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Visual outcome following phacoemulsification in English Cocker Spaniels with suspected progressive retinal atrophy: A retrospective multicenter study of 54 cases (2002-2017)
疑似进行性视网膜萎缩的英国可卡犬接受超声乳化术后的视觉效果：54 例病例的多中心回顾性研究（2002-2017 年）

Sarah Koll-Hampp 1 1 ^(1){ }^{1} | Andra-Elena Enache 2 2 ^(2){ }^{2} | Elena Fenollosa-Romero 3 3 ^(3){ }^{3} | Yu-Mei Chang 1 1 ^(1){ }^{1} | Claudia Busse 3 3 ^(3)^{3} | James Oliver 2 2 ^(2){ }^{2} | Charlotte Dawson 1 ( D ) 1 ( D ) ^(1)^((D)){ }^{1}{ }^{(D)} | Màrian Matas Riera 1 1 ^(1){ }^{1}
Sarah Koll-Hampp 1 1 ^(1){ }^{1} | Andra-Elena Enache 2 2 ^(2){ }^{2} | Elena Fenollosa-Romero 3 3 ^(3){ }^{3} | Yu-Mei Chang 1 1 ^(1){ }^{1} | Claudia Busse 3 3 ^(3)^{3} | James Oliver 2 2 ^(2){ }^{2} | Charlotte Dawson 1 ( D ) 1 ( D ) ^(1)^((D)){ }^{1}{ }^{(D)} | Màrian Matas Riera 1 1 ^(1){ }^{1}

1 1 ^(1){ }^{1} Ophthalmology Service, Royal Veterinary College (RVC), University of London, North Mymms, UK
1 1 ^(1){ }^{1} 英国伦敦大学皇家兽医学院（RVC）眼科服务处，北迈姆斯
2 2 ^(2){ }^{2} Unit of Comparative Ophthalmology, Animal Health Trust (AHT), Newmarket, UK
2 2 ^(2){ }^{2} 英国纽马克特动物健康信托基金（AHT）比较眼科部
3 3 ^(3){ }^{3} Ophthalmology Service, Dick White Referrals (DWR), Six Mile Bottom, UK
3 3 ^(3){ }^{3} 眼科服务，迪克-怀特转诊中心（DWR），英国六英里底

Correspondence 通信

Sarah Koll-Hampp, Ophthalmology Service, Royal Veterinary College (RVC), University of London, North Mymms, UK. Email: skoll@rvc.ac.uk
Sarah Koll-Hampp，英国伦敦大学皇家兽医学院（RVC）眼科服务处，北迈姆斯。电子邮件：skoll@rvc.ac.uk

Abstract 摘要

Objective: To describe the visual outcome following phacoemulsification in English Cocker Spaniels (ECS) affected by cataracts and suspected progressive retinal atrophy (PRA). Animals studied: Fifty-four client-owned dogs. Procedures: A multicenter, retrospective study was performed including ECS with suspected PRA which underwent phacoemulsification. PRA was suspected on ophthalmic examination before and after surgery, and/or after electroretinography (ERG) was performed. Visual outcome was assessed by menace response per eye at seven time periods post-surgery ( P 1 = 25 − 90 ( P 1 = 25 − 90 (P1=25-90(\mathrm{P} 1=25-90 days, P 2 = 91 − 180 P 2 = 91 − 180 P2=91-180\mathrm{P} 2=91-180 days, P 3 = 181 − 364 P 3 = 181 − 364 P3=181-364\mathrm{P} 3=181-364 days, P4 = 365 − 549 = 365 − 549 =365-549=365-549 days, P 5 = 550 − 729 P 5 = 550 − 729 P5=550-729\mathrm{P} 5=550-729 days, P 6 = 730 − 1094 P 6 = 730 − 1094 P6=730-1094\mathrm{P} 6=730-1094 days, and P7 ≥ 1095 ≥ 1095 >= 1095\geq 1095 days). Descriptive statistics were performed. Generalized estimating equations were used to identify predictors associated with vision after surgery. Odds ratio and confidence intervals were reported. Significance was set at P < 0.05 P < 0.05 P < 0.05P<0.05. Owners were invited to participate in a questionnaire. Results: Phacoemulsification was performed in 85 eyes. Median age at surgery was 9.09 years (min. 2.17 years, max. 13.49 years). At all re-examinations, up to and including P5, significantly more eyes were visual than before surgery ( P ≤ 0.003 P ≤ 0.003 P <= 0.003P \leq 0.003 ). Odds for vision were significantly increased for eyes that underwent surgery. Electroretinograms were performed in 75/85 eyes that underwent surgery, demonstrating low b-wave amplitudes. There was no significant effect of the age, gender, vision before surgery, presence of dazzle reflex, cataract stage or abnormality on gonioscopy on visual outcome. The questionnaire response rate was 48.2 % 48.2 % 48.2%48.2 \%. Most participants ( 92.5 % 92.5 % 92.5%92.5 \% ) felt that cataract surgery led to improvement of the dog’s quality of life.
目的描述对患有白内障和疑似进行性视网膜萎缩（PRA）的英国可卡犬（ECS）进行超声乳化术后的视觉效果。研究动物：54 只客户饲养的狗。手术过程：进行了一项多中心回顾性研究，研究对象包括接受了超声乳化术的疑似 PRA 的可卡犬。手术前后的眼科检查和/或进行视网膜电图（ERG）检查后怀疑有 PRA。通过术后七个时间段（ ( P 1 = 25 − 90 ( P 1 = 25 − 90 (P1=25-90(\mathrm{P} 1=25-90 天、 P 2 = 91 − 180 P 2 = 91 − 180 P2=91-180\mathrm{P} 2=91-180 天、 P 3 = 181 − 364 P 3 = 181 − 364 P3=181-364\mathrm{P} 3=181-364 天、P4 = 365 − 549 = 365 − 549 =365-549=365-549 天、 P 5 = 550 − 729 P 5 = 550 − 729 P5=550-729\mathrm{P} 5=550-729 天、 P 6 = 730 − 1094 P 6 = 730 − 1094 P6=730-1094\mathrm{P} 6=730-1094 天和P7 ≥ 1095 ≥ 1095 >= 1095\geq 1095 天）每只眼睛的视力反应来评估视觉结果。进行了描述性统计。使用广义估计方程确定与术后视力相关的预测因素。报告了比值比和置信区间。显著性设定为 P < 0.05 P < 0.05 P < 0.05P<0.05 。邀请车主参与问卷调查。结果：85只眼睛接受了乳化手术。手术年龄中位数为 9.09 岁（最小 2.17 岁，最大 13.49 岁）。在所有复查中，包括第五次复查在内，视力明显高于手术前的眼睛( P ≤ 0.003 P ≤ 0.003 P <= 0.003P \leq 0.003 )。接受过手术的眼睛视力的几率明显增加。对 75/85 只接受手术的眼睛进行了视网膜电图检查，结果显示 b 波振幅较低。年龄、性别、术前视力、有无眩晕反射、白内障分期或眼底检查异常对视力结果均无明显影响。问卷回复率为 48.2 % 48.2 % 48.2%48.2 \% 。大多数参与者（ 92.5 % 92.5 % 92.5%92.5 \% ）认为白内障手术提高了狗的生活质量。

Conclusions: English Cocker Spaniels with suspected PRA may benefit from phacoemulsification with vision up to 2 years following surgery.
结论：疑似患有 PRA 的英国可卡犬可从乳化手术中获益，术后视力可达 2 年。

