Wu 2019

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Received: 1 May 2019 

|
  Revised: 6 August 2019 
|  Accepted: 23 August 2019

DOI: 10.1111/vop.12709

ORIGINAL ARTICLE

Ocular findings and selected ophthalmic diagnostic tests in a


group of young commercially available Guinea and Skinny pigs
(Cavia porcellus)

Doris Wu1,2  | Michala de Linde Henriksen1   | Krystan Grant3  | Tanya Lyakhova1  |


Julia L. Sharp   4
| Joshua B. Daniels 5

1
Comparative Ophthalmology, Department
of Clinical Sciences, College of Veterinary
Abstract
Medicine, Colorado State University, Fort Objective: The purpose of this study is to evaluate a group of young commercially
Collins, CO, USA available Skinny pigs, to gain information regarding ocular findings in this breed of
2
Oahu Veterinary Specialty Center and
guinea pig. Comparisons of ocular findings are to be made between Skinny pigs and
VCA Family Animal Hospital, Pearl City,
HI, USA haired guinea pigs.
3
PetSmart, Phoenix, AZ, USA Animal studied: Ten haired guinea pigs and ten Skinny pigs were examined.
4
Department of Statistics, College Procedure: A complete ophthalmic examination including Schirmer tear test‐II
of Natural Sciences, Colorado State (STT‐II), phenol red thread test (PRTT), rebound tonometry with TonoVet PLUS,
University, Fort Collins, CO, USA
5
Fluorescein and Rose Bengal stain was performed. Microbiology swabs for aerobic
Veterinary Diagnostic Laboratory, College
of Veterinary Medicine, Colorado State bacterial growth were collected from conjunctiva of both eyes prior to the ophthal-
University, Fort Collins, CO, USA mic examination.
Results: The ophthalmic examination revealed seven abnormal ocular findings: tri-
Correspondence
Michala de Linde Henriksen, Comparative chiasis, mucopurulent discharge, hyperemia/chemosis of the conjunctiva, corneal fi-
ophthalmology, Department of Clinical brosis, corneal vascularization, and foreign body on the cornea or conjunctiva. Skinny
Sciences, College of Veterinary Medicine,
Colorado State University, 300 West Drake
pigs had a significantly higher amount of mucopurulent discharge (P = .0133) and a
Road, Fort Collins, CO 80525, USA. significantly higher STT‐II (P < .001) than haired guinea pigs. Although not signifi-
Email: [email protected] cant, trichiasis, keratitis with corneal vascularization, and foreign body presence were
more common in Skinny pigs. Significantly more Skinny pigs had Pasteurellaceae
isolated from their conjunctiva than haired guinea pigs (P = .0112). Antimicrobial
susceptibility for the five Pasteurellaceae organisms isolated revealed susceptibility
toward oxytetracycline, tobramycin, ciprofloxacin, and ofloxacin, whereas resistance
was found toward erythromycin, trimethoprim‐sulfamethoxazole, and moxifloxacin.
Conclusion: Young Skinny pigs have a higher risk of Pasteurellaceae‐associated
conjunctivitis. Oxytetracycline, tobramycin, ciprofloxacin, and ofloxacin were iden-
tified as topical antibiotics that may be useful for Pasteurellaceae‐associated con-
junctivitis in Skinny pigs.

KEYWORDS
conjunctivitis, guinea pigs, microbiology, ophthalmic diagnostic tests, ophthalmic diseases,
Pasteurellaceae, skinny pigs

Veterinary Ophthalmology. 2019;00:1–11. wileyonlinelibrary.com/journal/vop © 2019 American College of Veterinary     1 |


Ophthalmologists
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2       WU et al

1  |   IN TRO D U C T ION two ectodermal derivatives including the skin, apocrine


glands, and parts of the eyes.6-8 Corneal and conjunctival
Guinea pigs (Cavia porcellus) are domesticated diurnal ro- epithelial cells as well the lacrimal gland originate from the
dents from South America.1,2 Although they are commonly surface ectoderm.9 A human study reported that in patients
used as laboratory animals, guinea pigs are increasing in with ED, ocular complaints particularly dry eye symptoms
their popularity as pets.3 The Skinny pig is an almost hairless were observed.7 X‐linked hypohidrotic ectodermal dys-
breed of guinea pig that typically has hair on their muzzle, plasia (EDA) is the most frequent form of EDA,8,10,11 and
feet, and legs but is hairless over the remainder of their bodies the lack of sebaceous glands have been reported in both
(Figure 1). The modern Skinny pig breed likely originated German shepherds and humans. A study of Tabby mice,
from crossing haired guinea pigs with a hairless strain. The which serve as a model for EDA in humans, demonstrated
hairless strain is related to a spontaneous genetic mutant that characteristic abnormalities in the ocular surface including
was first identified in 1978 in a Hartley Guinea Pig Colony.4 neovascularization, keratitis, ulceration, and the absence of
A study looking into the anatomy of hairless guinea pig skin meibomian glands.8
revealed that their skin is similar to human skin and is there- To our knowledge, there is no literature on Skinny pig oc-
fore a useful animal model for human dermatological stud- ular health and no information found on ectodermal dysplasia
ies.5 Similar to hairless dogs, the Skinny pig's lack of normal with or without glandular abnormalities in this breed. Given
hair coat is being promoted for its “hypoallergenic nature” the high prevalence of ocular disease in guinea pigs with
resulting in their popularity as pets.6 cataracts as the most common finding12 and reported ocular
Hairless dogs such as the Chinese crested breed demon- abnormalities in other hairless species, the purpose of this
strate a hairless phenotype that is classified as a form of ec- study is to evaluate a group of young commercially available
todermal dysplasia (ED).6 Ectodermal dysplasia is a group Skinny pigs, to gain information regarding ocular findings in
of genetic disorders that involves a primary defect in at least this breed of guinea pig.

