Tear meniscometry test in wild animals

Teste de meniscometria lacrimal em animais silvestres

Arianne Pontes Oriá Ana Cláudia Santos Raposo Vinícius José da Silva Cardoso de Brito Nayone Lima Lantyer Cordeiro de Araújo Maria Madalena Souza Oliveira Isaac Manoel Barros Albuquerque About the authors

ABSTRACT:

This study aimed to describe strip meniscometry test values for Amazona aestiva (turquoise-fronted amazon), Ara ararauna (blue-and-yellow macaw) and Caiman latirostris (broad-snouted caiman). Twenty-one Amazona aestiva and 11 Ara ararauna, healthy, adults of unknown sex, and 37 healthy adult Caiman latirostris (27 males and 10 females), were used in this investigation. All animals were manually restrained and I-Tear® Test strip was inserted for 5 s at the edge of the lower tear meniscus, without touching the eyelid or ocular surface, immediately followed by measurement (millimeter per 5 seconds). No differences were reported between left and right eyes for Amazona aestiva (P = 0.824), Ara ararauna (P = 0.262) and Caiman latirostris (P = 0.679). Median and confidence interval were 2.0 (2.25-3.56) mm/5s for Amazona aestiva, 3.0 (2.93-4.15) mm/5s for Ara ararauna and 3.0 (2.55-4.90) mm/5 s for Caiman latirostris. These values for strip meniscometry tear test can be used as parameters for each species and may be helpful for diagnosis and treatment of tear-production disorders in birds and reptiles.

Key words:
bird; strip meniscometry tube; reptile; tear meniscus; tear production

RESUMO:

O objetivo deste estudo foi descrever os valores do teste de meniscometria lacrimal para Amazona aestiva (papagaio-verdadeiro), Ara ararauna (arara-canindé) e Caiman latirostris (jacaré-de-papo-amarelo). Vinte e um Amazona aestiva, 11 Ara ararauna adultos, de sexo desconhecido, e 37 Caiman latirostris adultos (27 machos e 10 fêmeas), foram utilizados nesta investigação. Todos os animais foram contidos manualmente e uma tira do I-Tear® test foi inserida por 5 segundos na borda do menisco inferior, sem tocar a pálpebra ou a superfície ocular, e imediatamente mensurada (milímetro por 5 segundos). Não foram encontradas diferenças entre os olhos esquerdos e direitos para Amazona aestiva (P = 0,824), Ara ararauna (P = 0,262) e Caiman latirostris (P = 0,679). Mediana e intervalo de confiança foram de 2,0 (2,25-3,56) mm/5 s para Amazona aestiva, 3,0 (2,93-4,15) mm/5 s para Ara ararauna e 3,0 (2,55-4,90) mm/5 s para Caiman latirostris. Estes valores para o teste de meniscometria podem ser utilizados como parâmetros para estas espécies e podem ser úteis para diagnosticar e tratar distúrbios de produção lacrimal em aves e répteis.

Palavras-chave:
ave; meniscometria; menisco lacrimal; produção de lágrima; réptil

INTRODUCTION:

