Evaluation of clinical characteristics and bacterial isolates in dogs with bacterial keratitis: 97 cases (1993–2003)

Erica L. Tolar Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996-4544

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Diane V. H. Hendrix Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996-4544

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Barton W. Rohrbach Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996-4544

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Caryn E. Plummer Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608

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Dennis E. Brooks Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608

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Kirk N. Gelatt Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608

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Abstract

Objective—To evaluate clinical characteristics and breeds affected with bacterial keratitis and compare patterns of resistance in bacterial isolates over time in dogs.

Design—Retrospective cross-sectional study.

Animals—97 dogs with bacterial keratitis.

Procedure—Dogs with bacterial keratitis were identified from teaching hospital medical records at the Universities of Tennessee and Florida during the years 1993 to 2003. Data were collected pertaining to breed, Schirmer tear test results, treatments administered at the time of initial examination, bacterial species isolated, and resistance to selected antimicrobials.

Results—66% of the dogs were brachycephalic, 54% had tear production < 15 mm/min, and 29% were receiving a corticosteroid at the time of initial examination. The most common bacteria isolated were Staphylococcus intermedius (29%), β-hemolytic Streptococcus spp (17%), and Pseudomonas aeruginosa (21%). Staphylococcus intermedius isolates had limited resistance to certain antimicrobials. More than 80% of β-hemolytic Streptococcus spp isolates were resistant to neomycin, polymyxin B, and tobramycin. Isolates of P aeruginosa were susceptible to tobramycin and gentamicin and had limited resistance to ciprofloxacin and enrofloxacin. Among bacterial species isolated, there was no evidence of development of antimicrobial resistance over time.

Conclusions and Clinical Relevance—Data suggested that administration of ciprofloxacin or a combination of a first-generation cephalosporin and tobramycin may be used in the treatment of bacterial keratitis while awaiting results of bacterial culture and susceptibility testing. Evidence suggests that current methods of medical management of bacterial keratitis are not associated with increased antimicrobial resistance.

Abstract

Objective—To evaluate clinical characteristics and breeds affected with bacterial keratitis and compare patterns of resistance in bacterial isolates over time in dogs.

Design—Retrospective cross-sectional study.

Animals—97 dogs with bacterial keratitis.

Procedure—Dogs with bacterial keratitis were identified from teaching hospital medical records at the Universities of Tennessee and Florida during the years 1993 to 2003. Data were collected pertaining to breed, Schirmer tear test results, treatments administered at the time of initial examination, bacterial species isolated, and resistance to selected antimicrobials.

Results—66% of the dogs were brachycephalic, 54% had tear production < 15 mm/min, and 29% were receiving a corticosteroid at the time of initial examination. The most common bacteria isolated were Staphylococcus intermedius (29%), β-hemolytic Streptococcus spp (17%), and Pseudomonas aeruginosa (21%). Staphylococcus intermedius isolates had limited resistance to certain antimicrobials. More than 80% of β-hemolytic Streptococcus spp isolates were resistant to neomycin, polymyxin B, and tobramycin. Isolates of P aeruginosa were susceptible to tobramycin and gentamicin and had limited resistance to ciprofloxacin and enrofloxacin. Among bacterial species isolated, there was no evidence of development of antimicrobial resistance over time.

Conclusions and Clinical Relevance—Data suggested that administration of ciprofloxacin or a combination of a first-generation cephalosporin and tobramycin may be used in the treatment of bacterial keratitis while awaiting results of bacterial culture and susceptibility testing. Evidence suggests that current methods of medical management of bacterial keratitis are not associated with increased antimicrobial resistance.