KEYWORDS 关键词

cataract, phacoemulsification, progressive retinal atrophy
白内障、超声乳化术、进行性视网膜萎缩

1 | INTRODUCTION 1 简介

Cataracts are a common cause of blindness in dogs. Possible causes of cataract include inherited, congenital, aging, progressive retinal atrophy (PRA), and diabetes mellitus. 1 , 2 1 , 2 ^(1,2){ }^{1,2} As the cataract progresses, secondary complications such as lens-induced uveitis and secondary glaucoma can develop, which may cause ocular discomfort or pain. 1 , 2 1 , 2 ^(1,2){ }^{1,2} Surgical removal of the cataract holds the best prognosis for restoring vision and improving the overall ocular health, compared to medical management only or no treatment at all. 3 3 ^(3){ }^{3} Surgical success rates of 85 % − 90 % 85 % − 90 % 85%-90%85 \%-90 \% have been reported. 4 , 5 4 , 5 ^(4,5){ }^{4,5} Long-term complications after phacoemulsification include posterior capsular opacification, corneal lipid opacity, intraocular hemorrhage, glaucoma, and retinal detachment, which may lead to blindness or enucleation. 4 , 6 , 7 4 , 6 , 7 ^(4,6,7){ }^{4,6,7}
白内障是导致狗狗失明的常见原因。导致白内障的可能原因包括遗传、先天、衰老、进行性视网膜萎缩 (PRA) 和糖尿病。 1 , 2 1 , 2 ^(1,2){ }^{1,2} 随着白内障的发展，会出现继发性并发症，如透镜引起的葡萄膜炎和继发性青光眼，这可能会引起眼部不适或疼痛。 1 , 2 1 , 2 ^(1,2){ }^{1,2} 与只进行药物治疗或不进行任何治疗相比，手术摘除白内障在恢复视力和改善眼部整体健康方面的预后最好。 3 3 ^(3){ }^{3} 据报道，手术成功率为 85 % − 90 % 85 % − 90 % 85%-90%85 \%-90 \% 。 4 , 5 4 , 5 ^(4,5){ }^{4,5} 乳化术后的长期并发症包括后囊不透明、角膜脂质不透明、眼内出血、青光眼和视网膜脱离，这些并发症可能导致失明或眼球摘除。 4 , 6 , 7 4 , 6 , 7 ^(4,6,7){ }^{4,6,7}
Progressive retinal atrophy is a broad term for a variety of progressive, inherited diseases of the retina, that manifest as degeneration of the photoreceptor layer and/ or the retinal pigmented epithelium in many different dog breeds. 10 , 11 10 , 11 ^(10,11){ }^{10,11} It has been reported to be the third most common cause of cataracts accounting for 7.6 % 7.6 % 7.6%7.6 \% and 12.5 % 12.5 % 12.5%12.5 \% of cases in two retrospective studies. 12 , 13 12 , 13 ^(12,13){ }^{12,13} Cataracts secondary to PRA have been described to develop at advanced stages of PRA in some breeds. 11 , 14 11 , 14 ^(11,14){ }^{11,14} Historically, cataract surgery has not been recommended routinely in dogs affected by PRA, as these dogs will progressively lose vision despite the surgery. 15 15 ^(15){ }^{15} Disease onset and progression, as well as the underlying genetic mutations causative of PRA, vary between and within breeds. 16 , 17 16 , 17 ^(16,17){ }^{16,17} Many breeds are affected by a progressive rod-cone degeneration (prcd) with an identical mutation in the prcd locus, which is responsible for a late-onset form PRA. 17 17 ^(17){ }^{17} Interestingly, phenotypic differences have also been reported between breeds affected by the same prcd mutation. The English Cocker Spaniel (ECS) demonstrated a slower rate of photoreceptor degeneration histologically, compared to the Miniature Poodle (MP) and American Cocker Spaniel (ACS). 17 , 19 17 , 19 ^(17,19){ }^{17,19} Furthermore, ECS showed a mosaic of disease stages across the meridians of the fundus, with areas of delayed retinal degeneration. On ERG examination, MP’s lost their remaining b-wave function twice as fast as ECS. 19 19 ^(19){ }^{19} Supported by these findings in the ECS, the frequent presentation of this breed with cataracts and anecdotal clinical experiences of late-onset vision loss, the authors have performed cataract surgery in ECS following careful owner counseling.
进行性视网膜萎缩是多种进行性遗传性视网膜疾病的统称，表现为许多不同犬种的感光层和/或视网膜色素上皮变性。 10 , 11 10 , 11 ^(10,11){ }^{10,11} 据报道，它是白内障的第三大常见病因，在两项回顾性研究中分别占 7.6 % 7.6 % 7.6%7.6 \% 和 12.5 % 12.5 % 12.5%12.5 \% 例。 12 , 13 12 , 13 ^(12,13){ }^{12,13} 据描述，继发于 PRA 的白内障会在某些品种的 PRA 晚期出现。 11 , 14 11 , 14 ^(11,14){ }^{11,14} 一直以来，我们都不建议对患有 PRA 的狗进行白内障手术，因为尽管进行了手术，这些狗的视力还是会逐渐下降。 15 15 ^(15){ }^{15} 疾病的发生和发展以及导致 PRA 的潜在基因突变在不同品种之间和品种内部都各不相同。 16 , 17 16 , 17 ^(16,17){ }^{16,17} 许多犬种都会受到进行性杆-锥体变性（prcd）的影响，prcd 基因座上的相同突变会导致晚发型 PRA。 17 17 ^(17){ }^{17} 有趣的是，受相同prcd基因突变影响的犬种之间也存在表型差异。与迷你贵宾犬（MP）和美国可卡犬（ACS）相比，英国可卡犬（ECS）在组织学上表现出的光感受器退化速度较慢。 17 , 19 17 , 19 ^(17,19){ }^{17,19} 此外，ECS在眼底各经络中表现出不同的疾病阶段，并有延迟视网膜变性的区域。在 ERG 检查中，MP 患者丧失剩余 b 波功能的速度是 ECS 的两倍。 19 19 ^(19){ }^{19} 基于在 ECS 身上的这些发现、该犬种经常出现的白内障以及晚期视力丧失的临床经验，作者在仔细咨询了犬主之后，为 ECS 实施了白内障手术。
The main objective of this retrospective study was to describe the visual outcome at various re-examination periods following phacoemulsification in ECS with suspected PRA. The second objective was to investigate any predictors associated with a positive visual outcome following surgery.
这项回顾性研究的主要目的是描述疑似 PRA 的 ECS 患者在接受超声乳化术后不同复查时期的视觉结果。第二个目的是研究与术后积极视觉结果相关的任何预测因素。