The corneal and scleral surface are covered by the tear film which possess a protective function and nutritional properties for maintenance of ocular health (ROLANDO & ZIERHUT, 2001ROLANDO, M.; ZIERHUT, M. The ocular surface and tear film and their dysfunction in dry eye disease. Survey of Ophthalmology, v.45, n.2, p.S203-S210, 2001. Available from: <Available from: http://dx.doi.org/10.1016/S0039-6257(00)00203-4 >. Accessed: Aug. 30, 2018. doi: 10.1016/S0039-6257(00)00203-4.
http://dx.doi.org/10.1016/S0039-6257(00)...
). The eyelid blinking spreads the tear fluid over the ocular surface, inferior and superior meniscus, and conjunctival sac (TIFFANY, 2008TIFFANY, J.M. The normal tear film. Developments in Ophthalmology, v.41, p.1-20, 2008. Available from: <Available from: http://dx.doi.org/10.1159/000131066 >. Accessed: Aug. 17, 2018. doi: 10.1159/000131066.
http://dx.doi.org/10.1159/000131066...
). Thus, changes in tear turnover or production may result in changes in distribution and induce ophthalmopathies (ROLANDO & ZIERHUT, 2001ROLANDO, M.; ZIERHUT, M. The ocular surface and tear film and their dysfunction in dry eye disease. Survey of Ophthalmology, v.45, n.2, p.S203-S210, 2001. Available from: <Available from: http://dx.doi.org/10.1016/S0039-6257(00)00203-4 >. Accessed: Aug. 30, 2018. doi: 10.1016/S0039-6257(00)00203-4.
http://dx.doi.org/10.1016/S0039-6257(00)...
). Establishment of lacrimal production values is an important tool for routine semiotechnique, and for wild animals Schirmer tear test (STT), endodontic absorbent paper point tear test (EAPPTT) and phenol red thread tear test (PRTT) can be used (ORIÁ et al., 2013aORIÁ, A.P.; et al. Ophthalmic diagnostic tests, orbital anatomy, and adnexal histology of the broad-snouted caiman (Caiman latirostris). Veterinary Ophthalmology , v.18, n.1, p.30-39, 2013a. Available from: <Available from: http://dx.doi.org/10.1111/vop.12115 >. Accessed: Aug. 23, 2018. doi: 10.1111/vop.12115.
http://dx.doi.org/10.1111/vop.12115...
, 2013bORIÁ, A.P.; et al. Conjunctival flora, Schirmer’s tear test, intraocular pressure, and conjunctival cytology in neotropical primates from Salvador, Brazil. Journal of Medicine Primatology, v.42, n.6, p.287-292, 2013b. Available from: <Available from: http://dx.doi.org/10.1111/jmp.12059 >. Accessed: Aug. 15, 2018. doi: 10.1111/jmp.12059.
http://dx.doi.org/10.1111/jmp.12059...
; MONÇÃO-SILVA et al., 2016aMONÇÃO-SILVA, R.; et al. Ophthalmic diagnostic tests in parrots (Amazona amazônica) and (Amazona aestiva). Journal of Exotic Pet Medicine, v.25, n.3, p.186-193, 2016a. Available from: <Available from: http://dx.doi.org/10.1053/j.jepm.2016.05.002 >. Accessed: Aug. 23, 2018. doi: 10.1053/j.jepm.2016.05.002.
http://dx.doi.org/10.1053/j.jepm.2016.05...
, 2016bMONÇÃO-SILVA, R.M.; et al. Ophthalmic parameters of Blue-and-yellow Macaws (Ara ararauna) and Lear’s Macaws (Anodorhynchus leari). Avian Biology Research, v.9, n.4, p.240-249, 2016b. Available from: <Available from: http://dx.doi.org/10.3184/175815516X14725499175746 >. Accessed: Aug. 23, 2018. doi: 10.3184/175815516X14725499175746.
http://dx.doi.org/10.3184/175815516X1472...
; FALCÃO et al., 2017aFALCÃO, M.S.A.; et al. Reference values for selected ophthalmic tests of the blue-and-yellow macaw (Ara ararauna). Pesquisa Veterinária Brasileira, v.37, n.4, p.389-394, 2017a. Available from: <Available from: http://dx.doi.org/10.1590/S0100-736X2017000400014 >. Accessed: Sep. 07, 2018. doi: 10.1590/S0100-736X2017000400014.
http://dx.doi.org/10.1590/S0100-736X2017...
, 2017bFALCÃO, M.S.A.; et al. Modified Schirmer tear test and rebound tonometry in bluefronted Amazon parrot (Amazona aestiva). Pesquisa Veterinária Brasileira, v.37, n.8, p.871-873, 2017b. Available from: <Available from: http://dx.doi.org/10.1590/S0100-736X2017000800015 >. Accessed: Sep. 07, 2018. doi: 10.1590/S0100-736X2017000800015.
http://dx.doi.org/10.1590/S0100-736X2017...
). These evaluations are similar once the test strips are inserted in the conjunctival sac, for basal and reflex tear quantification, without anesthetic eye drops (TROST et al., 2007TROST, K.; et al. Schirmer tear test, phenol red thread tear test, eye blink frequency and corneal sensitivity in the guinea pig. Veterinary Ophthalmology , v.10, n.3, p.143-146, 2007. Available from: <Available from: http://dx.doi.org/10.1111/j.1463-5224.2007.00521.x >. Accessed: Sep. 07, 2018. doi: 10.1111/j.1463-5224.2007.00521.x.
http://dx.doi.org/10.1111/j.1463-5224.20...
). However, studies estimate that the region of tear meniscus may contain up to 90% of the total volume of tear fluid in humans (SHEN et al., 2008SHEN, M; et al. Diurnal Variation of Upper and Lower Tear Menisci. American Journal of Ophthalmology, v.145, n.5, p.801- 806, 2008. Available from: <Available from: https://doi.org/10.1016/j.ajo.2007.12.024 >. Accessed: Apr. 09, 2019. doi: 10.1016/j.ajo.2007.12.024.
https://doi.org/10.1016/j.ajo.2007.12.02...
), and because of this, tear meniscometry test may complement tear production evaluation in wild animals. Different methods of tear meniscus quantification have been reported for humans, including evaluations using optical coherence tomography, but high cost limits their use (SHINZAWA et al., 2018SHINZAWA, M.; et al. Application of CASIA SS-1000 optical coherence tomography tear meniscus imaging in testing the efficacy of new strip meniscometry in dry eye diagnosis. Eye & Contact Lens, 2018. Available from: <Available from: http://dx.doi.org/10.1097/ICL.0000000000000312 >. Accessed: Aug. 17, 2018. doi: 10.1097/ICL.0000000000000312.
http://dx.doi.org/10.1097/ICL.0000000000...
).

