Acute and chronic effects of intravitreal bevacizumab on lung biomarkers of angiogenesis in the rat exposed to neonatal intermittent hypoxia

References

• Lalwani GA, Berrocal AM, Murray TG, Buch M, Cardone S, Hess D, et al. Off-label use of intravitreal bevacizumab (Avastin) for salvage treatment in progressive threshold retinopathy of prematurity. Retina. 2008; 28(3 Suppl):S13–S18. doi:10.1097/IAE.0b013e3181644ad2.
   PubMed Web of Science ®Google Scholar
• Mintz-Hittner HA, Kennedy KA, Chuang AZ, BEAT-ROP Cooperative Group, et al. Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity. N Engl J Med. 2011;364(7):603–615. doi:10.1056/NEJMoa1007374.
   PubMed Web of Science ®Google Scholar
• Gergely K, Gerinec A. Retinopathy of prematurity–epidemics, incidence, prevalence, blindness. Bratisl Lek Listy. 2010;111(9):514–517.
   PubMed Web of Science ®Google Scholar
• Martin RJ, Di Fiore JM, Macfarlane PM, Wilson CG. Physiologic basis for intermittent hypoxic episodes in preterm infants. Adv Exp Med Biol. 2012;758:351–358. doi:10.1007/978-94-007-4584-1_47.
   PubMed Web of Science ®Google Scholar
• Martin RJ, Wang K, Köroğlu O, Di Fiore J, Kc P. Intermittent hypoxic episodes in preterm infants: do they matter? Neonatology. 2011;100(3):303–310. doi:10.1159/000329922.
   PubMed Web of Science ®Google Scholar
• Di Fiore JM, Martin RJ, Gauda EB. Apnea of prematurity-Perfect storm. Respir Physiol Neurobiol. 2013;189(2):213–222. doi:10.1016/j.resp.2013.05.026.
   PubMed Web of Science ®Google Scholar
• Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. The Lancet. 2008;371:19–25.
   PubMed Web of Science ®Google Scholar
• Beharry KD, Cai CL, Sharma P, et al. Hydrogen peroxide accumulation in the choroid during intermittent hypoxia increases risk of severe oxygen-induced retinopathy in neonatal rats. Invest Ophthalmol Vis Sci. 2013;54(12):7644–7657. doi:10.1167/iovs.13-13040.
   PubMed Web of Science ®Google Scholar
• Karaca C, Oner AO, Mirza E, Polat OA, Sahiner M. Bilateral effect of unilateral bevacizumab injection in retinopathy of prematurity. JAMA Ophthalmol. 2013;131(8):1099–1101. doi:10.1001/jamaophthalmol.2013.400.
   PubMed Web of Science ®Google Scholar
• Sato T, Wada K, Arahori H, et al. Serum concentrations of bevacizumab (Avastin) and vascular endothelial growth factor in infants with retinopathy of prematurity. Am J Ophthalmol. 2012;153(2):327–333. doi:10.1016/j.ajo.2011.07.005.
   PubMed Web of Science ®Google Scholar
• Theophanous C, Schechet S, Rodriguez SH, Blair M. Bilateral vitreous hemorrhage following bilateral intravitreal injections of bevacizumab in an infant with retinopathy of prematurity. Ophthalmic Surg Lasers Imaging Retina. 2018;49(11):893–896. doi:10.3928/23258160-20181101-11.
   PubMed Web of Science ®Google Scholar
• Seto R, Yamada H, Wada H, Osawa M, Nagao T, Nakano Y. Diffuse alveolar haemorrhage may be associated with intravitreal injection of bevacizumab in a patient with systemic risk factors. BMJ Case Rep. 2011;2011:bcr0820103224. doi:10.1136/bcr.08.2010.3224.
   PubMedGoogle Scholar
• Tan J, Cai CL, Shrier EM, et al. Ocular adverse effects of intravitreal bevacizumab are potentiated by intermittent hypoxia in a rat model of oxygen-induced retinopathy. J Ophthalmol. 2017;2017:4353129. doi:10.1155/2017/4353129.
   PubMed Web of Science ®Google Scholar
• Moshfeghi D, Berrocal A. Retinopathy of prematurity in the time of bevacizumab: incorporating the BEAT-ROP results into clinical practice RSS. Ophthalmology. 2011;118(7):1227–1228. doi:10.1016/j.ophtha.2011.04.028.
   PubMed Web of Science ®Google Scholar
• Asikainen TM, Chang LY, Coalson JJ, et al. Improved lung growth and function through hypoxia-inducible factor in primate chronic lung disease of prematurity. FASEB J. 2006;20(10):1698–1700. doi:10.1096/fj.06-5887fje.
