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Home , Diabetic retinopathy, Retinopathy

ORIGINAL ARTICLE

Axial and its Influence on Diabetic Haroon Tayyab, Muhammad Ali Haider and Syed Ali Haider Bukhari Shaheed

ABSTRACT Objective: To evaluate the correlation between axial myopia and . Study Design: Cross-sectional study. Place and Duration of Study: Eye Department of Postgraduate Medical Institute, Lahore General Hospital, from August 2012 to February 2013. Methodology: A total of 258 participants suffering from type-2 diabetic retinopathy were included. Axial length was measured by two optometrists using contact type ultrasound biometer. Colored retinal photographs, free retinal photographs and Angiography (FFA) were performed on all patients using standard fundus camera. All fundus photographs and angiograms were independently reviewed and graded by two qualified vitreoretinal fellows. Results: Out of 258 patients, 163 were males (63.2%) and 95 (36.8%) were females. Average age of patients was 56.30 ± 7.57 years. Average axial length of right and left eyes were 23.16 mm and 23.15 mm respectively. There was statistically significant negative correlation between axial length and severity of diabetic retinopathy in the right eye, (Spearman correlation = -0.511, p = 0.0001) as well as the left eye (Spearman correlation = -0.522, p = 0.0001). Conclusion: There is a protective influence of longer axial length of on the stage and severity of diabetic retinopathy. This study may help in modifying the protocol for diabetic retinopathy amongst patients of differing axial lengths.

Key Words: Myopia. Diabetic retinopathy. Axial length. Clinically significant .

INTRODUCTION Likewise, recent trials have shown the influence of Mellitus (DM) is one of the major causes of certain modifying factors, which are protective towards morbidity and mortality in the world and its occurrence in development and progression of diabetic retinopathy. middle age population is on constant incline.1 In one Optic atrophy and myopia are few of such factors that 6 study, conducted in the province of Punjab (Pakistan), have shown trend of having a protective influence. prevalence of type-2 DM was found to be 13.14%.2 The Recently, researchers have started to focus on the cause of this chronic disease is multifactorial and it pathophysiology of myopia that is in play towards having results in a myriad of cardiac and vascular accidents that a protective effect on DR.7 Meanwhile, the researchers result in long-term morbidity. try to find the pathophysiologic relationship between Diabetic Retinopathy (DR) is one of the most common myopia and diabetic retinopathy, there have been many and devastating microvascular complications of DM.3 studies that have shown the progression of DR is slowed 8,9 According to Wisconsin Epidemiological Study of in the presence of myopia, but the evidence still Diabetic Retinopathy (WESDR), in Northern America, remains to be inconclusive as the myopia could have 10 DR is the most common factor responsible for new been axial or non-axial in most of these studies. cases of blindness between the ages 25 - 74 years.3 The The rationale of this study was to demonstrate a occurrence of DR was found to be 29.1% in self reported statistically conclusive relationship between axial diabetics.4 There have been many clinical and myopia and its effects on the development and epidemiological studies that have looked into the progression of DR. This study can further help the possible risk factors in diabetics that lead to visual clinicians to modify the screening and therapeutic impairment. After a careful evaluation, it has been protocols of DR in patients with differing Axial Length postulated that neuropathy, microalbuminuria, age more (AL). than 60 years and presence of nuclear sclerosis are risk The objective of this study was to evaluate the factors for in diabetic retinopathy.5 correlation between axial myopia and diabetic retinopathy. Department of Eye, Unit III, Postgraduate Medical Institute, Lahore General Hospital, Lahore. METHODOLOGY Correspondence: Dr. Haroon Tayyab, House SUH-24, Askari This cross-sectional study was conducted in Eye XI, Cobbe Lane, Near Qasim Market, Rawalpindi. Department of Postgraduate Medical Institute, Lahore E-mail: [email protected] General Hospital, from August 2012 to February 2013. Received: September 07, 2013; Accepted: May 23, 2014. A total of 516 eyes of 258 participants suffering from

