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BMC Ophthalmology

, 18:83 | Cite as

Prevalence and risk factors of retinopathy of prematurity in Iran: a systematic review and meta-analysis

  • Milad Azami
  • Zahra Jaafari
  • Shoboo Rahmati
  • Afsar Dastjani Farahani
  • Gholamreza Badfar
Open Access
Research article
Part of the following topical collections:
  1. Retina

Abstract

Background

Retinopathy of prematurity (ROP) refers to the developmental disorder of the retina in premature infants and is one of the most serious and most dangerous complications in premature infants. The prevalence of ROP in Iran is different in various parts of Iran and its prevalence is reported to be 1–70% in different regions. This study aims to determine the prevalence and risk factors of ROP in Iran.

Methods

This review article was conducted based on the preferred reporting items for systematic review and meta-analysis (PRISMA) protocols. To find literature about ROP in Iran, a comprehensive search was done using MeSH keywords in several online databases such as PubMed, Ovid, Science Direct, EMBASE, Web of Science, CINAHL, EBSCO, Magiran, Iranmedex, SID, Medlib, IranDoc, as well as the Google Scholar search engine until May 2017. Comprehensive Meta-analysis Software (CMA) Version 2 was used for data analysis.

Results

According to 42 studies including 18,000 premature infants, the prevalence of ROP was reported to be 23.5% (95% CI: 20.4–26.8) in Iran. The prevalence of ROP stages 1, 2, 3, 4 and 5 was 7.9% (95% CI: 5.3–11.5), 9.7% (95% CI: 6.1–15.3), 2.8% (95% CI: 1.6–4.9), 2.9% (95% CI: 1.9–4.5) and 3.6% (95% CI: 2.4–5.2), respectively. The prevalence of ROP in Iranian girls and boys premature infants was 18.3% (95% CI: 12.8–25.4) and 18.9% (95% CI: 11.9–28.5), respectively. The lowest prevalence of ROP was in the West of Iran (12.3% [95% CI: 7.6–19.1]), while the highest prevalence was associated with the Center of Iran (24.9% [95% CI: 21.8–28.4]). The prevalence of ROP is increasing according to the year of study, and this relationship is not significant (p = 0.181). The significant risk factors for ROP were small gestational age (p < 0.001), low birth weight (p < 0.001), septicemia (p = 0.021), respiratory distress syndrome (p = 0.036), intraventricular hemorrhage (p = 0.005), continuous positive pressure ventilation (p = 0.023), saturation above 50% (p = 0.023), apnea (p = 0.002), frequency and duration of blood transfusion, oxygen therapy and phototherapy (p < 0.05), whereas pre-eclampsia decreased the prevalence of ROP (p = 0.014).

Conclusion

Considering the high prevalence of ROP in Iran, screening and close supervision by experienced ophthalmologists to diagnose and treat the common complications of pre-maturity and prevent visual impairment or blindness is necessary.

Keywords

Meta-analysis Retinopathy of prematurity Iran Prevalence Risk factor 

Abbreviations

CI

Confidence interval

GA

Gestational age

IVH

Intraventricular hemorrhage

PRISMA

Preferred Reporting Items for Systematic Reviews and Meta-Analyses Protocols

RDS

Respiratory Distress Syndrome

ROP

Retinopathy of prematurity

W

Week

Background

Retinopathy of prematurity (ROP) refers to the developmental disorder of the retina in premature infants and is one of the most serious and most dangerous complications in premature infants.

Embryonic retinal arteries start to grow in the third month of pregnancy and their development ends at birth. Therefore, the stages of evolution of the eye are defective in premature infants, and the growth of the vessels is either stopped or unusual, and ultimately, the vessels become very fragile, which can lead to visual impairment in severe cases [1].

Despite considerable progress made in the treatment of ROP, it is still a common cause of reduced vision in children in developed countries, and its prevalence is increasing [2, 3, 4]. This is a preventable disease and responds to treatments appropriately if diagnosed at early stages, but in case of delayed diagnosis and treatment, it may lead to blindness [5].

The first incidences of ROP were reported in the 1940s and 1950s, mainly as a result of the use of supplemental oxygen without supervision (first epidemic). Although the survival of premature infants improved in the following decades, and despite improved monitoring methods for oxygen supplements, ROP emerged with an increasing incidence (second epidemic) [6]. Over the past decade, the increasing incidence of ROP blindness has been recorded in low-income countries. Studies show that ROP is the leading cause of blindness in China, Southeast Asia, South America, Latin America, and Eastern Europe, especially in urban centers of newly industrialized countries, and this is referred to as the “third epidemic” [7].

ROP is a multifactorial disease and the most important risk factors are preterm delivery, especially before the 32nd week of gestation and birth weight less than 1500 g. Apnea, intraventricular hemorrhage, various maternal factors (diabetes, preeclampsia, mother’s smoking), respiratory disorders, infection, vitamin E deficiency, heart disease, increased blood carbon dioxide, increased oxygen (O2) consumption, decreased PH, decreased blood O2, bradycardia, transfusion, amount of received oxygen and duration of ventilation are other risk factors for ROP [8, 9, 10].

The prevalence of ROP in different regions of Iran is different and its prevalence is reported to be 1–70% in different regions [11, 12, 13, 14]. Considering the abovementioned issues and the importance of the subject, as well as the diversity of reports in Iranian studies, it is necessary to carry out more extensive and precise studies. Meta-analysis is a method that collects and analyzes multiple research data with a common purpose to provide a reliable estimate of the impact of some interventions or observations in medicine [15, 16]. Obviously, the sample size in meta-analysis becomes larger by collecting data from several studies and therefore the range of changes and probabilities will be reduced; therefore, the significance of statistical results increases [16, 17]. This study aims to determine the incidence and risk factors for ROP in Iran.

Methods

Study protocol

This review article was conducted based on the preferred reporting items for systematic review and meta-analysis (PRISMA) protocols [16]. The study was conducted in five stages: design and search strategy, a collection of articles and their systematic review, evaluation of inclusion and exclusion criteria, qualitative evaluation and statistical analysis of data. To avoid bias in the study, each of the above steps was carried out by two researchers independently. In case of differences in the results obtained by the two researchers, a third researcher intervened to reach an agreement.

Search strategy

To find literature about ROP in Iran, a comprehensive search was done using the terms (Retinopathy of Prematurity [MeSH]) AND (“Incidence” [MeSH] OR “Epidemiology” [MeSH]), OR (“Prevalence” [MeSH]) AND (“Iran” [MeSH]) in 7 international databases including PubMed, Ovid, Science Direct, EMBASE, Web of Science, CINAHL, EBSCO, and 5 national databases including Magiran, Iranmedex, SID, Medlib, IranDoc, as well as Google Scholar search engine until May 2017. References to all relevant articles were reviewed. Due to the inability of Iranian databases to search using Boolean operators (AND, OR and NOT), searches on these databases were only performed using the keywords.

