Long-term outcome of sudden acquired retinal degeneration syndrome in dogs

Jane A. Stuckey Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Jacqueline W. Pearce Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211.

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Elizabeth A. Giuliano Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211.

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Leah A. Cohn Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211.

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Ellison Bentley Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Amy J. Rankin Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Margi A. Gilmour Department of Veterinary Clinical Sciences, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

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Christine C. Lim Department of Veterinary Clinical Sciences, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108.

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Rachel A. Allbaugh Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506.

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Cecil P. Moore Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211.

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Richard W. Madsen Department of Biostatistics, School of Medicine, University of Missouri, Columbia, MO 65211.

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Abstract

Objective—To investigate long-term outcomes and owner-perceived quality of life associated with sudden acquired retinal degeneration syndrome (SARDS) in dogs.

Design—Survey study.

Animals—100 dogs with SARDS examined at 5 academic veterinary institutions from 2005 to 2010.

Procedures—The diagnosis was based on documented acute vision loss, normal results of ophthalmic examinations, and evaluation of extinguished bright-flash electroretinograms. Primary owners of affected dogs completed a questionnaire addressing outcome measures including vision, systemic signs, and perceived quality of life for their dogs.

Results—Age at diagnosis was significantly correlated with positive outcome measures; dogs in which SARDS was diagnosed at a younger age were more likely to have alleged partial vision and higher owner-perceived quality of life. Polyphagia was the only associated systemic sign found to increase in severity over time. Medical treatment was attempted in 22% of dogs; visual improvement was not detected in any. Thirty-seven percent of respondents reported an improved relationship with their dog after diagnosis, and 95% indicated they would discourage euthanasia of dogs with SARDS.

Conclusions and Clinical Relevance—Blindness and concurrent systemic signs associated with SARDS appeared to persist indefinitely, but only polyphagia increased in severity over time. Most owners believed their pets had good quality of life and would discourage euthanasia of dogs with SARDS.

Abstract

Objective—To investigate long-term outcomes and owner-perceived quality of life associated with sudden acquired retinal degeneration syndrome (SARDS) in dogs.

Design—Survey study.

Animals—100 dogs with SARDS examined at 5 academic veterinary institutions from 2005 to 2010.

Procedures—The diagnosis was based on documented acute vision loss, normal results of ophthalmic examinations, and evaluation of extinguished bright-flash electroretinograms. Primary owners of affected dogs completed a questionnaire addressing outcome measures including vision, systemic signs, and perceived quality of life for their dogs.

Results—Age at diagnosis was significantly correlated with positive outcome measures; dogs in which SARDS was diagnosed at a younger age were more likely to have alleged partial vision and higher owner-perceived quality of life. Polyphagia was the only associated systemic sign found to increase in severity over time. Medical treatment was attempted in 22% of dogs; visual improvement was not detected in any. Thirty-seven percent of respondents reported an improved relationship with their dog after diagnosis, and 95% indicated they would discourage euthanasia of dogs with SARDS.

Conclusions and Clinical Relevance—Blindness and concurrent systemic signs associated with SARDS appeared to persist indefinitely, but only polyphagia increased in severity over time. Most owners believed their pets had good quality of life and would discourage euthanasia of dogs with SARDS.

Sudden acquired retinal degeneration syndrome is an acute retinal disorder of dogs characterized by sudden loss of vision in ophthalmoscopically normal eyes and is often associated with systemic signs and clinicopathologic laboratory abnormalities.1 It is diagnosed in affected dogs on the basis of clinical findings, including sudden vision loss, normal fundus appearance, and a nonrecordable electroretinogram.2 Despite considerable scientific investigation, the cause of this uncommon, permanently blinding disease is unknown and consistently successful treatments to reverse vision loss have not been identified.3–5

