ABSTRACT
Background
Breed‐specific reference intervals for the Schirmer tear test (STT) and intraocular pressure (IOP) in Hamdani crossbred sheep have not been established.
Objectives
To determine reference intervals for STT and IOP in healthy Hamdani crossbred sheep.
Methods
A total of 200 clinically healthy animals were stratified into four age groups: < 6 months, 6 months to 1 year, 1–2 years, and > 2 years. Each group comprised equal numbers of males (n = 25) and females (n = 25). Tear production was evaluated using STT‐1, and IOP was measured with a rebound tonometer. Group‐based mean values were calculated using representative values obtained by averaging measurements from both eyes.
Results
Mean values and reference intervals for STT and IOP were established for each age group. No sex‐related differences were observed in STT values. However, age‐related differences were observed only in females, with higher STT values in hoggets than lambs (p < 0.01). For IOP, ewes had higher values than rams (p < 0.01). Age‐related differences in IOP were observed only in males, with rams showing lower IOP values than suckling lambs and hoggets (p < 0.01).
Conclusions
This study establishes reference intervals for STT and IOP in healthy Hamdani crossbred sheep and provides clinically relevant baseline data for ophthalmic assessment.
Keywords: hamdani crossbred sheep, intraocular pressure, reference intervals, schirmer tear test
This study establishes reference intervals for Schirmer tear test (STT) and intraocular pressure (IOP) in healthy Hamdani crossbred sheep. STT values were lower and IOP values higher than previously reported, highlighting the importance of breed‐specific reference ranges in clinical ophthalmic evaluation.
1. Introduction
Hamdani sheep are widely raised in northern Iraq, Iran and southeastern Türkiye (Aziz and Al‐Oramary 2005; Bingöl and Bingöl 2016, 2018). This breed is well adapted to local agro‐ecological conditions and is valued for its meat, milk and wool production. It is characterised by a fat tail, a broad white body, long ears, a black‐brown head and long limbs (Öztürk 1998; Alkass and Juma 2005).
A thorough ophthalmic examination is essential for the early and accurate diagnosis of ocular abnormalities and diseases. The Schirmer tear test (STT) and intraocular pressure (IOP) measurement are essential components of the ophthalmic assessment (Gelatt et al. 2013). In routine ophthalmic evaluations, tear production is commonly assessed using STT‐1, a method that does not require topical anaesthetics (Beech et al. 2003; Gelatt et al. 2013; Gelatt 2021). Although several techniques are available for measuring IOP, rebound tonometry has gained prominence in clinical practice due to its practicality, rapidity and noninvasive nature (Pereira et al. 2011).
Knowledge of species‐ and breed‐specific STT and IOP reference intervals (normal ranges) is essential for the accurate evaluation of ocular conditions in veterinary medicine (Peche and Eule 2018; Gelatt 2021; Kurt et al. 2021; Kovalcuka et al. 2023). Therefore, establishing such reference intervals is crucial to avoid misdiagnosis and inappropriate treatment decisions (Ofri et al. 2008; Kurt et al. 2021). Numerous studies have investigated STT and IOP reference intervals in a variety of domestic and wild animal species; however, research specifically focusing on sheep remains limited. These parameters have been investigated in Sanjabi (Ghaffari et al. 2011), Latvian Darkhead (Kovalcuka et al. 2023), Sakız (Kurt et al. 2021; Çakmakçi and Belge 2025), Çine Çaparı (Çakmakçi and Belge 2025), Merinos (İşler et al. 2013) and Chios and Florina sheep, as well as Lacaune mixed‐breed sheep (Dedousi et al. 2019).
A review of the literature indicates that data on STT and IOP values in Hamdani or Hamdani crossbred sheep are lacking. Therefore, this study aimed to determine STT and IOP values in healthy Hamdani crossbred sheep, to establish reference intervals for these parameters, and to evaluate the effects of sex and age on these measurements.
2. Materials and Methods
2.1. Ethics Statement
All procedures were conducted in accordance with animal welfare regulations and ethical standards. Informed consent was obtained from the animal owners, and permission was granted by the relevant authorities. Ethical approval was provided by the Siirt University Animal Researches Local Ethic Committee, Siirt, Türkiye (Decision No. 2024/08/50).
