Intramedullary Spinal Tumors

Intramedullary spinal cord tumours (IMSCTs) arise from within the substance of the spinal cord parenchyma and make up 4-10% of all central nervous system tumours. The commonest types are ependymoma (60%), astrocytoma (30%) and haemangioblastoma (3-5%). Removing a tumour from inside the cord is a distinctive surgical problem: microsurgical technique is needed to maximise resection while preserving neurological function.

Recognition. The features to recognise are a progressive myelopathy with sensory and motor deficits, a central cord pattern of dissociated sensory loss and upper limb weakness, and an MRI showing intramedullary enhancement with expansion of the cord. The lesion is typically solitary, the exception being haemangioblastoma in von Hippel-Lindau disease.

Histology decides the operation. The histological type determines the surgical approach, the resectability and the prognosis, and ependymomas have the best outcomes with gross total resection (GTR).

The cross-section. The butterfly-shaped grey matter lies centrally, motor neurons ventral and sensory neurons dorsal, and the white matter tracts surround it in columns. The central canal, a remnant of the neural tube, is a potential site of syrinx formation. The anterior median fissure and the posterior median sulcus are the midline landmarks.

The tracts at risk. Each must be preserved during the myelotomy:

• Dorsal columns (posterior): proprioception and fine touch
• Lateral corticospinal tracts: motor function, crossed
• Spinothalamic tracts (anterolateral): pain and temperature, crossed

The blood supply. A single anterior spinal artery supplies the anterior two-thirds of the cord and the paired posterior spinal arteries the posterior third. Segmental radicular arteries add a supply of variable anatomy, and the major anterior radicular artery, the artery of Adamkiewicz (T9-L2), is critical to preserve.

The surgical corridor. The posterior median sulcus is an avascular midline entry point, and passing through the dorsal columns is the least morbid route to an intramedullary lesion.

How the tumour injures the cord. The first route is mechanical. Direct pressure from the expanding tumour interrupts axonal transport and nerve conduction in the tracts, venous congestion and oedema build up around it, and the result is progressive weakness and sensory loss. The second is vascular: the tumour compresses radicular arteries, its neovascularisation "steals" blood supply, its mass effect produces venous hypertension, and manipulation at surgery carries a risk of cord infarction.

The syrinx. A syrinx is reported in a substantial minority to a majority of patients depending on tumour type; in the haemangioblastoma series cited on this page, peritumoral oedema or syringomyelia was present in 82%. The tumour obstructs CSF flow around it, fluid dissects into the central canal, and a cavity forms progressively rostral and caudal to the tumour, producing dissociated sensory loss and weakness. The syrinx often resolves after tumour resection, and resolution follows removal of the tumour without needing to enter the cavity.

Ependymoma. It arises from the ependymal cells lining the central canal. Most are WHO grade II; grade III (anaplastic) tumours are rare. Macroscopically it is well encapsulated and pushes rather than infiltrates; microscopically it shows perivascular pseudorosettes and true ependymal rosettes. The cervical and cervicothoracic cord is the commonest site (60%), and a rostral or caudal syrinx accompanies 60%.

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Astrocytoma. It arises from neoplastic astrocytes and is WHO grade II (low-grade) or III-IV (high-grade, glioblastoma). It infiltrates, with indistinct margins and a less distinct plane, enlarges the cord, spans multiple segments and carries a poorer prognosis. The background is fibrillary, with nuclear atypia and, in high-grade tumours, mitoses. The thoracic cord is the commonest site in adults and the cervical cord in children, and a syrinx is less commonly associated.

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Haemangioblastoma. It arises from the pial vessels and subpial region and is WHO grade I (benign): a highly vascular, pial-based nodule with feeding vessels, made of stromal cells and abundant capillaries. It lies in the cervical and thoracic cord, often dorsally. Von Hippel-Lindau syndrome (autosomal dominant) accounts for 25% of cases.

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Frequencies below are approximate conventional teaching ranges rather than measurements from a cited cohort - the verified numbers on this page belong to the surgical series in the Evidence Base.

Motor dysfunction is the commonest feature, present in the large majority. Weakness progresses over months to years with indolent tumours, in an upper motor neuron pattern of spasticity, hyperreflexia and clonus, with lower motor neuron signs if the anterior horn cells are involved, and with gait disturbance and ataxia.

Sensory disturbance affects most patients. Dissociated sensory loss, with pain and temperature impaired and proprioception preserved, indicates central cord involvement of the spinothalamic tract. Paraesthesiae and dysaesthesiae occur, a sensory level points to the tumour's location, and posterior column involvement impairs vibration and proprioception.