Inclusion and exclusion criteria

Articles with the following characteristics were chosen for meta-analysis: 1. Original research papers published either in Persian or English; 2. Medical dissertations; 3. Review of the prevalence or risk factors for ROP. The exclusion criteria were: 1. Non-random sample for estimating the prevalence; 2. Being irrelevant to the topic; 3. Congress papers; 4. Sample size other than premature infants; 5. Non-Iranian studies; 6. Review articles, case reports, editorials; 7. Duplicate studies and 8. Low-quality studies.

ROP detection criteria

ROP was diagnosed by an expert through examination of retinas of infants using indirect ophthalmoscope.

Selection of studies

First, all related articles (articles with affiliations containing Iranian authors) were collected and a list of titles was prepared at the end of the search and removal of duplicates. After blinding the specifications of the articles by on researcher (Milad Azami), including the name of the journal and the name of the author, the full text of the articles was presented to the researchers. Each article was studied by two researchers independently (Gholamreza Badfar, Afsar Dastjani Farahani). If the article was rejected, the reason for this rejection was mentioned. In case of disagreement between the two authors, the article was judged by the team of researchers.

Quality of studies

Using the standard modified Newcastle Ottawa Scale (NOS) checklist [18], which included 8 sections. Thus, the minimum and maximum score available on this checklist were 0 and 8, respectively. Accordingly, the studies were divided into three categories: 1. low quality with a score less than 5; 2. moderate quality with a score of 5–6; and 3. high quality with a score of 7–8. Finally, the moderate to high quality studies were selected for the meta-analysis stage.

Data extraction

The raw data of the prepared articles were extracted using a premade checklist. The checklist includes the name of the authors, published year the year of study, the location of the study, the study design, quality score, sample size, the prevalence of ROP, the ROP detection criteria, the prevalence of ROP based on gender (ROP) and ROP risk factors.

Statistical analysis

In each study, the prevalence of ROP was considered as the probability of binomial distribution. To evaluate the heterogeneity of the studies, Cochran’s Q test and I2 index were used [19]. There are three categories for the I2 index: heterogeneity lower than 25%, heterogeneity between 25% and 75% and heterogeneity more than 75%. Considering the heterogeneity of the studies, a random effects model was used to combine ROP prevalence. For ROP risk factors, the fixed effects model and the random effects model were used, respectively in the case of low heterogeneity and high heterogeneity in the meta-analysis [20, 21]. Sensitivity analysis was performed to identify the influence of a single study on the combined result incidence or any risk factors (with ≥ 7 studies). In order to identify the cause of heterogeneity of ROP prevalence, sub-groups analysis of ROP were carried out based on geographical region, province and quality of studies, while the meta-regression model (method of moments) was carried out based on the year of studies [22]. Egger and Begg’s tests were used to identify publications bias. Data analysis was performed using Comprehensive Meta-Analysis Software Version 2 and the significance level in the tests was considered to be lower than 0.05.

Results

Search results and characteristics

In the initial search, 452 studies were found to be related to the topic. Two independent researchers reviewed the title and the abstract. If the title or abstract was likely to be related to the topic, the full text was reviewed. After reviewing the full text of 74 relevant articles, 30 articles were omitted due to lacking the necessary criteria and finally 44 qualified studies entered the qualitative assessment stage (Fig. 1). Table 1 shows the characteristics of each study.
Fig. 1

PRISMA flowchart for the selection of studies

Table 1

Summary of demographic characteristics in studies into a meta-analysis

Ref.

First author, Published Year

Year of study

GAa (week)

BWb (gr)

Place

Sample size

Prevalence (%)

Quality

All

Non-ROPc

ROP

[11]

Naderian Gh, 2011

2009

< 34

And ≤ 1800

Isfahan

100

71

29

29

Moderate

[11]

Naderian Gh(1), 2011

2009

< 34

And ≤ 1800

Isfahan

100

58

42

42

Moderate

[12, 13]

Mostafa Gharebagh M, 2012

2008

< 34

Tabriz

71

41

30

 

High

[14]

Nakhshab M, 2016

2014

< 30 or < 34d

Sari

146

122

24

16.44

High

[52]

Naderian G, 2009

2002

25–34

And 600–1800

Isfahan

796

662

134

16.8

Moderate

[53]

Hosseini H, 2009

2006

< 34

Shiraz

1024

1004

20

1.95

High

[54]

Karkhaneh R, 2005

2000

≤ 37

And ≤ 2500

Tehran

185

162

23

12.4

High

[55]

Naderian G, 2010

2003

Isfahan

604

498

106

17.5

High

[56]

Mansouri M, 2007

2004

≤ 32

And ≤ 1500

Tehran

147

103

44

29.9

High

[57]

Nakshab M, 2003

2001

≤ 2500

Sari

68

60

8

11.7

High

[58]

Daraie G, 2016

2008

< 37

Or < 2000

Semnan

270

267

3

1.1

Moderate

[59]

Fayazi A,2009

2005

< 32

Or < 1500 or 1500–2500*

Tabriz

399

370

29

7.26

Moderate

[60]

Sadeghi K, 2008

2006

< 36

And < 2000

Tabriz

150

124

26

17.3

Moderate

[61]

Ebrahimiadib N, 2016

2011

< 37

Or < 3000

Tehran

1896

1326

570

30.06

Moderate

[62]

Ghaseminejad A, 2011

2006

≤ 36

And ≤ 2500

Kerman

83

59

24

29

High

[63]

Khatami F, 2008

2000

< 34

Or < 2000

Mashhad

50

36

14

28

Moderate

[64]

Sabzehei MK, 2013

2007

< 1500

Tehran

414

343

71

17.14

Moderate

[65]

Saeidi R, 2009

2005

≤ 32

Or < 1500

Mashhad

47

43

4

8.5

Moderate

[66]

Azin Far B, 2005

2001

< 29

And < 1500

Babol

100

56

44

44

High

[67]

Karkhanehyousefi N, 2009

2009

Babol

100

61

39

39

Moderate

[68]

Ebrahimzadeh A, 2009

2003

Tehran

1343

874

469

34.9

High

[69]

Mirzaee SA, 2010

2008

< 2000

Tehran

74

50

24

324

Moderate

[70]

Mousavi Z, 2009

2001

24–36

And 600–2900

Tehran

797

540

257

32.24

Moderate

[71]

Fouladinejad M, 2009

2004

≤ 34

Gorgan

89

84

5

5.6

High

[72]

Mousavi S, 2008

2001

24–36

And 600–2800

Tehran

693

474

219

31.6

Moderate

[73]

Sadeghzadeh M, 2016

2001

450–3000

Zanjan

78

77

1

1.2

Moderate

[74]

Bayat-Mokhtari M, 2010

2006

<  1500 Or 1500–2000*

Shiraz

199

115

84

42

High

[75]

Karkhaneh R, 2001

1997

< 37

Or < 2500

Tehran

150

141

9

6

High

[76]

Babaei H, 2012

2009

≤ 1500

Kermanshah

84

73

11

13.1

Moderate

[77]