2.2. Animal Material and Groups
The animal material of this study consisted of 200 clinically healthy Hamdani crossbred sheep. These animals belonged to different flocks managed under a nomadic husbandry system, all of which were maintained under similar environmental conditions. The animals were stratified by age into four groups, each consisting of equal numbers of males and females.
Group 1: < 6 months (suckling lambs) (n = 50)
Group 2: 6 months to 1 year (growing lambs) (n = 50)
Group 3: 1–2 years (hoggets) (n = 50)
Group 4: > 2 years (rams and ewes, up to 5 years of age) (n = 50)
2.3. STT and IOP Measurements
On the first day of each flock visit, all animals in the predefined age groups underwent clinical and ophthalmic examinations. Based on these examinations, animals considered clinically healthy were included in the study, and their ear tag numbers were recorded.
The general clinical examination comprised a physical examination, measurement of vital parameters (body temperature, respiratory rate and heart rate), and assessment of general condition. The ophthalmic examination included inspection of the eyelids, conjunctiva and cornea under appropriate lighting conditions; fluorescein staining to detect corneal defects; and evaluation for ocular discharge, inflammation and structural abnormalities. Neuro‐ophthalmic and visual function assessments included the menace response, dazzle reflex and both direct and indirect pupillary light reflexes. Both eyes were examined using a PanOptic ophthalmoscope (Welch Allyn, Hillrom, NY, USA) for monocular ophthalmoscopy, without the use of topical mydriatic agents.
All measurements were performed between May and July to ensure the inclusion of animals from all predefined age groups. Measurements were conducted in flocks located within the same geographical area under similar field conditions. All procedures were performed by the same investigator during the daytime (10:00 AM–4:00 PM) to minimise the effects of circadian variation. Animals were gently restrained manually without sedation. Lambs were maintained in a standing position with minimal handling, whereas adult sheep were restrained by an assistant supporting the head and body. Particular care was taken to avoid pressure on the neck or jugular veins, and excessive restraint was avoided to minimise stress. The head was maintained in a natural, upright position during measurements. In each animal, STT was performed first, followed by IOP measurement, to avoid reflex tearing and ensure measurement accuracy.
STT was performed by placing the bent end of a standard sterile STT‐1 strip (ERC, Ankara, Türkiye) into the lower conjunctival fornix and leaving it in place for 60 s (Figure 1a). After removal, tear production was recorded in millimetres.
FIGURE 1.
Measurement procedures for STT‐1 and IOP in sheep. (a) Application of the STT strip to evaluate tear production. (b) Measurement of IOP using a rebound tonometer.
IOP was measured using a rebound tonometer (Icare TONOVET Plus, Icare Finland Oy, Vantaa, Finland) (Figure 1b). The device was calibrated and used in canine mode. Measurements were obtained in serial mode (the device automatically performs six measurements), and the mean of three consecutive readings was calculated. During measurements, the animal's head was maintained in a natural, upright position, avoiding pressure on the neck or periocular structures. The probe was held perpendicular to the central cornea at a distance of approximately 4–8 mm to ensure proper alignment.
2.4. Statistical Analysis
Statistical analyses were performed using Minitab (v21). Descriptive statistics for STT and IOP measurements were expressed as mean, standard error, standard deviation, minimum, median and maximum. Reference intervals for STT and IOP were estimated using Minitab software by calculating the lower and upper limits of the means with a 95% confidence interval. The Shapiro–Wilk test was used to evaluate distribution of the data. As the data were normally distributed, parametric tests were used. The independent samples t‐test was used to compare mean STT (average of left and right eyes) and IOP (average of left and right eyes) values between males and females within each group. Comparisons among groups were performed using one‐way ANOVA. Statistical significance was considered at p < 0.05.
3. Results
The mean ± SD STT values for both eyes in each group were 5.48 ± 1.55, 5.61 ± 1.72, 7.00 ± 2.47 and 6.13 ± 1.61 mm/min, respectively. The corresponding reference intervals for STT were 5.03–5.92, 5.12–6.10, 6.29–7.70 and 5.67–6.59 mm/min (Table 1).
