The Demography and Aetiology of Strabismus Patients in a Tertiary Eye Centre in North China, 2014-2019

Background analyse the epidemiology and clinical characteristics of patients in China. Methods


Abstract Background
To analyse the epidemiology and clinical characteristics of strabismus patients in north China.

Methods
The records of strabismus patients at Qingdao Eye Hospital from January 2014 to December 2019 were reviewed retrospectively. The characteristics analysed included gender, regional distribution, constituent ratio of age and type of strabismus. Changes during the periods 2014-2016 and 2017-2019 were compared and analysed.

Results
A total of 5746 strabismus patients were recruited. The number of strabismus patients was relatively stable each year from 2014 to 2016 but gradually increased each year from 2017 to 2019. Of these, 51.7% (2868/5746) were male, and 48.3% (2778/5746) were female. The majority (89.8%, 5159/5746) of the patients were from Shandong Province. The statistical results of the constituent ratio of age showed that 32.4% (1860/5746) were 7-12 years old(primary school level). Patients under 12 years of age (preschool and primary school level) accounted for 60.0% (3447/5746) of all the patients. In terms of the types of strabismus, exotropia accounted for 63.5% (3650/5746), followed by esotropia and vertical rotational strabismus at 13.2% (758/5746) and 9.7% (555/5746), respectively. Intermittent exotropia was the most common type among the exotropia patients, accounting for 71.3% (2604/3650). Among the patients with intermittent exotropia, 62.5% (1627/2604) were children aged 4-12 years, and the basic type of intermittent exotropia was the main type. Four percent (231/5746) of the patients, of which adult patients comprised the main population, required reoperation.

Conclusion
Patients with strabismus at primary school level comprised the largest group of strabismus patients in north China. Exotropia was the most common type of strabismus, and intermittent exotropia was the most common type of exotropia. The rate of exotropia to esotropia was 5:1.

Background
Epidemiologic studies of strabismus focus predominantly on Western countries. In Asian countries, they are mainly concentrated in Singapore and Japan. However, due to differences in ethnicity, population size and regional distribution, the ndings of these studies can only provide reference for clinicians in China and cannot really guide their clinical work. In China, because of differences in diagnostic and treatment levels, many hospitals do not carry out strabismus surgery or carry out fewer strabismus surgeries. It is therefore di cult to obtain data on strabismus surgery distribution without a large sample. For this study, a retrospective analysis of strabismus patients during a 6-year period in a tertiary eye centre in north China was conducted to understand the regional distribution and constituent ratios of age and types of strabismus. This study therefore sought to determine the distribution of strabismus in northern China and to provide a reference for the epidemiology of strabismus in China.

Methods
The data of 5746 patients who underwent strabismus surgery in the Strabismus Department of Qingdao Eye Hospital from January 2014 to December 2019 were collected retrospectively. All the clinical records were provided by the information centre system of Qingdao Eye Hospital. This information included each patient's name, gender, age, address and diagnosis, among other details. In each case, the naked and corrected binocular vision, intraocular pressure, refractive state, anterior segment and ocular fundus were examined prior to surgery. The 6 m and 33 cm degrees of horizontal or vertical deviation were measured using the Hirschberg method and prism cover test. The deviation degrees of the other directions and binocular visual function were checked according to the needs of the surgery. The diagnosis and classi cation of strabismus were based on expert consensus (Strabismus and Paediatric Ophthalmology Group of the Ophthalmology Branch of the Chinese Medical Association, 2015) on strabismus classi cation in China [1]. SPSS version 22.0 statistical software was used to analyse the data in this retrospective study. The enumeration data were compared using a chi-squared (X 2 ) test, and P<0.05 was considered statistically signi cant.
The study was approved by the Ophthalmology Ethics Committee of Qingdao Eye Hospital(approval no.2020-21). Written informed consent was obtained from all the patients who participated in the study or their legal representatives.Written consent was obtained from a parent or guardian on behalf of any participants under the age of 16 before the study.
The data of 5746 patients who underwent strabismus surgery in the Strabismus Department of Qingdao Eye Hospital from January 2014 to December 2019 were collected retrospectively. All the clinical records were provided by the information centre system of Qingdao Eye Hospital. This information included each patient's name, gender, age, address and diagnosis, among other details. In each case, the naked and corrected binocular vision, intraocular pressure, refractive state, anterior segment and ocular fundus were examined prior to surgery. The 6 m and 33 cm degrees of horizontal or vertical deviation were measured using the Hirschberg method and prism cover test. The deviation degrees of the other directions and binocular visual function were checked according to the needs of the surgery. The diagnosis and classi cation of strabismus were based on expert consensus (Strabismus and Paediatric Ophthalmology Group of the Ophthalmology Branch of the Chinese Medical Association, 2015) on strabismus classi cation in China [1]. SPSS version 22.0 statistical software was used to analyse the data in this retrospective study. The enumeration data were compared using a chi-squared (X 2 ) test, and P<0.05 was considered statistically signi cant.
The study was approved by the Ophthalmology Ethics Committee of Qingdao Eye Hospital(approval no.2020-21). Written informed consent was obtained from all the patients who participated in the study or their legal representatives.Written consent was obtained from a parent or guardian on behalf of any participants under the age of 16 before the study.