The syndrome has been well described in retrospective studies. Median age of affected dogs is 8.5 years, and females represent approximately 60% of dogs with SARDS.1 Dachshunds, Miniature Schnauzers, and mixed-breed dogs are consistently overrepresented.6 Up to 40% of dogs with SARDS have concurrent systemic signs, including polyuria, polydipsia, polyphagia, and weight gain; these signs may occur weeks to months before or soon after diagnosis.1,4 Similar systemic signs are often associated with hyperadrenocorticism; however, this endocrinopathy has been diagnosed in only a few dogs with SARDS.7 Serum biochemical abnormalities also resemble those of hyperadrenocorticism and may include hypercholesterolemia, high serum aspartate aminotransferase and alanine aminotransferase activities, and high serum activity of the corticosteroid-induced isoenzyme of alkaline phosphatase.5,6,8 A stress leukogram, thrombocytosis, isosthenuria, proteinuria, and systemic hypertension are inconsistently present.1,2

The pathogenesis of SARDS is poorly understood. Histologic evaluation of affected retinas reveals that rods and cones are equally affected by photoreceptor apoptosis with minimal inflammatory cell infiltrate.9 Conversely, a recent study8 that used optical coherence tomography revealed primary damage in the nerve fiber layer of the retina, suggesting a defect in the retinal ganglion cells and not the photoreceptors.8 Several studies evaluated SARDS as an autoimmune disorder and found inconsistent and controversial results. In 1988, 5 dogs with SARDS were identified as having serum antibodies against pooled bovine retinal antigen that were not detected in 3 healthy control dogs.10 More recently, Braus et al6 found that 6 of 24 dogs with SARDS had neuron-specific enolase autoantibodies, whereas none of the clinically normal control dogs had these specific autoantibodies. Improved navigation skills or rod-cone pupillary light reflex without return of a menace response following IV immunoglobulin administration in a small group of dogs with SARDS also supports an immune-mediated etiology.8,a However, evaluation of sera from dogs with SARDS was not suggestive of anti-retinal antibody formation in a study by Keller et al.11 Clinical signs in dogs with SARDS have some similarity to those in humans with cancer-associated retinopathy, an immune-mediated blinding disease. However, investigation of comparative pathogenesis between cancer-associated retinopathy and SARDS does not reveal a common etiology.12

Blindness from SARDS is considered permanent. The persistence of simultaneous systemic signs (polyuria, polydipsia, polyphagia, and weight gain) sometimes associated with SARDS has not been studied in a large population of affected dogs but may represent a larger and more difficult management issue than blindness itself. A pilot studyb of 15 dogs evaluated vision-loss adjustment, persistence of systemic signs, and concurrent medical conditions associated with SARDS. Most dog owners in that small studyb reported that their dogs adjusted well to vision loss, did not develop additional medical problems, and had no resolution of concurrent systemic signs associated with SARDS.

The objective of the study reported here was to investigate long-term outcomes in dogs affected by SARDS by means of an electronic questionnaire completed by primary owners.

Materials and Methods

Medical records from 2005 to 2010 at 5 veterinary teaching hospitals (Kansas State University, University of Missouri, Oklahoma State University, University of Wisconsin, and University of Minnesota) were searched. Dogs with a history of acute-onset blindness, absence of ophthalmic lesions consistent with the degree of vision loss, and a confirmed extinguished bright-flash electroretinogram were included as SARDS case animals.

One hundred twenty-three cases were identified. A survey consisting of 47 questions was used.c Medical records were cross-referenced whenever possible to confirm that data collected in the survey were accurate. Survey questions were designed to investigate signalment, the dogs’ current status (alive vs dead), euthanasia status if dead (vs other causes of death), and whether euthanasia was related to the SARDS diagnosis, owner-perceived quality of life for the dog, concurrent medical conditions, vision status, and concurrent systemic signs that have been reported to be associated with SARDS. Questions involved yes or no answers or scoring from 0 to 5 or contained specific lists for owners to choose from (additional diagnoses, drugs administered, or environmental changes enforced).

Statistical analysis—Statistical analysis was performed with software.d Considering that most variables were ordinal or categorical, nonparametric statistics were primarily used for analysis. Spearman correlation coefficients were used for data relating to polyuria, polydypsia, polyphagia, and weight gain. χ2 Analysis was used to examine the association between euthanasia and navigation ability. Comparisons relating to navigation ability as well as severity of systemic signs over time were analyzed with a Friedman test and a signed rank test, respectively. A Friedman test was also used to evaluate the behavioral scores. A Fisher exact test was used to investigate the relationship between quality of life and the decision to euthanize. A Spearman p test was used to assess the relationship between age and perceived quality of life. Associations with age at diagnosis were evaluated with the Wilcoxon rank sum test and the Kruskal-Wallis test. Significance was set at a value of P < 0.05.