TABLE 1.
Descriptive statistics and reference intervals for STT and IOP values.
| Variable | N | Mean | SE Mean | StDev | Minimum | Median | Maximum | Reference interval (95% CI) | |
|---|---|---|---|---|---|---|---|---|---|
| Group 1 | STT—Right | 50 | 5.46 | 0.27 | 1.90 | 2.00 | 5.00 | 9.00 | 4.91–6.00 |
| STT—Left | 50 | 5.50 | 0.24 | 1.70 | 2.00 | 5.00 | 9.00 | 5.01–5.98 | |
| STT—Average | 50 | 5.48 | 0.22 | 1.55 | 2.00 | 5.50 | 9.00 | 5.03–5.92 | |
| IOP—Right | 50 | 24.38 | 0.60 | 4.26 | 17.00 | 24.00 | 33.00 | 23.16–25.59 | |
| IOP—Left | 50 | 23.98 | 0.63 | 4.51 | 16.00 | 23.00 | 33.00 | 22.69–25.26 | |
| IOP—Average | 50 | 24.18 | 0.59 | 4.20 | 17.00 | 24.00 | 32.00 | 22.98–25.37 | |
| Group 2 | STT—Right | 50 | 5.46 | 0.23 | 1.64 | 3.00 | 5.00 | 10.00 | 4.99–5.92 |
| STT—Left | 50 | 5.76 | 0.31 | 2.20 | 3.00 | 5.00 | 12.00 | 5.13–6.38 | |
| STT—Average | 50 | 5.61 | 0.24 | 1.72 | 3.00 | 5.50 | 10.50 | 5.12–6.10 | |
| IOP—Right | 50 | 22.54 | 0.48 | 3.44 | 16.00 | 22.50 | 31.00 | 21.56–23.51 | |
| IOP—Left | 50 | 22.52 | 0.53 | 3.75 | 15.00 | 22.50 | 29.00 | 21.45–23.58 | |
| IOP—Average | 50 | 22.53 | 0.48 | 3.40 | 15.50 | 23.00 | 30.00 | 21.56–23.49 | |
| Group 3 | STT—Right | 50 | 7.02 | 0.35 | 2.51 | 2.00 | 7.00 | 15.00 | 6.30–7.73 |
| STT—Left | 50 | 6.98 | 0.38 | 2.70 | 3.00 | 6.50 | 18.00 | 6.21–7.74 | |
| STT—Average | 50 | 7.00 | 0.34 | 2.47 | 4.00 | 6.75 | 16.00 | 6.29–7.70 | |
| IOP—Right | 50 | 23.24 | 0.63 | 4.51 | 14.00 | 23.00 | 34.00 | 21.95–24.52 | |
| IOP—Left | 50 | 23.50 | 0.70 | 4.95 | 12.00 | 23.50 | 35.00 | 22.09–24.90 | |
| IOP—Average | 50 | 23.37 | 0.64 | 4.58 | 13.00 | 23.00 | 34.50 | 22.06–24.67 | |
| Group 4 | STT—Right | 50 | 6.10 | 0.27 | 1.90 | 3.00 | 6.00 | 12.00 | 5.55–6.64 |
| STT—Left | 50 | 6.16 | 0.24 | 1.71 | 3.00 | 6.00 | 9.00 | 5.67–6.64 | |
| STT—Average | 50 | 6.13 | 0.22 | 1.61 | 3.00 | 6.00 | 10.50 | 5.67–6.59 | |
| IOP—Right | 50 | 22.16 | 0.63 | 4.51 | 12.00 | 22.50 | 34.00 | 20.87–23.44 | |
| IOP—Left | 50 | 21.78 | 0.64 | 4.53 | 14.00 | 21.50 | 33.00 | 20.49–23.06 | |
| IOP—Average | 50 | 21.97 | 0.60 | 4.28 | 14.00 | 21.75 | 33.50 | 20.75–23.18 |
Note: Group 1: < 6 months; Group 2: 6 months‐1 year; Group 3: 1–2 years; Group 4: > 2 years.
