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Incidence of brain injuries in premature infants with gestational age ¡Ü34 weeks in ten urban hospitals in China
Hui-Jin Chen, Ke-Lun Wei, Cong-Le Zhou, Yu-Jia Yao, Yu-Jia Yang, Xiu-Fang Fan, Xi-Rong Gao, Xiao-Hong Liu, Ji-Hong Qian, Ben-Qing Wu, Gao-Qiang Wu, Qing-Mei Zhang, Xiao-Lan Zhang
Shanghai, China
Author Affiliations: Shanghai Institute for Pediatric Research, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China (Chen HJ); The Second Affiliated Hospital of China Medical University, Shenyang 110004, Liaoning Province, China (Wei KL); Peking University First Hospital, Beijing 100034, China (Zhou CL); West China Second University Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China (Yao YJ); Xiangya Hospital of Central South University, Changsha 410008, Hunan Province, China (Yang YJ); Jinan Women & Children Hospital, Jinan 250012, Shandong Province, China (Fan XF); Hunan Children's Hospital, Changsha 410007, Hunan Province, China (Gao XR); Shenzhen Children's Hospital, Shenzhen 518026, Guangdong Province, China (Liu XH); Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China (Qian JH); Shenzhen City People's Hospital, the Second Affiliated Hospital of Jinan University Medical College, Shenzhen 518020, Guangdong Province, China (Wu BQ); Ulumuqi Women & Children Hospital, Ulumuqi 830000, Xinjiang Uyghur Autonomous Region, China (Wu GQ); Shenyang Women Hospital, Shenyang 110014, Liaoning Province, China (Zhang QM); Shenzhen Maternity and Child Healthcare Hospital, Shenzhen 518028, Guangdong Province, China (Zhang XL)
Corresponding Author: Hui-Jin Chen, MD, Professor of Pediatrics, Shanghai Institute for Pediatric Research, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China (Tel: +86-21-65790000-6471; Fax: +86-21-65791316; Email: hjchenk@163.com)
doi: 10.1007/s12519-012-0395-8
Background: There is a large number (1.5 million per year) of premature births in China. It is necessary to obtain the authentic incidences of intraventricular hemorrhage (IVH) and periventricular leukomalacia (PVL), the common brain injuries, in Chinese premature infants. The present multicenter study aimed to investigate the incidence of brain injuries in premature infants in ten urban hospitals in China.
Methods: The research proposal was designed by the Subspecialty Group of Neonatology of Pediatric Society of the Chinese Medical Association. Ten large-scale urban hospitals voluntarily joined the multicenter investigation. All premature infants with a gestational age ¡Ü34 weeks in the ten hospitals were subjected to routine cranial ultrasound within three days after birth, and then to repeated ultrasound every 3-7 days till their discharge from the hospital from January 2005 to August 2006. A uniform data collection sheet was designed to record cases of brain injuries.
Results: The incidences of overall IVH and severe IVH were 19.7% (305/1551) and 4.6% (72/1551), respectively with 18.4% (56/305) for grade 1, 58.0% (177/305) for grade 2, 17.7% (54/305) for grade 3 and 5.9% (18/305) for grade 4 in nine hospitals. The incidences of overall PVL and cystic PVL were 5.0% (89/1792) and 0.8% (14/1792) respectively, with 84.3% (75/89) for grade 1, 13.5% (12/89) for grade 2, and 2.2% (2/89) for grade 3 in the ten hospitals. The statistically significant risk factors that might aggravate the severity of IVH were vaginal delivery (OR=1.883, 95% CI: 1.099-3.228, P=0.020) and mechanical ventilation (OR=4.150, 95% CI: 2.384-7.223, P=0.000). The risk factors that might result in the development of cystic PVL was vaginal delivery (OR=21.094, 95% CI: 2.650-167.895, P=0.000).
Conclusions: The investigative report can basically reflect the incidence of brain injuries in premature infants in major big cities of China. Since more than 60% of the Chinese population live in the rural areas of China, it is expected to undertake a further multicenter investigation covering the rural areas in the future.