Pain is present in a majority. It may be local back or neck pain at the tumour level, radicular pain in a dermatomal distribution, or central neuropathic pain, burning or dysaesthetic. Nocturnal pain is common, and Valsalva manoeuvres make it worse.

Autonomic dysfunction is seen in a minority, usually late. Bladder urgency, frequency or retention, constipation and sexual dysfunction indicate advanced cord involvement and are associated with poorer outcomes.

A syrinx adds its own signs: cape-like sensory loss over the shoulders and arms, dissociated in the same way, Charcot (neuropathic) joints, and Horner syndrome if the syrinx is cervical.

Examination. A thorough neurological examination localises the tumour level and sets the pre-operative baseline against which the post-operative state is compared. Look for:

• Sensory level - the dermatomal level of the deficit localises the tumour
• Pyramidal signs - hyperreflexia, spasticity, a positive Babinski response, clonus
• Impaired proprioception - dorsal column dysfunction, a positive Romberg test, ataxia
• Neurogenic bladder - urgency, frequency, retention; measure the post-void residual
• Atrophy - wasting from anterior horn involvement or chronic denervation
• Lower motor neuron signs - fasciculations and hyporeflexia at the tumour level if the anterior horn is affected

The level shapes the picture.

• Cervical - upper limb weakness, proximal more than distal at first; intrinsic hand wasting if C8-T1; an inverted radial reflex with a C5-C6 tumour; Horner syndrome with T1 involvement; respiratory compromise if high cervical (C3-C5)
• Thoracic - truncal ataxia and gait disturbance, abnormal abdominal wall reflexes, a sensory level on the trunk, lower limb spasticity and weakness, and bladder dysfunction, which is common
• Conus and cauda - lower limb weakness in a mixed upper and lower motor neuron pattern, saddle anaesthesia, early bladder and bowel dysfunction, erectile dysfunction and absent ankle reflexes

Differential diagnosis. The cardinal task is separating a true intramedullary neoplasm from extramedullary compression and from non-neoplastic intramedullary signal change: vascular, inflammatory or demyelinating, infective, transverse myelitis and metabolic myelopathies. The table gives the high-yield discriminators.

The diagnostic pathway.

1. Whole-spine MRI with gadolinium - the gold standard
2. Assess for a syrinx, present in 40-60%
3. Exclude the extramedullary differential diagnoses
4. Consider von Hippel-Lindau screening if the lesion is a haemangioblastoma
5. Pre-operative neurophysiological assessment

The MRI protocol. Sagittal and axial sequences of the whole spine; T1-weighted images before and after gadolinium; T2-weighted images for cord signal and the syrinx; STIR or fat-suppressed sequences; and thin (3 mm) slices through the tumour.

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Reading the scan. The expanded cord typically spans 2-3 vertebral levels. Pial enhancement suggests a pial-based tumour or leptomeningeal spread, and haemosiderin staining marks previous haemorrhage, as in haemangioblastoma. Measure the extent of the syrinx, which may need drainage in addition to tumour resection.

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Before surgery. The rest of the work-up prepares the patient and looks for disease elsewhere:

• MRI brain - excludes intracranial lesions, especially with a haemangioblastoma
• Spine radiographs - spinal alignment and bony anatomy
• CT chest, abdomen and pelvis - staging if the tumour is high-grade or has metastatic potential
• Cardiac and respiratory assessment - fitness for anaesthesia
• Urodynamic studies - if bladder dysfunction is present

Von Hippel-Lindau screening, if the tumour is a haemangioblastoma:

• Genetic testing for a VHL gene mutation
• Retinal examination for retinal angiomas
• MRI brain for cerebellar haemangioblastomas
• Abdominal ultrasound or CT for renal cell carcinoma and pancreatic tumours
• Family history
• Annual surveillance imaging if VHL is confirmed

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Neurophysiology. Pre-operative SSEPs and MEPs record the baseline motor and sensory function, intraoperative monitoring assesses the cord in real time during resection, and post-operative studies document any neurological change.

Tissue diagnosis. Intraoperative frozen section confirms the tumour pathology, separates tumour from gliosis or demyelination and guides the extent of resection, though its accuracy is limited compared with permanent sections. Permanent histopathology uses haematoxylin and eosin with immunohistochemistry: GFAP for astrocytoma and EMA for ependymoma. The Ki-67 proliferation index predicts tumour behaviour, and the WHO grade determines the need for adjuvant therapy.

