The diagnostic value of optic disc evaluation in acute elevated intracranial pressure

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Article

Reference

The diagnostic value of optic disc evaluation in acute elevated intracranial pressure

STEFFEN, Heimo, et al.

Abstract

Ophthalmologists often are asked to evaluate the optic disc for evidence of acute increased intracranial pressure (ICP). The authors studied the incidence of papilledema in a population of patients with a documented acute increase in ICP.

STEFFEN, Heimo, et al . The diagnostic value of optic disc evaluation in acute elevated intracranial pressure. Ophthalmology , 1996, vol. 103, no. 8, p. 1229-1232

DOI : 10.1016/s0161-6420(96)30518-6 PMID : 8764791

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The Diagnostic Value of Optic Disc Evaluation in Acute

Elevated Intracranial Pressure

Heimo Steffen, MD,l Birgit Eifert, MD,²Alfred Aschoff, MD,² Gerold H. Kolling, MD,l Hans E. V olcker, MDI

Purpose: Ophthalmologists often are asked to evaluate the optic disc for evidence of acute increased intracranial pressure (ICP). The authors studied the incidence of papilledema in a population of patients with a documented acute increase in ICP.

Methods: Included in this study were 37 patients with acute elevated ICP due to a spontaneous hemorrhage or craniocerebral trauma. In all patients, the ICP was monitored continuously. Fundus examination was performed twice daily on at least 7 consecutive days.

Results: According to the level and duration of the ICP, the patients were divided into three groups. Group 1 included 13 patients who had a slightly elevated ICP (range, 20-30 mmHg) on at least 3 consecutive days. In this group, 3 of 13 patients demonstrated venous congestion on the fifth or sixth day. No swelling of the optic disc was seen in this group. Group 2 included seven patients with an elevated ICP, with values ranging from 30 to 70 mmHg lasting for at least 3 consecutive days. In this group, one patient had a blurred disc margin on the sixth day. Group 3 included 17 patients with short- lasting ICP values, ranging from 30 to 60 mmHg for less than 72 hour. Neither papilledema nor abnormalities of fundus vessels were seen in this group.

Conclusion: Papilledema in acute elevation of ICP is an uncommon event. Its ab- sence does not preclude the presence of ICP elevation.

Ophthalmology 1996; 1 03: 1229-1232

In patients with craniocerebral trauma (CCT) or cerebral bleeding, the therapy and the outcome may depend on the intracranial pressure (ICP). Neuroradiologic imaging and even invasive measurements cannot always give the actual ICP; therefore, ophthalmologists often are asked to evaluate the optic disc for papilledema. The presence of papilledema then is regarded to be an additional sign

indicative of an elevated ICP. Nevertheless, how long and to what amount the ICP must be elevated to induce a visible papilledema remains a controversial issue, despite several clinical investigations and experimental studies addressing this problem. The current study assesses the incidence of papilledema in patients with a documented acute elevation of ICP.

Originally received: November I, 1995.

Revision accepted: May I, 1996.

1 Department of Ophthalmology, University of Heidelberg, Heidelberg, Germany.

2 Department of Neurosurgery, University of Heidelberg, Heidelberg, Germany.

Presented at the American Academy of Ophthalmology Annual Meeting, Atlanta, Oct/Nov 1995.

The authors have no proprietary interest in any of the materials used in this study.

Reprint requests to Heimo Steffen, MD, Department of Ophthalmology University of Heidelberg, INF 400,69120 Heidelberg, Germany.

Pathogenesis of Optic Disc Edema

The pathogenesis of optic disc edema in ICP has been elucidated by many investigations. '-4 Tso and Hayreh5.6

demonstrated that swelling ofaxons is the primary change in optic disc edema. During ICP elevations, the pressure in the subarachnoid space is transmitted via the optic nerve sheath to the optic disc,⁷resulting in an elevated tissue pressure within the optic nerve. The raised tissue pressure in the optic nerve impairs the

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Ophthalmology Volume 103, Number 8, August 1996 axoplasmic flOW.3,8-11 This results in an accumulation

of axoplasm with a consecutive swelling of optic nerve fibers. Previously, no unanimous explanation existed regarding why the site of disturbance of the axoplasmic flow is almost always at the lamina cribrosa. Whether primary mechanical (hydrostatic) factors or vascular factors are responsible for the impairment of the axoplasmic flow still remains controversial. 1,9, 10. 12, 13 Tso and Minckler3,6,11 as well as Radius and Anderson^l2 demonstrated that the swelling of the optic nerve fibers in optic disc edema is a direct consequence of an alter- ation of the slow component of the axoplasmic transport. The fast component of the axoplasmic transport is involved only secondarily as a result of the swollen axons. This can be deduced from the observation that, in papilledema, a blockage of the fast axonal transport is seen only in some axons, although all axons may be swollen.¹²

Hayreh and Hayreh^l4,15 demonstrated that, in optic disc edema, the swollen axons compress the fine, thin- walled vessels of the prelaminar region and the nerve fiber layer. These vessels, mostly capillaries and venous chan- nels, are part of the low-pressure system and are therefore compressed first. The vascular changes seen in optic disc edema (e.g., formation of micro aneurysms, hemorrhages, venous stasis, and venous congestion) are therefore a secondary phenomenon and arise only after manifestation of the optic disc edema.