Abrishami M, 2013

2006

<  32

Mashhad

122

90

32

26.2

High

[78]

Riazi-Esfahani M, 2008

2002

≤ 37

And ≤ 2500

Tehran

165

125

40

24.24

Moderate

[79]

Alizadeh Y, 2015

2005

≤ 36

And ≤ 2500

Rasht

310

246

64

20.6

High

[80]

Mousavi SZ, 2010

2003

Tehran

605

415

190

31.4

Moderate

[81]

Mousavi Z, 2010

2003

Tehran

1053

673

380

36.1

High

[82]

Feghhi M, 2012

2006

< 32

And ≤ 2000

Ahvaz

576

393

183

32

High

[83]

Afarid M, 2012

2006

≤ 32

And ≤ 2000

Shiraz

787

494

293

37.2

Moderate

[84]

Ahmadpourkacho M, 2014

2009

< 28

And < 1500 or 1500–2000*

Babol

256

76

180

70.31

High

[85]

AhmadpourKacho M, 2014

2007

< 34

And < 2000

Babol

155

85

70

45.2

Moderate

[86]

Rasoulinejad SA, 2016

2007

< 36

And < 2500

Babol

680

374

306

45

High

[87]

Karkhaneh R, 2008

2003

<  37

Tehran

953

624

329

34.5

High

[88]

Khalesi N, 2015

2013

Tehran

120

60

60

 

Moderate

[89]

Ebrahim M, 2010

2004

<  37

Babol

173

140

33

19.1

High

[90]

Roohipoor R, 2016

2012

≤ 37

And ≤ 3000

Tehran

1932

1362

570

3

High

[91]

Mansouri M, 2016

2013

<  34

Or < 2000

Sanandaj

47

42

5

10.6

High

aGestational age; bBirth weight; cRetinopathy of prematurity; dWith unstable condition

Prevalence

Reviewing 42 studies with a total sample size of 18,000 premature infants, the prevalence of ROP in Iran was estimated to be 23.5% (95% CI: 20.4–26.8). The lowest and highest prevalence was related to the studies in Semnan (2008) (1.1%) (58) and in Babol (2009) (70.3%) (84), respectively (Fig. 2).
Fig. 2

The prevalence of retinopathy of prematurity in Iran. Random effects model

Sensitivity analysis and cumulative analysis for ROP

The sensitivity analysis of the prevalence or risk factors of ROP and its 95% confidence interval (CI) was estimated simultaneously regardless of one study and the results showed that the incidence or risk factors of ROP were not significantly changed before and after the deletion of each study. (Fig. 3a). Cumulative analysis for incidence of ROP based on the year of publication is shown in Fig. 3b.
Fig. 3

Sensitivity analysis (a) and cumulative analysis based on the year of publication (b) for prevalence of retinopathy of prematurity in Iran. Random effects model

Subgroup analysis of ROP prevalence based on geographic region

In the reviewed studies, 2, 4, 12, 4, and 20 studies were related to the West, East, North, South, and Center of Iran, respectively. The prevalence of ROP in the five regions of Iran is shown in Table 2 and the lowest incidence of ROP was in west of Iran (12.3% [95% CI: 7.6–19.1]), while the highest prevalence was related to the center of Iran (24.9% [95% CI: 21.8–28.4]) (Table 2).
Table 2

The prevalence of ROP based on region, gender, provinces and quality of studies

Variable

Studies (Na)

Sample (N)

Heterogeneity

95% CIb

Prevalence (%)

I2

P-Value

Region

Center

20

12,355

93.65

< 0.001

21.8 to 28.4

24.9

East

4

302

57.79

0.07

17 to 33

24.1

North

12

2626

97.09

< 0.001

15.9 to 37.1

25

South

4

2586

98.60

< 0.001

9.2 to 37.1

20.5

West

2

131

0

0.67

7.6 to 19.1

12.3

Test for subgroup differences: Q = 9.67, df(Q) = 4, P = 0.046

Gender

Boys

11

1467

92.65

< 0.001

11.9 to 28.5

18.9

Girls

11

1184

85.02

< 0.001

12.8 to 25.4

18.3

Rate ratio of boys to girls: ORc = 1.07(0.86 to 1.33, P = 0.501)

Provinces

Khozestan

1

576

0

28.3 to 35.9

32

Mazandaran

8

1678

95.77

< 0.001

23.5 to 48.2

34.8

Isfahan

4

1600

92.48

< 0.001

16.5 to 35

24.6

Golestan

1

89

0

2.3 to 12.8

5.6

Kerman

1

83

0

20.3 to 39.6

29

Kermanshah

3

84

0

7.4 to 22.1

13.1

Razavi Khorasan

3

219

67.89

0.044

12.4 to 34.2

21.3

Guilan

1

310

0

16.5 to 25.5

20.9

Kurdistan

1

47

0

4.5 to 23.1

10.6

Semnan

1

270

0

0.4 to 3.4

1.1

Fars

3

2010

99.09

< 0.001

4 to 50.8

17.2

East Azarbaijan

2

549

91.32

0.001

4.6 to 25

11.3

Tehran

14

10,407

91.32

< 0.001

25.1 to 31

28

Zanjan

1

78

0

0.2 to 8.5

1.2

Test for subgroup differences: Q = 97.59, df(Q) = 13, P < 0.001

Quality

Medium

20

7760

63.68

< 0.001

16.6 to 28.0

23.5

High

22

10,240

96.65

< 0.001

19.1 to 28.7

23.5

Test for subgroup differences: Q = 0, df(Q) = 1, P = 0.995

aNumber

bConfidence interval

Subgroup analysis of ROP prevalence based on province

Table 2 and Fig. 4 show the prevalence of ROP based on Iran’s provinces. The highest prevalence was in provinces of Mazandaran (34.8%) and Khuzestan (32%), and the lowest prevalence was in the provinces of Semnan (1.1%) and Zanjan (1.2%).
Fig. 4

Geographical distribution of retinopathy of prematurity in Iran

Subgroup analysis of ROP prevalence based on the quality of studies

The prevalence of ROP in moderate and high-quality studies was 23.5% (95% CI: 16.6–28.0) and 23.5% (95% CI: 19.1–28.7), respectively, and the difference was not statistically significant (p = 0.995) (Table 2).

The prevalence of ROP based on gender

The prevalence of ROP in girls and boys premature infants was 18.3% (95% CI: 12.8–25.4) and 18.9% (95% CI: 11.9–28.5), respectively. Their difference was not statistically significant (P = 0.501) (Table 2).