The strip meniscometry tube (SMT) evaluates the tear volume present in the palpebral meniscus rapidly and non-invasively (DOGRU et al., 2006DOGRU, M.; et al. Strip meniscometry: a new and simple method of tear meniscus evaluation. Investigative Ophthalmology & Visual Science, v.47, n.5, p.1895-1901, 2006. Available from: <Available from: http://dx.doi.org/10.1167/iovs.05-0802 >. Accessed: Aug. 15, 2018. doi: 10.1167/iovs.05-0802.
http://dx.doi.org/10.1167/iovs.05-0802...
; IBRAHIM et al., 2011IBRAHIM, O.M.; et al. The efficacy, sensitivity, and specificity of strip meniscometry in conjunction with tear function tests in the assessment of tear meniscus. Investigative Ophthalmology & Visual Science, v.52, p.2194-2198, 2011. Available from: <Available from: http://dx.doi.org/10.1167/iovs.10-5986 >. Accessed: Aug. 23, 2018. doi: 10.1167/iovs.10-5986.
http://dx.doi.org/10.1167/iovs.10-5986...
; KAZAMA et al., 2014KAZAMA, Y.; et al. A novel method of lacrimal function testing: strip meniscometry. The Globe - Newsletter of the International Society ofVeterinary Ophthalmology , p.5-6, jul. 2014. Available from: <Available from: http://isvo.info/wp-content/uploads/2014/12/Issue-Summer-2014.pdf >. Accessed: Apr. 06, 2019.
http://isvo.info/wp-content/uploads/2014...
; RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
) and these technical features are important for wild animals, once the physically restraining time must be fast (MARCO et al., 2006MARCO, I.; et al. Capture myopathy in little bustards after trapping and marking. Journal of Wildlife Diseases, v.42, n.4, p.889-891, 2006. Available from: <Available from: http://dx.doi.org/10.7589/0090-3558-42.4.889 >. Accessed: Aug. 23, 2018. doi: 10.7589/0090-3558-42.4.889.
http://dx.doi.org/10.7589/0090-3558-42.4...
). The use of SMTs has been reported for some domestic species, such as dogs, cats and rabbits (KAZAMA et al., 2014KAZAMA, Y.; et al. A novel method of lacrimal function testing: strip meniscometry. The Globe - Newsletter of the International Society ofVeterinary Ophthalmology , p.5-6, jul. 2014. Available from: <Available from: http://isvo.info/wp-content/uploads/2014/12/Issue-Summer-2014.pdf >. Accessed: Apr. 06, 2019.
http://isvo.info/wp-content/uploads/2014...
; RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
; MIYASAKA et al., 2019MIYASAKA, K.; et al. A novel strip meniscometry method for measuring aqueous tear volume in dogs: Clinical correlations with the Schirmer tear and phenol red thread tests. Veterinary Ophthalmology , p.1-8, 2019. Available from: <Available from: https://doi.org/10.1111/vop.12664 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12664.
https://doi.org/10.1111/vop.12664...
), and studies in non-domestic species are described only in monkeys (RAPOSO et al., 2018RAPOSO, A.C.; et al. Evaluation of lacrimal production, osmolarity, crystallization, proteomic profile, and biochemistry of capuchin monkeys’ tear film. Journal of Medicine Primatology, 2018. Available from: <Available from: http://dx.doi.org/10.1111/jmp.12368 >. Accessed: Aug. 15, 2018. doi: 10.1111/jmp.12368.
http://dx.doi.org/10.1111/jmp.12368...
).

The present study aimed to evaluate and establish reference parameters for SMT tests in Amazona aestiva (turquoise-fronted amazon), Ara ararauna (blue-and-yellow macaw) and Caiman latirostris (broad-snouted caiman), as an ophthalmic semi-technical instrument for measuring lacrimal production in wild animals.

MATERIALS AND METHODS:

Animals

Twenty-one Amazona aestiva (turquoise-fronted amazon) and 11 Ara ararauna (blue-and-yellow macaw) adults, of unknown sex, obtained from the Triage Center of Wild Animals (Salvador, Bahia, Brazil); and 37 adult Caiman latirostris (27 males and 10 females) obtained from a commercial establishment (Mister Cayman LTDA, Maceió, Alagoas, Brazil), were used in this investigation. All animals were manually restrained and the evaluations were performed in the morning hours, with average temperature and humidity of 24.61 ºC and 59.3%, respectively.

Physical and ophthalmic examinations were performed by the technical staff and veterinary ophthalmologist (UFBA). All animals were subjected after SMT, to inspection of the eye and periocular region in normal light for gross abnormalities with a binocular magnifying loupe 3X and a transilluminator. Routine ophthalmic tests, such as fluorescein were also conducted to ensure the health of the eye. Animals that presented any clinical signs of systemic disease or gross abnormalities of the eye or periocular region were excluded.

Meniscometry tear test:

One I-Tear® Test strip (Imed, Dollard-des-Ormeaux, Canada) was carefully inserted in each eye, slightly off-center temporally, for 5 seconds at the edge of the lower tear meniscus, without touching the eyelid or the ocular surface (Figure 1), and then immediately measured, without the use of topical anesthesia, as described by Miyasaka et al. (2019MIYASAKA, K.; et al. A novel strip meniscometry method for measuring aqueous tear volume in dogs: Clinical correlations with the Schirmer tear and phenol red thread tests. Veterinary Ophthalmology , p.1-8, 2019. Available from: <Available from: https://doi.org/10.1111/vop.12664 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12664.
https://doi.org/10.1111/vop.12664...
). The eyelid position remained neutral with no manual eversion. The duration of the test was timed with a stopwatch. Length of the blue stained tear column in the central membrane ditch (in millimeters) was considered as the meniscometry strip value for that eye in mm/5 s.

Figure 1
Tear meniscometry test (I-Tear® Test) in wild animals. (A) Tear meniscometry test strip inserted at the edge of the lower tear meniscus in Ara ararauna. (B) Tear meniscometry test strip inserted at the edge of the lower tear meniscus in Caiman latirostris.

Statistical analysis:

Shapiro-Wilk test was used to assess the normality of the SMT values. Wilcoxon test for paired groups was used to compare results between left and right eyes. For analysis, the SPSS program (version 22.0) was used and the level of significance was set to 5%.