Bacterial keratitis is a common and potentially vision-threatening disease. Recognition that an infectious process is underlying the changes in an affected eye is necessary for initiation of appropriate diagnostic testing and effective treatment. Prompt and intense treatment measures are necessary to prevent loss of vision secondary to extensive scarring or corneal perforation. Clinical signs of bacterial keratitis include corneal edema, stromal cellular infiltrate, collagenolytic activity, and stromal loss. Bacterial culture of the cornea should be performed prior to initiating antimicrobial treatment when bacterial keratitis is suspected. Adjustments in antimicrobial treatment can be made on the basis of results of culture and susceptibility testing. Unfortunately, many dogs have substantial stromal loss prior to the initiation of appropriately aggressive treatment, necessitating surgical treatment with keratectomy and conjunctival graft placement. Dual treatment with cefazolin and tobramycin, or monotherapy with ciprofloxacin, is commonly used to treat dogs with suspected or confirmed bacterial keratitis. These drugs provide a broad spectrum of antimicrobial coverage for most pathogenic bacteria. Although most dogs that receive appropriate medical and surgical treatment retain vision, the cost of surgery is prohibitive for many owners; therefore, early diagnosis and treatment are essential to reduce morbidity and the risk of blindness.

Regional differences in the organisms isolated from humans with bacterial keratitis have been reported.1–4 Although gram-positive bacteria are most commonly isolated, the percentage of cases of bacterial keratitis in which Pseudomonas spp are isolated varies among studies. In addition, resistance patterns among bacterial isolates vary regionally and temporally. Regional variation in isolates cultured and resistance patterns are theorized to result from seasonal changes and differing etiologies for the ulcers.1,2,5,6

Few studies have been undertaken to evaluate patterns in isolates detected and resistance among veterinary patients with bacterial keratitis. A study7 in horses in Florida revealed resistance of Streptococcus equisubsp zooepidemicus isolates to gentamicin; however, no change in resistance patterns was detected in isolates from horses with bacterial keratitis examined at the University of Tennessee.8

Previous reports9–13 have addressed the surgical treatment of severe ulcerative keratitis in dogs, but antimicrobial resistance and breed susceptibilities have not been evaluated. The purpose of the study reported here was to assess the clinical characteristics of dogs with bacterial keratitis and evaluate regional and temporal changes in the species of bacteria isolated and patterns of resistance to antimicrobials. We also hypothesized that there would be a correlation between brachycephalic breed and prevalence of bacterial keratitis.

Criteria for Selection of Cases

Dogs with bacterial keratitis were identified through a search of medical records and submissions to the microbiology laboratory at the UTVTH and the UFVMTH. Criteria for inclusion in the study included a diagnosis of corneal ulceration and positive results of bacterial culture obtained by means of a corneal swab during the years 1993 to 2003. The reference hospital population included all dogs accessed by either institution for reasons other than bacterial keratitis during the same time period.

Procedures

Information extracted from medical records included date of diagnosis, breed, Schirmer tear test results, whether medical treatment with atropine or corticosteroids had been provided, genus and species of the bacteria isolated, and susceptibility to selected antimicrobials. Samples for bacterial culture from dogs at both university hospitals were acquired by use of a sterile culture swab prior to application of topical anesthetic. Details of the sample collection procedure were not available for outside submissions. In vitro antimicrobial susceptibility assessments were performed by use of Kirby-Bauer disk diffusion methods. Swab specimens were initially inoculated on chocolate agar, enrichment blood agar, and colistin-nalidixic acid plates; MacConkey 2 agar; and a thioglycollate broth. Antimicrobials tested included amikacin, ampicillin, bacitracin, ceftiofur, cephalothin, chloramphenicol, ciprofloxacin, erythromycin, enrofloxacin, gentamicin, neomycin, polymyxin B, and tobramycin. The antimicrobials tested varied over time and between hospitals. The laboratories graded isolates as susceptible, intermediately susceptible, or resistant. Those graded as intermediately susceptible were considered susceptible to a particular antimicrobial.1,14