   PubMed Web of Science ®Google Scholar
• Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol. 2001;280(6):C1358–C1366. doi:10.1152/ajpcell.2001.280.6.C1358.
   PubMed Web of Science ®Google Scholar
• Le Cras TD, Markham NE, Tuder RM, Voelkel NF, Abman SH. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am J Physiol Lung Cell Mol Physiol. 2002;283(3):L555–L562. doi:10.1152/ajplung.00408.2001.
   PubMed Web of Science ®Google Scholar
• Kendall RL1, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci USA. 1993;90(22):10705–10709. doi:10.1073/pnas.90.22.10705.
   PubMed Web of Science ®Google Scholar
• Tambunting F, Beharry KD, Waltzman J, Modanlou HD. Impaired lung vascular endothelial growth factor in extremely premature baboons developing bronchopulmonary dysplasia/chronic lung disease. J Investig Med. 2005;53(5):253–262. doi:10.2310/6650.2005.53508.
   PubMed Web of Science ®Google Scholar
• Keenaghan M, Cai CL, Kumar D, et al. Response of vascular endothelial growth factor and angiogenesis-related genes to stepwise increases in inspired oxygen in neonatal rat lungs. Pediatr Res. 2013;73(5):630–638. doi:10.1038/pr.2013.21.
   PubMed Web of Science ®Google Scholar
• Lassus P, Turanlahti M, Heikkilä P, et al. Pulmonary vascular endothelial growth factor and Flt-1 in fetuses, in acute and chronic lung disease, and in persistent pulmonary hypertension of the newborn. Am J Respir Crit Care Med. 2001;164(10 Pt 1):1981–1987. doi:10.1164/ajrccm.164.10.2012036.
   PubMed Web of Science ®Google Scholar
• Micieli JA, Micieli A, Smith AF. Identifying systemic safety signals following intravitreal bevacizumab: systematic review of the literature and the Canadian Adverse Drug Reaction Database Can. Can J Ophthalmol. 2010;45(3):231–238. doi:10.3129/i10-027.
   PubMed Web of Science ®Google Scholar
• Hu J, Blair MP, Shapiro MJ, Lichtenstein SJ, Galasso JM, Kapur R. Reactivation of retinopathy of prematurity after bevacizumab injection. Arch Ophthalmol. 2012;130(8):1000–1006. doi:10.1001/archophthalmol.2012.592.
   PubMed Web of Science ®Google Scholar
• Ittiara S, Blair MP, Shapiro MJ, Lichtenstein SJ. Exudative retinopathy and detachment: a late reactivation of retinopathy of prematurity after intravitreal bevacizumab. J AAPOS. 2013;17(3):323–325. doi:10.1016/j.jaapos.2013.01.004.
   PubMed Web of Science ®Google Scholar
• Jalali S, Balakrishnan D, Zeynalova Z, Padhi TR, Rani PK. Serious adverse events and visual outcomes of rescue therapy using adjunct bevacizumab to laser and surgery for retinopathy of prematurity: the Indian Twin Cities Retinopathy of Prematurity Screening database Report number 5. Arch Dis Child Fetal Neonatal Ed. 2013;98(4):F327–F333. doi:10.1136/archdischild-2012-302365.
   PubMed Web of Science ®Google Scholar
• Morin J, Luu TM, Superstein R, the Canadian Neonatal Network and the Canadian Neonatal Follow-Up Network Investigators, et al. Neurodevelopmental outcomes following bevacizumab injections for retinopathy of prematurity. Pediatrics. 2016;137(4):e20153218. doi:10.1542/peds.2015-3218.
   PubMed Web of Science ®Google Scholar
• Chang M, Bany-Mohammed F, Kenney C, Beharry K. Effects of a superoxide dismutase mimetic on biomarkers of lung angiogenesis and alveolarization during hyperoxia with intermittent hypoxia. Am J Transl Res. 2013;5(6):594–607.
   PubMed Web of Science ®Google Scholar
• Valencia AM, Cai CL, Tan J, et al. Intravitreal bevacizumab alters type IV collagenases and exacerbates arrested alveologenesis in the neonatal rat lungs. Exp Lung Res. 2017;43(3):120–133. doi:10.1080/01902148.2017.1306897.
   PubMed Web of Science ®Google Scholar
• Aranda JV, Cai CL, Ahmad T, et al. Pharmacologic synergism of ocular ketorolac and systemic caffeine citrate in rat oxygen-induced retinopathy. Pediatr Res. 2016;80(4):554–565. doi:10.1038/pr.2016.105.
   PubMed Web of Science ®Google Scholar
• Di Fiore JM, Kaffashi F, Loparo K, et al. The relationship between patterns of intermittent hypoxia and retinopathy of prematurity in preterm infants. Pediatr Res. 2012;72(6):606–612. doi:10.1038/pr.2012.132.