Methods

Patients who were included in this study had an acute elevation of the ICP due to a spontaneous hemorrhagic event (subarachnoidal [SAH] or intracerebral hemorrhage [ICH]) or a CCT with extradural or intradural hemorrhage or cerebral contusion. In all patients, ICP was monitored continuously. For this purpose, an epidural probe was used in 15 patients, an external ventricular drainage in 17, and a combination of both techniques in 10. In 13 of the 15 patients with epidural probes, we used Spiegelberg probes (Spiegelberg KG, Hamburg, Germany) because they are considered to be especially unaffected by uneve- ness of the dura. In the other two patients, we used a Gaeltec probe (Gaeltec, Novotronic & Stephan GmbH, Bonn, Germany) and a Camino probe (Camino, San Diego, CA). For measuring the ICP by external ventricular drainage, Codman catheters (Codman, Randolph, MA) and Sensonor transducers (Sensonor, Oslo, Norway) were used. During the measurement of the ICP, the exact po- sition and function of catheters as well as the registration unit were tested rep~atedly. For each measurement, a new calibration of the baseline was required, which ensured the highest possible quality of measurements. There was a close correlation between the measured ICP and the clinical situation of the patients, the neuroradiologic findings, and the electro physical tests performed. Fundus examination was performed every 12 to 24 hom;s on at least 7 consecutive days. The optic disc and the peripapillary retina were assessed using direct and indirect ophthal-

moscopy. All of the patients included in this study were treated in an intensive care unit. Therefore, in the vast majority, the pupils could not be dilated for fundus examination. However, the width of the pupils was sufficient to evaluate the optic discs reliably. The 37 patients who were included in the study ranged in age from 21 to 54 years.

Results

According to the amount and the duration of the elevated ICP, the patients were divided into the following three groups.

Group I included 13 patients (8 with SAH and 5 with CCT) who had a slightly elevated ICP, with values ranging from 20 to 30 mmHg on at least 3 consecutive days. In two of these patients, a vitreous hemorrhage on both sides interfered with the fundus examination; both of these patients had an SAH. None of the remaining II patients showed any prominence or blurring of the optic disc. In three patients (2 with an SAH and I with a CCT), venous congestion was evident on the fifth or sixth day without additional vascular or retinal change.

Group 2 consisted of seven patients (6 with SAH and I with ICH), with ICP values ranging from 30 to 70 mmHg on at least 3 consecutive days. In this group, a vitreous hemorrhage made fundus examination impossible in one patient, who had an SAH. In only one ofthe seven patients of this group, papilledema developed without additional ocular pathology. This patient was a 20-year-old woman with an SAH due to an aneurysm of the bifurcation of the carotid artery on the left side. Even though a clipping of the aneurysm, an external ventricular drainage, and a craniectomy were performed, a cerebral edema and an infarction of the anterior and medial cerebral artery developed. During the first 4 days, ICP measurements ranged from 25 to 40 mmHg. The patient died 3 days later, with ICP values of approximately 60 mmHg, The time course of the ICP of this patient is demonstrated in Figure I.

The remaining five patients in this group showed neither

80 70 60 50

ICP 40

(mmHg) 30 20

10 0 24 48 72 96 120 144

time (h)

Figure 1. Time course of intracranial pressure (ICP) of the patient with papilledema (group 3).

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Steffen et al . Optic Disc Evaluation in Acute Elevated Iep Table 1. Amount and Duration of Intracranial

Pressure Elevation ICP Duration of ICP

Group (mmHg) Elevation (days) No. of Patients

20 ^~30 ^~3 13

II 30-70 ^~3 7

III 20-60 <3 17

ICP = intracranial pressure.

abnormalities of the optic disc nor of the remaining fundus.

Group 3 included 17 patients (6 with SAH, 7 with ICH, and 4 with CCT), with ICP values ranging from 20 to 60 mmHg for less than 72 hours. In this group, therapeutic procedures lowered the elevated ICP to normal in less than 72 hours. In two patients (1 with SAH and 1 with CCT), vitreous hemorrhage obscured the optic disc evaluation. Neither papilledema nor fundus vessel abnormalities or retinal changes were seen in the remaining 15 patients. The results are summarized in Tables 1 and 2.

Discussion

Our results show that papilledema is not necessarily an early sign of elevated ICP. Of 37 patients, papilledema developed in only 1, and in 3 additional patients fundus changes were seen, which was considered to be a secondary sign of papilledema. 14.15 This finding is consistent with the clinical observations of other authors. 16-18 According to Wertheimer et al19 and Levatin and Raskind 16 and confirmed by Selhorst and co-workers, 17 the development of papilledema in patients with cerebral bleeding and consecutive elevation of ICP is rare. Of more than 400 patients with craniocerebral trauma, papilledema developed in only 3.5%, which became clinically significant as late as 4 days after the incident in more than half of the patients. Fahmy18 examined 192 patients with ruptured intracranial aneurysm and found papilledema in only 16%. No correlation was found between the extent of the cerebral bleeding or edema and the development of papilledema. The report of Pagani20 who observed the de-

velopment of papilledema in three patients as soon as 2 hours after a cerebral hemorrhage is in contrast to the findings of Levatin and Raskind 16 who reported a delay of up to 13 days between the event of cerebral bleeding, with acute elevation of ICP and manifestation of papilledema. Even days after the elevated ICP returned to normal, papilledema developed. 16 Therefore, even when ICP has returned to normal, a papilledema still may develop.