Statistical analysis—Categoric characteristics of dogs with bacterial keratitis were summarized and compared between institutions. The proportion of dogs that received atropine at the time of diagnosis and that had Schirmer tear test results < 15 mm/min was compared with the proportion of dogs that did not receive atropine but that had low tear production. The proportions of each bacterial species isolated; antimicrobial resistance of all bacterial isolates; and resistance of Staphylococcus intermedius, β-hemolytic Streptococcus spp, andPseudomonas aeruginosa isolates to selected antimicrobials were compared between institutions and during the periods from 1993 to 1998 and 1999 to 2003. Comparisons were analyzed by use of an unadjusted χ2 or Fisher exact test, depending on whether an expected cell value was < 5. The ages of dogs admitted to each institution were compared with a nonparametric ANOVA.a Associations between breed and bacterial keratitis were tested by comparing the odds of each breed of dog having a diagnosis of bacterial keratitis with the odds of an index population of mixed-breed dogs having bacterial keratitis. The Pekingese, Shih Tzu, Boston Terrier, Pug, and Lhasa Apso breeds were considered brachycephalic; all other breeds were considered nonbrachycephalic. Breeds included in analyses were restricted to those with 1 or more cases of bacterial keratitis and 100 or more dogs in the reference hospital population. Confidence intervals of the ORs were adjusted for multiple comparisons by use of the Bonferroni technique.15 Exact confidence limits of the ORs were reported when 1 or more expected cell counts in the 2 × 2 table were < 5; otherwise, asymptotic confidence limits were reported. Statistical evaluations were performed with a commercially available software program.b Values of P ≤ 0.05 were considered significant.

Results

One hundred nineteen isolates from 97 dogs with bacterial keratitis were evaluated. Of those, 66 isolates (52 from dogs examined at the hospital and 14 from outside submissions to the hospital laboratory) were from the UTVTH and 53 isolates were from 45 dogs examined at the UFVMTH. Complete records were available for 40 of the dogs from the UTVTH and for all 45 of the dogs from the UFVMTH (Table 1).

Table 1—

Selected characteristics of 85 dogs with bacterial keratitis at the UTVTH and the UFVMTH from 1993 to 2003.

CharacteristicUTVTH (n = 40)UFVMTH (45)
Age*7.5 (1–13)7 (0.25–17)
Breed
   Brachycephalic27 (68)29 (67)
   Other13 (33)16 (33)
Schirmer tear test results
   ≥ 15 mm/min16 (53)12 (39)
   ≤ 14 mm/min14 (47)19 (61)
Prior treatment with corticosteroids14 (35)11 (25)

Values given as median (range).

Values given as number (%).

Denominator varies because of missing information from some records.

For comparison of clinical characteristics and breeds of affected dogs, data for the 85 dogs for which complete records were available was used. There were no significant differences between universities in any of the dogs' characteristics. Fifty-six of the 85 (66%) dogs were of brachycephalic breeds. The breeds most commonly represented were Pekingese (n = 22 [26%]), Shih Tzu (17 [20%]), Boston Terrier (9 [11%]), and Pug (7 [8%]). Tear production as determined by the Schirmer tear test was recorded in 61 dogs. Thirty-three (54%) of those dogs had tear production ≤ 14 mm/min, and 28 (46%) had production ≥ 15 mm/min. All but 5 (n = 28 [85%]) of the dogs with tear production < 15 mm/min were of brachycephalic breeds. There was no significant difference between the proportion of dogs that were being treated with atropine at the time of examination and that had low tear production (4/6) and the proportion of dogs that were not being treated with atropine and that had low tear production (29/55 [53%]; P = 0.7). Twenty-five (29%) dogs were receiving a topically administered ophthalmic or systemically active corticosteroid at the time of initial examination. Seventy-seven (91%) dogs with bacterial keratitis were of a brachycephalic breed, had low tear production, or were being treated with corticosteroids.

For comparison of antimicrobial susceptibility patterns, data from all 119 isolates were evaluated (Table 2). Twelve dogs at the UTVTH and 8 dogs at the UFVMTH had polymicrobial infections. The most common bacterial species isolated during the period from 1993 to 2003 were S intermedius (35/119 [29%]), β-hemolytic Streptococcus spp (20/119 [17%]), and P aeruginosa (25/119 [21%]). Although there were no significant differences between hospitals in the bacterial species isolated during the overall period from 1993 to 2003 or when comparing isolates from both hospitals for each bacterial species during the periods from 1993 to 1998 and 1999 to 2003, there was a higher proportion of P aeruginosa isolated during 1999 to 2003; however, the difference was not significant (P = 0.06). When only data from dogs at UTVMTH were evaluated, there were significantly fewer β-hemolytic Streptococcus spp (P = 0.001) and more P aeruginosa spp (P = 0.01) isolated from dogs during 1999 to 2003 than during 1993 to 1998.

