Historical Vignette

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Q7 Q5 Q1Intraventricular Hemorrhage in Premature Infants: A Historical Review 61
Q6
4 Q4 Jennifer Deger1, Eric A. Goethe1, Melissa A. LoPresti1, Sandi Lam2 62
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6 64
7 65
8 Key words Intraventricular hemorrhage (IVH) is common in premature newborns and poses 66
9 - Endoscopic third ventriculostomy 67
a high risk for morbidity with lifelong disability. We searched the available
10 - Hydrocephalus 68
- Neonatal intraventricular hemorrhage
literature for original and secondary literature regarding the epidemiology,
11 69
12 - Ventriculoperitoneal shunt pathogenesis, and treatment of IVH in order to trace changes in the management 70
13 of this disease over time. 71
Abbreviations and Acronyms
14 We examined IVH pathogenesis and epidemiology and reviewed the history of 72
CSF: Cerebrospinal fluid
15 DRIFT: Drainage, irrigation, and fibrinolytic therapy medical and surgical treatment for intraventricular hemorrhage in preterm 73
16 IVH: Intraventricular hemorrhage children. Initial medical management strategies aimed at correcting coagul- 74
17 MSC: Mesenchymal stem cell opathy and eventually targeted mediators of perinatal instability including 75
18 VPS: Ventriculoperitoneal shunt 76
respiratory distress. Surgical management centered around cerebrospinal fluid
19 From 1Department of Neurosurgery, Baylor College of diversion, initially through serial lumbar punctures, progressing to ven- 77
20 Medicine, Division of Neurosurgery, Texas Children’s triculoperitoneal shunting, with more recent interventions addressing intra- 78
21 Hospital, Houston, Texas; and 2Department of Neurosurgery, 79
Northwestern University School of Medicine, Division of
ventricular clot burden.
22 80
Neurosurgery, Lurie Children’s Hospital, Chicago, Illinois, We provide a historical review of the evolution of treatment for IVH in newborns.
23 81
24
USA While the management of IVH has grown significantly over time, IVH remains a 82
25
To whom correspondence should be addressed: common neurosurgical disease that continues to affect patient and caregiver 83
Sandi Lam, M.D.
26 [E-mail: sandilam@gmail.com]
quality of life and health care costs. Despite advances in treatment over more 84
27 Citation: World Neurosurg. (2021).
than a century, IVH remains a significant cause of morbidity and mortality in 85
28 https://doi.org/10.1016/j.wneu.2021.06.043 premature infants, and an understanding of past approaches may inform the 86
29 Journal homepage: www.journals.elsevier.com/world- development of new treatments. 87
30 neurosurgery 88
31 Available online: www.sciencedirect.com 89
32 1878-8750/$ - see front matter ª 2021 Elsevier Inc. All United States, and the combined lifetime underdeveloped germinal matrix, 90
33 rights reserved.
care costs for these children exceed $3.6 immature cerebral autoregulatory 91
34 billion.10 We review the evolution of mechanisms, and greater fluctuations in 92
35 treatment for IVH of prematurity to learn hemodynamics due to underdeveloped 93
36 INTRODUCTION 94
from prior techniques and approaches to cardiopulmonary systems.8
37 Intraventricular hemorrhage (IVH) is the shed light on innovations and future 95
38 most frequent and severe neurologic directions of research. Neonatal IVH was 96
39 complication of preterm birth, occurring MEDICAL MANAGEMENT OF 97
first described in the 1920s. Before the INTRAVENTRICULAR HEMORRHAGE
40 in 20% to 40% of all infants born weigh- advent of ultrasound and computed 98
41 ing under 1500 gm worldwide.1,2 tomography (CT), epidemiologic data Early treatment efforts focused on prevent- 99
42 Prematurity is the most well-known and were mostly derived from autopsy data.3 ing IVH by addressing a potential underlying 100
43 well-understood risk factor for IVH, with coagulopathy (Figure 1, Table 1). In 1939, 101
44 over half of premature births occurring in Waddell and Guerry from the University of 102
45 developing countries.3-5 Despite PATHOPHYSIOLOGY OF Virginia observed that oral vitamin K 103
46 improving survival, mortality ranges from INTRAVENTRICULAR HEMORRHAGE administration treated hemorrhage in 104
47 30%
60%,6 and survivors are at risk for Neonatal IVH is thought to arise from the newborns and suggested that vitamin K 105