RESULTS AND DISCUSSION:

Evaluation of tear volume is considered important for the diagnosis of diseases such as dry eye (IBRAHIM et al., 2010IBRAHIM, O.M.; et al The application of Visante optical coherence tomography tear meniscus height measurement in the diagnosis of dry eye disease. Ophthalmology, v.117, p.1923-1929, 2010. Available from: <Available from: http://dx.doi.org/10.1016/j.ophtha.2010.01.057 >. Accessed: Aug. 23, 2018. doi: 10.1016/j.ophtha.2010.01.057.
http://dx.doi.org/10.1016/j.ophtha.2010....
, 2011IBRAHIM, O.M.; et al. The efficacy, sensitivity, and specificity of strip meniscometry in conjunction with tear function tests in the assessment of tear meniscus. Investigative Ophthalmology & Visual Science, v.52, p.2194-2198, 2011. Available from: <Available from: http://dx.doi.org/10.1167/iovs.10-5986 >. Accessed: Aug. 23, 2018. doi: 10.1167/iovs.10-5986.
http://dx.doi.org/10.1167/iovs.10-5986...
; KAZAMA et al., 2014KAZAMA, Y.; et al. A novel method of lacrimal function testing: strip meniscometry. The Globe - Newsletter of the International Society ofVeterinary Ophthalmology , p.5-6, jul. 2014. Available from: <Available from: http://isvo.info/wp-content/uploads/2014/12/Issue-Summer-2014.pdf >. Accessed: Apr. 06, 2019.
http://isvo.info/wp-content/uploads/2014...
; RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
; RAPOSO et al., 2018RAPOSO, A.C.; et al. Evaluation of lacrimal production, osmolarity, crystallization, proteomic profile, and biochemistry of capuchin monkeys’ tear film. Journal of Medicine Primatology, 2018. Available from: <Available from: http://dx.doi.org/10.1111/jmp.12368 >. Accessed: Aug. 15, 2018. doi: 10.1111/jmp.12368.
http://dx.doi.org/10.1111/jmp.12368...
; NICHOLS et al., 2004NICHOLS, K.K.; et al. The repeatability of clinical measurements of dry eye. Cornea, v.23, p.272-285, 2004. Available from: <Available from: https://insights.ovid.com/pubmed?pmid=15084861 >. Accessed: Apr. 06, 2019. doi: 10.1097/00003226-200404000-00010.
https://insights.ovid.com/pubmed?pmid=15...
; MARCO et al., 2006MARCO, I.; et al. Capture myopathy in little bustards after trapping and marking. Journal of Wildlife Diseases, v.42, n.4, p.889-891, 2006. Available from: <Available from: http://dx.doi.org/10.7589/0090-3558-42.4.889 >. Accessed: Aug. 23, 2018. doi: 10.7589/0090-3558-42.4.889.
http://dx.doi.org/10.7589/0090-3558-42.4...
). However, invasive methodologies may induce ocular irritation, discomfort or reflex lacrimation (TIFFANY, 2008TIFFANY, J.M. The normal tear film. Developments in Ophthalmology, v.41, p.1-20, 2008. Available from: <Available from: http://dx.doi.org/10.1159/000131066 >. Accessed: Aug. 17, 2018. doi: 10.1159/000131066.
http://dx.doi.org/10.1159/000131066...
; IBRAHIM et al., 2010IBRAHIM, O.M.; et al The application of Visante optical coherence tomography tear meniscus height measurement in the diagnosis of dry eye disease. Ophthalmology, v.117, p.1923-1929, 2010. Available from: <Available from: http://dx.doi.org/10.1016/j.ophtha.2010.01.057 >. Accessed: Aug. 23, 2018. doi: 10.1016/j.ophtha.2010.01.057.
http://dx.doi.org/10.1016/j.ophtha.2010....
). The SMT has been shown effective for measuring tear production, with the use of a single strip for both eyes and it can serve as an alternative method for evaluating tear production (IBRAHIM et al., 2011IBRAHIM, O.M.; et al. The efficacy, sensitivity, and specificity of strip meniscometry in conjunction with tear function tests in the assessment of tear meniscus. Investigative Ophthalmology & Visual Science, v.52, p.2194-2198, 2011. Available from: <Available from: http://dx.doi.org/10.1167/iovs.10-5986 >. Accessed: Aug. 23, 2018. doi: 10.1167/iovs.10-5986.
http://dx.doi.org/10.1167/iovs.10-5986...
; RAJAEI et al., 2017;RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
RAPOSO et al., 2018RAPOSO, A.C.; et al. Evaluation of lacrimal production, osmolarity, crystallization, proteomic profile, and biochemistry of capuchin monkeys’ tear film. Journal of Medicine Primatology, 2018. Available from: <Available from: http://dx.doi.org/10.1111/jmp.12368 >. Accessed: Aug. 15, 2018. doi: 10.1111/jmp.12368.
http://dx.doi.org/10.1111/jmp.12368...
).

The data were not normally distributed according to Shapiro-Wilk test. There were no significant differences between the left and right eyes for Amazona aestiva (P = 0.824), Ara ararauna (P = 0.262) and Caiman latirostris (P = 0.679). Results are shown in table 1.

Table 1
Median and confidence interval (CI) for strip meniscometry tube (SMT) test in Amazona aestiva, Ara ararauna and Caiman latirostris.