Key words: incidence; intraventricular hemorrhage; multicenter investigation; periventricular leukomalacia; premature infants
World J Pediatr 2013;9(1):17-24
Introduction
Intraventricular hemorrhage (IVH) and periventricular leukomalacia (PVL), the common brain injuries in premature infants, are major causes for early death in the neonatal period and later motor and cognitive disabilities. Post-hemorrhagic hydrocephalus and periventricular hemorrhagic infarction are major complications of IVH. PVL is an intractable brain injury in premature infants, pathologically characterized by focal necrosis and diffuse injury.[1] Ischemia and infection are believed to be the main pathogenic factors for PVL in premature infants. Especially, the peroxynitrite generated from lipopolysaccharide-activated microglia mediates the destruction of pre-oligodendrocytes (preOLs).[2] Either by periventricular hemorrhagic infarction following IVH or PVL induced by ischemia or infection, hypomyelination takes place finally because of a damage or loss of preOLs, leading to the sequelae of cerebral palsy and mental retardation.
In consideration of the higher absolute number (1.5 million per year) of premature births in China[3] and the severity of brain injuries in premature infants, a multicenter investigation for brain injuries in premature infants was conducted in China by the Subspecialty Group of the Neonatology of Pediatric Society, the Chinese Medical Association. This report describes the incidences of brain injuries (IVH and PVL) in premature infants with ¡Ü34 weeks of gestational age in ten large-scale urban hospitals in China.
Methods
Participating hospitals
Ten large-scale urban hospitals that were the biggest hospitals at provincial level and all belonged to the Third Class and A Level (the highest level) in China participated in the multicenter investigation. Nine hospitals were involved in investigations of IVH and PVL incidences, and one hospital was only investigated for PVL incidence. Permission for the study was obtained from the human research committees of the participating hospitals, and informed consent was obtained from the relatives of the infants enrolled in this study.
Subjects and study course
Premature infants with the gestational age of ¡Ü34 weeks were investigated from January 2005 to August 2006. Malformed premature infants were excluded.
Methods
Research proposal
The research proposal was drafted by the Subspecialty Group of Neonatology of the Pediatric Society, the Chinese Medical Association. The proposal was discussed and amended by famous neonatologists in the field of neonatal brain injuries in China. A uniform sheet for data collection was designed for recording cases of brain injuries.
Cranial ultrasound scan
An initial bedside real-time cranial sonography was performed by radiologists for all premature infants from the ten hospitals within 3-7 days of birth. Most infants had one or more follow-up examinations at intervals varying from every other day to weekly until discharge. IVH was graded 1 to 4 according to the system of Papile et al,[4] and grades 3 and 4 were considered "severe" IVH. Post-hemorrhagic hydrocephalus was diagnosed when there was progressive ventricular dilation on sonography. PVL was graded 1 to 4 according to the classification of de Vries et al,[5] and grade II and above was defined as cystic PVL, a more severe pathological type.
Statistical analysis
All data were taken from the records and entered into Foxpro software for analyses. Statistical analysis was made with Student's t test (unpaired), the chi-square test, and odds ratio with SPSS 11.5 software. Differences between the groups were considered statistically significant when P<0.05.
Results
General clinical data
Totally 1792 premature infants with ¡Ü34 weeks of gestational age were enrolled for investigating the incidence of brain injuries. Of whom, 1551 were admitted to the nine hospitals that participated in the investigation of IVH incidence. IVH was found in 305 infants. Their average gestational age was 31.7¡À2.2 weeks (n=303, range: 27.0-34 weeks), and birth weight was 1751.1¡À462.7 g (n=305, range: 860-2500 g). The ratio of male to female of the premature infants was 1.63:1. Fourty-two infants were outborn. The Apgar score was 8.1¡À2.2 (n=285, range: 1-10) at one minute, including 18 infants with Apgar score ¡Ü3; 9.0¡À1.7 (n=228, range: 1-10) at five minutes, including 5 infants with Apgar score ¡Ü3. Vaginal delivery was taken in 149 infants, cesarean birth in 153, and forceps delivery in 3.