Molecular markers are emerging:

• IDH1/2 mutations - prognostic in astrocytomas
• MGMT methylation - predicts response to chemotherapy
• 1p/19q codeletion - distinguishes oligodendroglioma
• BRAF mutations - potential for targeted therapy

Indications for surgery.

• Symptomatic tumour with a progressive neurological deficit
• Radiological progression on serial imaging
• Diagnostic uncertainty requiring a tissue diagnosis
• Symptomatic syrinx associated with the tumour

Contraindications.

• Medically unfit for general anaesthesia
• Tumour spanning more than 8 vertebral levels (relative)
• Severe pre-existing neurological deficit, Frankel A (relative)
• Disseminated disease with limited life expectancy

The consent discussion. The risk of neurological deterioration is 10-30%, depending on the tumour and on cord function. The patient should hear the degree of resection the imaging predicts, that the natural history without surgery is progressive neurological decline, what role adjuvant radiotherapy or chemotherapy may play, and what function and rehabilitation to expect realistically.

The goal is set by the histology. Aim for gross total resection in ependymoma and haemangioblastoma, and for maximal safe (subtotal) resection in infiltrative astrocytoma; completeness is never pursued at the cost of function. Intraoperative neuromonitoring (SSEP and MEP) is mandatory throughout the resection.

PositioningExposureMyelotomyResectionClosure and Post-Op

The patient lies prone on a radiolucent table with chest rolls. Cervical tumours are held in Mayfield 3-pin fixation, which prevents head movement; thoracic and lumbar cases are padded prone. The arms are tucked at the sides or extended on arm boards, and the abdomen is kept free of compression, which reduces epidural venous engorgement.

Neuromonitoring electrodes are placed during setup: SSEPs from the median and tibial nerves, MEPs by transcranial stimulation. Fluoroscopy confirms the exact vertebral levels of the tumour, marks a skin incision centred over it, and plans the extent of the laminectomy.

Approach. A midline skin incision over the affected levels, subperiosteal muscle dissection from the spinous processes and laminae, and self-retaining retractors. Keep to the midline, identified by the spinous processes and interspinous ligaments.

Laminectomy. A wide laminectomy spans the tumour plus one level above and below. Preserve the facet joints, resecting less than 50% of each to avoid instability. Remove the ligamentum flavum and expose the dura widely, laterally to the nerve roots. Send the bone for autograft if fusion is anticipated.

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Dural opening. A midline durotomy, tacked open with a running suture, lets CSF drain and the cord relax. Inspect the cord surface under the operating microscope and identify the swollen segment and any feeding vessels.

The myelotomy, step by step.

1. Identify the posterior median sulcus, the avascular midline raphe
2. Confirm the absence of vessels with a micro-Doppler
3. Coagulate the pia along the intended line with bipolar
4. Open the midline sharply with an 11 blade or microscissors
5. Deepen the myelotomy through the dorsal columns to the tumour
6. Hold it open with micro-retractors, at minimal retraction pressure

Recognising the tumour. The tumour is often discoloured, grey-pink against the white matter. An ependymoma presents a glistening capsule and a well-defined plane, an astrocytoma an infiltrative and indistinct one, and a haemangioblastoma is highly vascular, with feeder vessels.

Ependymoma. A tumour-cord interface is present in 90%. Dissect circumferentially along it with microdissection, handling the cord gently to avoid traction injury; open and collapse polar cysts to reduce the mass effect, and take the tumour en bloc if feasible. The excellent plane allows GTR in 80-90%, but anchor the number to histology rather than quoting one figure for all tumours: 23 of 23 in McCormick's benign ependymoma series, 71% across the 85 mixed intraspinal ependymomas in Halvorsen, and 46 of 57 mixed intramedullary tumours in Cannizzaro, against 44% radical resection for anaplastic astrocytoma and none for glioblastoma in McGirt.

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Astrocytoma. There is no clear plane between tumour and cord. Debulk internally first to reduce the mass effect, then resect subtotally to the functional boundaries, preserving the eloquent tracts and stopping if the MEPs drop. Because of the infiltration, GTR is rarely achievable (less than 20%).

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Haemangioblastoma. The tumour is highly vascular, so obtain proximate control of the feeding vessels first, coagulating and dividing the arterial feeders early. It is often pial-based with a good plane: dissect the nodule from the cord interface, remove it en bloc, and drain an associated cyst if present. GTR is achievable if vascular control is obtained.