(A) (B)

(C)

F I G U R E 1   The appearance of Skinny


pigs. A, The Skinny pigs are almost hairless
with hairs on their nose and feet. B, Skinny
pigs are available in many different colors.
C, A Skinny pig compared to a normal
haired guinea pig
WU et al   
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   3

2  |  M ATE R IA L S A N D ME T HODS aerobic culture to Colorado State University's Veterinary


Diagnostic Laboratory (Department of Microbiology,
Twenty systemically healthy guinea pigs (10 haired guinea Colorado State University). Following instillation of 1
pigs of various breeds and 10 Skinny pigs) were examined. drop (0.05 mL) of 0.5% proparacaine hydrochloride oph-
These animals were selected from a population of guinea thalmic solution (Bausch and Lomb) to induce corneal
pigs to be sold as household pets at a local pet store lo- anesthesia in each eye, and removal of excess with a con-
cated in Fort Collins, Colorado. The study was performed junctival swab 20  seconds after instillation,13 quantifi-
in compliance with Colorado State University guidelines cation of tear production with Schirmer Tear Test (STT)
for research via the Institutional Animal Care and Use (OptiTech Eye Care) and phenol red thread test (PRTT)
Committee (protocol number 17‐7517A). Written consent (AYUMI Pharmaceutical Corporation) were performed in
was granted by the pet store prior to study enrollment of both eyes. Since previous studies comparing STT‐I and
their guinea pigs. An in‐house veterinarian was present STT‐II values in guinea pigs were not significantly dif-
during ophthalmic examination of all guinea pigs. Any ferent indicating limited corneal reflex tearing in this spe-
guinea pig diagnosed with an ocular disease was started on cies,14 it was decided to only perform STT‐II in this study
appropriate treatment. to minimize any discomfort that may be caused by STT‐I.
Information on age, sex, and neuter status was obtained for The STT strip was folded at the notch and placed in the
all guinea pigs included in the study. A brief physical exam- inferior conjunctival fornix for 60  seconds. The amount
ination was performed on all study animals by the pet store's of wetting was recorded as 0  mm if the moistened strip
veterinarian. Any animal with evidence of systemic disease was below or at 0 mm. The PRTT was performed 5 min-
including nasal discharge, evidence of decreased appetite, utes after completion of STT‐II. A 3‐mm indentation at
gastrointestinal disease, and poor body condition would have the end of the thread was inserted with a curved micro-
been disqualified from the study; however, all animals were surgical tying forceps in the inferior conjunctival sac for
apparently healthy. 15 seconds. The wetted length of thread was measured in
A complete ophthalmic examination was performed by millimeters (mm) (Figure 2).
two board‐certified veterinary ophthalmologists (DW and Rebound tonometry to measure intraocular pressures
MdLH) on each guinea pig including a neuro‐ophthalmic (IOP mmHg) was performed with a TonoVet PLUS (Icare,
examination with assessment of menace reflex, dazzle Helsinki, Finland) in the “Rabbit” calibration setting in ac-
response, pupillary light reflex (direct and indirect), and cordance with manufacturer directions (Figure 3). Since diur-
palpebral reflex. The adnexa and anterior segment of all nal variation is known to alter IOP in many species including
eyes were then evaluated by means of slit‐lamp biomicros- the guinea pig,1,15,16 the time of day that IOP was being mea-
copy (Kowa SL‐ 17; Kowa CO. Ltd). Bacterial swab speci- sured was recorded. Fluorescein and Rose Bengal staining
mens were then obtained from each eye by placing a sterile of the cornea was performed using a cobalt blue light and
cotton‐tipped swab (BD BBL™ CultureSwab™, Fisher white light, respectively (both stain tests from OptiTech Eye
Scientific) moistened with sterile saline into the inferior Care). Pharmacological dilation with one drop (0.05 mL) of
fornix of each eye followed by gentle rotation as outlined 1.0% Tropicamide ophthalmic solution (Bausch and Lomb)
in the study by Costa and colleagues from 2008.13 The allowed for complete binocular indirect ophthalmoscopy of
swab specimens were refrigerated at 4°C for 12‐48 hours both eyes to take place at least 15 minutes following pupil-
after collection and submitted for standard bacterial lary dilation. Indirect ophthalmoscopy was performed with

(A) (B)

F I G U R E 2   Measurement of tear
production. A, Schirmer tear test‐II (STT‐II)
was used to test tear production in both
haired guinea pigs and Skinny pigs. B,
15 min following STT‐II the phenol red
thread test (PRTT) was performed. The
thread was placed in the lower eyelid with
tying forceps
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4       WU et al

between type of guinea pig and frequency of certain conditions


and types of bacteria present. A false discovery rate (FDR) ad-
justment was made to the FET p‐values to account for multiple
comparisons. SAS v 9.4 was used for all statistical analyses and
a P‐value of ≤.05 was considered statistically significant.