Table 2—

Bacterial species (No. [%]) isolated from 97 dogs with bacterial keratitis at the UTVTH and UFVMTH from 1993 to 2003.

Bacterial isolate1993–19981999–2003
UTVTH (n = 39)UFVMTH (37)Total (76)UTVTH (27)UFVMTH (16)Total (43)
Staphylococcus intermedius7 (26)5 (31)12 (28)11 (28)12 (32)23 (30)
β-hemolytic Streptococcus4 (15)4 (25)8 (19)1 (3)11 (30)12 (29)
Pseudomonas aeruginosa3 (11)2 (13)5 (12)15 (38)5 (14)20 (26)
Escherichia coli2 (7)1 (6)3 (7)2 (5)1 (3)3 (4)
Staphylococcus aureus02 (13)2 (5)02 (5)2 (3)
Klebsiella pneumoniae1 (4)01 (2)2 (5)1 (3)3 (4)
Enterobacter aerogenes2 (7)02 (5)1 (3)01 (1)
Other*8 (30)2 (13)10 (23)7 (18)6 (16)13 (17)

Isolates detected in ≤2 cases. Pathogens included Staphylococcus schleferi, α-hemolytic Streptococcus spp, unidentified gram-negative rod, Pasteurella multocida, Enterobacter cloacae, Corynebacterium spp, Enterococcus spp, Pantoea spp, Micrococcus agglomerans, Pseudomonas fluorescens, Staphylococcus spp (other), and Acinetobacter baumannii.

Antimicrobial susceptibility patterns of all bacterial isolates were summarized (Table 3). No significant differences in resistance to any of the selected antimicrobials were observed between the periods from 1993 to 1998 and 1999 to 1003. An increase in resistance to bacitracin, cephalothin, and chloramphenicol was observed, but the differences were not significant. Staphylococcus intermedius isolates had limited resistance to the selected antimicrobials (Table 4). All isolates of S intermedius were susceptible to bacitracin, ciprofloxacin, enrofloxacin, and cephalothin. More than 80% of β-hemolytic Streptococcus spp isolates were resistant to neomycin, polymyxin B, and tobramycin, and > 20% were resistant to gentamicin. More than 80% of P aeruginosa isolates were resistant to bacitracin, chloramphenicol, and cephalothin. Isolates of P aeruginosa had limited or no resistance to tobramycin, gentamicin, ciprofloxacin, and enrofloxacin.

Table 3—

Resistance of bacterial isolates cultured from dogs with bacterial keratitis from 1993 to 1998 and 1999 to 2003.

IntervalAntimicrobial
BacCepChlCipEfxGenNeoPolyTob
1993–199810/388/406/420/141/204/4114/4114/4112/41
(26)(20)(14)(0)(5)(10)(34)(34)(29)
1999–200325/6627/7617/751/292/616/7618/6816/6814/69
(38)(36)(23)(3)(3)(8)(26)(24)(69)

Values given as number resistant/total number of isolates (%).

Bac = Bacitracin. Cep = Cephalothin. Chl = Chloramphenicol. Cip = Ciprofloxacin. Efx = Enrofloxacin. Gen = Gentamicin. Neo = Neomycin. Poly = Polymyxin. Tob = Tobramycin.

Table 4—

Resistance of S intermedius, β-hemolytic Streptococcus spp, and P aeruginosa isolates detected in dogs with bacterial keratitis from 1993 to 2003.

BacteriaAntimicrobial
BacCepChlCipEfxGenNeoPolyTob
S intermedius0/300/351/340/90/184/342/311/313/31
(0)(0)(3)(0)(0)(12)(6)(3)(10)
β-hemolytic Streptococcus0/190/190/190/30/154/1918/1917/1916/19
(0)(0)(0)(0)(0)(21)(95)(89)(84)
P aeruginosa17/2025/2522/251/153/230/253/220/220/22
(85)(100)(88)(7)(13)(0)(14)(0)(0)

See Table 3 for key.