48 cerebral palsy, hydrocephalus, seizures, interplay of fragile germinal matrix vessels could be used to prevent intracranial 106
49 and intellectual disability.7,8 Data from and rapid hemodynamic fluctuations to hemorrhage.12 Subsequent studies in the 107
50 developing countries regarding risk which preterm infants are predisposed.11 following decades were inconsistent. Some 108
51 factors for and outcomes of IVH are Neonates can experience ischemia due to promoted vitamin K as effective 109
52 limited given less consistent access to low cardiac output, followed by prevention, with antenatal vitamin K 110
53 prenatal care and follow-up.5,9 The reperfusion as ventricular function reducing IVH rates by 20%.13 However, 111
54 impact of IVH is substantial in terms of improves in the first few days of life. Such this was not consistently replicated. 112
55 quality of life for patients and caregivers precipitous ischemia-reperfusion events Multiple subsequent studies examined 113
56 and economically. Annually, 3600 new can stress the germinal matrix vessels and vitamin K in combination with other 114
57 cases of people affected by intellectual lead to IVH.11 This process is thought to agents, confounding analysis of its 115
58 disability are attributable to IVH in the occur in premature infants due to potential benefit.13 A recent meta-analysis 116

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117 of 7 trials determined that, while antenatal More recently, angiogenic inhibitors porencephaly.33 In 1983, McComb et al34 175
118 vitamin K was associated with reduced rates have demonstrated potential in IVH treat- designed a low-profile subcutaneous de- 176
119 of severe IVH, this effect was not statistically ment by stabilizing the germinal matrix vice consisting of a reservoir attached to a 177
120 significant after exclusion of low-quality vasculature and preventing IVH. The COX- ventricular catheter used for repeat aspi- 178
121 studies.14 Today, vitamin K is not indicated 2 inhibitor celecoxib and the vascular ration to treat posthemorrhagic hydro- 179
122 specifically for IVH prevention but is endothelial growth factor R2 inhibitor cephalus in premature neonates. This was 180
123 routinely administered to newborns to ZD6474 reduce the incidence and severity designed to be a safe and effective 181
124 minimize vitamin K deficient bleeding.13 of germinal matrix hemorrhage in human temporizing strategy and an alternative to 182
125 In 1973, an Australian trial demon- preterm infants.23 While these findings are repeated ventricular punctures, external 183
126 strated that prophylactic treatment with promising, they require further study ventricular drainage, or permanent 184
127 coagulation factors reduced the incidence before wide adoption into clinical care. shunting. Further study has supported this 185
128 of IVH from 33% to 13% in a cohort of observation, demonstrating significantly 186
129 mechanically ventilated newborns.15 After reduced morbidity and mortality with 187
130 the application of cranial ultrasound SURGICAL MANAGEMENT OF reservoirs compared with external devices 188
131 further enabled more widespread clinical INTRAVENTRICULAR HEMORRHAGE and a lower rate of shunt dependence 189
132 diagnosis of IVH in the early 1980s, Lumbar puncture to drain IVH emerged as among those treated with reservoirs.35 190
133 Beverly et al at Leeds General Infirmary an initial treatment modality in 1905, when In 1987, Rhodes et al36 proposed external 191
134 in England demonstrated lower rates of Devraigne demonstrated that lumbar ventricular drainage as an initial treatment 192
135 IVH in preterm infants who were puncture ceased an infant’s convulsions.24 for posthemorrhagic hydrocephalus, but 193
136 administered fresh frozen plasma after By the 1920s, publications advocated for their cohort was small and notably 194
137 birth (14% vs. 41%).1 However, lumbar puncture and ventricle aspiration accompanied by complications. In 1998, 195
138 subsequent study has yielded conflicting for intraventricular hemorrhage.24 Hudgins et al37 examined 140 infants, the 196
139 results. Coagulation factors are thus not Symptomatic improvement after the largest series at that time, to study 197
140 routinely administered to prevent IVH.16 removal of 15