Altogether 1792 premature infants were admitted to the ten hospitals participating in the investigation of PVL incidence, and PVL was diagnosed in 89 infants. Their average gestational age was 32.0¡À1.9 weeks (n=87, range: 26.6-34 weeks), and birth weight was 1810.8¡À449.1 g (n=89, range: 960-2300 g). The ratio of male to female in the premature infants was 2.3:1. There were 15 outborn infants. The Apgar score was 7.8¡À2.4 (n=80, range: 1-10) at one minute, and 6 infants had an Apgar score ¡Ü3. The Apgar score was 9.0¡À1.6 (n=60, range: 3-10) at five minutes, and one infant had an Apgar score ¡Ü3. Vaginal delivery was taken in 45 infants, cesarean birth in 43, and forceps delivery in 3.
Incidence of brain injuries
The overall incidences of IVH and severe IVH (Table 1) were 19.7% (305/1551) and 4.6% (72/1551) in the nine hospitals, consisting of 18.4% (56/305) for grade 1, 58.0% (177/305) for grade 2, 17.7% (54/305) for grade 3 and 5.9% (18/305) for grade 4. Of the 305 infants 244 had bilateral IVH. The overall incidences of PVL and cystic PVL were 5.0% (89/1792) and 0.8% (14/1792) in the ten hospitals, which consist of 84.3% (75/89) for grade 1, 13.5% (12/89) for grade 2, and 2.2% (2/89) for grade 3. There were 58 infants with IVH complicated by PVL. Another 12 IVH infants were associated with infarction of central branches or cortical branches of the either left or right middle cerebral artery.
Gestational age in premature infants with IVH or PVL (Table 2) indicated the decreased incidence of brain injury in premature infants with increasing gestational age.
Possible perinatal risk factors for the occurrence of severe brain injuries in premature infants
There were no significant differences (P>0.05 for all) in the perinatal risk factors that might aggravate the severity of brain injuries, including fetal distress, abnormal fetal position, premature rupture of membranes, placental abruption, placenta previa, amniotic fluid contamination, cord around the neck, pregnancy-induced hypertension, gestational diabetes, uterus infection and perinatal asphyxia. The risk factors of statistical significance were mechanical ventilation (P=0.000) and vaginal delivery (P=0.020), which might aggravate the severity of IVH, and vaginal delivery (P=0.000) which might result in the development of cystic PVL (Table 3).
Outcome of infants with brain injuries
Among the 305 premature infants with IVH, 4 showed changes from grade 1 to grade 2 or above, 9 from grade 2 to grade 3 or above, and another 22 from grade 3 to grade 2. The rates for changes from mild to severe and from severe to mild were 5.6% (13/233) and 30.6% (22/72), respectively. The mean duration of hospitalization in the 305 infants was 24.3¡À17.8 days (range: 1-98 days, median: 19 days). Twelve infants with severe IVH were complicated by hydrocephalus. Totally 256 infants with IVH were discharged with resolution or improvement. Forty-one infants left the hospital against medical advice, with a mean hospitalization duration of 12.1¡À11.2 days (range: 1-53 days, median: 7 days). Six IVH infants whose mean gestational age was 29.3¡À2.3 weeks (range: 27.1-33.1 weeks) died from pulmonary hemorrhage, respiratory failure, grade 4 IVH or growth failure. Their mean death age was 12.3¡À11.8 days after birth (range: 2-31 days, median: 8.5 days).