3  |  RESULTS
Twenty systemically healthy guinea pigs were enrolled into
the study: 10 were haired guinea pigs of various breeds and
10 were of the Skinny pig breed. All guinea pigs were in-
tact males and under 6 months of age. Exact birth dates were
unknown for each individual guinea pig. All guinea pigs'
(haired guinea pigs and Skinny pigs) physical examination
parameters were within normal limits.

3.1  |  Ophthalmic examination findings


Neuro‐ophthalmic examination revealed that all guinea pigs
appeared visual with an absent menace response, a weak posi-
tive dazzle response, and an incomplete pupillary response re-
flex (PLR; direct and indirect) when examined with the diffuse
F I G U R E 3   The intraocular pressure (IOP) was obtained with the light beam at maximal intensity with the slit lamp. All guinea
newer rebound tonometer “TonoVet PLUS” on “rabbit” setting pigs were noted to have a weak palpebral response in compari-
son to other companion animals such as dogs, cats, and horses.
a binocular headset (Keeler Instrument Inc), and a 40D Table 1 summarizes the results of ophthalmic examination
and 60D lens (Volk Optical Inc). All examinations and di- findings on all haired guinea pigs and Skinny pigs. All clini-
agnostics were performed in the right eye prior the left eye cal ocular abnormalities detected involved either the adnexa
for every animal. Photographic documentation of external or cornea with no intraocular abnormalities found within the
findings was provided using a Nikon digital camera (Nikon anterior or posterior segment. The ocular abnormalities were
D750; Nikon Inc). listed into seven categories: mucopurulent ocular discharge,
trichiasis, hyperemia/chemosis of the conjunctiva, corneal fi-
brosis, keratitis with corneal vascularization, and foreign body.
2.1  |  Statistical analysis
Trichiasis was not present in any (0%) of the haired
Descriptive statistics (mean ± SD for quantitative measures and guinea pigs but was present in three out of 10 (30%)
percentage (frequency) for categorical measures) were com-
puted for each group of guinea pig. For descriptive statistics, the T A B L E 1   Results of ophthalmic examination findings on all
right and left eye quantitative measures (eg, IOP, STT, PRTT) haired guinea pigs and Skinny pigs
were averaged for the same animal and categorical measures (eg,
Fluorescein stain, Rose Bengal stain, mucopurulent discharge, Haired guinea Skinny pig
Diagnosis pig (n = 10) (n = 10) P value
trichiasis, hyperemia/chemosis of conjunctiva, corneal fibro-
sis, keratitis with vascularization, foreign body) were classified Trichiasis 0% (n = 0) 30% (n = 3) —
as “present” if the condition was present in either eye. Linear Mucopurulent 30% (n = 3) 80% (n = 8) .0266*
mixed‐effects models were used to compare haired guinea pig discharge
and Skinny pig IOP, STT, and PRTT using the type of guinea pig Hyperemia/chemosis 20% (n = 2) 60% (n = 6) .1240
as a fixed effect, and pig as a random effect to account for meas- Corneal fibrosis 20% (n = 2) 30% (n = 3) .6403
urements on both eyes for each guinea pig. A similar analysis Keratitis with corneal 0% (n = 0) 10% (n = 1) —
was conducted to compare IOP between morning and afternoon. vascularization
Generalized linear mixed‐effects models were used to compare Foreign body 0% (n = 0) 70% (n = 7) —
Skinny pigs and haired guinea pig data for categorical meas-
Note: Interpreted as either percent of guinea pigs or eyes with the condition. GP,
ures to account for binary outcomes. Due to small sample sizes, guinea pig, *, indicates statistical significance using a 0.05 significance level; —,
Fisher's exact test (FET) was used to compare the association indicates no statistical test performed due to n = 0 in the haired guinea pig group.
WU et al   
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Skinny pigs (four eyes out of 20 eyes, 20%) (Figure 4). haired guinea pigs (P = .0266), with the odds of mucopuru-
Mucopurulent discharge was present in three out of 10 lent discharge for Skinny pigs about 25 times higher than for
(30%) haired guinea pigs (five out of 20 eyes, 25%) vs 8 out haired guinea pigs (OR: 25, 95% CI: 1.52, 500). The odds
of 10 (80%) Skinny pigs (16 out of 20 eyes, 80%) (Figure ratio (OR) confidence interval (CI) width is large likely due to
5A). Hyperemia/chemosis of the conjunctiva was present small sample sizes. No significant differences could be found
in two out of 10 (20%) haired guinea pigs (three out of 10 between haired guinea pigs versus Skinny pigs for the pres-
eyes, 15%) vs 6 out of 10 (60%) Skinny pigs (nine out of ence of hyperemia/chemosis or corneal fibrosis (P = .124 and
20 eyes, 45%) (Figure 5B). Corneal fibrosis was present in P = .640, respectively). Statistical comparisons for trichiasis,
two out of 10 (20%) haired guinea pigs (two out of 20 eyes, keratitis with corneal vascularization, and foreign body could
10%) vs 3 out of 10 (30%) Skinny pigs (three out of 20 not be performed due to small sample size (n  =  0) in the
eyes, 15%) (Figure 6). Keratitis with corneal vasculariza- haired guinea pig population.
tion was not found in any (0%) haired guinea pigs but was
found in 1 out of 10 (10%) Skinny pigs (one out of 20 eyes,
3.2  |  Diagnostic tests
5%) (Figure 6). Foreign body was not found in any (0%)
haired guinea pigs but was found as conjunctival or corneal Table 2 summarizes the results of STT, PRTT, IOP, fluores-
foreign body in seven out of 10 (70%) Skinny pigs (nine out cein stain, and Rose Bengal stain test that were performed on
of 20 yes, 45%) (Figure 7). It was noted on the ophthalmic all haired guinea pigs and Skinny pigs.
examination that all Skinny pigs had very elastic eyelids
that were easily opened compared to the haired guinea pigs.
3.2.1  |  Schirmer tear test‐II (STT‐II)
No intraocular abnormalities were detected. Indirect oph-
thalmoscopy revealed normal findings. Mean ± standard deviation (SD) STT‐II value for haired guinea
Statistical analysis revealed a significant difference in the pig was 1.00 ± 1.18 mm and Skinny pig was 3.45 ± 1.76 mm
log odds of mucopurulent discharge between Skinny pigs and with data pooled from the right and left eye of each individual
animal. Average STT‐II in haired guinea pigs was significantly
lower than STT‐II in Skinny pigs (P < .001).