Epidemiological characteristics of strabismus patients
The data of 5746 strabismus patients who visited Qingdao Eye Hospital from January 2014 to December 2019 were recorded and analysed. The patients' ages ranged from 1 to 84 years, with an average age of 15.2 years. The horizontal strabismus angle was 0-160 PD, and the vertical deviation was 0-90 PD.
The strabismus patients resided in three areas: within Qingdao, outside Qingdao(within Shandong Province) and outside Shandong Province. The statistical results over the 6-year study period showed that the majority of the patients were from Shandong Province: 47.5% (2730/5746) of the patients were from Qingdao, 42.3% (2429/5746) were from other cities in Shandong Province and 10.2% were from other provinces (587/5746) ( Table 1).
All the categorisations were based on the classi cation of strabismus formulated by the Strabismus and Paediatric Ophthalmology Group of the Ophthalmology Branch of Chinese Medical Association. Among the patients, the majority (63.5%, 3650/5746) had exotropia, followed by esotropia and vertical rotational strabismus at 13.2% (758/5746) and 9.7% (555/5746), respectively. Intermittent exotropia was the most common type of exotropia, accounting for 71.3% (2604/3650) of patients. Special types of strabismus made up 6.3% (360/5746) of the patient population. Among these, the most common type was dissociated vertical deviation (DVD), which accounted for 87.5% (315/360). A-V strabismus, nystagmus and central paralytic strabismus comprised a small proportion of the patients in this study at 4.1% (236/5746), 1.9% (112/5746) and 1.3% (75/5746), respectively. Among all the patients, the exotropia group was the largest, and intermittent exotropia was the most common type of exotropia. The differences in the types of strabismus became statistically signi cant as time passed (P=0.000).  The proportion of patients aged over 18 was 54.5% (123/231), which was the highest percentage among all the age groups. On the other hand, the proportion of patients aged 0-6 years was 3.5% (8/231), which was the lowest proportion among all the age groups. Adult patients were the main population group who underwent reoperation (Table 3).  Fig 2).

