cataracts are often not operated on in

low/middle income settings as late presentation gives very poor outcomes on account of dense

amblyopia. Studies published before 2000 onwards were also excluded as surgical techniques and the

provision of surgical services for children have improved over time.(14)

Eligibility criteria for considering studies for this review

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Papers in all languages and a wide range of study designs were included, i.e., papers reporting

epidemiological data or data from registers, surgical techniques, clinical trials, the outcome or

complications of surgery or delay in presentation for surgery. Papers were excluded if they reported

less than 20 bilateral cases or if they reported cases with long term follow up only, as this may reflect

gender differences in follow up as well as access to surgery.

Search methods for identifying studies

A systematic review of the published literature was conducted in MEDLINE (November 2014).

Reference lists in published papers were also reviewed. The search terms used are shown in the

Appendix.

<Appendix. Search terms used in the literature review>

Study selection

After removing duplicates, titles identified in the search were scanned by one reviewer and the

abstracts of selected titles were then reviewed. When case series reported different aspects from the

same group of children, such as delay in attendance in one paper and the outcome of surgery another,

only one was retained. Papers that fulfilled the eligibility criteria were read in full, even if unilateral

and bilateral cases were reported together. Attempts were made to contact authors reporting data on

unilateral and bilateral cases together to request data disaggregated by gender for bilateral cases only.

Some data provided by authors differs slightly from that in their publication with respect to the total

number operated and the proportion who were girls, as some reported only those attending for follow

up in denominator in the publication. The final list of papers was reviewed by both reviewers (NC and

CG).

Data collection and risk of bias assessment

Data were extracted and entered into an Excel spreadsheet using pre-determined headings which

included author, year of publication, country, study design, total number of children with bilateral

cataract undergoing surgery and the proportion who were girls. Manuscripts which reported cases

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attending long term follow up only (i.e. which did not present data on the whole cohort undergoing

surgery) as gender differences in follow rates would have biased the findings.

Data were prepared for countries classified as high-income by the World Bank, and other

countries were classified under each of the six World Bank geographical regions. The proportion of

children accessing cataract surgery who were girls was compared by region using the z-statistic, using

data from countries defined by the World Bank as high income as the reference.

Data synthesis and analysis

A meta-analysis was not planned due to the heterogeneous nature of the study designs. Findings are

reported narratively.

Ethical approval was not required for this study.

RESULTS

The search generated 1,342 titles, and 38 studies were included in the review (Figure 1). A total of

6,854 children were included in these studies, 2505 (36.5%) of whom were girls.

<Figure 1. Flow chart of articles identified and included in the review>

Ten studies from high income countries were identified, two from the United States of America, the

Republic of Korea and the United Kingdom (UK), and one each from Australia, Italy, Denmark and

Sweden (Table 1).

<Table 1. Gender distribution of children with bilateral cataract in high income economies and high income OECD members which are likely to be gender-neutral countries>

The UK study (2008) reports on children identified with cataract through a national surveillance study

who subsequently underwent surgery, 46.7% of whom were girls(15), being very similar to a further

study from the UK reported in 2015.(16) Data from the initial surveillance study identified 248

children with congenital or developmental cataract (i.e. excluding traumatic cataract) who presented to

ophthalmologists across the country over a 12 month period. 108 of these children had bilateral

cataract, and 48% of all cases were girls (i.e. unilateral and bilateral)(17). The Australian study was of

children attending two paediatric ophthalmology clinics in south east Australia for the management of

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cataract. In this study 52% of the 468 bilateral cases were girls(6). The large Danish study reports data

from the mandatory Danish National Register of Patients, in which 44% were girls(7). Across the ten

studies 42.5% - 54.5% were girls, the overall figure being 47.5%.

The majority of the other 28 studies were retrospective case series focussing on the outcome of

surgery (Table 2).

<Table 2. Gender distribution of children with bilateral cataract in other countries, by World Bank geographical region>

A few were prospective studies, or were undertaken to explore specific outcomes, such as nystagmus

or corneal thickness after surgery, or were clinical trials. One study in India was a retrospective review

of cases presenting to the hospital regardless of whether they had undergone cataract surgery(18). The

data show that the proportion of girls receiving surgery were comparable to that in high income

countries in the Middle East, North Africa and Central Asia region (48.6%) and the Latin America and

Caribbean region (43.7%) but were significantly lower in all other regions: sub-Saharan Africa

(41.1%), East Asia and Pacific (all from China)(36.0%), South Asia (29.1%)(Table 3).