Abbreviatons: CI, confidence interval; IOP, intraocular pressure (mmHg); SE Mean, standard error of the mean; StDev, standard deviation; STT, Schirmer tear test (mm/min).
When the effect of sex was evaluated, no statistically significant differences in STT values were observed among the groups (p > 0.05). In intergroup comparisons, STT values in females were significantly higher in hoggets than in suckling and growing lambs (p < 0.01), whereas no statistically significant difference was observed between hoggets and ewes. In males, no statistically significant differences in STT values were observed among the age groups (p > 0.05) (Table 2).
TABLE 2.
Comparison of STT and IOP measurements between sex and age groups (Mean ± SE).
| Group | Female | Male | p‐value | |
|---|---|---|---|---|
| STT | 1 | 5.32 ± 0.31b | 5.64± 0.31a | 0.47 |
| 2 | 5.26 ± 0.33b | s5.96 ± 0.35a | 0.15 | |
| 3 | 7.42 ± 0.32a | 6.58 ± 0.35a | 0.23 | |
| 4 | 6.30 ± 0.60ab | 5.96 ± 0.33a | 0.46 | |
| p‐value | 0.001 | 0.26 | ||
| IOP | 1 | 24.18 ± 0.97a | 24.18 ± 0.71a | 1.00 |
| 2 | 22.72 ± 0.76a | 22.34 ± 0.61ab | 0.69 | |
| 3 | 22.68 ± 0.94a | 24.06 ± 0.89a | 0.29 | |
| 4 | 23.94 ± 0.76a | 20.00 ± 0.78b | 0.001 | |
| p‐value | 0.47 | 0.001 |
Note: Values are presented as mean ± SE. Mean STT and IOP values represent the average of right and left eye measurements. Comparisons between females and males within each age group were performed using an independent samples t‐test. Comparisons among age groups within the same sex were performed using one‐way ANOVA. Different superscript letters (a and b) within the same column indicate statistically significant differences (p < 0.05).
Abbreviations: IOP, intraocular pressure (mmHg); SE, standard error of the mean; STT, Schirmer tear test (mm/min).
The mean ± SD IOP values for both eyes in each group were 24.18 ± 4.20, 22.53 ± 3.40, 23.37 ± 4.58 and 21.97 ± 4.28 mmHg, respectively. The corresponding reference intervals for IOP were 22.98–25.37, 21.56–23.49, 22.06–24.67 and 20.75–23.18 mmHg (Table 1).
When the effect of sex was evaluated, IOP values were significantly higher in ewes than in rams among adult sheep (p < 0.01). In intergroup comparisons, no statistically significant differences in IOP values were observed among age groups in females. In males, IOP values were significantly lower in rams than in suckling lambs and hoggets (p < 0.01), whereas no statistically significant difference was observed between growing lambs and rams (Table 2).
4. Discussion
In this study, reference intervals and mean values for STT and IOP were established in Hamdani crossbred sheep. To our knowledge, this is the first study to investigate these parameters in this breed, providing breed‐specific reference intervals and baseline data. The STT values obtained were lower than those reported in most previous studies in sheep, whereas the IOP values were relatively higher. Although the effects of age and sex were generally limited, statistically significant differences were observed in certain subgroups. These findings highlight the importance of using breed‐specific reference intervals in clinical ophthalmic assessment.
STT values reported for different sheep breeds in the literature are summarised in Table 3. The mean STT values obtained in the present study (5–7 mm/min) were markedly lower than those previously reported (11–18 mm/min).
TABLE 3.
Reported STT values in different sheep breeds.