3.2.2  |  Phenol red thread test (PRTT)


Mean  ±  SD PRTT value for haired guinea pig was
13.15 ± 3.31 mm and Skinny pig was 13.85 ± 5.72 mm with
data pooled from the right and left eye of each individual
animal. There was not a significant difference between aver-
age PRTT values in haired guinea pigs versus Skinny pigs
(P = .7635).

3.2.3  | Tonometry
Tonometry is used to estimate the intraocular pres-
F I G U R E 4   Trichiasis was found in a couple of the Skinny
sure (IOP) of the eye. Mean  ±  SD IOP value for haired
pigs (and in none of the haired guinea pigs). The hair(s) that caused
trichiasis (white arrow) protruded from a follicle located in the
guinea pig was 16.45 ± 1.34 mm Hg and Skinny pig was
temporal aspect of the eyelids 17.90 ± 2.04 mm Hg with data pooled from the right and

(A) (B)

F I G U R E 5   A, Mucopurulent
discharge was found in many of the
Skinny pigs. B, Hyperemia and chemosis
of the conjunctiva was found in many of
the Skinny pigs together with concurrent
mucopurulent discharge
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6       WU et al

significant differences for either diagnostic stain test found


between haired guinea pigs versus Skinny pigs (Fluorescein
stain; P = .6831, Rose Bengal stain; P = .0984).

3.3  |  Microbiological analysis


The microbiological results revealed that all 10 haired guinea
pigs and 10 Skinny pigs grew one or more bacteria from their
conjunctiva. Table 3 lists the different bacteria that were iso-
lated from the haired guinea pigs and Skinny pigs.
The three most common bacteria found in the haired
guinea pig population were Corynebacterium species (14 out
of 20 eyes, 70%), Beta‐hemolytic Streptococcus species (eight
out of 20 eyes, 40%) and alpha‐hemolytic Streptococcus spe-
cies (6 out of 20 eyes, 30%). The three most common bacteria
F I G U R E 6   One Skinny pig had corneal vascularization growing found in the Skinny pig population were organisms belonging
in from the dorsal aspect (white arrow) as well as corneal fibrosis to the family of Pasteurellaceae (19 out of 20 eyes, 95%),
(white asterisk) alpha‐hemolytic Streptococcus species (10 out of 20 eyes,
50%), and coagulase‐negative Staphylococcus species (6
left eye of each individual animal. There was not a signifi- out of 20 eyes, 30%). There were significantly more haired
cant difference between IOP values in haired guinea pigs guinea pigs (7 out of 10 animals, 70%) with Corynebacterium
vs Skinny pigs (P = .0766). In our study, all measurements species isolated from their conjunctiva compared to Skinny
for haired guinea pigs and five out of ten Skinny pigs were pigs (0 out of 10 animals, 0%) (P = .0248). There were sig-
obtained in the evening and the remaining five Skinny pigs nificantly more Skinny pigs (10 out of 10 animals, 100%)
were obtained in the morning. with organisms belonging to the family of Pasteurellaceae
There was not a significant difference between average isolated from their conjunctiva vs haired guinea pigs (2 out
IOP measurements in the morning vs the evening (P = .7801). of 10 animals, 20%) (P = .0112) (Table 3).
Partial 16s rDNA sequencing was performed to deter-
mine which Pasteurellaceae were cultured in the haired and
3.2.4  |  Fluorescein and Rose Bengal
Skinny pig population. Five different Pasteurellaceae or-
stain test
ganisms were isolated with Pasteurella multocida being the
Three out of 10 (30%) haired guinea pigs and four out of most commonly isolated (14 out of 24, 58.3%), followed by
10 (40%) Skinny pigs showed positive fluorescein stain up- unspeciated Pasteurellaceae organisms (5 out of 24, 20.8%),
take in one or both eyes. Four out of 10 (40%) haired guinea Necropsobacter spp. (3 out of 24 eyes, 12.5%), Mannheimia
pigs and nine out of 10 (90%) Skinny pigs showed positive caviae (1 out of 24, 4.2%), and Pasteurella pneumotropica
Rose Bengal stain uptake in one or both eyes. There were no (1 out of 24, 4.2%). Two out of 24 (8.3%) Pasteurellaceae