Operative Safety - Non-Negotiables

Resect through the posterior median sulcus only - lateral myelotomy injures the corticospinal and spinothalamic tracts. Run SSEP + MEP (D-wave where feasible) continuously; an amplitude drop greater than 50% is the alert, and a sustained MEP drop above 50% with a falling D-wave warns of permanent motor loss. Stop and rescue: pause, warm saline irrigation, reduce retraction, MAP above 85 mmHg. Abandon further resection if the deterioration persists.

Closure.

1. Meticulous haemostasis with bipolar cautery
2. Irrigate the myelotomy
3. Close the pia with 7-0 or 8-0 suture if feasible, restoring the cord contour
4. Watertight dural closure with running 4-0 suture
5. Dural sealant (DuraSeal, Tisseel)
6. No epidural drain (risk of CSF fistula)
7. Replace the bone or use laminoplasty if there is concern for kyphosis
8. Muscle and fascia in layers; subcuticular skin

Post-operative care.

• ICU monitoring for the first 24-48 hours, with neurological examination every 2 hours initially
• Mean arterial pressure above 85 mmHg for cord perfusion
• Log roll only for the first 48 hours
• Strict flat bed rest for 48 hours to reduce the risk of CSF leak
• Mobilise with physiotherapy from day 3
• Dexamethasone tapered over 1 week
• Foley catheter until mobilising (assess post-void residuals)

Extent of resection. Each term has a definition:

• Gross total resection - no visible tumour on post-operative MRI at 3 months. It is associated with the best long-term outcomes and lower recurrence rates.
• Subtotal resection - residual tumour visible on post-operative MRI; no validated percentage threshold defines it. It is often appropriate for infiltrative astrocytoma, may require adjuvant radiotherapy, and carries a higher risk of recurrence.
• Partial resection - more than 10% residual tumour. It is reserved for highly infiltrative tumours or those in eloquent locations, adjuvant therapy is usually indicated, and it may still provide symptomatic relief and a tissue diagnosis.

Radiotherapy. A typical dose is 45-54 Gy in 25-30 fractions. Radiotherapy for residual ependymoma is on the list below but remains contested (see Controversies). The indications:

• High-grade astrocytoma (WHO grade III-IV): definitive radiotherapy
• Residual ependymoma after subtotal resection
• Recurrent ependymoma
• Anaplastic ependymoma (WHO grade III)

Chemotherapy has a limited role in spinal cord gliomas. Temozolomide is used for high-grade astrocytoma, combined with radiotherapy (the Stupp protocol), with enrolment in clinical trials when appropriate.

Surveillance. MRI at 3 months sets the post-operative baseline, then every 6 months for 2 years and annually thereafter. Surveillance is lifelong because recurrence can be late.

A different site. Myxopapillary ependymoma arises almost exclusively from the filum terminale and conus medullaris, so it presents as a lumbosacral (cauda equina) lesion, with low back pain, radiculopathy, and bladder, bowel or sexual dysfunction, rather than as a cervical myelopathy. The filum terminale internum continues from the conus within the thecal sac and becomes the external filum at S1-S2.

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A different grade. The 2021 WHO CNS5 classification reclassified it as grade 2, up from grade 1, formally recognising that it recurs more readily than a cranial grade-1 ependymoma. The defining histological pattern is cuboidal and elongated tumour cells arranged around hyalinised fibrovascular cores, with myxoid material between them.

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The hazard is seeding. The tumour sits in the CSF-filled thecal sac and has a delicate capsule, so violating the capsule risks CSF (drop) metastasis and local recurrence, a particular problem in children. The surgical principle is therefore en bloc gross total resection, removing the involved filum intact. When the tumour is adherent to the conus or roots, a safe, function-preserving subtotal removal with adjuvant radiotherapy is accepted.

What carries the risk. Be precise here: the distinction that matters is total versus partial removal rather than one piece versus several. In Nakamura's 25-case series (PMID 19934795), nine of fifteen total resections were performed piecemeal and then irradiated, and fourteen of the fifteen were recurrence-free at a mean of 10.4 years, whereas all six patients left with a partial resection and a local radiotherapy field alone died of CSF dissemination.

Stage the neuraxis. The dissemination risk calls for craniospinal (whole-neuraxis) gadolinium MRI to look for drop metastases. Reserve adjuvant radiotherapy for subtotally resected, recurrent or disseminated disease, and keep surveillance lifelong because recurrence can be late.

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Why the spine deforms. A multilevel laminectomy removes the posterior tension band: the spinous processes, laminae, interspinous and supraspinous ligaments and, if violated, the facets. Without it the flexion moment is unopposed and a progressive post-laminectomy kyphosis follows, classically a "swan-neck" cervical kyphosis after cervical or cervicothoracic laminectomy.