The mean duration of hospitalization in 89 PVL infants was 22.0¡À15.4 days (range: 4-90 days, median: 8 days). Seventy-three PVL infants were discharged with resolution or improvement. Twelve infants left the hospital against medical advice, with a mean hospital stay of 17.5¡À13.7 days (range: 4-53 days, median: 14 days). Three PVL infants whose mean gestational age was 31.7¡À3.2 weeks (range: 28-33.9 weeks) died from hyaline membrane disease, respiratory failure, multiple organ failure or growth failure, and their mean death age was 25.3¡À34.4 days after birth (range: 5-65 days, median: 6 days).
Discussion
In recent years, the incidence of IVH, which was up to 40%-70% 20 years ago,[6] has declined obviously. Data from multicenter surveys or from the neonatal network and databases showed that the incidence of IVH decreased to about 25%, even under 10% in some European countries.[7,8] In developing countries such as Syria, the incidence of IVH was 44.7% in 2006.[9] The incidence of PVL reported in some countries was 19.8%-34.1% for overall PVL[10-13] and 2.5%-23% for cystic PVL.[14-16] The evidence of PVL in premature infants was found to be up to 75% in a pathological report.[17] Recent neuro-imaging research showed that the incidence of cystic PVL tended to decrease while non-cystic diffuse white matter injury became a main pathological type.[18,19]
The reported incidence of IVH in China was 40%-70% before 2004.[6] However, the data were from the episodic reports of some units and cannot objectively reflect the exact incidence of IVH in premature infants in this country. Moreover, the incidences of overall PVL and cystic PVL have not been reported in China except for some episodic reports on PVL cases. Thus this multicenter investigation for brain injuries in premature infants was conducted by the Subspecialty Group of the Neonatology of Pediatric Society, the Chinese Medical Association.
The investigation showed that the incidences of the overall IVH and severe IVH were 19.7% and 4.6% in nine hospitals; the incidences of the overall PVL and cystic PVL were 5.0% and 0.8% in ten large-scale hospitals, which were located in seven big cities in Beijing, Shanghai, Shenyang, Ulumuqi, Changsha, Jinan, Chengdu and Shenzhen. The clinical care patterns in all participating hospitals in this investigation were similar, and key management strategies were basically the same based on the guide issued by the Subspecialty Group of the Neonatology of Pediatric Society, the Chinese Medical Association. Therefore, the investigation can basically reflect the incidence of brain injuries in premature infants in major big cities in China.
Similar to the world's development tendency, the incidence of IVH decreases significantly in China. The incidence of PVL in the present investigation was lower than those reported elsewhere. The higher incidence of PVL was noticed to derive mainly from the single NICU or some developing countries,[14] and the lower incidence of PVL (<5%) was usually based on more than 500 cases.[15] The result of this investigation was obtained from 1792 premature infants at the gestational age of ¡Ü34 weeks. Besides, there was a lower incidence of PVL in the infants at the gestational age of 33-34 weeks.
The overall incidence of IVH was close to 40% in some general hospitals. The incidence of severe IVH reached 35% in the West China Second University Hospital, a local biggest general hospital. Synnes et al[20] reported an incidence of severe IVH of 2%-20.5% in 17 neonatal units. Similarlly, an incidence of 2.9%-21.4% for severe IVH in 24 neonatal units was reported from New Zealand.[21] Sick neonatal infants are usually referred to general or children's hospitals, thus proper managerial practices and organizational processes in neonatal units may probably affect the incidence of brain injuries.
About 25%-50% of IVH and most of PVL premature infants are usually overlooked because of the absence of symptoms. Neuroimaging examination can enhance obviously the detection rate of neonatal brain injuries. Since the etiology of brain injuries in premature infants is complicated, the rapid change of systemic pressure may induce an unstable fluctuation of cerebral blood flow and the damage of blood flow anto-regulation, thereby resulting in the occurrence of brain injuries.[22] Thus CT scan or MRI examination is not recommended in premature infants early after birth. The bedside cranial ultrasound is a most suitable way to detect brain injury in premature infants because of a high sensitivity in detecting cerebral injuries in the central site of the brain and a facility for users. A bedside cranial ultrasound has been used as a routine approach for the diagnosis of brain injuries in premature infants in most countries.[23,24] A guide of "diagnostic suggestion for periventricular-intraventricular hemorrhage and periventricular leukomalacia in premature infants" was also issued by the Subspecialty Group of the Neonatology of Pediatric Society, the Chinese Medical Association in 2007,[10] in which a routine initial cranial ultrasound within 3 days of age and a follow-up examination each week are recommended for premature infants of ¡Ü34 weeks of gestational age. It will be helpful to enhance the detection rate of neonatal brain injuries, to track clinical progress, and to adjust the treatment and intervention timely.