<Table 3. Proportion of girls accessing cataract surgery by World Bank Region>

DISCUSSION

This review demonstrates that in some regions of the world the proportion of girls accessing surgery

for bilateral cataract is lower than anticipated, particularly in countries in Asia. There are several

possible explanations. Firstly, cataract may have a different pattern of aetiology in Asian countries

than elsewhere, with X-linked forms being more prevalent, which would lead to a gender difference in

the incidence. However, X-linked inheritance is the least common mode of inheritance of cataract in

children.(19) Another explanation is that girls with bilateral cataract have a higher mortality rate than

boys. Although children who are blind have a higher mortality rate than their sighted counterparts,

there are no mortality data by cause of visual loss, or by gender.(20) However, there is some evidence

that disabled children have lower immunization rates than non-disabled children (21), and if cataract

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blind girls have lower immunization coverage for conditions such as measles which have high

mortality rates, then this might lead to higher mortality rates amongst cataract blind girls. Another

explanation for gender differences in cataract surgery is sex differences in birth rates, as has been

reported in China and in some areas of India (22). Recent data from the United Nations Population

Division shows that 86% of children aged 0-9 years in China are girls, and in India 90% are girls,

reflecting parent’s gender preference for sons. This is despite more boys usually being born than girls

in countries without marked gender preference. Gender differences in birth rates due to selective

termination of pregnancy, female infanticide and sex preference in communities with access to family

planning, as reported in Nepal (23), may also lead to a greater number of boys with cataract than girls,

but this is conjectural.

The authors consider the most likely explanation is that in some regions families have different

health seeking behaviour for their sons than for their daughters. Indeed, a recent study of 21 tertiary

eye care centres for children in 11 countries in Africa showed that almost twice as many boys as girls

underwent surgery for congenital or developmental cataract. However, some of the traumatic cases

may have been misclassified, and only half the centres were able to provide data disaggregated by

gender.(14)

Gender bias has been reported across the spectrum of child health care (24), with girls having

poorer nutritional status and lower rates of immunization (25). Girls tend to present late to services for

severe conditions such as diarrhoea, and have lower uptake of surgery for serious complaints such as

congenital heart disease (26) with the differences being more pronounced in Asian countries. The

study on access to congenital heart surgery, which included interviews with parents is perhaps, of

most relevance to our study. In this study girls from households with higher socio-economic status

were more likely to undergo surgery than children from poorer families, and a quarter of parents of

girls felt the need to conceal their child’s condition from family and friends compared with 1.5% of

parents of boys. Parents of 62% of girls were concerned that the operation scar would be detrimental

to their marriage prospects compared with 6% of boys. Reasons given for late presentation differed

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depending on the gender of the child, with lack of finances being the major reason for boys, but lack

of support from relatives being the major reason for girls. Parents were also fearful of the surgery, and

were apprehensive about visiting big cities. Few studies have been undertaken to assess barriers to

accessing surgery for cataract among children, but a community based study in Malawi showed that

low socio-economic status and low education of mothers were associated with not accessing services.

In this study levels of awareness of cataract and its causes and treatment were low, and the main

barriers were distance, no felt need, a preference for traditional healers/herbalists, fear of the

operation, and acceptance of hereditary cataract as being God-given (10). A similar study has been

undertaken in Tanzania (8) showing barriers at different levels: individual, family, community and

institutional. However, neither of these studies reported on gender differences.

There are several models which conceptualize health seeking behaviour, including the

behavioural and psychosocial models. The latter describes the complex interplay of factors which

influence health seeking behaviour, including assessment of the seriousness of the condition, and the

cost and benefits of seeking care. The cultural, economic and social context in which the individual

and family live is, therefore, a powerful determinant of health seeking behaviour. However, in a study

of household decision making in Nepal in relation to child health, the author adds another component,

arguing that the initial perception of illness is critically important.(27) In the Nepal study data were

analysed from a community based survey, showing that parents of girls were significantly less likely

to report common illnesses (fever, diarrhoea, others) than parents of boys, with the differences being

greater among poorer households and where mothers were less well educated. However, having

perceived that their child was ill, there were no gender differences in subsequent decision making,

except more money was spent on treating diarrhoea in boys than in girls. This is in contrast to a large

scale study in India which demonstrated a higher rate of hospitalization for boys than girls, with the

gender difference being even more pronounced when money to pay for services had to be borrowed or

assets sold(28). To date there have been no studies of out of pocket expenditure incurred by parents of

children undergoing cataract surgery, which, given the relatively high cost of providing cataract

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services for children (29-30) are likely to be considerable in settings where fees for cataract surgery

are higher than for adult surgery.

The overall explanation for the lower access to surgery by girls with bilateral cataract is likely

to reflect a complex interplay of social, economic and attitudinal factors, with poverty, low levels of

maternal education and cultural norms being key factors.

A limitation of this review is that many published studies could not be included as they did not

report unilateral cases separately from bilateral cases, and authors could not be contacted. However,

this is unlikely to have biased the findings. A high proportion of the studies from low and middle-

income countries were reported by high volume tertiary centres, many of which are not government

facilities. This may have biased the findings as fees are usually charged for surgery in the private not-

for-profit sector as well as in the private for-profit sector, which may present more of a barrier to

parents of girls than of boys.