The prevalence of ROP based on stage

The prevalence of stages 1, 2, 3, 4 and 5 were reported in 10, eight, nine, five, and five studies, respectively. Fig. 5 shows the prevalence of ROP at different stages. The prevalence of stages 1, 2, 3, 4 and 5 was 7.9% (95% CI: 5.3–11.5), 9.7% (95% CI: 6.1–15.3), 2.8% (95% CI: 1.6–4.9), 2.9% (95% CI: 1.9–4.5), and 3.6% (95% CI: 2.4–5.2), respectively.
Fig. 5

The prevalence of stages I (a), II (b), III (c), IV (d), V (e) retinopathy of prematurity. Random effects model

Meta-regression

Meta-regression model in Fig. 6 shows that the incidence of ROP is increasing according to the year of study, and this relationship is not statistically significant (meta-regression coefficient: 0.034, 95% CI -0.016 to 0.085, P = 0.181).
Fig. 6

Meta-regression of ROP prevalence based on years of studies

Publication bias

The significance level of publication bias in the reviewed studies was 0.003 and 0.002 according to Egger and Begg’s tests, respectively, which is shown in Fig. 7.
Fig. 7

Publication bias in the studies

ROP risk factors

The meta-analysis results of evaluating the risk factors of ROP are shown in Table 3. ROP risk factors include certain variables such as continuous positive pressure (CPAP) (P = 0.023), the prevalence of blood transfusion (P = 0.001), septicemia (P = 0.021), weight < 1000 g (P < 0.001), weight <  1500 g (P < 0.0001), frequency of phototherapy (P < 0.0001), the frequency of oxygen therapy (P = 0.049), apnea (P = 00.2), intraventricular hemorrhage (IVH) (P = 0.005), respiratory distress syndrome (RDS) (P = 0.036), gestational age (GA) ≤ 28 W(week) (P < 0.001), GA ≤32 W (P < 0.001), saturation over 50% (P < 0.001), mean GA (P < 0.001), mean weight (P < 0.0001), oxygen therapy duration (P < 0.001) and phototherapy duration (P < 0.0001); however, preeclampsia significantly decreases the prevalence of ROP (P = 0.014).
Table 3

Risk factor for retinopathy of prematurity in Iran

Variables

Studies(Na)

Sample (N)

Heterogeneity

OR (95%CIb)

P-Value

Model in Meta-analysis

Case

Control

I2

P-Value

Twin birth

4

804

1868

46.97

0.129

1.62 (0.94 to 2.81)

0.081

Randomc

Mechanical ventilation

6

1131

2493

73.35

0.002

1.81 (0.80 to 1.73)

0.39

Random

Continuous positive pressure ventilation

2

62

131

64.11

0.095

3.97 (1.21 to 13.01)

0.023

Random

Blood transfusion (N)

16

1820

4167

91.34

< 0.001

2.38 (1.43 to 3.94)

0.001

Random

Septicemia

11

1327

2965

80.75

< 0.001

1.96 (1.10 to 3.48)

0.021

Random

Birth weight < 1000 g

9

573

2093

59.65

0.011

4.16 (2.35 to 7.35)

< 0.001

Random

Birth weight < 1500 g

10

559

1984

43.34

0.069

3.74 (2.54 to 5.49)

< 0.001

Random

Phototherapy (N)

11

1380

3355

80.69

< 0.001

1.50 (1.00 to 2.27)

0.049

Random

Oxygen therapy (N)

14

726

3124

87.39

< 0.001

3.06 (1.29 to 7.27)

0.011

Random

Need for resuscitation

2

56

212

86.50

0.006

5.01 (0.18 to 135.71)

0.338

Random

Apnea

3

114

492

72.08

0.028

4.41 (1.70 to 11.40)

0.002

Random

Congenital heart disease

2

50

246

67.29

0.08

2.13 (0.10 to 45.62)

0.626

Random

Inter-ventricular hemorrhage

11

1223

3178

76.36

< 0.001

2.24 (1.2 to 3.95)

0.005

Random

Acidosis

3

132

296

62.62

0.069

2.56 (0.81 to 8.06)

0.106

Random

Cesarean section

4

375

830

47.88

0.124

1.08 (0.53 to 2.18)

0.82

Random

Preeclampsia

2

108

237

0

0.82

0.12 (0.02 to 0.65)

0.014

Fixedd

Respiratory distress syndrome

11

2039

2618

80.13

< 0.001

1.64 (1.03 to 2.61)

0.036

Random

Saturation above 50%

4

118

656

30.30

0.23

8.35 (3.14 to 22.18)

< 0.001

Random

Normal Vaginal Delivery

4

375

830

46.63

0.132

1.01 (0.50 to 2.02)

0.969

Random

Multiple pregnancy

6

1199

2518

40.20

0.137

0.92 (0.73 to 1.16)

0.517

Random

Gestational age ≤ 28

6

551

1440

75.88

< 0.001

5.20 (2.31 to 11.73)

< 0.001

Random

Gestational age ≤ 32

9

689

1885

64.84

0.004

7.88 (4.62 to 13.46)

< 0.001

Random

Birth weight (gr)

7

1495

2893

97.30

< 0.001

0.98 (0.97 to 0.99)

< 0.001

Random

Gestational age (week)

7

1495

2893

84.20

< 0.001

0.67 (0.59 to 0.770)

< 0.001

Random

Variables

Studies(Na)

Sample (N)

Heterogeneity

Mean Difference (95% CIb)

P-Value

 

Case

Control

I2

P-Value

Gestational age (weeks)

18

1835

4126

94.53

< 0.001

2.08(1.50 to 2.66)

< 0.001

Random

Birth weight (gr)

19

1782

4519

95.94

< 0.001

305.39(236.09 to 374.69)

< 0.001

Random

Oxygen therapy (day)

11

1399

3214

96.04

< 0.001

−4.36(−6.09 to −2.63)

< 0.001

Random

Phototherapy (days)

4

78

308

83.80

< 0.001

−2.08(−3.81 to −0.35)

< 0.001

Random

Apgar score in the first minute

3

174

216

63.30

0.66

1.07(0.45 to 1.68)

0.001

Random

Apgar score

3

64

272

76.34

0.015

0.43(−0.25 to −1.13)

0.21

Random

Mechanical ventilation (days)

2

114

154

88.81

0.003

−4.53(−9.17 to 0.10)

0.55

Random

Bilirubin (mg/di)

3

54

186

7.70

0.33

−0.27(−1.40 to 0.86)

0.63

Random

Blood transfusion (duration)

2

98

151

0

0.98

−0.69(−0.96 to − 0.42)

< 0.001

Fixed

clinical risk index for babies

2

161

250

58.84

0.11

−0.62(− 1.40 to 0.16)

0.11

Random

aNumber

bConfidence interval

cRandom effects model

dFixed effects model

Discussion

The present study is the first systematic and meta-analytic review on the prevalence and risk factors of ROP in Iran. The results of this meta-analysis showed that the prevalence of ROP in 18,000 Iranian premature infants was 23.5%, and the prevalence for stages 1, 2, 3, 4 and 5 was 7.9%, 9.7%, 2.8%, 2.9% and 3.6%, respectively. In this study, the level of heterogeneity was high for ROP studies (95.6%). The results of the subgroup analysis showed that geographic regions and the provinces could be a cause of high heterogeneity. However, this difference can be a reflection of studies conducted on different samples based on the GA or neonatal weight.