2 | MATERIALS AND METHODS
2 材料和方法

A retrospective multicenter study was performed. Databases of the Royal Veterinary College (RVC), the Animal Health Trust (AHT), and Dick White Referrals (DWR) were searched for ECS with suspected progressive retinal atrophy and cataracts, which underwent phacoemulsification between 2002 and 2017. Ethical approval was obtained from the RVC Clinical Research Ethical Review Board (CRERB, URN: M2015 0073) and AHT Clinical Research Ethics Committee (41-2016).
我们进行了一项回顾性多中心研究。研究人员在皇家兽医学院（RVC）、动物健康信托基金（AHT）和迪克-怀特转诊（DWR）的数据库中搜索了2002年至2017年期间接受过超声乳化术的疑似进行性视网膜萎缩和白内障的ECS。该研究获得了RVC临床研究伦理审查委员会（CRERB，URN：M2015 0073）和AHT临床研究伦理委员会（41-2016）的伦理批准。
Dogs were included if they underwent a full ophthalmic examination including slit-lamp biomicroscopy, indirect binocular ophthalmoscopy, and tonometry before and after surgery by a diplomate or a resident under the supervision of a diplomate of the European College of Veterinary Ophthalmologists (ECVO). Gonioscopy (Koeppe lens; Ocular Instruments Inc, Washington, DC) and ocular ultrasound results were reported from examinations before surgery. Furthermore, information about the presence of concurrent systemic disease or ocular diseases was collected.
由欧洲兽医眼科医师学会 (ECVO) 的认证医师或在认证医师监督下的住院医师在手术前后对犬只进行全面的眼科检查，包括裂隙灯生物显微镜检查、间接双目眼底镜检查和眼压测量。巩膜镜检查（Koeppe lens；Ocular Instruments Inc，华盛顿特区）和眼部超声波检查结果均来自手术前的检查报告。此外，还收集了有关并发全身性疾病或眼部疾病的信息。
A diagnosis or suspicion of PRA was made based on the patient history, signalment, and full ophthalmic examination before or after surgery and, in the majority of cases, supported by the ERG results. In all referral centers, a short “yes/ no” ERG protocol was employed to assess gross photoreceptor function. The protocols used among the centers varied. A summary of the ERG protocols used is demonstrated in Table 1. ERGs were performed in conscious dogs at the AHT and at DWR and under general anesthesia at the RVC. The ERG machines used were HMsERG system (Model 2000; OcuScience, Henderson, NV) at the RVC and DWR, and Photic stimulator (SLE, CPS-20; Medilec Synergy, VIASYS, Madison, WI) at the AHT. Dogs with a b-wave amplitude below 40 mV were included. The b-wave amplitude of the mixed/rod-cone response was used at the RVC, and the bwave amplitude of a cone dominated ERG curve was assessed at the AHT and DWR. The cases with no ERG, but with suspected PRA, were included following careful selection based on their history, signalment, full ophthalmic examination, the presence of attenuated retinal vascularization, and tapetal hyper-reflectivity on funduscopy and if visual deficits in low light were reported. ECS with uni-or bilateral phacoemulsification were evaluated.
PRA的诊断或怀疑是根据患者的病史、信号和手术前或手术后的全面眼科检查做出的，在大多数情况下，ERG结果也支持这一诊断或怀疑。所有转诊中心都采用简短的 "是/否 "ERG方案来评估大体感光器功能。各中心采用的方案各不相同。表 1 显示了所使用的 ERG 方案摘要。在 AHT 和 DWR，ERG 是在意识清醒的狗身上进行的，在 RVC 则是在全身麻醉的情况下进行的。RVC 和 DWR 使用的 ERG 仪器是 HMsERG 系统（2000 型；OcuScience，Henderson，NV），AHT 使用的是光刺激器（SLE，CPS-20；Medilec Synergy，VIASYS，Madison，WI）。b 波振幅低于 40 mV 的狗也被包括在内。在 RVC 使用混合/杆锥反应的 b 波振幅，在 AHT 和 DWR 评估锥体主导 ERG 曲线的 b 波振幅。根据病史、信号、全面的眼科检查、是否存在衰减的视网膜血管、眼底检查是否存在视网膜高反射以及是否有弱光下视力障碍的报告，经过仔细筛选，将没有ERG但疑似PRA的病例纳入其中。对采用单侧或双侧超声乳化术的 ECS 进行了评估。
Visual outcome post-surgery was assessed in all ECS presented at re-examinations by ophthalmic examination, particularly the menace response, at seven time periods post-surgery ( P 1 = 25 − 90 P 1 = 25 − 90 P1=25-90\mathrm{P} 1=25-90 days, P 2 = 91 − 180 P 2 = 91 − 180 P2=91-180\mathrm{P} 2=91-180 days, P 3 = P 3 = P3=\mathrm{P} 3= 181 − 364 181 − 364 181-364181-364 days, P 4 = 365 − 549 P 4 = 365 − 549 P4=365-549\mathrm{P} 4=365-549 days, P 5 = 550 − 729 P 5 = 550 − 729 P5=550-729\mathrm{P} 5=550-729 days, P 6 = P 6 = P6=\mathrm{P} 6= 730-1094 days, and p7 ≥ 1095 ≥ 1095 >= 1095\geq 1095 days). Other methods of visual assessment (obstacle/maze tests, tracking response, and visual placing response) were also reported in a number of cases, but not consistently in all dogs. The results of genetic testing were reported if available.
在手术后的七个时间段（ P 1 = 25 − 90 P 1 = 25 − 90 P1=25-90\mathrm{P} 1=25-90 天、 P 2 = 91 − 180 P 2 = 91 − 180 P2=91-180\mathrm{P} 2=91-180 天、 P 3 = P 3 = P3=\mathrm{P} 3= 181 − 364 181 − 364 181-364181-364 天、 P 4 = 365 − 549 P 4 = 365 − 549 P4=365-549\mathrm{P} 4=365-549 天、 P 5 = 550 − 729 P 5 = 550 − 729 P5=550-729\mathrm{P} 5=550-729 天、 P 6 = P 6 = P6=\mathrm{P} 6= 730-1094天和p7 ≥ 1095 ≥ 1095 >= 1095\geq 1095 天），通过眼科检查，特别是威胁反应，对所有接受复查的 ECS 进行手术后视觉结果评估。一些病例中还报告了其他视觉评估方法（障碍/迷宫测试、追踪反应和视觉放置反应），但并非所有狗都采用了这些方法。如果有基因检测结果，也会报告。
TABLE 1 Summary of ERG protocols used at the RVC, AHT and DWR
表 1 英国皇家癌症研究中心、英国皇家高山医院和英国皇家西北地区医院使用的 ERG 协议摘要
Mcd s/m², millicandelas second/square meter; s, second; ms, millisecond; Hz, Herz.
Mcd s/m²，毫坎德拉秒/平方米；s，秒；ms，毫秒；Hz，赫兹。
Owners were invited to participate in a simple questionnaire by email, letter, or telephone call, asking:
我们通过电子邮件、信件或电话邀请业主参与一份简单的问卷调查，内容包括
  1. Is your pet still visual or how long has he/she been visual in your opinion?
    在您看来，您的宠物还能看见东西吗？
  2. Do you feel that cataract surgery has improved your pet’s quality of life?
    您觉得白内障手术提高了宠物的生活质量吗？
Frequencies and percentages were reported for the categorical variables: gender, operated eye, menace response per eye, ERG, the presence of a flat trace, and postoperative complications. The RVC databank RxWorks 5.2.4195 was searched to investigate the frequency of ECS presented to the RVC in general and to the ophthalmology department between 2002 and 2017. Medians (minimum, maximum) were reported for numerical variables like age and ERG b-wave amplitudes per eye. McNemar’s tests were performed to compare visual outcome before and after surgery. Generalized estimating equations (GEE) with binomial logit link function were used to assess association between age,
报告了以下分类变量的频数和百分比：性别、手术眼、每只眼的威胁反应、ERG、是否存在平迹以及术后并发症。为了调查2002年至2017年期间向皇家眼科中心和眼科部门报告的ECS频率，我们搜索了皇家眼科中心数据库RxWorks 5.2.4195。报告了每只眼睛的年龄和ERG b波振幅等数字变量的中位数（最小值、最大值）。为比较手术前后的视觉效果，进行了 McNemar 检验。使用带有二叉对数链接函数的广义估计方程（GEE）来评估年龄与ERG b波振幅之间的关系、
gender, center, the presence of a dazzle reflex, cataract grade, abnormalities on gonioscopy or ocular ultrasound, the presence of vision before surgery, or a flat trace on ERG with the postoperative visual outcome. Odds ratio (OR) and 95 % 95 % 95%95 \% confidence intervals (CI) are presented for results of the generalized estimating equation. Statistical significance was set at P < 0.05 P < 0.05 P < 0.05P<0.05. All analyses were performed with IBM SPSS Statistics (Version 24; IBM Corp., Armonk, NY). Graphic illustrations were created with GraphPad Prism (Version 7.00 for Windows, GraphPad Software, La Jolla, CA) and R (Version 3.4.2, R Foundation for Statistical Computing, Vienna, Austria).
性别、中心、有无眩晕反射、白内障等级、眼底镜检查或眼部超声波检查有无异常、术前有无视力或 ERG 平扫与术后视力结果的关系。概括估计方程的结果显示了比值比（OR）和 95 % 95 % 95%95 \% 置信区间（CI）。统计显著性设定为 P < 0.05 P < 0.05 P < 0.05P<0.05 。所有分析均使用 IBM SPSS 统计软件（第 24 版；IBM 公司，纽约州阿蒙克市）进行。图表使用 GraphPad Prism（Windows 7.00 版，GraphPad Software，La Jolla，CA）和 R（3.4.2 版，R Foundation for Statistical Computing，Vienna，Austria）制作。