(A) (B) (C)

F I G U R E 7   A, A Skinny pig with cornea foreign bodies located on the cornea/tear film. These foreign bodies (white arrows) could not easily
be flushed off with eye wash but had to be removed with a cotton‐tipped swab. B, A Skinny pig with foreign body material present in the medial
canthus (white arrow). C, The foreign body in Figure 7B had to be removed with a cotton‐tipped swab which appeared to be organic bedding
material (white arrow)
WU et al   
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were isolated from haired guinea pigs; one haired guinea pharmacokinetic (PK) or pharmacodynamic (PD) informa-
pig had unspeciated Pasteurellaceae isolated from the con- tion exist for topical antibiotics, the interpretations as sus-
junctiva, and one haired guinea pig had Mannheimia caviae ceptible or resistant were based on systemic breakpoints
isolated from the conjunctiva. Twenty‐two out of 24 (91.7%) for either dogs or human beings using current Clinical and
Pasteurellaceae were isolates from Skinny pigs (Table 4). Laboratory Standards Institute (CLSI) criteria for other
Antimicrobial susceptibility testing was performed for gram‐negative bacteria. An organism susceptible to a sys-
representative isolates of the Pasteurellaceae using broth temic antibiotic will likely be susceptible to the topical form
microdilution (Sensititre JoEye panel; Thermo‐Fisher). due to presence of high concentration of the drug (relative
The antimicrobial agents tested were as follows: bacitra- to plasma drug concentration) at the target site.17 Four out
cin, ceftiofur, chloramphenicol, ciprofloxacin, doxycycline, of five (80%) of the Pasteurellaceae were resistant to eryth-
erythromycin, gentamicin, moxifloxacin, neomycin, oflox- romycin; only Pasteurella pneumotropica was susceptible to
acin, oxytetracycline, polymyxin‐B, ticarcillin, tobramycin, erythromycin. All five (100%) Pasteurellaceae were resis-
and trimethoprim‐sulfamethoxazole (Table 5). Because no tant to trimethoprim‐sulfamethoxazole, and all five (100%)
Pasteurellaceae were resistant to Moxifloxacin. The five
representative Pasteurellaceae were susceptible to all other
T A B L E 2   Results for Schirmer tear test‐II (STT‐II), phenol red
thread test (PRTT), intraocular pressure (IOP), fluorescein stain and
antibiotic agents tested.
rose bengal stain test performed on all haired guinea pigs and Skinny
pigs

Mean (SD): n = no. Haired guinea Skinny pigs


4  |  DISCUSSION
of guinea pigs pigs (n = 10) (n = 10) P value
To our knowledge, this is the first study that has provided
STT 1.00 (1.18) 3.45 (1.76) 0.0018*  information regarding ophthalmic examination findings and
PRTT 13.15 (3.31) 13.85 (5.72) 0.7635 conjunctival microbiology in systemically healthy Skinny
IOP 16.45 (1.34) 17.90 (2.04) 0.0766 pigs. The group of Skinny pigs tested had significantly more
Fluorescein stain 30% (n = 3) 40% (n = 4) 0.6831 Pasteurellaceae‐associated conjunctivitis than the haired
positive guinea pigs in this study. This study also revealed that the tear
Rose Bengal positive 40% (n = 4) 90% (n = 9) 0.0984 production evaluated by STT‐II and the presence of mucopu-
*Indicates statistically significant difference between haired and Skinny guinea
rulent discharge was significantly lower in haired guinea pigs
pigs at 0.05 level. when compared to Skinny pigs. The increased tear production

T A B L E 3   Results of bacteria cultured from the conjunctiva of haired and Skinny pigs