| Breed | Sex | Age | Mean ± SD (mm/min) | Reference interval (mm/min) | References |
|---|---|---|---|---|---|
| Sanjabi | M | 2–3 years | 18.52 ± 2.55 | 13.5–22 | Ghaffari et al. (2011) |
| Latvian Darkhead | F | 1–8 years | 13.68 ± 4.09 | 12.52–14.84 | Kovalcuka et al. (2023) |
| Latvian Darkhead | F/M | 1–3 months | 13.12 ± 3.91 | 12.00–14.23 | Kovalcuka et al. (2023) |
| Merinos | Unspecified | 1–1.5 years | 18.55 ± 1.98 | NR | İşler et al. (2013) |
| Merinos | Unspecified | 2–2.5 years | 18.24 ± 1.89 | NR | İşler et al. (2013) |
| Merinos | F | 15–20 days | 16.06 ± 1.52 | NR | İşler et al. (2013) |
| Merinos | M | 15–20 days | 15.51 ± 1.61 | NR | İşler et al. (2013) |
| Sakız | F | 2 years | 18.87 ± 0.51 | NR | Çakmakçi and Belge (2025) |
| Çine Çaparı | F | 2 years | 15.82 ± 0.61 | NR | Çakmakçi and Belge (2025) |
| Chios, Florina, Lacaune mixed‐breed | F | 2 years | 18.45 ± 3.93 | 10.8–26.2 | Dedousi et al. (2019) |
| Sakız | F/M | Adult | 11.8 ± 3.35 | NR | Kurt et al. (2021) |
Note: STT, Schirmer tear test; values are presented as mean ± standard deviation (SD); F, female; M, male; NR, not reported.
Similar differences have been reported previously, and several factors have been proposed to explain them, including breed, season, geographic location, housing conditions and circadian rhythm (Dedousi et al. 2019; Kurt et al. 2021; Kovalcuka et al. 2023; Çakmakçi and Belge 2025). In addition, Rothschild et al. (2004) and İşler et al. (2013) emphasised methodological factors. Although the differences observed in the present study are likely multifactorial, breed‐related factors and geographic location appear to be the most influential. Hamdani sheep, a breed of Iraqi origin, and their crossbreeds are commonly raised in regions characterised by a hot climate (Bingöl and Bingöl 2016, 2018). This breed is well adapted to such environmental conditions, and this adaptation is reflected in certain morphological traits (e.g., long ears and a broad white body) (Öztürk 1998; Alkass and Juma 2005). Therefore, this adaptation, together with breed‐specific anatomical and physiological characteristics, may influence tear production. Schaumberg et al. (2001) and Koç et al. (2005) also suggested that anatomical differences may play a role. In addition, climatic conditions may contribute to increased tear film evaporation or altered lacrimal gland function.
In the present study, sex had no significant effect on STT values. With respect to age, STT values were higher in female hoggets than in female lambs. Similarly, İşler et al. (2013) reported that sex had no significant effect on STT in Merinos lambs and that STT values in lambs were significantly lower than those in adult sheep. However, the same authors indicated no difference in STT values between sheep aged 1–1.5 years and those aged 2–2.5 years.
IOP values reported for different sheep breeds in the literature are summarised in Table 4. The mean IOP values obtained in the present study (21–24 mmHg) were relatively higher than those previously reported (8–20 mmHg).
TABLE 4.
Reported IOP values in different sheep breeds.
| Breed | Sex | Age | Tonometry | Mean ± SD (mmHg) | Reference interval (mmHg) | References |
|---|---|---|---|---|---|---|
| Sanjabi | M | 2–3 years | Applanation | 9.37 ± 2.45 | 6–14.5 | Ghaffari et al. (2011) |
| Latvian Darkhead | F | 1–8 years | Rebound | 19.16 ± 3.24 | 18.24–20.08 | Kovalcuka et al. (2023) |
| Latvian Darkhead | F/M | 1–3 months | Rebound | 14.04 ± 3.68 | 13.00–15.08 | Kovalcuka et al. (2023) |
| Merinos | Unspecified | 1–1.5 years | Schiotz | 19.86 ± 2.36 | NR | İşler et al. (2013) |
| Merinos | Unspecified | 2–2.5 years | Schiotz | 20.40 ± 3.53 | NR | İşler et al. (2013) |
| Merinos | F | 15–20 days | Schiotz | 18.54 ± 3.72 | NR | İşler et al. (2013) |
| Merinos | M | 15–20 days | Schiotz | 16.46 ± 4.25 | NR | İşler et al. (2013) |
| Sakız | F | 2 years | Rebound | 16.40 ± 0.42 | NR | Çakmakçi and Belge (2025) |
| Çine Çaparı | F | 2 years | Rebound | 15.75 ± 0.60 | NR | Çakmakçi and Belge (2025) |
| Sakız | F/M | Adult | Applanation | 17.7 ± 4.57 | NR | Kurt et al. (2021) |
| Magra | F | Adult | PT100 non‐contact tonometer | 8.72 ± 0.25 | NR | Arvinder et al. (2022) |
Note: IOP, intraocular pressure; values are presented as mean ± standard deviation (SD); F, female; M, male; NR, not reported.