Results

One hundred completed questionnaires corresponding to 100 dogs with SARDS were obtained for statistical analysis. Of these cases, 30 were diagnosed at Kansas State University, 29 at the University of Missouri, 18 at the University of Minnesota, 12 at Oklahoma State University, and 11 at the University of Wisconsin-Madison. At the time of survey completion, 46 dogs were alive and 54 were deceased. Of the 54 deceased dogs, 15 (27.8%) died and 39 (72.2%) had been euthanized. Approximately one-quarter (10/39 [25.6%]) of the dogs that were euthanized were euthanized because of SARDS. Females accounted for 60% of the population. Mean ± SD age at diagnosis was 8.2 ± 2.2 years, with a median of 8 years and a range of 4 to 16 years. The following breeds represented 5% or more of the sample population: mixed breed (n = 17), Dachshund (15), Miniature Schnauzer (9), Pug (7), Brittany Spaniel (6), Bichon Frise (5), and Maltese (5). No significant seasonal or monthly differences in numbers of dogs with SARDS were detected.

Most dogs had concurrent systemic signs associated with SARDS; these included polyuria (52%), polydipsia (58%), polyphagia (69%), and weight gain (75%). Forty-two percent of the study population had all 4 of these signs, whereas only 16% had no clinical signs other than blindness. Owners were asked to rate severity of clinical signs (0 to 5 scale) at the time of diagnosis of SARDS and at > 1 year following diagnosis. Eighty-three dogs were still alive at least 1 year following SARDS diagnosis. Polyphagia was the only clinical sign to have increased significantly (P = 0.047) over time. The severity scores for polyuria, polydipsia, and weight gain changed little from the time of diagnosis. Age at diagnosis was not related to systemic signs over time.

Thirty-four percent of the study population had no known medical conditions other than SARDS or the systemic signs often associated with SARDS. The remaining dogs had various comorbidities. Ten percent of the respondents reported recurrent hypersensitivity responses (environmental, vaccine, or food allergies). Endocrinopathies were commonly reported; hyperadrenocorticism had been diagnosed by a veterinarian in 10 dogs, hypothyroidism had been diagnosed in 8, and diabetes mellitus had been diagnosed in 4. Additional nonspecific comorbidities included some form of neoplasia (n = 6), kidney disease (5), and liver disease (3).

In this study, 78% of survey respondents did not pursue any form of treatment for their dog's blindness. Of the 22 dogs that were treated, corticosteroids were most frequently administered (n = 13). Nutritional supplements (n = 3), melatonin (2), and doxycycline (2) were also administered. None of the dog owners believed their dog had visual improvement with treatment.

Owners were asked to score each dog's behavior following the diagnosis of SARDS on a scale of 0 to 5, with 0 representing no change and 5 representing profound change (Figure 1). Following the diagnosis of SARDS, owners were significantly more likely to report that dogs were more cautious, played less, slept more, and seemed to have more signs of depression, compared with reporting that dogs were reclusive or seemed uncomfortable. Owners were even less likely to report aggression to strangers or family or increased play.

Figure 1—
Figure 1—

Mean ± SD scores (scale, 0 to 5) for various behaviors in dogs (n = 100) with SARDS reported by 100 owners on a survey questionnaire. a–cValues for behaviors with different letters are significantly (P < 0.05) different.