Percentage (n = no. of guinea


pigs) Haired (n = 10) Skinny Pig (n = 10) FET P‐value FDR Adjusted P
Pasteurellaceae 20% (n = 2) 100% (n = 10) 0.001 0.011* 
Strep. Alpha hemolytic 50% (n = 5) 80% (n = 8) 0.350 0.632
Strep. Bet hemolytic 70% (n = 7) 30% (n = 3) 0.179 0.561
Strep. Agalactiae 0% (n = 0) 30% (n = 3) 0.211 0.561
Strep. Pneumoniae 0% (n = 0) 20% (n = 2) 0.474 0.632
Staph. Coagulase negative 40% (n = 4) 40% (n = 4) 1.000 1.000
Staph. Aureus 0% (n = 0) 20% (n = 2) 0.474 0.632
Trueperella pyogenes 0% (n = 0) 20% (n = 2) 0.474 0.632
Samonella 0% (n = 0) 10% (n = 1) 1.000 1.000
Bacillus sp 0% (n = 0) 10% (n = 1) 1.000 1.000
E‐coli 30% (n = 3) 0% (n = 0) 0.211 0.561
Micrococcus 50% (n = 5) 0% (n = 0) 0.033 0.173
Enrococcus 20% (n = 2) 0% (n = 0) 0.474 0.632
Corynebacterium 70% (n = 7) 0% (n = 0) 0.003 0.025* 
Gram negative non‐fermenter 10% (n = 1) 0% (n = 0) 1.000 1.000
No growth 20% (n = 2) 0% (n = 0) 0.474 0.632
*Indicates statistical significance using a 0.05 significance level.
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8       WU et al

T A B L E 4   Results of Pasteurellaceae
Haired guinea pig Skinny pig eyes
organisms detected and the number of eye(s)
Pasteurellaceae isolated eyes (n) (n) Total
that had a positive bacterial culture for each
Pasteurella multocida 0 14 14 subspecies (n = number of eyes)
Pasteurellaceae (unspeciated) 2 3 5
Necropsobacter spp. 0 3 3
Mannheimia caviae 1 0 1
Pasteurella pneumotropica 0 1 1
Total 3 21 24

T A B L E 5   Results of antimicrobial susceptibility testing of five Pasteurellaceae organisms obtained from conjunctival swab specimens

Antibiotic susceptibility Pasteurella Pasteurellaceae Necropsobacter Pasteurella Mannheimia


tested for five Pasteurellaceae multocida (unspeciated) SP10 species pneumotropica caviae
organisms SP6 (OD) (OS) SP2 (OD) SP6 (OS) HP9 (OD)
Bacitracin NA NA NA NA NA
Ceftiofur S S S S S
Chloramphenicol S S S S S
Ciprofloxacin S S S S S
Doxycycline S S S S S
Erythromycin R R R S R
Gentamicin S S S S S
Moxifloxacin NS NS NS NS NS
Neomycin S S S S S
Ofloxacin S S S S S
Oxytetracycline S S S S S
Polymyxin B NA NA NA NA NA
Ticarcillin S S S S S
Tobramycin S S S S S
Trimethoprim Sulfamethoxazole NS NS NS NS NS
Abbreviations: HP, Haired guinea pig; NA, Not interpreted; NS, Not sensitive; OD, Right eye; OS, Left eye; R, Resistance; S, Sensitive; SP, Skinny pig.

and mucopurulent discharge in the Skinny pigs could be due cornea and conjunctiva. Trichiasis that was detected in four
to the fact that the Skinny pigs had Pasteurellaceae conjunc- eyes of three Skinny pigs was likely a result of curly wired
tivitis. Although the presence of other ocular abnormalities, hair growing from hair follicles located temporal to the lat-
such as trichiasis, keratitis with corneal vascularization, and eral canthus (Figure 5). Two out of four eyes with trichia-
foreign body, were not significantly more common in Skinny sis had concurrent corneal ulcerations, one of which also
pigs, the Skinny pigs were over‐represented in the small had the presence of foreign material on the corneal surface.
sample. Although both trichiasis and foreign bodies were not found
A single superficial blood vessel was noted in one Skinny in haired breeds in this study, ocular irritation as a result of
pig eye that was diagnosed with non‐ulcerative keratitis and trichiasis or plant material has been documented in haired
corneal vascularization but with absence of foreign body. guinea pig breeds, the former being more of a concern in
The foreign bodies found in the Skinny pigs adhered to the the Texel breed.12 The Texel guinea pig has curly long hair
cornea or were embedded within the conjunctival surface and all haired guinea pigs enrolled in this study did not
appeared to resemble hay or other plant material; two eyes appear to have a coat texture similar to the Texel breed.
of Skinny pigs with foreign body presence were also diag- This study by Williams (2010) found that the most com-
nosed with concurrent corneal ulcerations. It was noted on mon ocular abnormality in guinea pigs were lenticular ab-
the ophthalmic examination that Skinny pigs' eyelids were normalities including cataracts and nuclear sclerosis.12 No
more elastic and easier to open than the haired guinea pigs. lenticular abnormalities were found in this current study.
We therefore speculate that eyelid function could predis- Nuclear sclerosis was not expected to be found due to the
pose Skinny pigs to adherence of foreign material to their young population of guinea pigs. Cataracts that were found
WU et al   
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   9