The results of these clinical investigations contradict experimental studies performed by Hayreh and co- workers I4.15.21.22 in rhesus monkeys. They introduced an inflatable balloon in the temporal subarachnoidal space of these animals and thus generated an acute elevation of ICP. The changes of the optic disc and the peripapillary retina were registered using direct ophthalmoscopy, color stereoscopic photography of the optic disc, and stereoscopic fluorescein fundus angiography. Twenty-four hours after the balloon catheter was inserted, papilledema had developed in 30% of the monkeys. Papilledema was pres- ent in 50% of the monkeys after 2 days and in more than 90% after 5 days.14.22 In Hayreh and Hayreh'sI4.22 experiments, there were characteristic stages as papilledema developed. Initially, only the lower pole of the optic disc was swollen, followed by swelling of the upper pole. A swelling of the nasal part of the optic disc then developed.

Finally, the temporal margin became prominent. Vascular changes, such as increase in the diameter of the veins, were noted much later and only if a significant papilledema could be seen. In an earlier study23 with 35 animals, the onset of papilledema was noted between days 2 and 7. In a few rare cases, those changes did not develop until after 17 days.23 Hayreh and Hayreh 14.22 explained that, in the earlier studies, the optic disc was evaluated using direct ophthalmoscopy only, whereas in the second study stereoscopic fundus photographs were taken, enlarged, and analyzed. This is also pointed out by Walsh and Hoyt24 in their discussion of Hayreh's results. From these observations, it might be concluded that recognition of early stages of papilledema is difficult by funduscopic examination alone. Hayreh and Hayreh²²considered routine direct ophthalmoscopy totally unsuitable for detecting mild elevation of the optic disc. They advocate using color fundus photography supplemented by fluorescein angiography.15.22 This method of assessing the optic disc is not applicable in emergency situations in which an acutely elevated ICP is suspected. In contrast to Hayreh and Hay- reh,22 we consider the magnification of a direct ophthal-

Table 2. Results of Fundus Examination * Additional Retinal

Group Papilledema Changes T erson Disease

None 3 2

II 1 None 1

III None None 2

SAH = subarachnoidal hemorrhage; ICH = intracerebral hemorrhage; CCT = craniocerebral trauma .

• See text for further explanations.

SAH ICH CCT

8 None 5

6 1 None

6 7 4

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Ophthalmology Volume 103, Number 8, August 1996 moscope, which is approximately 15 times, to be sufficient

to allow recognition of papilledema, even at an early stage when the optic disc and the peripapillary retina are evaluated carefully.

Our results in clinical patients and those found in animal experiments contradict because, under experimental conditions, the exact morphology of the optic disc before ICP becomes elevated is known and documented. This was not the case in our study nor in any of the other studies including clinical patients. Under clinical conditions, the optic disc of a patient can be compared only with what in general is considered to be normal. Minimal changes (e.g., a slight elevation of the optic disc margin) which will only appear as pathologic when compared with the patient's own papilla before the ICP becomes elevated thus will remain unnoticed.

The clinical use of Hayreh and Hayreh's14.15.22 results of the animal experimental studies is difficult to judge.

An important objection one could rise is that Hayreh and Hayreh14 did not monitor the ICP during their experiments. Hayreh and Hayreh 14 artificially induced an elevated ICP using an inflatable balloon. The ICP was varied by injecting different amounts of fluid in the balloon. This in vivo model cannot be used as an exact replica of the clinical situation of humans with acute ICP elevation for several reasons. In the animal experiments, the ICP is highest when measured in the vicinity of the inflatable balloon. The further away from the balloon that the ICP is measured, the lower it will be. Due to an osmotic gra- dient, fluid may be exchanged between the inflated balloon and the cerebrospinal fluid, which may further lead to a change of the ICP. Therefore, as stated above, a direct correlation between the experimental situation and the clinical condition of a patient is difficult. Why a large percentage of acutely elevated ICPs without the imminent development of a papilledema is still unknown.

The primary change of papilledema is swelling ofaxons.

This swelling results when raised ICP leads-via an elevated tissue pressure of the optic nerve-to an impairment of the slow component of the axoplasmic flow.

The accumulation of axoplasm at the level of the lamina cribrosa and later on at the level of the optic disc is visible as optic disc edema.

It may be speculated that acute ICP elevation leads to both a blockage of the anterograde and the retrograde component of the axoplasmic flow, thus making it difficult for a papilledema to develop. Additional investigations and experimental work about the influence of definite ICP elevations need to be done to explain all aspects of papilledema as well as why certain conditions seem to produce papilledema more acutely than others.

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