Citation: Journal of the American Veterinary Medical Association 243, 10; 10.2460/javma.243.10.1426

Despite these behavioral changes, 37% of owners reported that the relationship with their dog improved after SARDS diagnosis, and of that subset, 79% scored the improvement to be moderate to profound. Only 17% reported the relationship with their dog worsened following a diagnosis of SARDS. Eighty-seven percent of owners reported their dog to have moderate to excellent (3 to 5) scores for navigation ability in the house, and 81% reported similar scores for navigation ability in the yard. Only 41% of owners reported moderate to excellent scores for navigation ability in new surroundings. Mean scores for navigation ability were significantly better in the home than in the yard and significantly (P < 0.001) better in the home, compared with unfamiliar areas. Forty-eight percent of those surveyed did not make special provisions for their blind dog. Twenty-eight percent of owners provided baby gates to ensure pet safety, 11% built fences, 5% used restraints such as cages, and 4% built ramps to assist with stairs. Other creative strategies for improved navigation and accommodation were carpeting pathways to important locations (2%), use of auditory clues or scents to signify certain locations (2%), and teaching dogs verbal commands to alert them to changes in topography (3%).

Forty-five percent of owners reported their pets had partial vision at times. Dogs with owner-perceived partial vision had SARDS diagnosed at a younger age than those reported to have no owner-perceived evidence of partial vision (P = 0.007).

When owners were asked to rank quality of life on a scale of 1 (poor) to 5 (excellent), 76% of owners ranked quality of life of their dog as moderate to excellent (3 to 5 score). Only 9 dogs were deemed to have a poor quality of life. When owners were asked what factors had the most effect on quality of life, they indicated blindness (62%) and concurrent clinical signs (12%) had the most influence. Greater age (> 9 years) and low owner-perceived quality of life scores were associated, albeit not significantly (P = 0.052). When owners were asked what the most frustrating aspect of SARDS was, 69% said blindness, 8% said increased urination, 7% said increased appetite, and 6% said weight gain.

Owners of dogs with SARDS were asked whether they would encourage or discourage euthanasia if advising other owners of dogs with newly diagnosed SARDS. Ninety-five percent of owners indicated they would discourage euthanasia. Of the 10 owners who euthanized their dogs because of SARDS, only 2 recommended euthanasia of other dogs with SARDS. Of the 5 owners who encouraged euthanasia of other dogs with SARDS, only 2 euthanized their own dogs because of SARDS.

Discussion

Results of the present study suggested that dogs with SARDS were considered by their owners to have a good to excellent quality of life. Approximately half the dogs were deceased at the time of the survey. This may be a reflection of chronology of case selection or the fact that onset of SARDS occurred later in life. The small number of dogs (n = 10) euthanized because of SARDS suggested that the disease may have minimal effects on quality of life, assuming that quality of life is linked to euthanasia status.13 Middle-aged female dogs were overrepresented in our study population of dogs with SARDS, consistent with previous reports.2,b Breed data in this investigation were congruent with previous studies,2,12 which found mixed-breed dogs, Dachshunds, Miniature Schnauzers, Pugs, Brittany Spaniels, and Malteses to be predisposed. The present study also identified Bichon Frise as an at-risk breed, comprising 5% of the total population of evaluated dogs with SARDS. A regional influence on the Bichon Frise study population was not detected. Although a previous study5 identified a seasonal increase in incidence of SARDS, with up to 46% of SARDS cases diagnosed in December and January, our study failed to confirm this finding, with no appreciable link between season and incidence.

In the present study, concurrent systemic signs associated with SARDS were common, with polyuria, polydipsia, polyphagia, and weight gain found in > 50% of dogs. In previous retrospective studies,1,2 systemic signs were identified in 28% to 39% of dogs. The subset of dogs with SARDS without concurrent systemic signs (only 16% in our study) may represent a different disease process and warrants further study. Of the concurrent systemic signs, only the severity score of polyphagia increased significantly over time. Metabolic rate in dogs decreases with age; therefore, an increase of polyphagia over time is more likely associated with SARDS than aging.14 In addition, changes in metabolic rate relative to age are not likely to affect this finding because age at diagnosis was not significantly associated with any of the concurrent systemic signs over time. Dysregulation of melatonin concentrations has been associated with polyphagia in humans15,16 and could be a potential etiology of the increased polyphagia detected over time in dogs with SARDS. Ongoing hormonal changes or endocrinopathies could also play a role.1,17,18 Definitive etiologic determination for the increase in polyphagia of dogs with SARDS was beyond the scope of the study reported here, and despite owner reports of increased food consumption, owners did not report corresponding weight gain. Although a small case seriesb that described resolution of polyuria and polydipsia in 2 of 5 dogs with SARDS was published, these clinical signs remained static in the present study, which was larger.