As a supplementary way, diffusion weighted imaging is highly sensitive to edema stage during early PVL. As a predictor of outcome for cerebral palsy, MRI at near-term in very low birth weight preterm neonates is superior to ultrasound for the improvement of brain assessment and the detection of anatomic abnormalities.[25] It is recommended that as a routine level care, all at-risk preterm infants with normal or abnormal early ultrasound findings should be given a brain MRI examination before their discharge from the hospital or at 40 weeks of postmenstrual age.
The possible risk factors resulting in brain injuries in premature infants included perinatal asphyxia, vaginal delivery, low birth weight, outborn, hypothermia, mechanical ventilation, respiratory distress syndrome, air leak, metabolic acidosis and hypercapnia. This investigation showed that the risk factors aggravating the severity of IVH were vaginal delivery and mechanical ventilation and that the risk factor that might result in cystic PVL was vaginal delivery. Other IVH risk factors reported recently are male sex, transport of premature infant, acute placental damage, eclampsia, no or incomplete antenatal steroid course, early sepsis, and use of vasopressors.[11,12,26-29] PVL risk factors include placental inflammation, chorioamnionitis, premature rupture of membranes, hyperoxia, hypocarbia and vaginal delivery.[13,30-36] Utero methamphetamine exposure, late-onset circulatory dysfunction and neonatal cardiac surgery are also correlated with the development of PVL.[37-39] Avoidance of hypertension and abnormal gas change in the immediate neonatal period are important for reducing the incidence of brain injuries in premature infants.
Despite the development of sophisticated care techniques, the survival rate of critically ill infants or very low birth weight infants in the NICU continues to increase over the last decades. The incidence of neurodevelopmental disability among the survivors in NICU remains high. The extremely premature infants in particular appear to sustain a more severe course with appreciable mortality and morbidity. The long-term follow-up is important and necessary for premature infants with brain injuries. The follow-up result of the premature infants with brain injuries in this investigation was described in another report.[40] There were 58 IVH infants complicated by PVL, and the presence of IVH usually increased the risk of PVL.[41] Besides, the branch infarction of cerebral arteries and hypoxic-ischemia brain injuries which usually have characteristic appearances on ultrasound, CT or MRI[42] are also not uncommon in the premature infants.
The multicenter investigation reflects the incidence of brain injuries in premature infants in big cities of China. However, the number of the participating hospitals and the duration of the investigation are limited. It is expected to encourage more urban hospitals including those in medium or small cities to participate in the future investigation, and there may be a longer period of investigation. There are usually more sick infants in general hospitals than in maternity and infant hospitals. It is possible that the occurrence of brain injuries is more frequent in critical premature infants, which may be the major reason for the increased incidence of IVH in the 31-34 week group in the present investigation. The incidences of brain injuries in general hospitals and maternity and infant hospitals may be separately investigated in the future study. Since over 60% of the Chinese population live in the rural areas, there may be a higher incidence of brain injuries in premature infants because of limited medical sources in the rural areas. A more objective and perfect multicenter investigation for the incidence of brain injuries in premature infants is needed in this country covering the rural areas and medium and small cities.