3 | RESULTS 3 结果

There were 54 ECS included in this study (RVC 14 cases, AHT 32 cases, and DWR 8 cases), comprising 28 (51.9%) males and 26 ( 48.1 % 48.1 % 48.1%48.1 \% ) females. Phacoemulsification was performed in 85 of 108 eyes, comprising 41 right eyes (48.2%)
本研究共纳入 54 例 ECS（RVC 14 例、AHT 32 例和 DWR 8 例），其中男性 28 例（51.9%），女性 26 例（ 48.1 % 48.1 % 48.1%48.1 \% ）。108 只眼睛中有 85 只进行了乳化手术，其中 41 只为右眼（48.2%）。
and 44 left eyes (51.8%). Bilateral phacoemulsification was performed in 31 dogs (57.4%) and unilateral in 23 dogs (42.6%). Seventy-three (85.9%) intraocular lenses (IOL) were placed. Phacoemulsification was performed on separate days in 8 / 54 8 / 54 8//548 / 54 dogs ( 14.8 % 14.8 % 14.8%14.8 \% ) and on the same day in 46 / 54 46 / 54 46//5446 / 54 dogs ( 85.2 % 85.2 % 85.2%85.2 \% ). The median age at surgery was 9.09 years (Min. 2.17 years, Max. 13.49 years).
其中 31 只狗（57.4%）进行了双侧乳化手术，23 只狗（42.6%）进行了单侧乳化手术。31只狗（57.4%）进行了双侧乳化手术，23只狗（42.6%）进行了单侧乳化手术。安置了 73 个（85.9%）眼内人工晶体 (IOL)。 8 / 54 8 / 54 8//548 / 54 犬（ 14.8 % 14.8 % 14.8%14.8 \% ）的超声乳化手术在不同的日子进行， 46 / 54 46 / 54 46//5446 / 54 犬（ 85.2 % 85.2 % 85.2%85.2 \% ）的超声乳化手术在同一天进行。手术时的中位年龄为 9.09 岁（最小 2.17 岁，最大 13.49 岁）。
The ECS was the fourth most common breed (4% of the total population), presented to the RVC between 2002 and 2017 and the second most common breed ( 7 % 7 % 7%7 \% of the total population) presented to the ophthalmology department of the RVC during the same time period. Funduscopy supported the suspicion of PRA in all operated eyes either before surgery (4/85, 4.7%) or at re-examinations (81/85, 95.3%) following surgery. Funduscopic details like tapetal hyper-reflectivity (78/85, 91.8%), attenuated retinal vascularization (67/85, 78.8 % 78.8 % 78.8%78.8 \% ), and a pale or atrophied optic nerve head (11/85, 12.9 % 12.9 % 12.9%12.9 \% ) were described in most patient records. Clinicians have used the general term progressive retinal atrophy to describe funduscopic findings in all cases.
2002年至2017年期间，ECS是RVC最常见的第四大犬种（占总人口的4%），也是同期RVC眼科最常见的第二大犬种（占总人口的 7 % 7 % 7%7 \% ）。眼底检查结果显示，所有接受手术的眼睛在术前（4/85，4.7%）或术后复查时（81/85，95.3%）均怀疑患有 PRA。大多数患者的病历中都描述了眼底细节，如视网膜反射过强（78/85，91.8%）、视网膜血管减弱（67/85， 78.8 % 78.8 % 78.8%78.8 \% ）、视神经头苍白或萎缩（11/85， 12.9 % 12.9 % 12.9%12.9 \% ）。临床医生使用进行性视网膜萎缩这一通用术语来描述所有病例的眼底检查结果。
An ERG was performed in 75/85 (88.2%) operated eyes. All ERGs were consistent with reduced retinal function, and the median ERG b-wave amplitude was 10 mV (Min. 0 mV , max 40 mV max 40 mV max 40mV\max 40 \mathrm{mV} ) in all eyes. A flat ERG trace was found in 30 (40%) of the operated eyes. One dog was tested positive for the prcd gene mutation (Optigen, Ithaka, NY). Ten eyes of eight patients did not undergo an ERG, all of which demonstrated tapetal hyper-reflectivity, attenuated retinal vessels on funduscopy, and all of these patients were nyctalopic.
75/85（88.2%）只进行了ERG检查。所有ERG均显示视网膜功能减退，所有眼睛的ERG b波振幅中位数为10 mV（最小值为0 mV， max 40 mV max 40 mV max 40mV\max 40 \mathrm{mV} ）。30只（40%）手术眼的ERG轨迹平坦。一只狗的prcd基因突变检测呈阳性（Optigen，Ithaka，NY）。八名患者的十只眼睛没有进行ERG检查，所有这些眼睛都表现出视网膜反射过强，眼底检查显示视网膜血管变细，而且所有这些患者都有夜盲症。
A concurrent diagnosis of diabetes mellitus was not reported in any dog. Eight dogs had been diagnosed with keratoconjunctivitis sicca (KCS, 14.8%) at the time of the first examination.
没有任何一只狗同时被诊断患有糖尿病。首次检查时，有八只狗被诊断患有角结膜炎（KCS，14.8%）。
Cataracts were described as incipient ( 1 / 85 , 1.2 % 1 / 85 , 1.2 % 1//85,1.2%1 / 85,1.2 \% ), immature ( 40 / 85 , 47.1 % 40 / 85 , 47.1 % 40//85,47.1%40 / 85,47.1 \% ), mature ( 38 , 44.7 % 38 , 44.7 % 38,44.7%38,44.7 \% ), and hypermature ( 6 / 85 , 7.1 % 6 / 85 , 7.1 % 6//85,7.1%6 / 85,7.1 \% ). The cataract stage was significantly associated
白内障分为初期（ 1 / 85 , 1.2 % 1 / 85 , 1.2 % 1//85,1.2%1 / 85,1.2 \% ）、未成熟（ 40 / 85 , 47.1 % 40 / 85 , 47.1 % 40//85,47.1%40 / 85,47.1 \% ）、成熟（ 38 , 44.7 % 38 , 44.7 % 38,44.7%38,44.7 \% ）和超成熟（ 6 / 85 , 7.1 % 6 / 85 , 7.1 % 6//85,7.1%6 / 85,7.1 \% ）。白内障阶段与
with blindness before the surgery ( P = 0.004 ) ( P = 0.004 ) (P=0.004)(P=0.004). Following the surgery, there was no association between previous cataract grade and visual outcome. There were statistically significant associations at P4 ( P = 0.003 ) ( P = 0.003 ) (P=0.003)(P=0.003) and P5 ( P = 0.029 ) ( P = 0.029 ) (P=0.029)(P=0.029). However, these were considered questionable, due to the loss to follow up, as there were only 1 and 3 blind patients that presented for each period. A higher number of re-examined patients would be required to avoid bias. Gonioscopy was performed in 27 (25%) of 108 eyes in total with 16 (59.2%) abnormal findings of the iridocorneal angle (ICA). There were descriptions of seven narrow ICAs (7/27, 25.9%), six eyes with narrow ICAs alongside pectinate ligament dysplasia (PLD) (6/27, 22.2%), three eyes with PLD only (3/27, 11.1%), and 11 normal findings ( 11 / 27 , 40.7 % 11 / 27 , 40.7 % 11//27,40.7%11 / 27,40.7 \% ). An abnormal finding on gonioscopy did not affect the visual outcome of operated eyes in this study statistically, and none of these cases developed glaucoma following surgery ( P < 0.001 ) ( P < 0.001 ) (P < 0.001)(P<0.001). Ocular ultrasound was performed in 93 ( 86.1 % ) 93 ( 86.1 % ) 93(86.1%)93(86.1 \%) of 108 eyes and abnormalities were reported in 24 ( 22.2 % ) 24 ( 22.2 % ) 24(22.2%)24(22.2 \%) eyes. The most frequent finding was vitreal degeneration ( n = 22 , 20.3 % n = 22 , 20.3 % n=22,20.3%\mathrm{n}=22,20.3 \% ). There was a single case of lenticonus and one suspected persistent tunica vasculosa lentis, which was not confirmed following surgery. There were no cases of retinal detachment.
( P = 0.004 ) ( P = 0.004 ) (P=0.004)(P=0.004) 。手术后，先前的白内障等级与视力结果之间没有关联。在P4 ( P = 0.003 ) ( P = 0.003 ) (P=0.003)(P=0.003) 和P5 ( P = 0.029 ) ( P = 0.029 ) (P=0.029)(P=0.029) 阶段，两者之间存在统计学意义上的显著关联。 然而，由于每个阶段仅有1名和3名失明患者接受了随访，这些关联被认为是值得怀疑的。为避免偏差，需要对更多患者进行复查。在 108 只眼睛中，有 27 只（25%）进行了眼底镜检查，其中有 16 只（59.2%）发现虹膜角膜（ICA）异常。其中有 7 只眼睛的虹膜角膜狭窄（7/27，25.9%），6 只眼睛的虹膜角膜狭窄同时伴有栉状韧带发育不良（PLD）（6/27，22.2%），3 只眼睛的栉状韧带发育不良（PLD）（3/27，11.1%），11 只眼睛的检查结果正常（ 11 / 27 , 40.7 % 11 / 27 , 40.7 % 11//27,40.7%11 / 27,40.7 \% ）。据统计，在本研究中，眼底镜检查的异常发现并不影响手术眼的视力结果，这些病例中没有一例在术后发展为青光眼 ( P < 0.001 ) ( P < 0.001 ) (P < 0.001)(P<0.001) 。108只眼睛中的 93 ( 86.1 % ) 93 ( 86.1 % ) 93(86.1%)93(86.1 \%) 只进行了眼部超声波检查， 24 ( 22.2 % ) 24 ( 22.2 % ) 24(22.2%)24(22.2 \%) 只报告了异常情况。最常见的发现是玻璃体变性（ n = 22 , 20.3 % n = 22 , 20.3 % n=22,20.3%\mathrm{n}=22,20.3 \% ）。有一例光斑和一例疑似持续性静脉曲张光斑，但手术后未得到证实。没有视网膜脱离病例。
Before surgery, 19 (22.4%) of the operated eyes demonstrated a positive menace response and 66 (77.6%) eyes had a negative response. However, significantly more eyes had a positive menace response post operatively from re-examination period P1 until and including P5 ( P ≤ 0.003 P ≤ 0.003 P <= 0.003P \leq 0.003 ), compared to the menace response before surgery. See Table 2/Figures 1 and 2.
手术前，19 只眼睛（22.4%）的威胁反应为阳性，66 只眼睛（77.6%）的威胁反应为阴性。然而，与手术前的威胁反应相比，手术后从复查期 P1 开始到 P5（包括 P5）期间（ P ≤ 0.003 P ≤ 0.003 P <= 0.003P \leq 0.003 ）出现阳性威胁反应的眼睛明显更多。见表 2/图 1 和 2。