The odds of a diagnosis of bacterial keratitis were significantly higher for 6 breeds, including Pekingese, Shih Tzu, Pug, Boston Terrier, Miniature Pinscher, and Bichon Frise, compared with mixed-breed dogs (Table 5).

Table 5—

Odds ratios for bacterial keratitis in dogs of various breeds (case series), compared with a reference hospital population, from 1993 to 2003.

BreedNo. of dogs
Case seriesReference hospital populationORAdjusted confidence interval
Mixed dogs413,5041.0NA
Pekingese22607122.424.1–620.5
Shih Tzu171,28344.78.5–234.6
Pug750845.97.1–302.3
Boston Terrier970942.97.1–257.5
Miniature Pinscher229023.31.8–308.9
Bichon Frise236318.61.4–246.5
Maltese251613.11.0–173.1
Lhasa Apso16015.60.2–57.2
Cocker Spaniel42,4085.60.7–46.1
Golden Retriever22,4132.80.2–36.9
Yorkshire Terrier21,3315.10.4–66.9
West Highland White Terrier133010.20.4–286.9
Boxer21,2525.40.4–71.2
Greyhound14577.40.3–206.9
Miniature Schnauzer21,1246.00.5–79.3
English Springer Spaniel13549.50.3–267.4
Siberian Husky14537.50.3–208.8

Discussion

The precise pathogenesis of bacterial keratitis in dogs is not known. Failure of the protective mechanisms of the eye (eg, healthy palpebral fissure, preocular tear film, and normal corneal sensitivity) is thought to be an important contributing factor. In the present study, 4 brachycephalic breeds (Pekingese, Shih Tzu, Pug, and Boston Terrier) and 2 nonbrachycephalic breeds (Miniature Pinscher and Bichon Frise) had an association with bacterial keratitis. Brachycephalic dogs lack many of the protective mechanisms operant in mesocephalic or dolicocephalic breeds. The pronounced globe position of brachycephalic dogs predisposes the eye to ocular trauma, and exophthalmia (secondary to the shallow orbits of brachycephalic breeds) prevents normal palpebral apposition and leads to lagophthalmos. In addition, many brachycephalic dogs have trichiasis from facial folds, medial aberrant dermis, medial entropion, or distichia, any of which can incite corneal ulceration or prevent normal epithelialization. Brachycephalic dogs often have a thin lipid layer in the tear film and decreased aqueous coverage in the central cornea as a result of incomplete blinking.16 Moreover, corneal sensitivity in brachycephalic dogs is lower, compared with sensitivity in mesocephalic and dolichocephalic dogs.17 The inherently lower corneal sensitivity and protrusion of the globe in brachycephalic dogs negatively affect function of the cornea's protective mechanisms, lead to an increased opportunity for traumatic injury, and allow ulcers in the early stages to go unnoticed by owners.

More than half (54%) of the dogs in our study had tear production < 15 mm/min, suggesting that KCS plays a role in the pathogenesis of bacterial keratitis. Atropine is commonly used in the treatment of corneal ulceration and is known to decrease tear production; however, it was not believed to play a role in this study because KCS occurred with similar frequency among dogs that were being treated with atropine at the time of diagnosis and dogs that were not. A study18 of clinically normal dogs revealed that although there was a decrease in tear production from baseline measurements, tear production was still maintained within reference limits during treatment with atropine. Dogs with KCS have higher numbers of conjunctival bacteria because bacteria are not washed from the conjunctiva effectively and accumulate in the conjunctiva and on the cornea.19 Antibacterial enzymes that normally suppress bacteria are not present in normal quantities in dogs with KCS.20 Low tear production can cause corneal ulceration and inhibit the reepithelialization process.21

One third of the dogs in our study were receiving treatment with topically administered or systemically active corticosteroids at the time of initial examination at the hospital. Topical administration of corticosteroids decreases epithelial migration and wound healing.22,23 Although we were unable to evaluate corticosteroid use as a risk factor for bacterial keratitis, topically administered prednisone interfered with the ability of antimicrobials to clear bacteria in a murine model of P aeruginosa keratitis.24 Observations of slower epithelial healing and suppression of inflammation secondary to treatment with corticosteroids have led to the hypothesis that use of corticosteroids potentiates corneal disease.22,25,26