The test was more difficult to execute with birds due to the nictitating membrane reflex when the strip approached the inferior eyelid. Sometimes, during the test (strip inserted at the edge of the lower tear meniscus), incursion of the nictitating membrane removed the strip from the site and a rapid increase in tear production was observed. As these changes were not foreseen and could not be avoided, the obtained data were retained in the final result. These behaviors were not observed for Caiman latirostris. Difficulties in the evaluation of tear production in non-collaborative animals are described in other studies, as the use of PRT in birds, also due to incursion of the nictitating membrane (BECKWITH-COHEN et al., 2015BECKWITH-COHEN, B.; et al. Differences in ocular parameters between diurnal and nocturnal raptors. Veterinary Ophthalmology, Oxford, v.18, p.98-105, 2015. Available from: <Available from: https://doi.org/10.1111/vop.12126 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12126.
https://doi.org/10.1111/vop.12126...
; BLISS et al., 2015BLISS, C. D.; et al. Ocular findings and reference values for selected ophthalmic diagnostic tests in the macaroni penguin (Eudyptes chrysolophus) and southern rockhopper penguin (Eudyptes chrysocome). Veterinary Ophthalmology, Oxford, v.18, p.86-93, 2015. Available from: <Available from: https://doi.org/10.1111/vop.12123 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12123.
https://doi.org/10.1111/vop.12123...
; MONÇÃO-SILVA et al., 2016bMONÇÃO-SILVA, R.M.; et al. Ophthalmic parameters of Blue-and-yellow Macaws (Ara ararauna) and Lear’s Macaws (Anodorhynchus leari). Avian Biology Research, v.9, n.4, p.240-249, 2016b. Available from: <Available from: http://dx.doi.org/10.3184/175815516X14725499175746 >. Accessed: Aug. 23, 2018. doi: 10.3184/175815516X14725499175746.
http://dx.doi.org/10.3184/175815516X1472...
). Faster filling of the strip capillary might have been caused by tearing during eyelid incursion, which may be attributed to a renewal in the tear reservoir present in the meniscus (UCHIDA et al., 2007UCHIDA, A.; et al. Noninvasive interference tear meniscometry in dry eye patients with Sjögren Syndrome. American Journal of Ophthalmology, v.144, n.2, p.232-237, 2007. Available from: <Available from: http://dx.doi.org/10.1016/j.ajo.2007.04.006 >. Accessed: Sep. 07, 2018. doi: 10.1016/j.ajo.2007.04.006.
http://dx.doi.org/10.1016/j.ajo.2007.04....
).

The animals constantly moved their heads during the investigation, which made it difficult to perform the test; although, the manipulators had undergone prior training as suggested by IBRAHIM et al. (2011IBRAHIM, O.M.; et al. The efficacy, sensitivity, and specificity of strip meniscometry in conjunction with tear function tests in the assessment of tear meniscus. Investigative Ophthalmology & Visual Science, v.52, p.2194-2198, 2011. Available from: <Available from: http://dx.doi.org/10.1167/iovs.10-5986 >. Accessed: Aug. 23, 2018. doi: 10.1167/iovs.10-5986.
http://dx.doi.org/10.1167/iovs.10-5986...
). RAJAEI et al. (2007)RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
also reported agitation in rabbits and cats during the test, possibly induced by the strip approaching of the animal’s eye.