728 Journal of the College of Physicians and Surgeons Pakistan 2014, Vol. 24 (10): 728-731 Axial myopia and its influence on diabetic retinopathy type-2 DM were included in this study from the Outdoor dations of ETDRS. CSMO was found to be present Patient Department. All participants aged 35 years and when there was retinal thickening within 500 microns of above were physician diagnosed cases of type-2 DM macula, exudation within 500 microns of macula, if under treatment of Diabetic Clinic of Lahore General associated with retinal thickening which may be outside Hospital. Self reported cases of diabetes and those who 500 microns of macula and retinal thickening 1500 had undergone extraction were excluded from microns or larger, any part of which may be within 1500 the study. microns of center of macula. Informed consent was taken from all participants of the Statistical analysis was performed using Statistical study. Approval for this study was obtained from Ethical Package for Social Sciences (SPSS) version 12. For Committee of Postgraduate Medical Institute, Lahore qualitative data like gender and severity of diabetic General Hospital. There were no conflict of interests in retinopathy, the data was presented in the form of this study. frequency (%). Histogram was made for age of the Axial Length (AL) was measured by two independent patients. To see correlation in severity of diabetic trained optometrists using contact type Axis-II PR A retinopathy, CSMO and axial length, Spearman rank Scan ultrasound Biometer (Quantel Medical, Cedex, correlation was calculated and was considered France). Ten readings by each optometrist were statistically significant at p ≤ 0.05. recorded and the average AL was finally documented for analysis. AL was categorized in 4 quartiles. First quartile RESULTS had AL equal to or less than 19.5 mm. Second quartile Out of a total 258 patient (516 eyes) recruited in the had AL more than 19.5 mm and equal to or less than 22 study, 163 were males (63.2%) whereas rest of 95 mm. Third quartile had AL more than 22 mm and equal (36.8%) were females. Average age of patients was to or less than 24.5 mm. Fourth quartile had AL more 56.30 ± 7.57 years with minimum age observed as 38 than 24.5 mm. years and maximum of 76 years. Average axial length of Autorefraction was performed using Topcon RM 8000B eyes was 23.15 mm (average right eye axial length = Autorefractor Keratometer (Topcon Medical Systems, 23.16 mm, left eye axial length = 23.15 mm). Oakland, NJ, USA). Five consecutive readings were Clinically Significant Macular Oedema (CSMO) was recorded. After this, subjective refraction was performed present in majority (318 eyes; 61.62%) of patients (right by certified optometrist. Spherical equivalent was eye 161; 50.62% and left eye 157; 49.31%). Two defined as the sum of sphere and half of cylinder and hundred and forty seven (47.9%) eyes had mild diabetic was documented for final analysis. retinopathy (right eye in 125; 50.6% and left eye in 122; Colored retinal photographs, red free retinal photo- 49.3%). Sixty two (12%) eyes had moderate diabetic graphs and fundus were retinopathy (right eye in 32; 51.6% and left eye in 30; performed on all patients using standard fundus camera 48.3%). Twenty two (4.2%) eyes had severe diabetic (Topcon TRC 50DX, Topcon Medical Systems, Oakland, retinopathy (right eye in 9; 40.91% and left eye in 13; NJ, USA). All fundus photographs and angiographs were 59%). One hundred and thirty three (25.8%) eyes had independently reviewed and graded by two qualified proliferative diabetic retinopathy (right eye in 67; 50.3% vitreoretinal fellows. In case of any difference of opinion and left eye in 66; 49.6%). Fifty two (10.1%) eyes had regarding DR grading, a third independent opinion was advanced disease (right eye in 25; 48.1% and left eye in sought by qualified personnel. We used modified Airlie 27; 51.9%). House classification for staging of DR and categorized Regarding axial length in both eyes, 10 (2%) eyes were patients in following 5 groups in order of increasing in first quartile (right eye in 5; 50% and left eye in 5; 50% severity. Group-1 had mild diabetic retinopathy [no signs each). (28.5%) eyes were in second quartile (right eye in of non-Proliferative Diabetic Retinopathy (NPDR), very 74; 50.3% and left eye in 73; 49.6%). Two hundred and mild NPDR, mild NPDR]. Group-2 had moderate sixteen (41.9%) eyes were in 3rd quartile [whose axial diabetic retinopathy (Moderate NPDR). Group-3 had length 22.1 - 24.5 mm] (right eye in 107; 49.5% and left severe diabetic retinopathy (severe NPDR, very severe eye in 109; 50.4%). One hundred forty three (27.8%) NPDR), Group-4 had proliferative diabetic retinopathy eyes were in 4th quartile [whose axial length > 24.5 mm] [mild-moderate Proliferative Diabetic Retinopathy (right eye in 72; 50.3% and left eye in 71; 49.6%). (PDR), high risk PDR]. Group-5 had advanced diabetic The average duration of disease in recruited patients . Group-5 did not include patients with was 8.56 ± 4.31 years with a minimum of 2 years and tractional involving macula, severe maximum of 23 years. There was significant negative obscuring fundus details and sub- correlation between AL and severity of DR in both eyes, hyaloid hemorrhage covering entire macula to ensure with Spearman correlation of -0.511 and p < 0.0001 accurate biometry findings. (right eye Spearman correlation = -0.469, p < 0.0001 The presence of Clinically Significant Macular Oedema and left eye Spearman correlation = -0.552, p < 0.0001, (CSMO) was documented according to recommen- Table I).