20 mL of blood-stained treatment of posthemorrhagic 198
141 Prenatal glucocorticoids represented a CSF was reported in the 1940s.25 Today, hydrocephalus with a ventricular access 199
142 revolutionary development in the pulmo- lumbar punctures are used in some device similar to that used by McComb 200
143 nary management of premature infants. It practices to drain CSF and lower ICP in et al,34 inserted via a frontal approach and 201
144 is not surprising that by associated path- posthemorrhagic hydrocephalus.26 accessed for CSF daily. Ventricular access 202
145 ophysiology, prenatal glucocorticoids were If posthemorrhagic hydrocephalus pro- device treatment as a temporizing 203
146 linked to IVH prevention after identifica- gresses, temporary or permanent CSF measure had benefits in its simplicity, as 204
147 tion of an association between IVH and diversion may be required. Among infants it could be used for several months, and 205
148 acute respiratory distress syndrome.8 A who require intervention for post- also enabled ease of intraventricular 206
149 landmark study in 1972 demonstrated hemorrhagic hydrocephalus, 35%
60% medication administration if needed.37 207
150 that antenatal corticosteroid therapy receive a ventriculoperitoneal shunt (VPS), Ventriculosubgaleal shunts, which drain 208
151 reduced respiratory distress syndrome a strategy first employed by Ferguson in to a pocket within the scalp, have also 209
152 incidence and mortality.17 A study in 1981 1898 and greatly enhanced by the devel- been proposed as a temporary method to 210
153 observed a 0.28 relative risk for IVH with opment of “silastic” or silicon rubber in divert CSF.26 In some studies, these 211
154 perinatal betamethasone treatment, with 1946 and its first incorporation into VPS shunts are associated with a high rate of 212
155 betamethasone reducing severity of systems in 1956 by Holter and Pudenz.27-29 CSF infection, theorized to be due to CSF 213
156 hyaline membrane disease.18 Prenatal After its advent, many problems with stasis just beneath the thin premature 214
157 steroids became part of the American CSF diversion became apparent: omental skin.26 However, multicenter retrospective 215
158 College of Obstetrics and Gynecology blockage, fibrous sheet growth, and study by the Hydrocephalus Clinical 216
159 guidelines in women between 24 and 34 infection.30 The need for shunt revision Research Network found no significant 217
160 weeks considered to be at risk for has been reported in up to 84% of difference between ventricular access 218
161 preterm delivery within 7 days.19 In 1995, infants with posthemorrhagic devices and ventriculosubgaleal shunts in 219
162 Ment et al20 identified a relative risk of hydrocephalus.31 Infection occurs in up terms of rates of conversion to VP shunt 220
163 0.55 for IVH with antenatal steroid to 22% of patients, and risks are higher or infection rates.35 Once patients meet 221
164 treatment. In 2017, a meta-analysis of in infants who are premature or low criteria for candidacy for VP shunting 222
165 6093 subjects further identified a relative birth weight and in those with after temporizing measures, VPSs are 223
166 risk for IVH of 0.55 with antenatal corti- posthemorrhagic hydrocephalus.32 typically used where feasible as the 224
167 costeroids.21 Today, antenatal steroids are Because of the high risk of infection with peritoneum allows for more ample fluid 225
168 commonly administered to women in VPS, physicians have sought alternative resorption.27 226
169 preterm labor, and the National Institute ways of draining CSF, ranging from In 1994, Whitelaw et al38 advocated 227
170 of Child Health and Human fontanelle taps to reservoirs to various intraventricular streptokinase fibrinolytic 228
171 Development reports that the overall rate diversion procedures. In addition to therapy for posthemorrhagic 229
172 of severe IVH dropped from 19% to 15% infectious risks with these procedures, hydrocephalus, hypothesizing that blood 230
173 in a 10-year span,22 temporally occurring repeated fontanelle taps used as clots in the CSF were responsible for 231
174 with this advance. temporizing measures may cause posthemorrhagic hydrocephalus and clot 232

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Figure 1. Timeline of therapies for intraventricular hemorrhage.
