Wu 2019
Wu 2019
Wu 2019
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Revised: 6 August 2019
| Accepted: 23 August 2019
DOI: 10.1111/vop.12709
ORIGINAL ARTICLE
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.
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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
(A) (B)
(C)
(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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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.
3.2.3 | 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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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)
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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
T A B L E 3 Results of bacteria cultured from the conjunctiva of haired and Skinny pigs
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
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
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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.
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ACKNOWLEDGMENT 15. Katz RS, Henkind P, Weitzman ED. The circadian rhythm of
the intraocular pressure in the New Zealand White rabbit. Invest
The authors would like to thank An‐vision for providing Ophthalmol Vis Sci. 1975 (abstract);14:775‐780.
items required for all diagnostic tests. 16. Del Sole MJ, Sande PH, Bernades JM, et al. Circadian rhythm of
intraocular pressure in cats. Vet Ophthalmol. 2007;10:155‐161.
17. Kaye S, Tuft S, Neal T, et al. Bacterial susceptibility to topical
ORCID antimicrobials and clinical outcome in bacterial keratitis. Invest
Michala Linde Henriksen https://orcid. Ophthalmol Vis Sci. 2010;51:362‐368.
18. Good KL, Maggs DJ, Hollingsworth SR, et al. Corneal sensitivity
org/0000-0002-7901-7790
in dogs with Diabetes mellitus. Am J Vet Res. 2003;64:7‐11.
19. Gum GG, Mackay E. Physiology of the eye. In Gelatt K, Gilger
B, Kern T, eds. Veterinary Ophthalmology. Hoboken, NJ: Wiley
R E F E R E NC E S
Blackwell. 5th edn. 2013;3:171‐207.
1. Cairo M, Pena MT, Rios J, et al. Assessment of Intraocular pres- 20. Asadi M, Rajaei SM, Golabdar S. Effects of oral administration
sure with applanation and rebound tonometry in guinea pigs of dif- of trimethoprim‐sulfamethoxazole on tear production in clinically
ferent ages. J Exotic Pet Med. 2018;27:25‐33. normal guinea pigs. Vet Ophthalmol. 2016;19(5):414‐417.
2. Quesenberry KE, Donnelly TM, Mans C. Biology, husbandry and 21. Mood AM, Mehdi‐Rajaei S, Sadjadi R, et al. Twenty‐four hour
clinical techniques of guinea pigs and chinchillas. In: Quesenberry measurement of intraocular pressure in guinea pigs (Cavia porcel-
KE, Carpenter J, eds. Ferrets, Rabbits and Rodents Clinical Medicine lus). J Am Assoc Lab Anim Sci. 2016;55:95‐97.
and Surgery. St. Louis, Missouri; Elsevier Saunders; 2012:279‐294. 22. Rajaei SM, Mood MA, Sadjadi R, et al. Intraocular pressure, tear
3. Donnelly TM, Brown CJ. Guinea pig and Chinchilla care and hus- production, and ocular echobiometry in guinea pigs (Cavia porcel-
bandry. Vet Clin North Am Exot Animal Pract. 2004;7:351‐373. lus). J Am Assoc Lab Anim Sci. 2016;55:475‐479.
4. Sueki H, Kligman AM. Cutaneous toxicity of chemical irritants on 23. Taskintuna I, Banker AS, Rao NA, et al. An animal model for cido-
hairless Guinea Pigs. J Dermatol. 2003;30(12):859‐870. fovir (HPMPC) toxicity: intraocular pressure and histopathologic
5. Sueki H, Gammel C, Kudoh K, et al. Hairless guinea pig skin: an- effects. Exp Eye Res. 1997;64(5):795‐806.
atomical basis for studies of cutaneous biology. Eur J Dermatol. 24. Mannheim W, Pohl S, Stenzel W. Unclassified pasteurella‐like
2000;10(5):357‐364. organisms isolated from guinea pigs (author’s transl.). Zentralbl
6. Mecklenburg L. An overview of congenital alopecia in domestic Bakteriol Orig A. 1978;241:329‐336.
animals. Eur Soc Vet Dermatol. 2006;17(6):393‐410. 25. Christensen H, Bojesen AM, Bisgaard M. Mannheimia caviae
7. Keklikci U, Yavuz I, Tunik S, et al. Ophthalmic manifestations in sp. nov., isolated from epidemic conjunctivitis and otitis media in
humans with Ecotodermal Dysplasia Syndromes. Adv Clin Exp guinea pigs. Int J Syst Evol Microbiol. 2011;61:1699‐1704.
Med. 2014;23(4):605‐610. 26. Boot R, Oosterom J, Walvoort HC. Recovery of members of the
8. Cui CY, Smith JA, Schlessinger D, et al. X‐linked anhidrotic ecto- Pasteuerella – Actinobacillus group from guinea pigs. Lab Anim.
dermal dysplasia disruption yields a mouse model for ocular sur- 1983;17:285‐289.
face disease and resultant blindness. Am J Path. 2005;167:89‐95. 27. Strik NI, Alleman AR, Wellehan JF. Conjunctival swab
9. Cook CS. Embryology and Congenital Malformations. In: Gelatt cytology from a guinea pig: it's elementary!. Vet Clin Pathol.
K, Gilger B, Kern T, eds. Veterinary Ophthalmology. Hoboken, 2005;34(2):169‐71.
NJ: Wiley Blackwell. 5th edn. 2013;1: 3‐38. 28. Williams DL. The guinea pig eye. Ophthalmology of Exotic Pets.
10. Wiener DJ, Gurtner C, Panacova L, et al. Clinical and histologi- Hoboken, NJ: Wiley Blackwell. 2013;5:56‐72.
cal characterization of hair coat and glandular tissue of Chinese 29. Gallego M. Bordetella bronchiseptica in pet guinea pigs? A review
crested dogs. Vet Dermatol. 2013;24(2):274‐e62. of the literature. SOJ Vet Sci. 2017;3(1):1‐3.
11. Leeb T. Animal models of Ectodermal Dysplasia. Head Face Med.
2012;8(Suppl 1):I9.
12. Williams DL, Sullivan A. Ocular disease in the guinea pig How to cite this article: Wu D, de Linde Henriksen
(Cavia porcellus): a survey of 1000 animals. Vet Ophthalmol. M, Grant K, Lyakhova T, Sharp JL, Daniels JB.
2010;13(Suppl 1):54‐62. Ocular findings and selected ophthalmic diagnostic
13. Costa M, Stiles J, Krohne S, et al. Results of diagnostic oph- tests in a group of young commercially available
thalmic testing in healthy guinea pigs. J Am Vet Assoc. Guinea and Skinny pigs (Cavia porcellus). Vet
2008;232(12):1825‐1833.
Ophthalmol. 2019;00:1–11. https://doi.org/10.1111/
14. Trost K, Skalicky M, Nell B. Schirmer tear test, phenol red thread
tear test, eye blink frequency and corneal sensitivity in the guinea
vop.12709
pig. Vet Ophthalmol. 2007;10(3):143‐146.