Journal of the College of Physicians and Surgeons Pakistan 2014, Vol. 24 (10): 728-731 729 Haroon Tayyab, Muhammad Ali Haider and Syed Ali Haider Bukhari Shaheed

Table I: Correlation of axial length and severity of diabetic retinopathy. Severity of diabetic retinopathy Mild diabetic Moderate diabetic Severe diabetic Proliferative diabetic Advanced disease Axial length retinopathy retinopathy retinopathy retinopathy < 19.5 mm 2 0 1 4 3 19.5 - 22 mm 25 18 10 61 33 22.1 - 24.5 mm 101 38 11 53 13 > 24.5 mm 119 6 0 15 3 Spearman Correlation = -0.511, p < 0.0001

Overall, a slightly positive correlation (Spearman vessels and resultant low pressure in vessels walls.18,19 correlation = 0.127; p = 0.004) between CSMO and AL With resultant decreased pressure in vessel wall, there (both eyes) was observed which was significant is less profound occurrence of typical signs of DR due to statistically (right eye Spearman correlation = 0.154; decreased leakage. p = 0.013 and left eye Spearman correlation = 0.099; It has also been shown that there is associated chorio- p = 0.127). retinal thinning with increasing myopia.20 Stefansson Similarly, on combined analysis, the correlation between demonstrated that chorioretinal thinning is associated the duration of diabetes was strongly positive with with decreased retinal metabolic demands which may severity of DR (Spearman correlation = 0.218). All these result in protection against DR.21 correlations were statistically significant (p < 0.001). The WESDR study has shown that patients with higher correlation between duration of diabetes was positive myopic refractive errors are protected against the with severity of DR when observed individually in right progression to PDR.3 Pierro has also demonstrated that and left eye (Spearman correlation regarding right eye patients having NPDR and PDR had shorter AL when being 0.219 and left eye being 0.217). compared to patients with no DR.22 In a recently concluded trial (Singapore Indian Eye study), it was DISCUSSION observed that patients with myopic refractive errors are This study was conducted to investigate the influence of less likely to have DR (OR, 0.68; 95% CI, 0.46 - 0.98) varying AL upon occurrence and severity of DR and but are more likely to have nuclear sclerosis.23 CSMO. The authors were able to substantially Therefore, it is important to correlate DR with axial demonstrate that people with type-2 DM and longer AL myopia than with overall refractive myopia (myopes are were protected from occurrence of and severe forms of more likely to develop nuclear sclerosis which adds to DR; however, this protective relationship could not be overall myopic error). Man provided an elaborate review established between longer AL and CSMO. This study of available evidence between myopia with its AL showed a linear and continuous protective effect of axial component, corneal curvature, nuclear changes and myopia on DR. There have been only few studies in past anterior chamber depth and its association with DR.24 to evaluate biometric parameters with DR;11 most of the He concluded that AL is the only variable contributing to studies have evaluated refractive myopia with DR. In this protective effect of myopia on DR. study, status of was not included in final Strengths of this study lie in the standardized protocol analysis due to confounding effects of nuclear sclerosis for biometric measurements, documentation of DR on overall refraction; thereby masking the actual axial through fundus photographs and fundus angiography refractive error and its corresponding effects on DR. This and removal of a potential bias of nuclear sclerosis is because nuclear sclerosis is likely to be present in which may have added to overall myopia of participants; patients over 50 years of age. Diabetics have earlier thus skewing the final results. The weakness of this and more profound lenticular changes than normal study lies in its cross sectional design because the onset population. and progression of DR is dependent on multiple factors. Although, exact mechanisms remain unclear regarding A prospective/longitudinal trial with more controlled the pathophysiology of axial myopia and its protective systemic variables will be more suitable for establishing effect on DR, most studies have attributed this effect to the answer for hypothesis under question. In this study, pathological changes occurring in due to the authors were not able to establish a protective elongation of globe. It has been shown that retinal relationship between axial myopia and CSMO. This flow increases with increasing severity of DR.12-15 This finding further stresses on the need of a longitudinal increased blood flow is associated with increasing study with controlled variables. Nevertheless, we were pressure in vessel wall (Laplace's law)13,16 and the able to further strengthen the clinical belief that myopic resultant leakage from retinal vessels in diabetics. patients are protected against the onset and progression Quigley inferred that increasing AL results in stretching of DR regardless of the pathogenic mechanisms of vessel walls.17 This result in reduced blood flow in responsible for this observation.