Improving childhood cataract surgical rates (31) in low-income settings will require greater

emphasis on proactive case detection, such as red reflex testing within six weeks of birth and during

immunization, as well as interventions to improve uptake of surgery, particularly among girls. Further

research is needed to explore attitudes towards disabling visual loss in children among community

members and affected families, in order to identify testable interventions. Increasing uptake will be

challenging, as demonstrated in Malawi, where counselling together with free surgery and transport

did not lead to universal uptake. Both mothers and fathers will need to be involved in any

intervention, as mothers usually detect the health problem and initiate health seeking behaviour, while

fathers provide the financial support. Authors of future studies are encouraged to present data on

bilateral cases disaggregated by gender, and further research is needed to assess gender differences in

access to services by children with other chronic, non-life threatening conditions.

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Table 1. Gender distribution of children with bilateral cataract in high income economies and high income OECD members which are likely to be gender-neutral countries

Author, year of study (ref) Country Type of study Bilateral

cases

N

Boys Girls

    N N %

Lundvall, 2002 (32) Sweden Outcome of surgery (R) 22 10 12 54.5%

Wirth, 2002 (6) Australia Hospital database 468 223 245 52.4%

Park, 2010 (33) Korea (Rep of) Outcome of surgery (R) 56 27 29 51.8%

Young, 2012 (34) USA Nystagmus after surgery (R) 56 29 27 48.2%

Lambert, 2006 (35) USA Outcome of surgery (R) 43 23 20 46.5%

Chak, 2008 (15) UK Initially identified through national surveillance 120 64 56 46.7%

Solebo, 2015 (16) UK Outcome of surgery (P) 147 77 70 47.6%

Haargaard, 2004 (7) Denmark Register 647 362 285 44.0%

Kim, 2012 (36) Korea (Rep of) Outcome of surgery (R) 37 21 16 43.2%

Magli, 2009 (37) Italy Outcome of surgery (R) 40 23 17 42.5%

TOTAL     1636 859 777 47.5%

USA = United States of America; UK = United Kingdom; Rep of = Republic ofR = retrospective; P=prospective

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Table 2. Gender distribution of children with bilateral cataract in other countries, by World Bank geographical region

World Bank region Country Study design All Boys GirlsAuthor, year of study (ref) N N N %Middle East and North Africa, Central Asia (3) Totan, 2008 (38) Turkey Outcome of surgery study (P) 39 16 23 59.0%Katibeh, 2013 (39) Iran Hospital register 55 28 27 49.1%Hafidi, 2013 (40) Morocco Outcome of surgery study (R) 85 48 37 43.5%Latin America and Caribbean (4)  Lupinacci, 2009 Brazil Study of corneal thickness (P) 34 14 20 58.8%Zimmermann-Paiz, 2011 Guatemala Outcome of surgery study (R) 168 94 74 44.0%Congdon, 2007 Mexico Outcome of surgery study (P) 203 118 85 41.9%Tartarella, 2014 Brazil Study of axial length (P) 25 16 9 36.0%SubSaharan Africa (5)  Bowman, 2007 Tanzania Outcome of surgery study (R) 243 127 106 43.6%Gradin, 2012 Kenya Outcome of surgery study (R) 96 64 42 43.8%Randrianotahina, 2014 Madagascar Outcome of surgery study (R) 29 15 12 41.4%Baden, 2013 Tanzania Outcome of surgery study (R) 108 65 43 39.8%Yorston, 2001  Kenya Outcome of surgery study (R) 71 49 22 31.0%East Asia and Pacific (3)    Lin, 2012  China Trial of SMS for follow up 231 143 88 38.1%You, 2011 China Outcome of surgery study (R) 113 72 41 36.3%Zhang, 2012 N China Outcome of surgery study (R) 314 206 108 34.4%South Asia (13)  Paryani, 2012 India Outcome of surgery study (P) 24 12 12 50.0%Khanna, 2013 India Outcome of surgery study (R) 215 131 84 39.1%Gogate, 2014 India Outcome of surgery study (P) 129 74 55 42.6%Gupta, 2012 India Outcome of surgery study (R) 131 81 50 38.2%Khokhar, 2012 (18) India Case series (R) 210 136 74 35.2%Vasavada, 2012 India Trial of LMW heparin 20 13 7 35.0%Assuari, 2006 India Trial of types of IOL 23 15 8 34.8%Khandeka, 2007 India Outcome of surgery study (R) 65 44 21 32.3%

Hennig, 2013  Nepal, India* Outcome of surgery study (R) 390 270 120 30.8%

Rai, 2014  Nepal, India* Outcome of surgery study (R) 144 103 41 28.5%

Wilson, 2011  Nepal Outcome of surgery study (R) 1849 1378 471 25.5%Ganesh, 2014  India Outcome of surgery study (P) 53 40 13 24.5%Ram, 2011 India Outcome of surgery study (R) 151 116 35 23.2%

Note: Some data differ from that in the published paper as some authors provided data on the number operated on while the publication focussed on the number presenting at follow upR = retrospective; P = prospective; LMWH = low molecular weight heparin*Children operated for cataract in Nepal who came from India

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Figure 1. Flow chart of articles identified and included in the review

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AcknowledgementsIris Gordon who compiled the search terms and removed duplicates.

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