ROP is still a major cause of potentially preventable blindness around the world [23]. According to guidelines published by the American Academy of Ophthalmology, the American Academy of Children, and the American Association for Ophthalmology for Children and Strabismus for ROP screening, infants weighing less than 1500 g or GA ≤ 30 weeks, and infants weighing between 1500 and 2000 g or GA > 30 weeks with an unstable clinical course should receive dilated ophthalmoscopy examinations for ROP [24].

The prevalence of ROP in various studies is mainly due to differences in mean GA and birth weight of infants in each study. Based on GA, the prevalence of ROP significantly decreases from 77.9% in GA 24–25 to 1.1% in GA 30–31, which indicates the direct role of GA in ROP incidence. These results are completely consistent with the data published in other literature [25, 26, 27, 28, 29, 30, 31]. Moreover, in a meta-analysis study in Iran, the prevalence of prematurity was reported to be 9.2% (95% CI: 7.6–10.7) [32]. Therefore, the high prevalence of ROP in Iran (23.5%) can be explained by the high prevalence of prematurity.

In a study by Tabarez-Carvajal et al. among 3018 premature infants, the incidence of stages 1, 2, 3, 4, and 5 was reported to be 8.34%, 8.78%, 1.9%, 0.03%, and 0.30%, respectively [33]. In another study by Abdel HA et al., the prevalence of ROP stage 1 was 10.4%, stage 2 was 5.2% and stage 3 was 3.45%, and none of the infants had ROP at stages 4 or 5 [34]. But in the present study, the prevalence of ROP stages 4 and 5 was higher.

ROP is a multi-factorial disease, and in the present study, the strongest risk factor for ROP was prematurity and low birth weight. Most studies have demonstrated that prematurity and low birth weight are the strongest predictive factors of ROP, which indicates the crucial role of factors associated with the progression of the ROP disease [35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45].

After low birth weight and prematurity, exposure to oxygen for a long period and saturation over 50% were the most important risk factors for ROP in this study, which was consistent with the results of many other studies [42, 43, 44, 45, 46, 47]. Due to inadequate antioxidant defense system, premature infants are not evolved to live in an oxygen-rich ectopic environment [48, 49]. Oxidative stress is the result of various organs’ exposure to free radicals of oxygen after being exposed to high concentrations of oxygen, which can lead to the progression of many pathogens such as ROP, necrotizing enterocolitis, IVH, bronchopulmonary dysplasia, and periventricular leukomalacia [50, 51].

In this study, other significant relationships with ROP were also found, including frequency and duration of blood transfusion, phototherapy, septicemia, apnea, IVH, and RDS. The comparison between the risk factors in our study and other reports is shown in Table 4.
Table 4

Risk factor for retinopathy of prematurity in other studies

Study details

GA (weeks)

BW (gr)

Risk factors

Reyes et al., 2017. Oman [46]

< 32

< 1500

low BW, low GA, duration of invasive ventilation, duration of oxygen therapy, duration of nasal CPAP, late onset clinical or proven sepsis

Shah et al., 2005 Singapore [40]

< 32

< 1500

Preeclampsia, low BW, prolonged duration of ventilation, pulmonary hemorrhage and CPAP

Yau et al., 2016, China [45]

< 32 and > 32

< 1500

low GA, low BW, preeclampsia, gestational diabetes mellitus, inotrope use, postnatal hypotension, apgar score (1 min, 5 min and 10 min), respiratory distress syndrome, bronchopulmonary dysplasia, invasive mechanical ventilation, surfactant use, oxygen supplement, patent ductus arteriosus, thrombocytopenia, blood transfusion, anemia, NSAID use, sepsis

Abdel HA et al., 2012, Egypt [34]

< 32 and > 32

< 1500 and > 1500

low GA, oxygen therapy, frequency of blood transfusions and sepsis

Chen et al., 2011, USA [41]

< 30

< 1500

low GA, Sepsis, oxygen exposure

Hadi and Hamdy, 2013, Egypt [37]

< 32

< 1250

low GA, low BW, Ventilation, blood transfusions, sepsis, Patent ductus arteriosus, IVH

Nair et al., 2001, Oman [36]

< 32

< 1500

low BW, Low GA, TPN

BW Birth weight, GA Gestational age, PDA Patent ductus arteriosus, CPAP Continuous positive pressure ventilation, IVH Intraventricular hemorrhage, TPN Total parenteral nutrition

Conclusion

Finally, it can be concluded that the present systematic review and meta-analysis summarizes the results of previous studies and provides a comprehensive view of ROP in Iran. Although the prevalence of ROP in Iran is similar to some developing countries, it is much higher than some other countries. Therefore, this fact highlights the importance of preventing and treating ROP and its following complications. To achieve a more favorable level and reduce the prevalence in the coming years, screening and close monitoring by experienced ophthalmologists are essential to diagnose and treat the common complications of prematurity and prevent visual impairment or blindness.

Notes

Acknowledgements

We thanks Behbahan University of Medical Sciences for the financial support.

Funding

Behbahan University of Medical Sciences.

Availability of data and materials

Because this article is a meta-analysis also the data extracted from the relevant articles in Iran.