The median values ​​reported for Amazona aestiva, Ara ararauna and Caiman latirostris for SMT were lower than the averages reported for dogs 9.78 ± 3.68 mm/5 s and 9.66 ± 2.15 mm/5 s (KAZAMA et al., 2014KAZAMA, Y.; et al. A novel method of lacrimal function testing: strip meniscometry. The Globe - Newsletter of the International Society ofVeterinary Ophthalmology , p.5-6, jul. 2014. Available from: <Available from: http://isvo.info/wp-content/uploads/2014/12/Issue-Summer-2014.pdf >. Accessed: Apr. 06, 2019.
http://isvo.info/wp-content/uploads/2014...
; RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
), cats 10.50 ± 0.7 mm/5 s (RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
), rabbits 4.72 ± 1.20 mm/5 s (RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
) and capuchin monkeys (Sapajus sp.) 8.0 ± 1.625 mm/5 s (RAPOSO et al., 2018RAPOSO, A.C.; et al. Evaluation of lacrimal production, osmolarity, crystallization, proteomic profile, and biochemistry of capuchin monkeys’ tear film. Journal of Medicine Primatology, 2018. Available from: <Available from: http://dx.doi.org/10.1111/jmp.12368 >. Accessed: Aug. 15, 2018. doi: 10.1111/jmp.12368.
http://dx.doi.org/10.1111/jmp.12368...
). However, the STT evaluations of tear production for domestic species (RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
) and capuchin monkeys (ORIÁ et al., 2013bORIÁ, A.P.; et al. Conjunctival flora, Schirmer’s tear test, intraocular pressure, and conjunctival cytology in neotropical primates from Salvador, Brazil. Journal of Medicine Primatology, v.42, n.6, p.287-292, 2013b. Available from: <Available from: http://dx.doi.org/10.1111/jmp.12059 >. Accessed: Aug. 15, 2018. doi: 10.1111/jmp.12059.
http://dx.doi.org/10.1111/jmp.12059...
; MONTIANI-FERREIRA et al., 2008MONTIANI-FERREIRA, F.; et al. Reference values for selected ophthalmic diagnostic tests of the capuchin monkey (Cebus apella). Veterinary Ophthalmology , v.11, n.3, p.197-201, 2008. Available from: <Available from: http://dx.doi.org/10.1111/j.1463-5224.2008.00620.x >. Accessed: Aug. 30, 2018. doi: 10.1111/j.1463-5224.2008.00620.x.
http://dx.doi.org/10.1111/j.1463-5224.20...
) are also higher than those reported for the species in the present study (ORIÁ et al., 2013aORIÁ, A.P.; et al. Ophthalmic diagnostic tests, orbital anatomy, and adnexal histology of the broad-snouted caiman (Caiman latirostris). Veterinary Ophthalmology , v.18, n.1, p.30-39, 2013a. Available from: <Available from: http://dx.doi.org/10.1111/vop.12115 >. Accessed: Aug. 23, 2018. doi: 10.1111/vop.12115.
http://dx.doi.org/10.1111/vop.12115...
; FALCÃO et al., 2017aFALCÃO, M.S.A.; et al. Reference values for selected ophthalmic tests of the blue-and-yellow macaw (Ara ararauna). Pesquisa Veterinária Brasileira, v.37, n.4, p.389-394, 2017a. Available from: <Available from: http://dx.doi.org/10.1590/S0100-736X2017000400014 >. Accessed: Sep. 07, 2018. doi: 10.1590/S0100-736X2017000400014.
http://dx.doi.org/10.1590/S0100-736X2017...
, 2017bFALCÃO, M.S.A.; et al. Modified Schirmer tear test and rebound tonometry in bluefronted Amazon parrot (Amazona aestiva). Pesquisa Veterinária Brasileira, v.37, n.8, p.871-873, 2017b. Available from: <Available from: http://dx.doi.org/10.1590/S0100-736X2017000800015 >. Accessed: Sep. 07, 2018. doi: 10.1590/S0100-736X2017000800015.
http://dx.doi.org/10.1590/S0100-736X2017...
). A statistical correlation between positive STT and tear meniscometry test for humans (DOGRU et al., 2006DOGRU, M.; et al. Strip meniscometry: a new and simple method of tear meniscus evaluation. Investigative Ophthalmology & Visual Science, v.47, n.5, p.1895-1901, 2006. Available from: <Available from: http://dx.doi.org/10.1167/iovs.05-0802 >. Accessed: Aug. 15, 2018. doi: 10.1167/iovs.05-0802.
http://dx.doi.org/10.1167/iovs.05-0802...
; IBRAHIM et al., 2010IBRAHIM, O.M.; et al The application of Visante optical coherence tomography tear meniscus height measurement in the diagnosis of dry eye disease. Ophthalmology, v.117, p.1923-1929, 2010. Available from: <Available from: http://dx.doi.org/10.1016/j.ophtha.2010.01.057 >. Accessed: Aug. 23, 2018. doi: 10.1016/j.ophtha.2010.01.057.
http://dx.doi.org/10.1016/j.ophtha.2010....
) and dogs (KAZAMA et al., 2014KAZAMA, Y.; et al. A novel method of lacrimal function testing: strip meniscometry. The Globe - Newsletter of the International Society ofVeterinary Ophthalmology , p.5-6, jul. 2014. Available from: <Available from: http://isvo.info/wp-content/uploads/2014/12/Issue-Summer-2014.pdf >. Accessed: Apr. 06, 2019.
http://isvo.info/wp-content/uploads/2014...
; RAJAEI et al. 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
; MIYASAKA et al., 2019MIYASAKA, K.; et al. A novel strip meniscometry method for measuring aqueous tear volume in dogs: Clinical correlations with the Schirmer tear and phenol red thread tests. Veterinary Ophthalmology , p.1-8, 2019. Available from: <Available from: https://doi.org/10.1111/vop.12664 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12664.
https://doi.org/10.1111/vop.12664...
) has been reported, so it is suggested that the values reported in our study are consistent with those expected for the evaluated species.

In the present study, the obtained median values were lower than other tear production tests placed in the conjunctival sac, including PRT (12.6 ± 2.6 mm/15 s and 19.12 ± 3.14 mm/15 s) and EAPPTT (13.1 ± 1.4 mm/min and 16.74 ± 1.38 mm/min) for Amazona aestiva and Ara ararauna respectively (MONÇÃO-SILVA et al., 2016aMONÇÃO-SILVA, R.; et al. Ophthalmic diagnostic tests in parrots (Amazona amazônica) and (Amazona aestiva). Journal of Exotic Pet Medicine, v.25, n.3, p.186-193, 2016a. Available from: <Available from: http://dx.doi.org/10.1053/j.jepm.2016.05.002 >. Accessed: Aug. 23, 2018. doi: 10.1053/j.jepm.2016.05.002.
http://dx.doi.org/10.1053/j.jepm.2016.05...
, 2016bMONÇÃO-SILVA, R.M.; et al. Ophthalmic parameters of Blue-and-yellow Macaws (Ara ararauna) and Lear’s Macaws (Anodorhynchus leari). Avian Biology Research, v.9, n.4, p.240-249, 2016b. Available from: <Available from: http://dx.doi.org/10.3184/175815516X14725499175746 >. Accessed: Aug. 23, 2018. doi: 10.3184/175815516X14725499175746.
http://dx.doi.org/10.3184/175815516X1472...
). Results for all tests (PRT, EAPPTT and SMT) were always lower for Amazona aestiva than Ara ararauna as well.