Thirty eyes (40%) undergoing cataract surgery demonstrated a flat trace on ERG. Before surgery, five (16.7%) of these eyes had a positive menace response and 25 eyes (83.3%) had a negative menace response. Of the five eyes with flat trace readings and positive menace responses, two ERGs were measured consciously, and three ERGs were measured under general anesthesia. Despite the flat ERG traces in
接受白内障手术的 30 只眼睛（40%）在 ERG 上显示出平坦的轨迹。手术前，其中 5 只眼睛（16.7%）的威胁反应为阳性，25 只眼睛（83.3%）的威胁反应为阴性。在这五只读数平坦且威胁反应呈阳性的眼睛中，有两只眼睛的ERG是在有意识的情况下测量的，有三只眼睛的ERG是在全身麻醉的情况下测量的。尽管
TABLE 2 Summary of visual outcome per eye before and after surgery and significance of visual improvement compared to before surgery
表 2 手术前后每只眼睛的视力结果摘要以及与手术前相比视力改善的意义
Time 时间 All eyes 所有的眼睛 McNemar P  McNemar  P (" McNemar ")/(P)\frac{\text { McNemar }}{P}
n Visual 视觉 Percent (%) 百分比 Blind 盲人 Percent (%) 百分比 Missing 失踪
Before surgery 手术前 85 19 22.4 66 77.6
P1* 85 75 88.2 10 11.8 0.000
P2* 63 58 92.1 5 7.9 22 0.000
P3* 46 44 96.7 2 4.3 39 0.000
P4* 32 31 96.9 1 3.1 53 0.000
P5* 19 16 84.2 3 15.8 66 0.003
P6 15 9 60.0 6 40.0 70 0.289
P7 10 6 60.0 4 40.0 75 0.453
Time All eyes (" McNemar ")/(P) n Visual Percent (%) Blind Percent (%) Missing Before surgery 85 19 22.4 66 77.6 P1* 85 75 88.2 10 11.8 0.000 P2* 63 58 92.1 5 7.9 22 0.000 P3* 46 44 96.7 2 4.3 39 0.000 P4* 32 31 96.9 1 3.1 53 0.000 P5* 19 16 84.2 3 15.8 66 0.003 P6 15 9 60.0 6 40.0 70 0.289 P7 10 6 60.0 4 40.0 75 0.453| Time | All eyes | | | | | | $\frac{\text { McNemar }}{P}$ | | :---: | :---: | :---: | :---: | :---: | :---: | :---: | :---: | | | n | Visual | Percent (%) | Blind | Percent (%) | Missing | | | Before surgery | 85 | 19 | 22.4 | 66 | 77.6 | | | | P1* | 85 | 75 | 88.2 | 10 | 11.8 | | 0.000 | | P2* | 63 | 58 | 92.1 | 5 | 7.9 | 22 | 0.000 | | P3* | 46 | 44 | 96.7 | 2 | 4.3 | 39 | 0.000 | | P4* | 32 | 31 | 96.9 | 1 | 3.1 | 53 | 0.000 | | P5* | 19 | 16 | 84.2 | 3 | 15.8 | 66 | 0.003 | | P6 | 15 | 9 | 60.0 | 6 | 40.0 | 70 | 0.289 | | P7 | 10 | 6 | 60.0 | 4 | 40.0 | 75 | 0.453 |
P , time period; P = P = P=P= significance level.
P ，时间段； P = P = P=P= 显著性水平。
30 eyes, there was significant improvement of vision from P1 to P4 ( P ≤ 0.031 P ≤ 0.031 P <= 0.031P \leq 0.031 ). See Table 3/Figure 3.
30只眼睛的视力从P1到P4都有明显改善（ P ≤ 0.031 P ≤ 0.031 P <= 0.031P \leq 0.031 ）。见表 3/图 3。
There were increased odds for vision if an eye underwent phacoemulsification compared to eyes not undergoing surgery at P 1 ( P < 0.001 , OR = 12.89 , CI = 4.33 , 38.8 ) P 1 ( P < 0.001 , OR = 12.89 , CI = 4.33 , 38.8 ) P1(P < 0.001,OR=12.89,CI=4.33,38.8)\mathrm{P} 1(P<0.001, \mathrm{OR}=12.89, \mathrm{CI}=4.33,38.8), P 2 ( P < 0.001 , OR = 23.70 , CI = 5.18 , 108.39 ) P 2 ( P < 0.001 , OR = 23.70 , CI = 5.18 , 108.39 ) P2(P < 0.001,OR=23.70,CI=5.18,108.39)\mathrm{P} 2(P<0.001, \mathrm{OR}=23.70, \mathrm{CI}=5.18,108.39), and P 3 ( P < 0.001 , OR = 157.55 , CI = 17.34 , 1431.43 ) ( P < 0.001 , OR = 157.55 , CI = 17.34 , 1431.43 ) (P < 0.001,OR=157.55,CI=17.34,1431.43)(P<0.001, \mathrm{OR}=157.55, \mathrm{CI}=17.34,1431.43). The GEE could not be performed for P4, P5, P6, and P7 as there were zero visual eyes in the group that had not undergone surgery. Abnormalities on ocular ultrasound did not have any statistical effect on the presence of a flat line on ERG or on the visual outcome of operated eyes in this study. The presence of a dazzle reflex before surgery did not have a significant effect on vision post-surgery. The presence or absence of an IOL did not have an effect on the presence of vision statistically. There was no significant effect of referral center, age, gender, or vision before surgery on visual outcome.
在 P 1 ( P < 0.001 , OR = 12.89 , CI = 4.33 , 38.8 ) P 1 ( P < 0.001 , OR = 12.89 , CI = 4.33 , 38.8 ) P1(P < 0.001,OR=12.89,CI=4.33,38.8)\mathrm{P} 1(P<0.001, \mathrm{OR}=12.89, \mathrm{CI}=4.33,38.8) 、 P 2 ( P < 0.001 , OR = 23.70 , CI = 5.18 , 108.39 ) P 2 ( P < 0.001 , OR = 23.70 , CI = 5.18 , 108.39 ) P2(P < 0.001,OR=23.70,CI=5.18,108.39)\mathrm{P} 2(P<0.001, \mathrm{OR}=23.70, \mathrm{CI}=5.18,108.39) 和P 3 ( P < 0.001 , OR = 157.55 , CI = 17.34 , 1431.43 ) ( P < 0.001 , OR = 157.55 , CI = 17.34 , 1431.43 ) (P < 0.001,OR=157.55,CI=17.34,1431.43)(P<0.001, \mathrm{OR}=157.55, \mathrm{CI}=17.34,1431.43) 时，与未接受手术的眼睛相比，接受超声乳化术的眼睛视力的几率增加。由于 P4、P5、P6 和 P7 组中未接受手术的视力为零，因此无法进行 GEE。在本研究中，眼部超声检查异常对 ERG 平线的出现或手术眼的视觉结果没有任何统计学影响。手术前是否出现眩光反射对手术后的视力没有明显影响。据统计，有无人工晶体对视力没有影响。转诊中心、年龄、性别或术前视力对视力结果没有明显影响。
Of all 85 eyes operated, 39 ( 45.9 % 45.9 % 45.9%45.9 \% ) presented with complications throughout the re-examination time periods. Complications included KCS ( n = 17 , 20.0 % n = 17 , 20.0 % n=17,20.0%\mathrm{n}=17,20.0 \%, not including previously diagnosed patients), glaucoma ( n = 11 , 12.9 % n = 11 , 12.9 % n=11,12.9%\mathrm{n}=11,12.9 \% ), corneal ulceration ( n = 6 , 7.1 % n = 6 , 7.1 % n=6,7.1%n=6,7.1 \% ), mineral or lipid deposits in the cornea ( n = 3 , 3.5 % n = 3 , 3.5 % n=3,3.5%\mathrm{n}=3,3.5 \% ), corneal endothelial disease ( n = 4 n = 4 n=4\mathrm{n}=4, 4.7 % 4.7 % 4.7%4.7 \% ), endophthalmitis ( n = 3 , 3.5 % n = 3 , 3.5 % n=3,3.5%\mathrm{n}=3,3.5 \% ), and intraocular artificial lens luxation ( n = 1 , 1.2 % n = 1 , 1.2 % n=1,1.2%\mathrm{n}=1,1.2 \% ). Four eyes of three dogs were enucleated due to secondary glaucoma. One eye was removed at day one following surgery; however, glaucoma was present in this eye before surgery. Two eyes of the same dog (only the left eye was operated) were enucleated 2.5 years and one eye 3.5 years following surgery. See Figure 4
在所有接受手术的 85 只眼睛中，有 39 只（ 45.9 % 45.9 % 45.9%45.9 \% ）在复查期间出现并发症。并发症包括KCS（ n = 17 , 20.0 % n = 17 , 20.0 % n=17,20.0%\mathrm{n}=17,20.0 \% ，不包括以前确诊的患者）、青光眼（ n = 11 , 12.9 % n = 11 , 12.9 % n=11,12.9%\mathrm{n}=11,12.9 \% ）、角膜溃疡（ n = 6 , 7.1 % n = 6 , 7.1 % n=6,7.1%n=6,7.1 \% ）、角膜矿物质或脂质沉积（ n = 3 , 3.5 % n = 3 , 3.5 % n=3,3.5%\mathrm{n}=3,3.5 \% ）、角膜内皮疾病（ n = 4 n = 4 n=4\mathrm{n}=4 、 4.7 % 4.7 % 4.7%4.7 \% ）、眼内炎（ n = 3 , 3.5 % n = 3 , 3.5 % n=3,3.5%\mathrm{n}=3,3.5 \% ）和眼内人工晶状体脱落（ n = 1 , 1.2 % n = 1 , 1.2 % n=1,1.2%\mathrm{n}=1,1.2 \% ）。三只狗的四只眼睛因继发性青光眼而被摘除眼球。其中一只眼睛在手术后第一天被摘除，但这只眼睛在手术前就患有青光眼。同一只狗的两只眼睛（仅左眼接受了手术）分别在术后 2.5 年和 3.5 年被摘除眼球。见图 4
Twenty-seven owners replied to the brief questionnaire (27/56, 48.2 % 48.2 % 48.2%48.2 \% reply rate). Most owners felt positive about the surgery and reported that the quality of life of their pet had improved ( 25 / 27 25 / 27 25//2725 / 27 replies, 92.5 % 92.5 % 92.5%92.5 \% ). The question for vision was not answered uniformly with yes or no, and some patients were deceased; therefore, this question was excluded from the results.
27 位主人回复了简短的问卷（27/56， 48.2 % 48.2 % 48.2%48.2 \% 回复率）。大多数主人对手术持肯定态度，并表示宠物的生活质量得到了改善（ 25 / 27 25 / 27 25//2725 / 27 回答， 92.5 % 92.5 % 92.5%92.5 \% ）。关于视力的问题，回答 "是 "或 "否 "的人并不一致，而且有些患者已经去世；因此，结果中没有包括这个问题。