   PubMed Web of Science ®Google Scholar
• Berkowitz BA, Kowluru RA, Frank RN, Kern TS, Hohman TC, Prakash M. Subnormal retinal oxygenation response precedes diabetic-like retinopathy. Invest Ophthalmol Vis Sci. 1999;40:2100–2105.
   PubMed Web of Science ®Google Scholar
• Romano MR, Biagioni F, Besozzi G, et al. Effects of bevacizumab on neuronal viability of retinal ganglion cells in rats. Brain Res. 2012;1478:55–63. doi:10.1016/j.brainres.2012.08.014.
   PubMed Web of Science ®Google Scholar
• Pan CK, Durairaj C, Kompella UB, Agwu O, et al. Comparison of long-acting bevacizumab formulations in the treatment of choroidal neovascularization in a rat model. J Ocul Pharmacol Ther. 2011;27(3):219–224. doi:10.1089/jop.2010.0158.
   PubMed Web of Science ®Google Scholar
• Johnsen-Soriano S, Arnal E, Sancho-Tello M, et al. Intravitreal injection of bevacizumab induces inflammatory alterations in a uveitis experimental model. Eur J Ophthalmol. 2011;21(4):427–433. doi:10.5301/EJO.2010.5842.
   PubMed Web of Science ®Google Scholar
• Gao H, Qiao X, Gao R, Mieler WF, McPherson AR, Holz ER. Intravitreal triamcinolone does not alter basal vascular endothelial growth factor mRNA expression in rat retina. Vision Res. 2004;44(4):349–356. doi:10.1016/j.visres.2003.09.027.
   PubMed Web of Science ®Google Scholar
• Tschanz SA, Makanya AN, Haenni B, Burri PH. Effects of neonatal high-dose short-term glucocorticoid treatment on the lung: a morphologic and morphometric study in the rat. Pediatr Res. 2003;53(1):72–80. doi:10.1203/00006450-200301000-00014.
   PubMed Web of Science ®Google Scholar
• Honda S, Hirabayashi H, Tsukahara Y, Negi A. Acute contraction of the proliferative membrane after an intravitreal injection of bevacizumab for advanced retinopathy of prematurity. Graefes Arch Clin Exp Ophthalmol. 2008;246(7):1061–1063. doi:10.1007/s00417-008-0786-7.
   PubMed Web of Science ®Google Scholar
• Al-Dhibi H, Khan AO. Bilateral response following unilateral intravitreal bevacizumab injection in a child with uveitic cystoid macular edema. J AAPOS. 2009;13(4):400–402. doi:10.1016/j.jaapos.2009.03.006.
   PubMed Web of Science ®Google Scholar
• Atchaneeyasakul LO, Trinavarat A. Choroidal ruptures after adjuvant intravitreal injection of bevacizumab for aggressive posterior retinopathy of prematurity. J Perinatol. 2010;30(7):497–499. doi:10.1038/jp.2009.166.
   PubMed Web of Science ®Google Scholar
• Jang SY, Choi KS, Lee SJ. Delayed-onset retinal detachment after an intravitreal injection of ranibizumab for zone 1 plus retinopathy of prematurity. J AAPOS. 2010;14(5):457–459. doi:10.1016/j.jaapos.2010.05.011.
   PubMed Web of Science ®Google Scholar
• Law JC, Recchia FM, Morrison DG, Donahue SP, Estes RL. Intravitreal bevacizumab as adjunctive treatment for retinopathy of prematurity. J AAPOS. 2010;14(1):6–10. doi:10.1016/j.jaapos.2009.10.011.
   PubMed Web of Science ®Google Scholar
• Nazari H, Modarres M, Parvaresh MM, Ghasemi Falavarjani K. Intravitreal bevacizumab in combination with laser therapy for the treatment of severe retinopathy of prematurity (ROP) associated with vitreous or retinal hemorrhage. Graefes Arch Clin Exp Ophthalmol. 2010;248(12):1713–1718. doi:10.1007/s00417-010-1430-x.
   PubMed Web of Science ®Google Scholar
• Suk KK, Berrocal AM, Murray TG, et al. Retinal detachment despite aggressive management of aggressive posterior retinopathy of prematurity. J Pediatr Ophthalmol Strabismus. 2010;47:e1–e4.
   PubMedGoogle Scholar
• Wu WC, Yeh PT, Chen SN, Yang CM, Lai CC, Kuo HK. Effects and complications of bevacizumab use in patients with retinopathy of prematurity: a multicenter study in Taiwan. Ophthalmology. 2011;118(1):176–183. doi:10.1016/j.ophtha.2010.04.018.
   PubMed Web of Science ®Google Scholar
• Jakkula M, Le Cras TD, Gebb S, et al. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol. 2000;279(3):L600–L607. doi:10.1152/ajplung.2000.279.3.L600.