Tear production values reported for Caiman latirostris were lower than those observed for EAPPTT (17.1 ± 2.5 mm/min), but are close to those reported for STT (mean 3.4 ± 3.6 mm/min and CI 2.01-4.78 mm/min) (ORIÁ et al., 2013aORIÁ, A.P.; et al. Ophthalmic diagnostic tests, orbital anatomy, and adnexal histology of the broad-snouted caiman (Caiman latirostris). Veterinary Ophthalmology , v.18, n.1, p.30-39, 2013a. Available from: <Available from: http://dx.doi.org/10.1111/vop.12115 >. Accessed: Aug. 23, 2018. doi: 10.1111/vop.12115.
http://dx.doi.org/10.1111/vop.12115...
). Differences in the results among tests can be correlated with factors such as methodology employed or absorption properties of each material (ORIÁ et al., 2013aORIÁ, A.P.; et al. Ophthalmic diagnostic tests, orbital anatomy, and adnexal histology of the broad-snouted caiman (Caiman latirostris). Veterinary Ophthalmology , v.18, n.1, p.30-39, 2013a. Available from: <Available from: http://dx.doi.org/10.1111/vop.12115 >. Accessed: Aug. 23, 2018. doi: 10.1111/vop.12115.
http://dx.doi.org/10.1111/vop.12115...
; BECKWITH-COHEN et al., 2015BECKWITH-COHEN, B.; et al. Differences in ocular parameters between diurnal and nocturnal raptors. Veterinary Ophthalmology, Oxford, v.18, p.98-105, 2015. Available from: <Available from: https://doi.org/10.1111/vop.12126 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12126.
https://doi.org/10.1111/vop.12126...
; SMITH et al., 2015SMITH, S. P.; et al. Evaluation of the phenol red thread tear test in Falconiformes. Journal of Avian Medicine and Surgery, v.29, p.25-29, 2015. Available from: <Available from: https://doi.org/10.1647/2008-050 >. Accessed: Apr. 09, 2019. doi: 10.1647/2008-050.
https://doi.org/10.1647/2008-050...
; MONÇÃO- SILVA et al., 2016aMONÇÃO-SILVA, R.; et al. Ophthalmic diagnostic tests in parrots (Amazona amazônica) and (Amazona aestiva). Journal of Exotic Pet Medicine, v.25, n.3, p.186-193, 2016a. Available from: <Available from: http://dx.doi.org/10.1053/j.jepm.2016.05.002 >. Accessed: Aug. 23, 2018. doi: 10.1053/j.jepm.2016.05.002.
http://dx.doi.org/10.1053/j.jepm.2016.05...
; MONÇÃO-SILVA et al., 2016bMONÇÃO-SILVA, R.M.; et al. Ophthalmic parameters of Blue-and-yellow Macaws (Ara ararauna) and Lear’s Macaws (Anodorhynchus leari). Avian Biology Research, v.9, n.4, p.240-249, 2016b. Available from: <Available from: http://dx.doi.org/10.3184/175815516X14725499175746 >. Accessed: Aug. 23, 2018. doi: 10.3184/175815516X14725499175746.
http://dx.doi.org/10.3184/175815516X1472...
; OLIVEIRA et al., 2017OLIVEIRA, M. M.; et al. Reference values for selected ophthalmic diagnostic tests in the Caatinga Parakeet (Eupsittula cactorum) and Yellow-chevroned Parakeet (Brotogeris chiriri). Avian Biology Research , v.10, n.4, p.211-217, 2017. Available from: <Available from: https://doi.org/10.3184/175815617X14951979279286 >. Accessed: Apr. 09, 2019. doi: 10.3184/175815617X14951979279286.
https://doi.org/10.3184/175815617X149519...
), as well as the anatomic and physiologic variability of each species (BECKWITH-COHEN et al., 2015BECKWITH-COHEN, B.; et al. Differences in ocular parameters between diurnal and nocturnal raptors. Veterinary Ophthalmology, Oxford, v.18, p.98-105, 2015. Available from: <Available from: https://doi.org/10.1111/vop.12126 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12126.
https://doi.org/10.1111/vop.12126...
; OLIVEIRA et al., 2017OLIVEIRA, M. M.; et al. Reference values for selected ophthalmic diagnostic tests in the Caatinga Parakeet (Eupsittula cactorum) and Yellow-chevroned Parakeet (Brotogeris chiriri). Avian Biology Research , v.10, n.4, p.211-217, 2017. Available from: <Available from: https://doi.org/10.3184/175815617X14951979279286 >. Accessed: Apr. 09, 2019. doi: 10.3184/175815617X14951979279286.
https://doi.org/10.3184/175815617X149519...
).

Despite the similar median results of SMT for Caiman latirostris and Ara ararauna, there are distinct anatomic characteristics, including palpebral fissure length, eye blink frequency, lacrimal gland and drainage system features that must be considered (ORIÁ et al., 2013; BECKWITH-COHEN et al., 2015BECKWITH-COHEN, B.; et al. Differences in ocular parameters between diurnal and nocturnal raptors. Veterinary Ophthalmology, Oxford, v.18, p.98-105, 2015. Available from: <Available from: https://doi.org/10.1111/vop.12126 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12126.
https://doi.org/10.1111/vop.12126...
; FALCÃO et al, 2017aFALCÃO, M.S.A.; et al. Reference values for selected ophthalmic tests of the blue-and-yellow macaw (Ara ararauna). Pesquisa Veterinária Brasileira, v.37, n.4, p.389-394, 2017a. Available from: <Available from: http://dx.doi.org/10.1590/S0100-736X2017000400014 >. Accessed: Sep. 07, 2018. doi: 10.1590/S0100-736X2017000400014.
http://dx.doi.org/10.1590/S0100-736X2017...
; MONÇÃO-SILVA et al, 2016bMONÇÃO-SILVA, R.M.; et al. Ophthalmic parameters of Blue-and-yellow Macaws (Ara ararauna) and Lear’s Macaws (Anodorhynchus leari). Avian Biology Research, v.9, n.4, p.240-249, 2016b. Available from: <Available from: http://dx.doi.org/10.3184/175815516X14725499175746 >. Accessed: Aug. 23, 2018. doi: 10.3184/175815516X14725499175746.
http://dx.doi.org/10.3184/175815516X1472...
; OLIVEIRA et al., 2017OLIVEIRA, M. M.; et al. Reference values for selected ophthalmic diagnostic tests in the Caatinga Parakeet (Eupsittula cactorum) and Yellow-chevroned Parakeet (Brotogeris chiriri). Avian Biology Research , v.10, n.4, p.211-217, 2017. Available from: <Available from: https://doi.org/10.3184/175815617X14951979279286 >. Accessed: Apr. 09, 2019. doi: 10.3184/175815617X14951979279286.
https://doi.org/10.3184/175815617X149519...
). However, there are no corneal surface abnormalities in the studied animals, supporting the hypothesis of a stable tear film (LAWTON, 2005; DELGADO et al., 2014; ORIÁ et al., 2013aORIÁ, A.P.; et al. Ophthalmic diagnostic tests, orbital anatomy, and adnexal histology of the broad-snouted caiman (Caiman latirostris). Veterinary Ophthalmology , v.18, n.1, p.30-39, 2013a. Available from: <Available from: http://dx.doi.org/10.1111/vop.12115 >. Accessed: Aug. 23, 2018. doi: 10.1111/vop.12115.
http://dx.doi.org/10.1111/vop.12115...
) that is adapted to the environment of each population; and studies demonstrated factors, such as composition and disposition of the tear film aiding the understand of homeostasis dynamic maintenance in the ocular surface for these species.