4 | DISCUSSION 4 | 讨论

Historically, due to the inevitable progressive loss of vision, reports that cataracts develop in the late stages of PRA and that phacoemulsification does not benefit patients with the underlying PRA, surgery has not been recommended routinely. 11 , 14 , 15 11 , 14 , 15 ^(11,14,15){ }^{11,14,15} The risks and complications of the surgery always need to be outweighed by the advantages, which could be improved vision and overall ocular health. Cataracts are not only an opacity leading to blindness, but may lead to lensinduced uveitis, lens luxation, or glaucoma. 1 − 3 1 − 3 ^(1-3){ }^{1-3} Therefore, in a study by Lim et al it was discussed that phacoemulsification could be performed to decrease risks of ocular disease secondary to the cataracts. 3 3 ^(3){ }^{3} In patients with PRA, it is expected
从历史上看，由于视力不可避免地会逐渐下降，有报告称白内障发生在 PRA 的晚期，而乳化手术对患有潜在 PRA 的患者并无益处，因此不建议常规进行手术。 11 , 14 , 15 11 , 14 , 15 ^(11,14,15){ }^{11,14,15} 手术的风险和并发症总是要大于手术的好处，手术的好处可能是改善视力和眼部的整体健康。白内障不仅是导致失明的翳膜，还可能导致晶状体诱发葡萄膜炎、晶状体脱位或青光眼。 1 − 3 1 − 3 ^(1-3){ }^{1-3} 因此，Lim 等人在一项研究中讨论说，可以进行超声乳化术来降低继发于白内障的眼部疾病的风险。 3 3 ^(3){ }^{3} 在 PRA 患者中，预计
Visual eyes vs. blind eyes (all operated eyes)
视力正常的眼睛与失明的眼睛（所有手术过的眼睛）
Time periods 时间段
FIGURE 1 Summary of visual and blind eyes before and after surgery. Missing eyes were lost to follow up. Significant improvement of visual outcome was marked with *
图 1 手术前后视力和失明眼睛的汇总。缺失的眼睛为失去随访的眼睛。视觉效果的显著改善以 * 标记。
FIGURE 2 Operated vs not operated eyes. One box represents the visual outcome of one eye per exam period. Development of an eye can be followed from left to right. Black boxes stand for blind eyes, grey boxes for visual eyes, white boxes stand for loss to follow up or menace response not specified
图 2 手术眼与未手术眼。一个方框代表一只眼睛每次检查的视觉结果。可从左到右追踪一只眼睛的发育情况。黑框代表盲眼，灰框代表视力正常的眼睛，白框代表失去随访或未说明威胁反应
that vision will be gradually lost, even after phacoemulsification of their secondary cataracts. However, there are breedrelated differences in the onset and progression of PRA. It has been reported that ECS are affected by a relatively late onset and slowly progressive form of PRA, as demonstrated by late changes on funduscopy, areas of delayed retinal degeneration on histology and delayed loss of the b-wave function on ERG in comparison to other breeds. 17 , 19 17 , 19 ^(17,19){ }^{17,19} There is a relatively
即使对继发性白内障进行了乳化手术，视力也会逐渐丧失。然而，在 PRA 的发病和发展过程中，存在着品种间的差异。据报道，与其他犬种相比，ECS 患 PRA 的发病时间相对较晚，进展缓慢，表现为眼底检查的晚期变化、组织学上的延迟视网膜变性区域以及 ERG 上 b 波功能的延迟丧失。 17 , 19 17 , 19 ^(17,19){ }^{17,19} 与其他犬种相比，PRA 的病程相对较长。
TABLE 3 Summary of visual outcome following surgery, of eyes that had a flat ERG trace before surgery and significance of visual improvement compared to before surgery
表 3 手术后视力结果摘要、术前 ERG 迹线平坦的眼睛以及与手术前相比视力改善的意义
Time 时间 Flat ERG before surgery
术前 ERG 平坦		 McNemar P  McNemar  P (" McNemar ")/(P)\frac{\text { McNemar }}{P}
n Visual 视觉 Percent (%) 百分比 Blind 盲人 Percent (%) 百分比 Missing 失踪
Before surgery 手术前 30 5 16.7 25 83.3
P1* 30 22 73.3 8 26.7 0.000
P2* 21 17 81.0 4 19.0 9 0.000
P3* 10 8 80.0 2 6.7 20 0.031
P4* 8 7 87.5 1 12.5 22 0.031
P5 5 4 80.0 1 3.3 25 0.250
P6 4 2 50.0 2 50.0 26 1.000
P7 3 2 66.7 1 33.3 27 1.000
Time Flat ERG before surgery (" McNemar ")/(P) n Visual Percent (%) Blind Percent (%) Missing Before surgery 30 5 16.7 25 83.3 P1* 30 22 73.3 8 26.7 0.000 P2* 21 17 81.0 4 19.0 9 0.000 P3* 10 8 80.0 2 6.7 20 0.031 P4* 8 7 87.5 1 12.5 22 0.031 P5 5 4 80.0 1 3.3 25 0.250 P6 4 2 50.0 2 50.0 26 1.000 P7 3 2 66.7 1 33.3 27 1.000| Time | Flat ERG before surgery | | | | | | $\frac{\text { McNemar }}{P}$ | | :---: | :---: | :---: | :---: | :---: | :---: | :---: | :---: | | | n | Visual | Percent (%) | Blind | Percent (%) | Missing | | | Before surgery | 30 | 5 | 16.7 | 25 | 83.3 | | | | P1* | 30 | 22 | 73.3 | 8 | 26.7 | | 0.000 | | P2* | 21 | 17 | 81.0 | 4 | 19.0 | 9 | 0.000 | | P3* | 10 | 8 | 80.0 | 2 | 6.7 | 20 | 0.031 | | P4* | 8 | 7 | 87.5 | 1 | 12.5 | 22 | 0.031 | | P5 | 5 | 4 | 80.0 | 1 | 3.3 | 25 | 0.250 | | P6 | 4 | 2 | 50.0 | 2 | 50.0 | 26 | 1.000 | | P7 | 3 | 2 | 66.7 | 1 | 33.3 | 27 | 1.000 |
P , time period; P P PP, significance level.
P ，时间段； P P PP ，显著性水平。