Previous studies have reported that IOP values may vary depending on factors such as breed, age, geographic location, season and environmental conditions (İşler et al. 2013; Kurt et al. 2021; Kovalcuka et al. 2023; Çakmakçi and Belge 2025). In addition to these factors, İşler et al. (2013) emphasised the type of tonometer used, whereas Kurt et al. (2021) highlighted the influence of circadian rhythm. In the present study, measurements were performed within a defined time interval (10:00 AM–4:00 PM) and under similar conditions to minimise circadian variation. Although the same tonometric method was used as in some previous studies (Kovalcuka et al. 2023; Çakmakçi and Belge 2025), the values obtained were partially higher. Given that all measurements were performed carefully by the same investigator under controlled conditions, the observed differences in IOP are likely attributable to breed‐related factors. These differences may be associated with anatomical variations in ocular structures specific to this breed.
In the present study, IOP values were higher in ewes than in rams within the same age groups. In contrast, İşler et al. (2013) reported that sex had no significant effect on IOP in Merinos lambs. In our study, among males, rams exhibited lower IOP values than suckling lambs and hoggets. Conversely, Kovalcuka et al. (2023) reported higher IOP values in Latvian Darkhead sheep than in lambs. Similarly, İşler et al. (2013) found that IOP values in Merinos lambs were significantly lower than those in ewes; however, no statistically significant difference was observed between ewes aged 1–1.5 years and those aged 2–2.5 years. It should also be noted that the lamb groups in both studies included individuals of both sexes. Kovalcuka et al. (2023) suggested that these differences may be related to ocular development and central corneal thickness. However, further comprehensive studies are needed to elucidate variations in IOP associated with sex and age.
This study has several limitations. As measurements were conducted over a three‐month period (May–July), seasonal and environmental factors may have influenced the results. The relatively wide age range and the sample size may have limited the ability to detect subtle differences. Although measurements were performed within a defined daytime interval, circadian variation cannot be entirely excluded.
5. Conclusion
This study establishes reference intervals for STT and IOP in Hamdani crossbred sheep, providing the first breed‐specific baseline data. The higher IOP and lower STT values compared to previous reports highlight the risk of misinterpretation when non‐specific reference intervals are used. These findings underscore the clinical importance of breed‐specific ophthalmic parameters for accurate diagnosis and field‐based assessments. Although the effects of sex and age require further clarification, the results suggest that breed‐related anatomical differences may contribute to the observed variations. Further studies are warranted to elucidate the roles of ocular anatomy, as well as seasonal and environmental factors, in tear production and IOP.
Author Contributions
Kadir Sulu: conceptualization, data curation, investigation, methodology, project administration, supervision, validation, visualization, writing – original draft, writing – review and editing. Mustafa Baris Akgul: investigation, data curation, writing – review and editing, methodology. Ali Osman Turgut: formal analysis, writing – review and editing. Ali Gulaydin: investigation, data curation, writing – review and editing, methodology. Bahar Erden: investigation, data curation, writing – review and editing. Maruf Yilmaz: investigation, data curation, writing – review and editing.
Ethics Statement
All experimental procedures were approved by the Siirt University Animal Researches Local Ethic Committee, Siirt, Türkiye (Decision No. 2024/08/50).
Conflicts of Interest
The authors declare no conflicts of interest.
Acknowledgements
This study was supported by the Siirt University Scientific Research Projects Coordinatorship (Project No. 2025‐SİÜVET‐012). Artificial intelligence‐assisted tools were used solely for language editing and proofreading and had no influence on the scientific content, data interpretation, or conclusions. All authors reviewed and approved the final version of the manuscript and take full responsibility for its content.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.