It has been theorized that SARDS is a consequence of some systemic disease, but comorbid conditions were not identified in all of the dogs in this study. Hyperadrenocorticism, which has been described in a small proportion of dogs with SARDS, was reported in 10 dogs in the present survey population.6 Although nearly half (42%) of survey respondents stated that their dog had all 4 of the concurrent systemic signs commonly associated with hyperadrenocorticism, not all of the dogs were tested for hyperadrenocorticism. A recent study19 found that in dogs with pituitary-dependent hyperadrenocorticism, alterations in retinal blood flow and concentrations of cortisol, triglycerides, and glucose were greater in dogs with noncompressive (SARDS-like) blindness than in dogs without vision loss. Allergies were one of the most common concurrent medical conditions reported in the present study, as described elsewhere.a The prevalence of hypersensitivity among dogs with SARDS may have been a coincidence rather than a correlation; hypersensitivity reactions are extremely common in dogs.20 Similarly, other concurrent medical conditions found in this study (hypothyroidism, renal disease, diabetes mellitus, and liver disease) are relatively common in the geriatric dog population. Similarities have been described between cancer-associated retinopathy in humans and SARDS in dogs,12 although no studies have confirmed that these conditions are the same. Montgomery et al2 found the prevalence of cancer in dogs with SARDS to be 0.8%. The study reported here identified cancer in 6% of dogs with SARDS, but these cancers occurred at any time after diagnosis and not necessarily at the time of diagnosis. It is important to recall that cancer is reported to have a prevalence of 0.2% to 0.38% in the general population of dogs, and the prevalence increases with age.21 Because the dogs in the present study had a mean age of 8 years at the time of diagnosis, it is plausible that development of cancer was age related.

Only 20% of dogs in this study received treatment for SARDS; systemic administration of glucocorticoids was the most common treatment. Glucocorticoids administered for SARDS on a short-term basis are unlikely to affect the long-term concurrent systemic signs that were evaluated in this study. This study was not designed to evaluate treatment, and reevaluation was not consistently performed by an ophthalmologist following treatment. Owner-perceived vision improvement was not reported for any of the 32 dogs that received treatment in this study, which supported the lack of consistently successful treatment for SARDS in the current literature.2,6 Intravenous administration of immunoglobulin, if performed soon after loss of retinal function, has been reported to allow improved navigation ability in a few dogs but not restoration of the menace response.a None of the dogs in the present study were administered immunoglobulin IV.

Despite documented negative behavioral changes following vision loss (decreased play, increased hours slept, and signs of depression), few owners reported a diminished relationship with their pet. Approximately 40% reported improvement in the client-pet relationship, and almost 80% of these owners rated the improvement as moderate to profound. Blindness may require additional client-pet interaction; this may have resulted in improvement of the pet-owner relationship. Few owners perceived the additional husbandry associated with SARDS or the concurrent systemic signs as an obstacle in their relationship with their dog. Not surprisingly, dogs with SARDS navigated better in the house and yard, compared with unfamiliar environments. Approximately half of the owners did not make special provisions for their dogs, suggesting that a normal routine is still reasonable in the management of dogs with SARDS. Provisions used by some of the owners included baby gates, kennels, ramps to assist with stairs, carpeted pathways to important locations, auditory or scent clues, and teaching dogs verbal commands associated with topography. This provision list may be of assistance to veterinarians who may be asked to advise on aids for managing blind dogs.

Almost half of the dogs in the present study were reported by owners to have partial vision at times. It is widely reported that dogs with SARDS do not regain vision or any retinal function.2,4,9,22 Repeat examination and electrodiagnostic testing would be required to validate whether these patients regained retinal function or partial vision. We believe that behavior attributed to vision was observed after the dog acclimated to blindness and was guided by improvement in other senses. Blind rats have good performance in the reference memory version of the Morris water maze, a behavioral procedure widely used to study spatial learning and memory.23 Dogs with owner-perceived partial vision had disease diagnosed at a significantly younger age. Higher sensory ability, better cognitive function, or general energy levels in younger dogs may be reasons why dogs in which SARDS develops at a younger age were more likely to have owner-perceived partial vision over time.