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260 lysis could reopen CSF channels, allowing treatment of posthemorrhagic clinical investigations given the observed 318
261 more effective reabsorption. In controlled hydrocephalus.39 relationship between the severity of IVH 319
262 clinical trials, streptokinase failed to Removing IVH blood products from the and subsequent risk of hydrocephalus.4 In 320
263 prevent shunt dependency or death.39 ventricular system early in the disease 2003, a surgical protocol to lavage IVH 321
264 Streptokinase is currently not used for course continues to be a strategy under blood, called drainage, irrigation, and 322
265 323
266 324
267 Table 1. Summary of Therapies for Intraventricular Hemorrhage 325
268 326
269 Therapy Year Benefits Risks 327
270 Ventriculoperitoneal 1898 Lowered ICP, durable solution Infection, secondary hemorrhage, need for
328
271 shunt26-29 reoperation in case of failure 329
272 330
Lumbar puncture24,25 1905 Lowered ICP without need for implanted device Infection, hemorrhage, damage to nerve roots,
273 331
repeated procedure
274 332
275 Ventricle aspiration25 1920 Lowered ICP without need for implanted device Hemorrhage, damage to intracranial structures, 333
276 repeated procedure 334
277 Prophylactic vitamin K12 1939 Reduced risk of vitamin K dependent bleeding Rare possibility of toxicity 335
278 Corticosteroids 20
1972 Reduced risk of IVH, respiratory distress, infection, and mortality Neonatal hypoglycemia, cortisol secretion
336
279 in infants 337
280 338
Ventricular access device37 1983 Repeated aspiration to treat posthemorrhagic hydrocephalus Infection, secondary hemorrhage
281 339
without a permanent shunt
282 340
283 DRIFT40-42 2003 Reduced mortality and severe disability Risk of secondary IVH 341
284 Neuroendoscopic lavage43,44 2014 Delayed shunt insertion, fewer procedures Risk of secondary IVH 342
285 343
Transplanted mesenchymal 2017 May mitigate brain injury by increasing BDNF Immune rejection, malignant transformation,
286 stem cells49 prothrombotic events
344
287 345
288 GSK3b inhibitors48 2019 Enhanced neurodevelopment, reduced neuronal apoptosis Potential for oncogenesis, uncharted territory 346
289 ICP, intracranial pressure; IVH, intraventricular hemorrhage; DRIFT, drainage, irrigation, and fibrinolytic therapy; BDNF, brain-derived neurotrophic factor. 347
290 348

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349 fibrinolytic therapy (DRIFT) reduced lesions occurred in neonates, early serial CONCLUSION 407
350 mortality (4.3%), disability rates, and the CSF taps did not have substantial benefit We reviewed the history of treatment of 408
351 need for shunt surgery (74% avoided to change outcomes. However, early IVH in premature infants to learn from 409
352 shunt placement) in a phase I trial.40 treatment of posthemorrhagic ventricular prior techniques and approaches and to 410
353 However, the trial had a small sample dilatation reduced impairments; therefore shed light on innovations in treatment. By 411
354 size (n ¼ 24) and used historical controlling hydrocephalus was thought to further refining treatment for IVH, the 412
355 controls. They also observed procedural prevent further brain injury but could not optimal treatment can be applied to 413
356 complications such as secondary IVH and heal injuries that had already been reduce mortality and morbidity. While 414
357 CSF infection.40 In a randomized, made.46 As many trials of intervention in medical and surgical technology has 415
358 multicenter trial, DRIFT failed to reduce neonatal IVH examined interventions advanced greatly over the past century, 416
359 mortality or need for subsequent CSF once ventricular size crossed the 97th only by reflecting on our history and 417
360 shunt surgery, and secondary IVH was a percentile, the ELVIS trial was designed evaluating our evolution can we better 418
361 major complication counteracting to compare intervention before and after understand what has been applied, what 419
362 potential therapeutic effects.39 In a 2-year this threshold. No effect was found on has worked, and where to focus future 420
363 follow-up for this randomized trial, the the primary outcome of death or study efforts to improve IVH treatment. 421
364 same group showed that despite an in- shunting between groups.27 However, 422
365 crease in secondary IVH, DRIFT reduced long-term follow-up of the subjects in 423
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