in Williams' study of 1000 guinea pigs suggested that cat- establish a comparison between different tonometer devices.
aracts may develop later in life since all stages of cataracts IOPs in adult guinea pigs have been reported for both “p”
were not detected in any of the 20 study guinea pigs in this (unspecified species), and “d” (dog) settings and show great
study. variation in results.1,21,22 Micromanometry reference values
Similar to previous reports, all guinea pigs in this study have been documented in guinea pigs but the use of seda-
had a higher PRTT value in comparison to the STT‐II value.14 tion for this invasive technique precludes direct comparison
According to the literature, it is unknown if this is due to a with results obtained via rebound or applanation tonometry
difference in the ability for the STT strip versus the PRTT in non‐sedated patient.23
thread to absorb tears in guinea pigs.14 Considering the size Circadian rhythm affects IOP fluctuation in many animal
of the STT strip (the strip is very large compared to the size species including the guinea pig. In a study documenting 24‐
of the guinea pig palpebral fissures as pictured in Figure 2A), hour measurements of IOP in guinea pigs, the results demon-
the low STT‐II values in guinea pigs as well as the fact that strated significantly lower IOP during the light period (07.00
there was no significant difference found for PRTT values to 19.00) when compared to IOP measurements during the
between the two groups, PRTT appears to be the preferred dark phase (20.00 to 06.00).21 In our study, all measurements
tear measurement test in guinea pigs.14 Improved accuracy of for haired guinea pigs and 5 out of 10 Skinny pigs were ob-
PRTT may be achieved if the method was either performed tained in the evening and the remaining five Skinny pigs were
prior to STT or a longer period of time was permitted be- obtained in the morning. Although, most measurements (7
tween tests to ensure re‐stabilization of the tear film.13,14 This out of 10 (70%) haired guinea pigs, 7 out of 10 (70%) Skinny
observation can especially be seen on the Skinny pigs PRTT pigs) were obtained within the light period between 0700 to
results that are similar to the haired guinea pigs whereas they 1900, further studies should attempt to obtain measurements
have a significant higher STT‐II result compared to haired of all animals within a narrow time period to allow for a
guinea pigs. more accurate comparison of IOP values between individual
It has been documented that guinea pigs have low cor- animals.
neal sensation, and frequency of blink compared to many Microbiological analysis in this study showed that the
domestic animals.14,18,19 Keratoconjunctivitis sicca (KCS) as most common conjunctival isolates from haired guinea
evidenced by quantitative tear film deficiency in combina- pigs included Corynebacterium spp. and alpha‐hemolytic
tion with consistent ocular pathology is infrequently docu- Streptococcus spp. These results are similar to a previous
mented in this species.12,20 The presence of low quantity of study by Costa and colleagues from 2008.13 The presence of
tears alone without concurrent clinical signs of KCS warrants bacterial growth in the majority of eyes (18 out of 20, 90%) of
further investigation into the tear quantity and quality of the haired guinea pigs including animals with no clinical ocular
lipid and mucin layer.12,14 The statistically significant differ- abnormalities suggest that these organisms are likely part of
ence in STT‐II between haired guinea pigs and Skinny pigs the normal conjunctival flora. In contrast, the most common
suggests that comparison of corneal touch threshold (CTT) bacteria found in the Skinny pig population were organisms
and frequency of eye blink between the two populations may belonging to the family, Pasteurellaceae, present in 10 out
be considered in a future study. of 10 (100%) Skinny pigs (19 out of 20 eyes, 95%), which
A study by Cairo and colleagues from 2018 comparing is significantly higher when compared to 2 out of 10 (20%)
tonometry techniques in guinea pigs revealed that rebound guinea pigs (2 out of 20 eyes, 10%). Some members of the
tonometry with the TonoVet was preferred when compared to Pasteurellaceae are considered pathogenic in guinea pigs.
applanation tonometry using the Tonopet Vet.1 In our study, Unclassified Pasteurellaceae isolates have been identified in
the newest tonometer, TonoVet PLUS appeared to be well a case of putrid conjunctivitis but also in an epidemic out-
tolerated and provided rapid results in all guinea pigs. To our break of conjunctivitis in a large group of guinea pigs.24,25
knowledge, this is the first study that provides IOP reference Boot and colleagues (1983) concluded that the Pasteurella
values using the TonoVet PLUS (rabbit setting) in guinea and Actinobacillus genera belonging to the Pasteurellaceae
pigs. The mean ± standard deviation (SD) for TonoVet PLUS must be considered as potentially pathogenic microorganisms
values in our study is higher than the mean ± SD TonoVet for guinea pigs.26 The statistically higher STT‐II and preva-
values in the “d” setting (TonoVet PLUS: Haired guinea lence of mucopurulent discharge indicating ocular discom-
pigs:16.45 ± 1.34 mm Hg; Skinny pigs 17.9 ± 2.04 mm Hg, fort in our Skinny pigs with a higher representation of ocular
versus TonoVet: Guinea pigs: 8.53  ±  1.28  mm  Hg).1 abnormalities (chemosis/hyperemia of the conjunctiva, tri-
Therefore, tonometry with repeated IOP measurements chiasis, keratitis with corneal vascularization, foreign body)
should be performed with the same tonometer and on the compared to haired guinea pigs suggests that the commonly
same setting to provide the most consistent and accurate re- isolated Pasteurellaceae in Skinny pigs may be considered
sults. Tonometers with specific calibrations for the guinea pathogenic. Only 2 out of 20 eyes of the haired guinea pigs
pig species are currently unavailable and may be warranted to were positive for Pasteurellaceae (one was an unspeciated
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10       WU et al