   PubMed Web of Science ®Google Scholar
• Remesal A, Pedraz C, San Feliciano L, Ludeña D. Pulmonary expression of vascular endothelial growth factor (VEGF) and alveolar septation in a newborn rat model exposed to acute hypoxia and recovered under conditions of air or hyperoxia. Histol Histopathol. 2009;24(3):325–330. doi:10.14670/HH-24.325.
   PubMed Web of Science ®Google Scholar
• Abman SH. Impaired vascular endothelial growth factor signaling in the pathogenesis of neonatal pulmonary vascular disease. Adv Exp Med Biol. 2010;661:323–335. doi:10.1007/978-1-60761-500-2_21.
   PubMed Web of Science ®Google Scholar
• Le Cras TD, Spitzmiller RE, Albertine KH, Greenberg JM, Whitsett JA, Akeson AL. VEGF causes pulmonary hemorrhage, hemosiderosis, and air space enlargement in neonatal mice. Am J Physiol Lung Cell Mol Physiol. 2004;287(1):L134–L142. doi:10.1152/ajplung.00050.2004.
   PubMed Web of Science ®Google Scholar
• Sclafani F, Cunningham D. Bevacizumab in elderly patients with metastatic colorectal cancer. J Geriatr Oncol. 2014;5(1):78–88. doi:10.1016/j.jgo.2013.08.006.
   PubMed Web of Science ®Google Scholar
• Lingkun K, Bhatt AR, Demny AB, et al. Pharmacokinetics of bevacizumab and its effects on serum VEGF and IGF-1 in infants with retinopathy of prematurity. Invest Ophthalmol Vis Sci. 2015;56(2):956–961. doi:10.1167/iovs.14-15842.
   PubMed Web of Science ®Google Scholar
• Wu LH, Yang YH, Lin CH, Lin YJ, Cheng CL. Hypotension associated with intravitreal bevacizumab therapy for retinopathy of prematurity. Pediatrics. 2016;137(2):e20152005. doi:10.1542/peds.2015-2005.
   PubMed Web of Science ®Google Scholar
• Meller S, Bhandari V. VEGF levels in humans and animal models with RDS and BPD: temporal relationships. Exp Lung Res. 2012;38(4):192–203. doi:10.3109/01902148.2012.663454.
   PubMed Web of Science ®Google Scholar
• Mura M, Han B, Andrade CF, et al. The early responses of VEGF and its receptors during acute lung injury: implication of VEGF in alveolar epithelial cell survival. Crit Care. 2006;10(5):R130. doi:10.1186/cc5042.
   PubMed Web of Science ®Google Scholar
• Alidzanovic L, Starlinger P, Schauer D, et al. The VEGF rise in blood of bevacizumab patients is not based on tumor escape but a host-blockade of VEGF clearance. Oncotarget. 2016;7(35):57197–57212. doi:10.18632/oncotarget.11084.
   PubMedGoogle Scholar
• Bocci G, Man S, Green SK, et al. Increased plasma vascular endothelial growth factor (VEGF) as a surrogate marker for optimal therapeutic dosing of VEGF receptor-2 monoclonal antibodies. Cancer Res. 2004;64(18):6616–6625. doi:10.1158/0008-5472.CAN-04-0401.
   PubMed Web of Science ®Google Scholar
• Anjana G. Effect of intermittent hypobaric hypoxia on efficacy & clearance of drugs. Indian J Med Res. 2012;135(2):211–216.
   PubMed Web of Science ®Google Scholar
• Ahasic AM, Zhai R, Su L, et al. IGF1 and IGFBP3 in acute respiratory distress syndrome. Eur J Endocrinol. 2012;166(1):121–129. doi:10.1530/EJE-11-0778.
   PubMed Web of Science ®Google Scholar
• Löfqvist C, Hellgren G, Niklasson A, the WINROP Consortium, et al. Low postnatal serum IGF-I levels are associated with bronchopulmonary dysplasia (BPD). ActaPaediatrica. 2012;101(12):1211–1216. doi:10.1111/j.1651-2227.2012.02826.x.
   PubMed Web of Science ®Google Scholar
• Hellström A, Engström E, Hård AL, et al. Postnatal serum insulin-like growth factor I deficiency is associated with retinopathy of prematurity and other complications of premature birth. Pediatrics. 2003;112(5):1016–1020. doi:10.1542/peds.112.5.1016.
   PubMed Web of Science ®Google Scholar
• Wang Z, Bonella F, Li W, et al. Gastroesophageal reflux disease in idiopathic pulmonary fibrosis: uncertainties and controversies. Respiration. 2018;96(6):571–587. doi:10.1159/000492336.
   PubMed Web of Science ®Google Scholar