Most owners reported moderate to excellent quality of life in dogs with SARDS. However, assessment of quality of life by owners and veterinarians is subjective and open to bias; a validated method of assessing quality of life in pets does not exist.13 The majority (62%) of owners indicated that blindness compromised quality of life the most for their pets; 69% of owners indicated it was the most frustrating aspect associated with SARDS. Some dogs with SARDS at an older age had a lower quality of life, although the difference was not significant. Such dogs are more likely to face age-related medical problems, reduced cognitive ability, and decreased sensory function, which may contribute to decreased quality of life.24,25 It was noteworthy that concurrent systemic signs (polyuria, polydipsia, polyphagia, and weight gain) were considered to be the most frustrating aspect of SARDS for only 6% to 8% of owners. These signs, particularly polyuria, may represent major management issues for owners.

Ninety-five percent of dog owners discouraged euthanasia for SARDS. This may be an indirect assessment of the dogs’ quality of life, considering that one would assume that dogs deemed to have acceptable quality of life would not be euthanized. Of the 10 owners who euthanized their dogs because of SARDS, only 2 recommended euthanasia of other dogs with SARDS, suggesting that most owners may have regretted the decision of euthanasia for SARDS. Less than half of owners who elected euthanasia because of SARDS felt it was an appropriate decision in retrospect (only 2/5 owners recommended euthanasia after euthanizing their own pet for SARDS). The high percentage of owners who discouraged euthanasia could reflect response bias because owners may not admit to convenience euthanasia because of guilt.

This owner-survey study had limitations. Quality of life or other outcome measures could not be compared between dogs with SARDS and other dogs because there was no control group of either blind dogs or dogs with normal vision. In addition, most outcome measures were based on owner perception and must not be misunderstood as objective facts. Additionally, diagnostic testing on all dogs to document or refute the presence of hyperadrenocorticism and other comorbid conditions was not uniformly available in review of medical records from the time of diagnosis.

Results of this study supported the persistence of blindness and concurrent clinical signs (polyuria, polydipsia, polyphagia, and weight gain) in dogs with SARDS. Although confirmed blind by means of ophthalmic examination, dogs with SARDS at a younger age were more likely to have owner-perceived partial vision. In general, owners perceived that dogs with SARDS have moderate to excellent quality of life and most owners discouraged euthanasia for dogs with SARDS.

ABBREVIATION

SARDS

Sudden acquired retinal degeneration syndrome

a.

Grozdanic SD, Kecova H, Harper MM, et al. Antibody mediated retinopathy—new mechanisms and treatment strategies (abstr). Vet Ophthalmol 2008;11:427.

b.

Gilmour MA. Clinical follow-up on 15 dogs with sudden acquired retinal degeneration syndrome (SARDS) (abstr). Vet Ophthalmol 2005;8:446.

c.

Copies of the survey questionnaire are available from the corresponding author on request.

d.

SAS, version 9.3, SAS Institute Inc, Cary, NC.

References

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  • Figure 1—

    Mean ± SD scores (scale, 0 to 5) for various behaviors in dogs (n = 100) with SARDS reported by 100 owners on a survey questionnaire. a–cValues for behaviors with different letters are significantly (P < 0.05) different.

  • 1. Carter RT, Oliver JW, Stepien RL, et al. Elevations in sex hormones in dogs with sudden acquired retinal degeneration syndrome (SARDS). J Am Anim Hosp Assoc 2009; 45:207214.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Montgomery KW, van der Woerdt A, Cottrill NB. Acute blindness in dogs: sudden acquired retinal degeneration syndrome versus neurological disease (140 cases, 2000–2006). Vet Ophthalmol 2008; 11:314320.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Vainisi SJ, Schmidt GM, West CS. Metabolic toxic retinopathy preliminary report. Trans Am Coll Vet Ophthalmol 1983; 14:7681.

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