Authors’ contributions

MA was involved in study concept and design, acquisition of data, search, quality evaluation of studies, drafting of the manuscript, analysis and interpretation of data, critical revision of the manuscript for important intellectual content, approval of final version, and accountable for accuracy and integrity of the work. ZJ was involved in search, interpretation of data, acquisition of data, quality evaluation of studies, drafting of the manuscript, and approval of final version. ShR was involved in search, analysis and interpretation of data, quality evaluation of studies, drafting of the manuscript, and approval of final version. GhB was involved in study concept and design, acquisition of data, quality evaluation of studies, drafting of the manuscript, critical revision of the manuscript for important intellectual content, approval of final version, administrative, technical or material support and accountable for accuracy and integrity of the work. ADF was involved in search critical revision of the manuscript for important intellectual content, and approval of final version.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.
    Zin A, Gole GA. Retinopathy of prematurity-incidence today. Clin Perinatol. 2013;40(2):185–200.CrossRefPubMedGoogle Scholar
  2. 2.
    Gergely K, Gerinec A. Retinopathy of prematurity--epidemics, incidence, prevalence, blindness. Bratisl Lek Listy. 2009;111(9):514–7.Google Scholar
  3. 3.
    Zin A. R etinopathyof P re maturity-I ncidence to day. 2013.Google Scholar
  4. 4.
    Kliegman RM, Behrman RE, Jenson HB,et al. Nelson textbook of pediatrics E-book: Elsevier health sciences; 2007.Google Scholar
  5. 5.
    Wilson CM, Ells AL, Fielder AR. The challenge of screening for retinopathy of prematurity. Clin Perinatol. 2013;40(2):241–59.CrossRefPubMedGoogle Scholar
  6. 6.
    Gibson DL, Sheps SB, Schechter MT, et al. Retinopathy of prematurity: a new epidemic? Pediatrics. 1989;83:486–92.PubMedGoogle Scholar
  7. 7.
    Augsburger JJBN. Yanoff M, Duker JS, editors. Ophtalmology. St. Louis, MO: Mosby 2004. p. 1097–102.Google Scholar
  8. 8.
    Senthil MP, Salowi MA, Bujang MA, et al. Risk factors and prediction models for retinopathy of prematurity. Malays J Med Sci. 2015;22(5):57.PubMedPubMedCentralGoogle Scholar
  9. 9.
    GEBEŞÇE A, USLU H, KELEŞ E, et al. Retinopathy of prematurity: incidence, risk factors, and evaluation of screening criteria. Turk J Med Sci. 2016;46(2):315–20.CrossRefPubMedGoogle Scholar
  10. 10.
    Edy Siswanto J, Sauer PJ. Retinopathy of prematurity in Indonesia: Incidence and risk factors. J Neonatal Perinatal Med. 2017;10(1):85-90.  https://doi.org/10.3233/NPM-915142.
  11. 11.
    Naderian GIR, Mohammadizadeh M, Najafabadi FBZ, et al. The frequency of retinopathy of prematurity in premature infants referred to an ophthalmology Clinic in Isfahan. J Isfahan Med Sch. 29(128):126–30.Google Scholar
  12. 12.
    Gharebagh M, Sadeghi K, Zarghami N, Mostafidi H. Evaluation of vascular endothelial growth factor, leptin and insulin-like growth factor in precocious retinopathy. Urmia Med J. 2012;23(2):183–90.Google Scholar
  13. 13.
    Gharehbaghi MM, Peirovifar A, Sadeghi K. Plasma leptin concentrations in preterm infants with retinopathy of prematurity (ROP). Iran J Neonatol. 2012;3(1):12–6.Google Scholar
  14. 14.
    Nakhshab MAA, Dargahi S, Farhadi R, et al. The incidence rate of retinopathy of prematurity and related risk factors: a study on premature neonates hospitalized in two hospitals in sari, Iran, 2014-2015. J Kerman Univ Med Sci. 2016;23(3):296–307.Google Scholar
  15. 15.
    Badfar G, Shohani M, Nasirkandy MP, et al. Epidemiology of hepatitis B in pregnant Iranian women: a systematic review and meta-analysis. Arch Virol. 2018;163(2):319-330.  https://doi.org/10.1007/s00705-017-3551-6.
  16. 16.
    Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.  https://doi.org/10.1371/journal.pmed.1000097. Epub 2009 Jul 21CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Sayehmiri K, Tavan H, Sayehmiri F, et al. Prevalence of epilepsy in Iran: a meta-analysis and systematic review. Iran J Child Neurol. 2014;8(4):9–17.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analysis. 2011. Available: www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 25 Nov 2012.
  19. 19.
    Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions, vol. 4. Hoboken: Wiley; 2011.Google Scholar
  20. 20.
    Ades A, Lu G, Higgins J. The interpretation of random-effects meta-analysis in decision models. Med Decis Mak. 2005;25(6):646–54.CrossRefGoogle Scholar
  21. 21.
    Borenstein M, Hedges LV, Higgins J, et al. A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods. 2010;1(2):97–111.CrossRefPubMedGoogle Scholar
  22. 22.
    Borenstein M, Hedges LV, Higgins J, Rothstein HR. Meta-Regression. Introduction to meta-analysis; 2009. p. 187–203.CrossRefGoogle Scholar
  23. 23.
    Clemett R, Darlow B. Results of screening low-birth-weight infants for retinopathy of prematurity. Curr Opin Ophthalmol. 1999;10:155–63.CrossRefPubMedGoogle Scholar
  24. 24.
    Ophthalmology AAoPSo. Screening examination of premature infants for retinopathy of prematurity. Pediatrics. 2013;131(1):189–95.CrossRefGoogle Scholar
  25. 25.
    Isaza G, Arora S. Incidence and severity of retinopathy of prematurity in extremely premature infants. Can J Opthalmol. 2012;47:296–300.CrossRefGoogle Scholar
  26. 26.
    Hwang JH, Lee EH, Kim EA. Retinopathy of prematurity among very-low-birth-weight infants in Korea: incidence, treatment, and risk factors. J Korean Med Sci. 2015;30(Suppl 1):S88S94.CrossRefGoogle Scholar
  27. 27.
    Gunn DJ, Cartwright DW, Gole GA. Incidence of retinopathy of prematurity in extremely premature infants over an 18-year period. Clin Exp Ophthalmol. 2012;40:93–9.CrossRefPubMedGoogle Scholar
  28. 28.
    Cerman E, Balci SY, Yenice OS, et al. Screening for retinopathy of prematurity in a tertiary ophthalmology Department in Turkey: incidence, outcomes, and risk factors. Ophthalmic Surg Lasers Imaging Retina. 2014;45:550–5.CrossRefPubMedGoogle Scholar
  29. 29.
    Mitsiakos G, Papageorgiou A. Incidence and factors predisposing to retinopathy of prematurity in inborn infants less than 32 weeks of gestation. Hippokratia. 2016;20(2):121–6.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Bas AY, Koc E, Dilmen U; ROP Neonatal Study Group. Incidence and severity of retinopathy of prematurity in Turkey. Br J Ophthalmol. 2015;99(10):1311-4.  https://doi.org/10.1136/bjophthalmol-2014-306286.
  31. 31.