Visual eyes vs Blind eyes (flat ERG before surgery)
肉眼与盲眼（手术前 ERG 平坦）

FIGURE 3 Summary of visual outcome of eyes that had a flat ERG trace before surgery. Significant improvement of visual outcome was marked with *
图 3 手术前 ERG 迹线平坦的眼睛的视觉效果汇总。视觉效果的显著改善以 * 标记。
high prevalence of prod mutations in this breed, which is a late-onset form of PRA. 16 , 21 16 , 21 ^(16,21){ }^{16,21} In the present study, all of the dogs included were ECS which is a very popular breed in the United Kingdom and one of the most common dog breeds presented to the RVC during the period of the study. When counseling the owners, it was discussed that the visual outcome and how long the dog could remain visual post-surgery were unknown at the time. The decision to operate one or both eyes was based on the clinician’s recommendation and the owner’s decision.
该犬种的突变率很高，属于晚发型 PRA。 16 , 21 16 , 21 ^(16,21){ }^{16,21} 在本研究中，所有被纳入研究的犬只都是ECS犬，这是英国非常流行的犬种，也是研究期间在RVC就诊的最常见犬种之一。在向狗主人提供咨询时，我们讨论到，手术后的视觉效果以及狗的视力能维持多久都是未知数。单眼或双眼手术的决定取决于临床医生的建议和狗主人的决定。
In this study, six eyes regained and maintained vision after surgery for over three years. The improvement of vision was significant until P5, which was the time period between 1.5 and 2 years post-surgery (see Figures 1 and 2 ). Considering that dogs affected by PRA were not routinely operated in the past, the authors were encouraged that many dogs in this study benefitted from vision improvement for such a long time.
在这项研究中，有六只眼睛在手术后恢复并保持视力超过三年。在术后 1.5 年到 2 年之间的 P5 阶段，视力改善非常明显（见图 1 和图 2）。考虑到受 PRA 影响的狗过去并不经常接受手术，作者对本研究中许多狗在如此长的时间内视力改善感到鼓舞。
FIGURE 4 Summary of complications diagnosed at re-examinations at all time periods post-surgery
图 4 手术后各时间段复查时诊断出的并发症摘要
Several eyes with an initial flat trace did regain vision after surgery, as reported in the results, which was found significant from P1 to P4. However, these findings raise questions about the accuracy of the different ERG readings and subjectivity of the menace response for vision testing. The ERG readings were likely affected by positioning, state of consciousness, type of anesthesia, and severity of the cataracts and noise, making it challenging to distinguish between a reduced b-wave amplitude and a flat line. 22 , 23 22 , 23 ^(22,23){ }^{22,23} This is considered a limitation of this study, as it was performed retrospectively and at different centers with various ERG protocols and ERG machines and various states of consciousness, which need to be considered when comparing ERG results with each other as it may have affected the results. 24 24 ^(24){ }^{24} In order to assess the validity of the ERG result in eyes with reduced photoreceptor function, the ERG protocols require standardization in several aspects. Ideally, the same ERG machines and the same protocol should have been used. The recommended protocols for diagnosis of photoreceptor disorders imply that all ERGs include twenty minutes of dark adaption, testing of a mixed rod-cone response, testing of cone function after ten minutes of light adaption, and a flicker test. 25 , 26 25 , 26 ^(25,26){ }^{25,26} These protocols, together with a standardized approach to perform the ERG either sedated or anaesthetized, in the same room and with the same ERG machine, would improve the validity of the ERG results, to allow a more accurate investigation into the presence of a photoreceptor disorder. This was a clinical study. A suspicion of PRA was made based on the history, signalment, and full ophthalmic examination before or after surgery and, in the majority of cases, supported by the ERG results. In this study, the suspicion of PRA was further supported in one case by genetic testing. The cases without an ERG were included following careful selection based on their history, signalment, full ophthalmic examination, the presence of attenuated retinal vascularization, and tapetal hyper-reflectivity on funduscopy and if nyctalopia was reported. The ERGs were performed to add weight to the suspicion of PRA. Repeating ERGs at later stages as well as using the standardized protocol for diagnosis of photoreceptor disorders could have further supported the diagnosis of PRA and aided in the assessment of the progression of vision loss. However, this would have meant that the patient would require several anesthesias or sedations, which is not feasible in a clinical setting, it may elicit phototoxic effects on the diseased retina and, in the authors’ opinion, would not have been in the best interest of the patient.
如结果报告所述，几只最初视力平平的眼睛在术后确实恢复了视力，这一点在 P1 到 P4 阶段都很明显。然而，这些发现对不同ERG读数的准确性和视力测试中威胁反应的主观性提出了质疑。ERG读数很可能受到体位、意识状态、麻醉类型、白内障严重程度和噪音的影响，因此区分b波振幅减弱和平线具有挑战性。 22 , 23 22 , 23 ^(22,23){ }^{22,23} 这被认为是本研究的局限性，因为研究是回顾性的，而且是在不同的中心进行的，采用了不同的ERG方案和ERG机，意识状态也各不相同，在比较ERG结果时需要考虑到这一点，因为这可能会影响结果。 24 24 ^(24){ }^{24} 为了评估感光功能减退眼的ERG结果的有效性，ERG方案需要在几个方面实现标准化。理想情况下，应使用相同的 ERG 仪器和相同的方案。光感受器疾病诊断的推荐方案意味着所有 ERG 都包括二十分钟的暗适应、杆-锥混合反应测试、十分钟光适应后的锥体功能测试和闪烁测试。 25 , 26 25 , 26 ^(25,26){ }^{25,26} 这些规程，加上在同一房间、同一台ERG机上进行镇静或麻醉ERG的标准化方法，将提高ERG结果的有效性，从而更准确地调查是否存在感光障碍。这是一项临床研究。 根据病史、信号和手术前或手术后的全面眼科检查来怀疑 PRA，在大多数病例中，ERG 结果也支持这一怀疑。在本研究中，一个病例的基因检测结果进一步证实了对 PRA 的怀疑。根据病史、信号、全面的眼科检查、视网膜血管是否衰减、眼底检查是否出现视网膜反射过强以及是否有夜视的报告，经过仔细筛选后，将没有ERG的病例包括在内。进行ERG检查是为了加重对PRA的怀疑。在后期阶段重复ERG检查，并使用感光细胞疾病诊断的标准化方案，可以进一步支持PRA的诊断，并有助于评估视力丧失的进展情况。然而，这意味着患者需要多次麻醉或镇静，这在临床环境中是不可行的，而且可能会对病变视网膜产生光毒性影响，作者认为这不符合患者的最佳利益。
Many clients mentioned that the photopic vision had returned; however, these observations were not reported routinely for every case, and therefore, these results were not used to report the visual outcome post-surgery. For consistency, the visual outcome was reported based on the presence or absence of menace responses in
许多受试者提到光视视力已经恢复；但是，这些观察结果并不是每个病例都会常规报告的，因此，这些结果并不用于报告手术后的视觉结果。为了保持一致，视觉结果的报告是基于以下方面是否存在威胁反应
clinical examinations. However, the menace response is only a crude test for vision and cannot provide detailed information about the degree of photoreceptor degeneration. Furthermore, it would be interesting to analyze the effect of the phototoxic effect of the operating microscope light on retinas with PRA as well as safe exposure time. The use of an ultraviolet radiation filter or a yellow filter could be considered to reduce phototoxicity in patients with PRA; however, there is no strong evidence in the literature that this measure would decrease photoreceptor destruction during surgery in cases with PRA. 27 , 28 27 , 28 ^(27,28){ }^{27,28}
临床检查。然而，威胁反应只是一种粗略的视力测试，无法提供有关感光细胞变性程度的详细信息。此外，分析手术显微镜光线的光毒性对患有 PRA 的视网膜的影响以及安全照射时间也很有意义。可以考虑使用紫外线辐射滤光器或黄色滤光器来减少PRA患者的光毒性；但是，文献中并没有有力的证据表明这种措施会减少PRA病例在手术过程中对光感受器的破坏。 27 , 28 27 , 28 ^(27,28){ }^{27,28}
There was no statistical effect of the referral center, age, gender, abnormality on gonioscopy or ocular ultrasound, cataract stage, dazzle reflex, vision before surgery, or IOL placement on the visual outcome post-surgery as assessed by GEE. The association of funduscopic findings with visual outcome could not be evaluated statistically. The detailed description of findings on fundoscopy varied between clinicians and therefore funduscopic findings were described only. For the same reasons, it was not possible to establish a standardized approach to assess the progression of the degree of funduscopic changes and their association with the visual outcome in this retrospective study; however, this would be an interesting question for future studies. The use of diagnostic imaging like fundus photography or OCT could be considered for standardization of the findings and to assess for progression of the degree of retinal atrophy.
经 GEE 评估，转诊中心、年龄、性别、眼底镜检查或眼部超声波检查异常、白内障分期、眩晕反射、术前视力或人工晶体植入对术后视觉效果没有统计学影响。眼底检查结果与视力结果之间的关系无法进行统计学评估。临床医生对眼底镜检查结果的详细描述各不相同，因此仅对眼底镜检查结果进行了描述。出于同样的原因，在这项回顾性研究中，也无法建立一种标准化的方法来评估眼底病变程度的进展及其与视力结果的关系；不过，这将是今后研究中一个有趣的问题。为了使研究结果标准化，并评估视网膜萎缩程度的进展，可以考虑使用眼底照相或 OCT 等诊断成像技术。
In this study, owners were contacted and asked about the perceived quality of life of their dog after surgery. The response rate to the questionnaire was 48.2 % 48.2 % 48.2%48.2 \%. This lies just below the mean response rate for academic studies, which could be explained by the long study period and that some dogs were already deceased at the time of the questionnaire. 29 29 ^(29){ }^{29} We cannot base conclusions out of this low response rate. However, we would like to report that, of all responses, 92.5 % 92.5 % 92.5%92.5 \% owners replied that the quality of life of their dog had improved significantly after surgery.
在这项研究中，我们与狗的主人取得了联系，并询问了他们对狗手术后生活质量的看法。调查问卷的回复率为 48.2 % 48.2 % 48.2%48.2 \% 。这略低于学术研究的平均回复率，原因可能是研究时间较长，而且有些狗在接受问卷调查时已经去世。 29 29 ^(29){ }^{29} 我们不能根据这一低回复率得出结论。不过，我们想报告的是，在所有回复中， 92.5 % 92.5 % 92.5%92.5 \% 主人回答说他们的狗在手术后生活质量得到了显著改善。
There are further limitations to this study, due to its retrospective nature, which may have influenced the results. There was loss to follow up, which increased with each reexamination time period and as demonstrated in the tables. Due to the descriptive nature of this study, we decided to still report all long-term results, even though this holds a small potential for overreaching conclusions. Furthermore, we described the PRA diagnosis as “suspected,” as most cases were diagnosed by history, signalment, clinical examination, and short ERG, but were not confirmed by the recommended protocol for diagnosis of photoreceptor disorders, multiple ERGs, or gene tests in the majority of cases. To address this, we only included cases with a sufficient follow-up and repeatedly confirmed suspicion/diagnosis by diplomates or residents under supervision of diplomates of the ECVO.
由于这项研究具有回顾性，因此还存在一些局限性，这些局限性可能会影响研究结果。如表中所示，随着每个复查时间段的延长，随访损失也在增加。鉴于本研究的描述性特点，我们决定仍然报告所有的长期结果，尽管这有可能会得出过高的结论。此外，我们将 PRA 诊断描述为 "疑似"，因为大多数病例是通过病史、信号、临床检查和短时 ERG 诊断出来的，但大多数病例并没有通过光感受器疾病诊断推荐方案、多次 ERG 或基因测试来确诊。为了解决这个问题，我们只纳入了有足够随访时间，并由欧洲视光学学会文凭医生或在文凭医生指导下的住院医生反复确认怀疑/诊断的病例。
Finally, the quality of life questionnaire answered by clients was subjective and further studies to validate a quality of life tool for this purpose are required.
最后，服务对象回答的生活质量问卷是主观的，因此需要进一步研究，以验证用于这一目的的生活质量工具。