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CONCLUSION 10. Mwale C, Karimurio J, Njuguna M. Refractive errors in type-2 diabetic patients. East Afr Med J 2007; 84:259-63. This study positively contributes to the clinical impression that patients with axial myopia are less likely 11. Man RE, Sasongko MB, Sanmugasundram S, Nicolaou T, Jing X, Wang JJ, et al. Longer axial length is protective of diabetic to develop severe forms of DR. It further intrigues retinopathy and macular edema. 2012; 119: researchers to find exact mechanisms responsible for 1754-9. protection of myopic fundi against harmful effects of DR. 12. Cuypers MH, Kasanardjo JS, Polak BC. Retinal blood flow This study may aid clinicians in improving the screening changes in diabetic retinopathy measured with the Heidelber protocols in myopic diabetics and may lead to revised scanning laser Doppler flowmeter. Graefes Arch Clin Exp protocols of management of DR in such patients. The Ophthalmol 2000; 238:935- 41. authors feel a strong need of further longitudinal studies 13. Patel V, Rassam S, Newsom R. Retinal blood flow in diabetic under more controlled conditions to isolate factors retinopathy. BMJ 1992; 305:678-83. leading to protection against vision threatening effects of 14. Patel V, Sailesh S, Panja S, Kohner E. Retinal perfusion DR. pressure and pulse pressure: clinical parameters predicting progression to sight-threatening diabetic retinopathy. Br J REFERENCES Diabetes Vasc Dis 2001; 1:80 -7. 1. Scheen AJ, Paquot N. Type-2 Diabetes: journey in the heart of 15. Konno S, Feke GT, Yoshida A. Retinal blood flow changes in a complex disease. Rev Med Liege 2012; 67:326-31. type-I diabetes: a long-term follow-up study. Invest Ophthalmol 2. Zafar J, Bhatti F, Akhtar N, Rasheed U, Bashir R, Humayun S, Vis Sci 1996; 37:1140-8. et al. Prevalence and risk factors for diabetes mellitus in a 16. Gardner TW, Antonetti DA, Barber AJ. Diabetic retinopathy: selected urban population of a city in Punjab. J Pak Med Assoc more than meets the eye. Surv Ophthalmol 2002; 47:S253- 62. 2011; 61:40-7. 17. Quigley M, Cohen S. A new pressure attenuation index to 3. Klein R, Klein BEK, Moss SE. The Wisconsin epidemiologic study evaluate retinal circulation: a link to protective factors in of diabetic retinopathy: a review. Diab Met Rev 1989; 5:559-70. diabetic retinopathy. Arch Ophthalmol 1999; 117:84 -9. 4. McKay R, McCarty CA, Taylor HR. Diabetic retinopathy in 18. Berisha F, Findl O, Lasta M. A study comparing ocular pressure Victoria, Australia: the visual impairment project. Br J Ophthalmol pulse and ocular fundus pulse in dependence of axial 2000; 84:865-70. eye length and ocular volume. Acta Ophthalmol 2010; 88: 5. Rani PK, Raman R, Gella L, Kulothungan V, Sharma T. 766-72. Prevalence of visual impairment and associated risk factors in 19. Benavente-Pérez A, Hosking SL, Logan NS, Broadway DC. subjects with type-2 diabetes mellitus: Sankara Nethralaya Ocular blood flow measurements in healthy human myopic diabetic retinopathy epidemiology and molecular genetics eyes. Graefes Arch Clin Exp Ophthalmol 2010; 248:1587-94. study (sn-dreams, report 16). Middle East Afr J Ophthalmol. 2012; 19:129-34. 20. Ursekar TN. Classification, etiology and pathology of myopia. Indian J Ophthalmol 1983; 31:709 -11. 6. Dogru M, Inoue M, Nakamura M, Yamamoto M. Modifying factors related to asymmetric diabetic retinopathy. Eye (Lond) 21. Stefansson E. Ocular oxygenation and the treatment of 1998; 12:929-33. diabetic retinopathy. Surv Ophthalmol 2006; 51:364-80. 7. Baker RS, Rand LI, Krolewski AS, Maki T, Warram JH, Aiello 22. Pierro L, Brancato R, Robino X. Axial length in patients with LM. Influence of HLA-DR phenotype and myopia on the risk of diabetes. Retina 1999; 19:401- 4. non-proliferative and proliferative diabetic retinopathy. Am J 23. Pan CW, Cheung CY, Aung T, Cheung CM, Zheng YF, Wu RY, Ophthalmol 1986; 102:693-700. et al. Differential associations of myopia with major age-related 8. Lim LS, Lamoureux E, Saw SM, Tay WT, Mitchell P, Wong TY. eye diseases: the Singapore Indian eye study. Ophthalmology Are myopic eyes less likely to have diabetic retinopathy? 2013; 120:284-91. Ophthalmology 2010; 117:524-30. 24. Man RE, Sasongko MB, Wang JJ, Lamoureux EL. Association 9. Moss SE, Klein R, Klein BE. Ocular factors in the incidence between myopia and diabetic retinopathy: a review of and progression of diabetic retinopathy. Ophthalmology 1994; observational findings and potential mechanisms. Clin Experiment 101:77-83. Ophthalmol 2013; 41:293-301.

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