The SMT may be useful in the diagnosis of changes in lacrimal production (DOGRU et al., 2006DOGRU, M.; et al. Strip meniscometry: a new and simple method of tear meniscus evaluation. Investigative Ophthalmology & Visual Science, v.47, n.5, p.1895-1901, 2006. Available from: <Available from: http://dx.doi.org/10.1167/iovs.05-0802 >. Accessed: Aug. 15, 2018. doi: 10.1167/iovs.05-0802.
http://dx.doi.org/10.1167/iovs.05-0802...
; RAJAEI et al., 2017RAJAEI, S.M.; et al. Strip meniscometry in dogs, cats, and rabbits. Veterinary Ophthalmology , v.21, n.2, p.210-213, 2017. Available from: <Available from: http://dx.doi.org/10.1111/vop.12486 >. Accessed: Aug. 15, 2018. doi: 10.1111/vop.12486.
http://dx.doi.org/10.1111/vop.12486...
; MIYASAKA et al., 2019MIYASAKA, K.; et al. A novel strip meniscometry method for measuring aqueous tear volume in dogs: Clinical correlations with the Schirmer tear and phenol red thread tests. Veterinary Ophthalmology , p.1-8, 2019. Available from: <Available from: https://doi.org/10.1111/vop.12664 >. Accessed: Apr. 09, 2019. doi: 10.1111/vop.12664.
https://doi.org/10.1111/vop.12664...
) and has been proven feasible for wild animals in particular, due to the fast manipulation and minimal discomfort of the subjects. Moreover, these results can provide information on tear dynamics once a relationship is established between tear meniscometry value and total tear volume (HOLLY, 1985HOLLY, F.J. Physical chemistry of the normal and disordered tear film. Transactions of the Ophthalmological Societies of the United Kingdom, v.104, p.374-380, 1985. Available from: <Available from: https://www.researchgate.net/publication/19300209_Physical_chemistry_of_the_normal_and_disordered_tear_film >. Accessed: Apr. 06, 2019.
https://www.researchgate.net/publication...
; IBRAHIM et al., 2010IBRAHIM, O.M.; et al The application of Visante optical coherence tomography tear meniscus height measurement in the diagnosis of dry eye disease. Ophthalmology, v.117, p.1923-1929, 2010. Available from: <Available from: http://dx.doi.org/10.1016/j.ophtha.2010.01.057 >. Accessed: Aug. 23, 2018. doi: 10.1016/j.ophtha.2010.01.057.
http://dx.doi.org/10.1016/j.ophtha.2010....
).

CONCLUSION:

The establishment of species-specific values can help in the diagnosis of ocular diseases and, when supplemented by other tests, may provide an understanding of the distribution of this important fluid across the ocular surface. Limitations encountered may be reduced by prior acquisition of manipulation skills and possible animal conditioning. SMT is shown to be a promising and feasible method in the ophthalmology of wild animals.

ACKNOWLEDGEMENTS

The authors are grateful to Triage Center for Wild Animals, Salvador-BA and Mister Cayman LTDA, Maceió-AL, from Brazil, for providing the birds and broad-snouted caiman. APO received strips for the clinical evaluations under-taken in this study and did not receive any grants, funding, or honorarium for the conduct of this research. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. APO is a research fellow from the National Council for Scientific and Technological Development (CNPq). ACSR (nº 88881.131559/2016-01), VJSCB (nº 88882.453698/2019-01), NLLCA (nº88882.453705/2019-01) are a PhD fellow from CAPES and MMO is a PhD fellow from Fundação de Amparo à Pesquisa do Estado da Bahia - Brasil (FAPESB) - Finance Code: BOL0439/2018.

REFERENCES

  • 0
    CR-2018-1002.R2

  • BIOETHICS AND BIOSSECURITY COMMITTEE APPROVAL

    This study was approved by the Biodiversity Authorization and Information System, Brazilian Ministry of the Environment and the Ethics Committee on Animal Experimentation of the School of Veterinary Medicine and Zootechnology of UFBA (n. 72.2016). It was conducted in accordance with the Association for Research in Vision and Ophthalmology (ARVO) Statement for the Use of Animals in Ophthalmic and Vision Research

Publication Dates

  • Publication in this collection
    21 Oct 2019
  • Date of issue
    2019

History

  • Received
    07 Dec 2018
  • Accepted
    03 Sept 2019
  • Reviewed
    28 Sept 2019
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