5 | CONCLUSION 5 结论

Phacoemulsification in ECS with suspected PRA and secondary cataract development can be recommended. Visual improvement can be obtained for some time, but as expected the day vision will be lost eventually. No predictor for a successful visual outcome following surgery could be identified. However, vision was present for up to two years in this study population, and this was significant when comparing to vision before surgery. ERGs were useful in supporting the suspicion of PRA but no conclusion on visual outcome associated with ERG results could be drawn, as the ERGs were not standardized. The response rate of the questionnaire was low; however, most participants reported an improved quality of life of their dogs.
对于怀疑有 PRA 和继发性白内障的 ECS，可以建议进行超声乳化手术。视力可在一段时间内得到改善，但正如预期的那样，日间视力最终会丧失。目前还没有找到手术后视力成功的预测因素。不过，在这项研究的人群中，视力可维持两年之久，这与手术前的视力相比意义重大。ERGs有助于支持对PRA的怀疑，但由于ERGs没有标准化，因此无法得出与ERG结果相关的视觉结果结论。调查问卷的回复率很低；不过，大多数参与者都表示他们的狗的生活质量得到了改善。

ACKNOWLEDGMENT 致谢

The leading authors would like to thank their mentors, Jane Sansom, David Donaldson, and Claudia Hartley for laying the foundation for this study and always looking beyond conventions.
主要作者要感谢他们的导师简-桑瑟姆、戴维-唐纳森和克劳迪娅-哈特利，感谢他们为本研究奠定了基础，并始终不墨守成规。

ORCID

Charlotte Dawson (iD https://orcid. org/0000-0001-9974-1244
Charlotte Dawson（iD https://orcid. org/0000-0001-9974-1244

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How to cite this article: Koll-Hampp S, Enache A-E, Fenollosa-Romero E, et al. Visual outcome following phacoemulsification in English Cocker Spaniels with suspected progressive retinal atrophy: A retrospective multicenter study of 54 cases (2002-2017). Vet Ophthalmol. 2019;22:591-599. https://doi.org/10.1111/ vop. 12627
本文引用方式Koll-Hampp S, Enache A-E, Fenollosa-Romero E, et al. 疑似进行性视网膜萎缩的英国可卡犬接受超声乳化术后的视觉效果：对 54 例病例的多中心回顾性研究（2002-2017 年）。Vet Ophthalmol.2019;22:591-599. https://doi.org/10.1111/ vop.12627