Discussion
The results of epidemiological studies of strabismus have shown that the prevalence of strabismus among different populations varies by region and ethnicity. The prevalence of strabismus among white and African American children from 6 to 71 months was 3.3% and 2.1%, respectively. Esotropia and exotropia accounted for half the strabismus cases [2]. These were 3.55% and 3.24%, respectively, among Asian and non-Hispanic white children. Strabismus was found to be higher in children aged 6-72 months [3]. In Singapore, the prevalence of strabismus among children aged 6-72 months was found to be 0.80%, and the ratio of exotropia to esotropia was 7:1, with 63% of exotropia being intermittent [4]. Among 2704 patients with horizontal strabismus in Hong Kong, exotropia was shown to be more common than esotropia. In addition, the proportion of patients with intermittent exotropia seemed to be increasing [5]. Meanwhile, paralytic strabismus was the most common strabismus among adults [6]. Esotropia is most common strabismus in the rst 10 years of life, and a population-based study found that accommodative and acquired nonaccommodative forms of childhood esotropia occur most frequently [7]. Intermittent exotropia and insu cient convergence are the most common forms of childhood exotropia [8]. The results of this study showed that exotropia accounted for the highest proportion of all strabismus cases at 63.5%, followed by esotropia at 13.2%. The ratio of exotropia to esotropia was thus 5:1. There are several reasons that could explain this result: (1) The incidence of different types of strabismus may be related to race, genetics and refractive errors. It has been reported that prematurity and maternal smoking during pregnancy are associated with a higher risk of paediatric esotropia and exotropia[9]. Furthermore, strabismus was associated with gestational age, hyperopic refractive error and astigmatism [10]. Esotropia, with lower gestational age and a heavier placenta; exotropia, with a maternal history of previously treated hypertension and maternal use of recreational drugs during early pregnancy [11]. (2) Early screening of children's vision and binocular visual function is associated with the incidence of exotropia. Early vision screening provides an opportunity for intermittent exotropia to be detected, which increases the diagnostic levels of the disease. intervention. Contrarily, surgery is the primary treatment for patients with exotropia. Early strabismus surgery could not only reduce the damage to binocular visual function caused by strabismus, but also facilitate the establishment of visual function after surgery.
Intermittent exotropia is the most common type of exotropia, accounting for 50-90% of all patients with exotropia [12]. The results of this study showed that intermittent exotropia makes up the highest proportion (71.3%) of all patients with exotropia. Furthermore, exotropia constitutes the highest proportion of all strabismus patients. It can be speculated that surgery for intermittent exotropia is currently the main type of strabismus surgery. In this study, the main surgical group of intermittent exotropia patients comprised preschool and primary school-aged children, and the basic type was the main type of intermittent exotropia. The number of strabismus patients was relatively stable each year from 2014 to 2016, but gradually increased annually over the 2017-2019 period. This reason for this can be explained as follows: Many patients or the parents of children understand and receive early strabismus treatment because of a concomitant improvement in the national quality of life and awareness of strabismus. Adult patients were the main population of patients who underwent reoperation, which may be related to the high recurrence rate of strabismus over time. Esotropia was the highest form of strabismus and exotropia the lowest in patients aged 0-6 years, and this may be related to esotropia often being associated with hyperopic refractive abnormalities. Furthermore, exotropia may be related to the occurrence and development of myopia.
It was found that patients with intermittent exotropia are at a great higher risk of visual fatigue in comparison with healthy individuals [13]. Strabismus patients showed a greater risk of developing thoracic scoliosis [14].The temporal integration for stereopsis is impaired in patients with IXT, requiring longer critical integration time to achieve elevated optimal stereoacuity [15].Children with untreated strabismus can develop impaired binocular vision, which can interfere with their ability to conduct social interactions with other children. Lack of binocularity and stereopsis in children is associated with signi cant motor skills impairment, in particular for static balance and catching tasks [16]. Children can subsequently develop a sense of inferiority and fail to lead normal lives. Both the child and their parents' HRQOL showed a trend toward correlating with clinical severity [17,18]. Strabismus surgery has a positive impact on children's physical and psychological functioning. Children with greater corrections experience greater improvements in their quality of life after surgery [19].The stereopsis and HRQOL in adults with childhood large angle exotropia can be improved after successful surgical correction [20]. At the same time, with improvements in the national quality of life and awareness of children's diseases, many parents of children with strabismus understand and accept that early treatment of strabismus can enable children to obtain good stereo vision. Importantly, populations with strabismus need early treatment. This study showed that, among the patients who underwent strabismus surgery, those at primary school level (i.e. 7-12 years old) comprised the largest group, while those at preschool and primary school level (i.e. aged 0-12 years) accounted for 60% of all patients who underwent strabismus surgery. The parents of children in the latter age group should choose early strabismus surgery. In addition to being concerned that strabismus may cause damage to binocular visual function, some parents also worry about the impact of strabismus on the normal psychological development of their children.
With improvements in living standards, the prevention and treatment of strabismus and amblyopia have gradually been carried out in various parts of China, and emphasis has been placed on children's diseases and the need for early interventions. Many children with strabismus in relatively economically developed areas are screened and treated in hospitals. In addition, with the continuous improvements in ophthalmologists' technical levels, the treatment of strabismus has become more professional, which has increased the probability of successful surgery. In areas with relatively less-advanced medical standards where there are a lack of professional ophthalmologists, some ophthalmologists have relatively little knowledge of strabismus or do not pay enough attention to the disease. They believe that strabismus surgery should be provided when the child is older, thus giving patients the wrong information and causing problems. These children miss the optimal time for surgery, impairing their binocular vision and/or missing the best age to establish binocular vision. At the same time, because of the economic prosperity in China, excessive medical treatment of strabismus and amblyopia has become a prominent, negative medical phenomenon. Excessive medical treatment of strabismus includes violations of treatment standards and expanded operative indications. Accordingly, every ophthalmologist should master the standardised operative indications for strabismus. Promotional efforts and education about strabismus should not only be carried out in hospitals, but also in communities and schools so that every citizen can acquire a certain level of knowledge of strabismus. At the same time, ophthalmologists should perform eye examinations on preschool children so that children with strabismus can be detected early.

Conclusion
This research collected data exclusively from patients who underwent strabismus surgery. However, many strabismus patients, especially mild Intermittent exotropia, can be managed with non-surgical methods. The majority of patients in this study were from Shandong Province, so this study is limited to some extent, and the results can therefore not be generalised. The data analysis showed that primary school children comprised the largest strabismus group in northern China. Exotropia was the most common type of strabismus, and intermittent exotropia was the most common type of exotropia.
Furthermore, the rate of exotropia to esotropia was 5:1. Strategies for strabismus should aim to educate children and their parents about strabismus, as well as the importance of early screening and interventions.

Declarations
Ethics approval and consent to participate The study was approved by the Ophthalmology Ethics Committee of Qingdao Eye Hospital(approval no.2020-21). Written informed consent was obtained from all the patients who participated in the study or their legal representatives.Written consent was obtained from a parent or guardian on behalf of any participants under the age of 16 before the study.