    Group ETfRoPC. The incidence and course of retinopathy of prematurity: findings from the early treatment for retinopathy of prematurity study. Pediatrics 2005;116(1):15–23.Google Scholar
  32. 32.
    Vakilian K, Ranjbaran M, Khorsandi M, et al. Prevalence of preterm labor in Iran: a systematic review and meta-analysis. Int J Reprod Biomed. 2015;13(12):743–8.CrossRefGoogle Scholar
  33. 33.
    Tabarez-Carvajal AC, Montes-Cantillo M, Unkrich KH, et al. Retinopathy of prematurity: screening and treatment in Costa Rica. Br J Ophthalmol. 2017;101(12):1709–13.  https://doi.org/10.1136/bjophthalmol-2016-310005. [Epub ahead of print]CrossRefPubMedGoogle Scholar
  34. 34.
    Abdel HA, Mohamed GB, Othman MF. Retinopathy of prematurity: a study of incidence and risk factors in NICU of al-Minya University Hospital in Egypt. J Clin Neonatol. 2012;1(2):76–81.  https://doi.org/10.4103/2249-4847.96755.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Bassiouny MR. Risk factors associated with retinopathy of prematurity: a study from Oman. J Trop Pediatr. 1996;42:355–8.CrossRefPubMedGoogle Scholar
  36. 36.
    Nair PM, Ganesh A, Mitra S, et al. Retinopathy of prematurity in VLBW and extreme LBW babies. Indian J Pediatr. 2003;70:303–6.CrossRefPubMedGoogle Scholar
  37. 37.
    Hadi AM, Hamdy IS. Correlation between risk factors during the neonatal period and appearance of retinopathy of prematurity in preterm infants in neonatal intensive care units in Alexandria, Egypt. Clin Ophthalmol. 2013;7:831–7.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Ratra D, Akhundova L, Das MK. Retinopathy of prematurity like retinopathy in full-term infants. Oman J Ophthalmol. 2017;10(3):167-172.  https://doi.org/10.4103/ojo.OJO_141_2016.
  39. 39.
    Sahin A, Sahin M, Türkcü FM, et al. Incidence of retinopathy of prematurity in extremely premature infants. ISRN Pediatr. 2014;2014:134347.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Shah VA, Yeo CL, Ling YL, et al. Incidence, risk factors of retinopathy of prematurity among very low birth weight infants in Singapore. Ann Acad Med Singap. 2005;34:169–78.PubMedGoogle Scholar
  41. 41.
    Chen M, Citil A, McCabe F, et al. Infection, oxygen, and immaturity: interacting risk factors for retinopathy of prematurity. Neonatology. 2011;99:125–32.CrossRefPubMedGoogle Scholar
  42. 42.
    Darlow BA, Hutchinson JL, Henderson-Smart DJ, et al. Prenatal risk factors for severe retinopathy of prematurity among very preterm infants of the Australian and New Zealand neonatal network. Pediatrics. 2005;115:990–6.CrossRefPubMedGoogle Scholar
  43. 43.
    Badriah C, Amir I, Elvioza SR, et al. Prevalence and 325 risk factors of retinopathy of prematurity. Paediatr Indones. 2012;52:138–44. 327CrossRefGoogle Scholar
  44. 44.
    Rizalya D, Rudolf T, Rohsiswatmo R. Screening for 328 retinopathy of prematurity in hospital with limited facil- 329 ities. Sari Pediatri. 2012;14:185–90.Google Scholar
  45. 45.
    Yau GS, Lee JW, Tam VT, et al. Incidence and risk factors of retinopathy of prematurity from 2 neonatal intensive care units in a Hong Kong Chinese population. Asia Pac J Ophthalmol. 2016;5(3):185–91.  https://doi.org/10.1097/APO.0000000000000167.CrossRefGoogle Scholar
  46. 46.
    Reyes ZS, Al-Mulaabed SW, Bataclan F, et al. Retinopathy of prematurity: revisiting incidence and risk factors from Oman compared to other countries. Oman J Ophthalmol. 2017;10(1):26–32.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Yu VY, Upadhyay A. Neonatal management of the growth-restricted infant. Semin Fetal Neonatal Med. 2004;9:403–9.CrossRefPubMedGoogle Scholar
  48. 48.
    Weinberger B, Laskin DL, Heck DE, et al. Oxygen toxicity in premature infants. Toxicol Appl Pharmacol. 2002;181:60–7.CrossRefPubMedGoogle Scholar
  49. 49.
    Hardy P, Beauchamp M, Sennlaub F, et al. New insights into the retinal circulation: inflammatory lipid mediators in ischemic retinopathy. Prostaglandins Leukot Essent Fatty Acids. 2005;72:301–25.CrossRefPubMedGoogle Scholar
  50. 50.
    O'Donovan DJ, Fernandes CJ. Free radicals and diseases in premature infants. Antioxid Redox Signal. 2004;6:169–76.CrossRefPubMedGoogle Scholar
  51. 51.
    Yoon HS. Neonatal innate immunity and toll-like receptor. Korean J Pediatr. 2010;53:985–8.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Naderian G, Parvaresh M, Rismanchiyan A, et al. Refractive errors after laser therapy for retinopathy of prematurity. Int J Ophthalmol. 2009;15(1):13–8.Google Scholar
  53. 53.
    Hosseini H, Farvardin M, Attarzadeh A, et al. Advanced retinopathy of prematurity at Poostchi ROP clinic, Shiraz. Bina J Ophthalmol 2009; 15(1):19–25.Google Scholar
  54. 54.
    Karkhaneh RER, Ghojehzadeh L, Kadivar M, et al. Incidence and risk factors of retinopathy of prematurity. Bina J Ophthalmol. 2005;11(1):81–90.Google Scholar
  55. 55.
    Nadeian GMH, Hadipour M, Sajjadi H. Prevalence and rsskfactor for retinopathy of prematuority in isfahan. Bina J Ophthalmol. 2010;15(3):208–13.Google Scholar
  56. 56.
    Mansouri MRKM, Karkhaneh R, Riazi Esfahani M, et al. Prevalence and risk factors of retinopathy of prematurity in very low birth weight or low gestational age infants. Bina J Ophthalmol. 2007;12(4):428–34.Google Scholar
  57. 57.
    Nakhshab MBG, Amiri A, Ashaghi M. Prevalence of preterm infant retinopathy in neonatal intensive care unit Buali Sari Hospital. J Mazandaran Univ Med Sci. 2003;13(39):63–70.Google Scholar
  58. 58.
    Daraie G, Nooripoor S, Ashrafi AM, et al. Incidence of retinopathy of prematurity and some related factors in premature infants born at amir–al-momenin hospital in Semnan. Iran Koomesh. 2016;17(2):297–303.Google Scholar
  59. 59.
    Fayazi AHM, Fayzollazade M, GHolzar A, et al. Prevalence of retinopathy in preterm infants admitted to neonatal intensive care unit of Alzahra hospital in Tabriz. J Tabriz Univ Med Sci. 2009;30(4):63–6.Google Scholar
  60. 60.
    Sadeghi KHA, Hashemi F, Haydarzade M, et al. Prevalence and risk factors of retinopathy in preterm infants. J Tabriz Univ Med Sc. 2008;30(2):73–7.Google Scholar
  61. 61.
    Ebrahimiadib N, Roohipour R, Karkhaneh R, et al. Internet-based versus conventional referral system for retinopathy of prematurity screening in Iran. Ophthalmic Epidemiol. 2016;23(5):292–7.CrossRefPubMedGoogle Scholar
  62. 62.
    Ghaseminejad A, Niknafs P. Distribution of retinopathy of prematurity and its risk factors. Iran J Pediatr. 2011;21(2):209.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Khatami SF, Yousefi A, Bayat GF, et al. Retinopathy of prematurity among 1000-2000 gram birth weight newborn infants. Iran J Pediatr. 2008;18(2):137–42.Google Scholar
  64. 64.