The most commonly isolated species of bacteria from dogs with bacterial keratitis in the present study were S intermedius, β-hemolytic Streptococcus spp and P aeruginosa. These bacteria also predominate in the normal conjunctival flora in dogs.27 We observed a significant increase in the frequency of isolation of P aeruginosa and a decrease in isolation of β-hemolytic Streptococcus spp at UTVTH from 1999 to 2003, compared with the period from 1993 to 1998. These findings may be because of the relatively small sample size and random variation. The proportion of Pseudomonas spp isolated from cases of bacterial keratitis in humans varies among studies.1,3,14

In dogs with bacterial keratitis from UTVTH and UFVMTH, there were no significant changes in the resistance patterns to selected antimicrobials over an 11-year period, a finding inconsistent with those reported in humans with bacterial keratitis. Although increased resistance to bacitracin, cephalothin, and chloramphenicol was observed in dogs, the increase can be attributed to the increased number of P aeruginosa isolates. At both institutions, resistance to fluoroquinolone antimicrobials was minimal among all isolates tested, indicating that ciprofloxacin is still an effective treatment for bacterial keratitis in dogs. Although tobramycin and gentamicin often have similar spectrums of antimicrobial activity, tobramycin is less toxic to epithelial cells in vitro than gentamicin and is therefore the preferred aminoglycoside to use when a bacterial species is sensitive to both.28 In humans, in vitro susceptibility of isolates of P aeruginosa to ciprofloxacin is high in Europe and the United States but is low in India, with 16% of isolates resistant to ciprofloxacin.1,3,5,6 In contrast, resistance of gram-positive bacterial isolates to fluoroquinolones is rapidly increasing.1,5,29

In our study, the odds of having bacterial keratitis were significantly higher for 6 breeds (ie, Pekingese, Shih Tzu, Pug, Boston Terrier, Miniature Pinscher, and Bichon Frise), compared with mixed-breed dogs. Although only 4 of these breeds are considered to have brachycephalic anatomy, Miniature Pinschers and Bichon Frises also have prominent globes and may have a similar lack of corneal protective mechanisms.

Bacterial keratitis can be an aggressive, visionthreatening disease in dogs. With the availability of numerous ophthalmic antimicrobial preparations that are active against a wide spectrum of bacteria, most dogs can successfully be treated with medical management alone. In general, a combination of cefazolin with tobramycin or ciprofloxacin may be used as broad-spectrum treatment for bacterial keratitis. Antimicrobial resistance in isolates from humans with bacterial keratitis has led to the use of polymicrobial treatment regimens and third and fourth-generation fluoroquinolone drugs. There is no evidence for the existence of similar trends in veterinary medicine at present. The first choice in veterinary ophthalmology for treatment of dogs with superficial, uncomplicated ulcers continues to be a solution containing neomycin, polymyxin B, and bacitracin. Veterinary patients do not frequently have the allergic sensitivities to these antimicrobials that are observed in humans, and most bacteria are susceptible to this drug combination. Brachycephalic conformation, KCS, and corticosteroid use can increase the risk of corneal trauma and reduce the rate of healing, enhancing the chances for bacterial infection. The aforementioned factors suggest that corneal ulcers in brachycephalic dogs and dogs with KCS should be managed more aggressively than those of mesocephalic and dolicocephalic breeds. Dogs undergoing treatment with either systemically or topically administered corticosteroids should be monitored for the development of corneal ulceration.

UTVTH

University of Tennessee Veterinary Teaching Hospital

UFVMTH

University of Florida Veterinary Medical Teaching Hospital

OR

Odds ratio

KCS

Keratoconjunctivitis sicca

a

PROC NPAR1WAY, SAS version 8.0, SAS Institute Inc, Cary, NC.

b

SAS statistical software, version 8.02, SAS Institute Inc, Cary, NC.

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