Pasteurellaceae, and the other was Mannheimia caviae) and conjunctivitis in this study and was the antibiotic choice
both eyes showed ocular abnormalities. Both haired guinea for treatment of the affected animals. The presence of
pigs were diagnosed with corneal ulceration, one with con- Chlamydia caviae or Bordetella species, both known to
current conjunctivitis and the second with corneal fibrosis cause conjunctivitis in guinea pigs13,27 were not identified
suggesting previous corneal pathology. A total of 15 differ- in this study group of guinea pigs. Should Chlamydia be
ent bacteria were identified in our study, with likely vari- detected or suspected, topical tetracycline ointment or oral
able opportunistic potential as keratitis pathogens, with doxycycline may be considered a reasonable treatment
Pasteurellaceae being the most notable. Conjunctival cytol- option.28 Guinea pigs with conjunctivitis as a result of
ogy was not performed in this study but has an important role Bordetella bronchiseptica infection often develop concur-
in confirming the presence of bacteria and their association rent respiratory and systemic signs of illness necessitating
with leukocytes, aiding initial identification of bacteria and supportive therapy as well as systemic antibiotic therapy
guiding interpretation of subsequent microbiology data for based on culture and susceptibility results.29 Other differ-
clinical significance. Chlamydia caviae and Bordetella spe- ential diagnoses for conjunctivitis in guinea pigs include
cies are known to cause conjunctivitis in guinea pigs.13,27 non‐infectious causes such as vitamin C deficiency, which
Bordetella species, if present, could have been identified is a potentially severe condition in this species.28
by routine bacterial culture methods employed in this study. Limitations of this study include a small sample size and
Detection of Chlamydia species would require cytologic only intact males under 6  months of age were evaluated.
identification of elementary or reticulate bodies within con- Therefore caution must be taken when using statistical results
junctival epithelial cells along with Polymerase chain reac- from this study to make an inference on the overall guinea pig
tion (PCR) as a complementary tool when organisms are not population.
observed and for accurate classification of the Chlamydia To our knowledge, specific genetic information or the di-
species.27 Future microbiological studies of Skinny pigs agnosis of ectodermal dysplasia has not been determined in
would ideally include conjunctival sample collection using Skinny pigs. A study of Tabby mice, the model for human
separate swabs to allow for cytology, bacterial culture and EDA, demonstrated characteristic abnormalities in the ocular
microbiome analysis. A theory regarding Skinny pigs being surface including neovascularization, keratitis, ulceration and
more likely to be immunocompromised than guinea pigs is the lack of meibomian glands.8 The former three ocular abnor-
circulating the exotic veterinary community but to the au- malities were identified in at least one eye of the Skinny pigs
thors' knowledge, the theory has not been verified with evi- in this study. Although all guinea pigs appeared to have meibo-
dence‐based studies. This study showed that younger Skinny mian gland openings on each eyelid margin, glandular presence
pigs could have an increased risk of Pasteurellaceae‐asso- cannot be determined without histopathology. Further studies
ciated conjunctivitis when compared to haired guinea pigs comparing diagnostic tests and ophthalmic examination find-
of similar age but more studies regarding the Skinny pig's ings in a larger population of Skinny pigs and specific purebred
immune system is needed before a correlation between im- haired guinea pigs of various ages are warranted to expand on
munocompromised and Pasteurellaceae conjunctivitis can be information gained from this study. Future knowledge into the
made in young Skinny pigs. genetics and histological findings from adnexa, globe and skin
Antimicrobial susceptibility testing for the five of Skinny pigs will provide clinicians with a better understand-
Pasteurellaceae organisms performed on select cultures ing of their ocular and dermatological diseases as well as valu-
revealed that topical erythromycin, moxifloxacin, and able information for continued translational research.
trimethoprim‐sulfamethoxazole may not be an appropri-
ate treatment choice for ocular surface disease in guinea
pigs infected with Pasteurellaceae organisms. Although 5  |  CONCLUSION
potentiated sulfonamide is one of few systemic antibiot-
ics approved for use in guinea pigs,20 this antibiotic may The significantly higher STT‐II values, higher prevalence of
also not be an appropriate first‐line medication to treat mucopurulent discharge and presence of potentially patho-
conjunctivitis since AST (antimicrobial susceptibility test) genic Pasteurellaceae in the conjunctiva suggests that young
results reveal that all five (100%) Pasteurellaceae organ- Skinny pigs are at higher risk of conjunctivitis and may war-
isms were resistant to trimethoprim‐sulfamethoxazole. rant microbiological testing to guide treatment. In vitro re-
All isolates were considered susceptible to polymyxin‐B, sults identified Oxytetracycline, tobramycin, ciprofloxacin
and all five Pasteurellaceae organisms were susceptible to and ofloxacin as topical antibiotics that may be effective
oxytetracycline, doxycycline, tobramycin, ciprofloxacin against Pasteurellaceae‐associated conjunctivitis in Skinny
and ofloxacin. Terramycin (oxytetracycline and polymyx- pigs. The study also documents the reliability and simplicity
in‐B) ophthalmic ointment would therefore be an accepted of rebound tonometry using the TonoVet PLUS for obtaining
treatment option for Skinny pigs with Pasteurellaceae IOP measurements in guinea pigs.
WU et al   
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