Acknowledgements
1. Study scheme: The study scheme was drafted by Prof. Hui-Jin Chen, and discussed and amended by the following experts: Prof. Ke-Lun Wei from the Second Affiliated Hospital of China Medical University, Prof. Yu-Jia Yao from the West China Second University Hospital, Sichuan University, Prof. Cong-Le Zhou from the Peking University First Hospital, Prof. Yu-Jia Yang from the Xiangya Hospital of Central South University, Prof. Shao-Zeng Fan* from the Children's Hospital, Fudan University, Prof. De-Min Huang from the Peking University Third Hospital, Prof. Wen-Lan Hong from the Children's Hospital of Zhejiang University School of Medicine, Prof. Tian-He Xu from the Children's Hospital, Chongqing University of Medical Sciences, Prof. Ren-Jie Yu from the Beijing Huaxin Hospital, Qinhua University, and Prof. Sheng-Mei Wu from the Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine. (*: deceased)
2. Participating hospitals: Department of Neonatology, Hunan Children Hospital, Hunan Province; Department of Neonatology, Jinan Women & Children Hospital, Shandong Province; Department of Neonatology, Shenzhen Children's Hospital, Guangdong Province; Department of Neonatology, Shenzhen Maternity and Child Healthcare Hospital, Guangdong Province; Department of Neonatology, Shenyang Women Hospital, Liaoning Province; Department of Neonatology, Ulumuqi Women & Children Hospital, XinJiang Uyghur Autonomous Region; Department of Pediatrics, Peking University First Hospital, Beijing; Department of Pediatrics, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai; Department of Neonatology, Shenzhen City People's Hospital, the Second Affiliated Hospital of Jinan University Medical College, Guangdong Province; Department of Pediatrics, West China Second University Hospital, Sichuan University, Sichuan Province.
3. We thank Prof. Xiao-Yu Zhu from Shenzhen Maternity and Child Healthcare Hospital, Prof. Su-Yun Liu from Ulumuqi Women & Children Hospital, XinJiang Uyghur Autonomous Region, and Prof. Shu-Yun Shen* from First Affiliated Hospital, Xinjiang Medical University for their support with this investigation; thank Drs. Kao-Wen Liang, Xing Li and Xi-Yong Fan from Peking University First Hospital, Dr. Hui Yang from Hunan Children Hospital, Drs. Xia Li, Wei-Wei Li, Qing Li, Rong-Rong Wang, Hong Liu and Jing Tan from Jinan Women & Children Hospital, Shandong Province, Dr. De-Yuan Li in West China Second University Hospital, Sichuan University, Drs. Yan-Ling Ma, Patiman and Wursiman from Ulumuqi Women & Children Hospital, Xinjiang Uyghur Autonomous Region for their cases collection; also thank colleagues from Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine: Ms. Guan-Yi Chen for sonograms collection, Associate Prof. Ya-Jun Zhu and Dr. Bei Wang for cases collection, Prof. Zhen-Juan He, Dr. Jia-Min He, Master's degree Candidates Juan Gao, Yi-Jun Zhou, and Ya-Fang He for their entering data into database, and Prof. Xiao-Xing Xu for her advise on data analysis. (*: deceased)
Funding: The multicenter investigation was sponsored by the Subspecialty Group of Neonatology of Pediatric Society, China Medical Association.
Ethical approval: All participating hospitals obtained the permission of human research committee of their hospital, and consent was obtained from all the family members of patients who were investigated.
Competing interest: None declared.
Contributors: Chen HJ contributed to the conception and design of the study, the analysis and interpretation of data, grafting and revising the article, and the final approval of the version to be published. Wei KL, Zhou CL, Yao YJ and Yang YJ contributed to the discussion and amendment of the research plan, the acquisition of data and the analysis and interpretation of data. Fan XF, Gao XR, Liu XH, Qian JH, Wu BQ, Wu GQ, Zhang QM, and Zhang XL contributed to the acquisition of data, and the analysis and interpretation of data derived from their own hospital. Zhou CL, Yao YJ, Fan XF, Gao XR, Liu XH, Qian JH, Wu BQ, Wu GQ, Zhang QM, and Zhang XL contributed equally to the paper.
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Received September 5, 2011 Accepted after revision December 7, 2011
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