    Sabzehei MK, Afjeh SA, Farahani AD, et al. Retinopathy of prematurity: incidence, risk factors, and outcome. Arch Iran Med. 2013;16(9):507.PubMedGoogle Scholar
  65. 65.
    Saeidi R, Hashemzadeh A, Ahmadi S, et al. Prevalence and predisposing factors of retinopathy of prematurity in very low-birth-weight infants discharged from NICU. Iran J Pediatr. 2009;19(1):59–63.Google Scholar
  66. 66.
    Azinfar MAM, Pasha Z, Amad M. Prevalence of premature newborns discharged from NICU and infants in Shafizadeh Ami Children's hospital [dissertation]. Babol, Iran; Babol Univ Med; 2005.Google Scholar
  67. 67.
    Karkhanehyousefi NRA, Mekaniki A. Prevalence of retinopathy in immature newborns referred to eye Clinic of Shahid Beheshti Hospital in Babol [dissertation]. Babol, Iran; Babol Univ Med; 2009.Google Scholar
  68. 68.
    Ebrahimzade MKR, Esfahani M, Kadpour M, et al. The prevalence of retinopathy in preterm infants in preterm infants referred to Farabi hospital from the beginning of the year 2002 to the beginning of 2008 and the evaluation of short-term laser therapy results [dissertation]. Tehran: Islamic Azad Univ Med; 2009.Google Scholar
  69. 69.
    Mirzaee SA, Mohagheghi P. Determine the prevalence of retinopathy (ROP) in infants admitted to the NICU department of Milad Hospital [dissertation]. Tehran: Islamic Azad Univ Med; 2010.Google Scholar
  70. 70.
    Mousavi SZ, Karkhaneh R, Riazi-Esfahani M, et al. Retinopathy of prematurity in infants with late retinal examination. J Ophthalmic Vis Res. 2009;4(1):24.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Foladinezhad MMM, GHarib M, SHishari F, Soltani M. Frequency, severity and some risk factors of retinopathy in premature infants of Taleghani Hospital in Gorgan. J Gorgan Univ Med Sc. 2009;11(2):51–4.Google Scholar
  72. 72.
    Mousavi SZKR, Riazi-Esfahani M, Mansouri MR, et al. Incidence, severity and risk factors for retinopathy ofPrematurity in premature infants with late retinal examination. Bina J Ophthalmol. 2008;13(4):412–7.Google Scholar
  73. 73.
    Sadeghzadeh M, Khoshnevisasl P, Parvaneh M, et al. Early and late outcome of premature newborns with history of neonatal intensive care units admission at 6 years old in Zanjan. Northwestern Iran Iran J Child Neurol. 2016;10(2):67.PubMedGoogle Scholar
  74. 74.
    Bayat-Mokhtari M, Pishva N, Attarzadeh A, et al. Incidence and risk factors of retinopathy of prematurity among preterm infants in shiraz/Iran. Iran J Pediatr. 2010;20(3):303.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Karkhaneh R, Shokravi N. Assessment of retinopathy of prematurity among 150 premature neonates in Farabi eye hospital. Acta Med Iran. 2001;39(1):35–8.Google Scholar
  76. 76.
    Babaei H, Ansari MR, Alipour AA, et al. Incidence and risk factors for retinopathy of prematurity in very low birth weight infants in Kermanshah. Iran World Appl Sci J. 2012;18(5):600–4.Google Scholar
  77. 77.
    Abrishami M, Maemori G-A, Boskabadi H, et al. Incidence and risk factors of retinopathy of prematurity in Mashhad. Northeast Iran Red Crescent Med J. 2013;15(3):229.CrossRefPubMedGoogle Scholar
  78. 78.
    Riazi-Esfahani M, Alizadeh Y, Karkhaneh R, et al. Retinopathy of prematurity: single versus multiple-birth pregnancies. J Ophthalmic Vis Res. 2008;3(1):47.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Alizadeh Y, Zarkesh M, Moghadam RS, et al. Incidence and risk factors for retinopathy of prematurity in north of Iran. J Ophthalmic Vis Res. 2015;10(4):424.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Mousavi SZ, Karkhaneh R, Roohipoor R, et al. Screening for retinopathy of prematurity: the role of educating the parents. J Ophthalmol. 2010;22(2):13–8.Google Scholar
  81. 81.
    MousavibS Zb EM, Roohipoor R, Jabbarvand M, et al. Characteristics of advanced stages of retinopathy of prematurity. J Ophthalmol. 2010;22(2):19–24.Google Scholar
  82. 82.
    Feghhi M, Altayeb SMH, Haghi F, et al. Incidence of retinopathy of prematurity and risk factors in the south-western region of Iran. Middle East Afr J Ophthalmol. 2012;19(1):101.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Afarid M, Hosseini H, Abtahi B. Screening for retinopathy of prematurity in south of Iran. Middle East Afr J Ophthalmol. 2012;19(3):277.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Ahmadpour-kacho M, Zahed Pasha Y, Rasoulinejad SA, et al. Correlation between retinopathy of prematurity and clinical risk index for babies score. J Tehran Univ Med S. 2014;72(6):404–11.Google Scholar
  85. 85.
    Ahmadpour-Kacho M, Jashni Motlagh A, Rasoulinejad SA, et al. Correlation between hyperglycemia and retinopathy of prematurity. Pediatr Int. 2014;56(5):726–30.CrossRefPubMedGoogle Scholar
  86. 86.
    Rasoulinejad SA, Montazeri M. Retinopathy of prematurity in neonates and its risk factors: a seven year study in northern iran. Open Ophthalmol J. 2016;10:17.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Karkhaneh R, Mousavi S-Z, Riazi-Esfahani M, et al. Incidence and risk factors of retinopathy of prematurity in a tertiary eye hospital in Tehran. Br J Ophthalmol. 2008;92(11):1446–9.CrossRefPubMedGoogle Scholar
  88. 88.
    Khalesi N, Shariat M, Fallahi M, et al. Evaluation of risk factors for retinopathy in preterm infant: a case-control study in a referral hospital in Iran. Minerva Pediatr. 2015;67(3):231–7.PubMedGoogle Scholar
  89. 89.
    Ebrahim M, Ahmad RS, Mohammad M. Incidence and risk factors of retinopathy of prematurity in Babol. North of Iran Ophthalmic Epidemiol. 2010;17(3):166–70.CrossRefPubMedGoogle Scholar
  90. 90.
    Roohipoor R, Karkhaneh R, Farahani A, et al. Retinopathy of prematurity screening criteria in Iran: new screening guidelines. Arch Dis Child Fetal Neonatal Ed. 2016;101(4):F288–F93.CrossRefPubMedGoogle Scholar
  91. 91.
    Mansouri M, Hemmatpour S, Sedighiani F, et al. Factors associated with retinopathy of prematurity in hospitalized preterm infants in Sanandaj. Iran Electronic physician. 2016;8(9):2931.CrossRefPubMedGoogle Scholar

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© The Author(s). 2018

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  • Milad Azami
    • 1
  • Zahra Jaafari
    • 2
  • Shoboo Rahmati
    • 2
  • Afsar Dastjani Farahani
    • 3
  • Gholamreza Badfar
    • 4
  1. 1.Student Research CommitteeIlam University of Medical SciencesIlamIran
  2. 2.Student Research CommitteeIlam University of Medical SciencesIlamIran
  3. 3.Iranian National ROP CommitteeTehranIran
  4. 4.Department of PediatricsBehbahan Faculty of Medical SciencesBehbahanIran

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