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Children are the high-risk group. The immature spine is uniquely vulnerable, with ligamentous laxity, more horizontally oriented facets, wedge-shaped cartilaginous vertebrae and ongoing growth, so multilevel laminectomy in a child carries a high rate of progressive kyphosis or scoliosis. The other risk factors are a cervical or cervicothoracic level, the number of levels, facet-joint violation (more than 50% resection) and pre-existing malalignment.

Prevention is decided at the tumour operation. The options, in escalating order:

1. Preserve the facets (the less-than-50% rule) and the posterior ligaments as far as the exposure allows
2. Osteoplastic laminoplasty rather than laminectomy, replacing or reconstructing the posterior arch, especially in children and over multiple levels
3. Prophylactic posterior instrumented fusion where the risk is high: extensive facet removal, pre-existing kyphosis, a very young child, or a long-segment cervicothoracic exposure

Established deformity is far harder. A symptomatic post-laminectomy kyphosis usually needs combined anterior-posterior reconstruction and instrumented fusion, so it is far better prevented than corrected.

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Global Epidemiology

• Intramedullary spinal cord tumours are rare, comprising roughly 4-10% of all CNS tumours and 20-30% of all intraspinal tumours in adults; they are proportionally more common in children, in whom astrocytoma predominates over ependymoma.
• In adults the order of frequency is ependymoma (around 60%), astrocytoma (around 30%) and hemangioblastoma (3-5%); in the paediatric population astrocytoma is the most common intramedullary tumour.
• Hemangioblastoma is associated with von Hippel-Lindau disease in roughly a quarter of cases; VHL is autosomal dominant (chromosome 3p25, VHL gene) with a 50% risk to offspring.
• Spinal ependymoma shows a slight male predominance and peaks in the third-to-fifth decades; myxopapillary ependymoma characteristically arises at the conus/filum.

Side-by-Side Guidance

There is no single dedicated international guideline for intramedullary tumours; practice is informed by neuro-oncology bodies and surgical society consensus. The table summarises where authoritative sources converge and where emphasis differs.

Registry & Outcome Notes

• Because these tumours are rare, robust data come from population cancer registries (e.g. CBTRUS in the US) and large single-/multi-centre surgical series rather than implant-style joint registries. CBTRUS-type data confirm the rarity and the histological distribution above.
• Reported gross total resection rates from high-volume centres are around 70-90% for ependymoma and over 90% for hemangioblastoma, but under 20-45% for infiltrative astrocytoma - figures that should temper consent discussions.

High- vs Limited-Resource Practice Variation

• High-resource settings: routine whole-spine 1.5-3T MRI with contrast, intraoperative neuromonitoring including D-wave, ultrasonic aspiration, neuro-anaesthesia and ICU support, molecular pathology, and access to conformal radiotherapy and genetic services for VHL.
• Limited-resource settings: MRI access and intraoperative monitoring may be restricted, shifting practice toward later presentation, more conservative (often subtotal) resection to avoid deficit without monitoring, and limited molecular/genetic testing. Outcomes are correspondingly more dependent on pre-operative neurological status, reinforcing the universal principle of operating before deficits become fixed.

Several management questions in intramedullary tumour surgery remain unresolved, and they are favourite examiner territory because they test understanding of the evidence rather than recall.

Timing of surgery for the minimally symptomatic tumour. Pre-operative neurological status is the most consistent predictor of outcome, which argues for early resection before deficits become fixed. Against this is the real operative risk of making a mildly symptomatic patient worse. There is no randomised evidence, and practice is individualised to tumour type, growth and patient preference.

MEP versus D-wave thresholds. A transient MEP drop with a preserved D-wave usually predicts only transient weakness, whereas a D-wave fall over 50% predicts permanent loss. The exact alarm criteria, and how aggressively to continue after a transient MEP change, are not standardised, and D-wave recording is not feasible in every cord segment or in young children.

Adjuvant radiotherapy for subtotally resected ependymoma. Some series support radiotherapy for residual or anaplastic disease, while others, including the original McCormick experience, achieved durable control with surgery alone. There is no level I evidence, and radiotherapy carries risks of myelopathy and second malignancy.

Radiotherapy for low-grade astrocytoma. Degree of resection does not change survival within grade, and the benefit of adjuvant radiotherapy is unproven for grade II tumours, so many centres observe after maximal safe resection and reserve radiotherapy for progression. Practice varies widely.

Surgery versus observation in VHL haemangioblastoma. Asymptomatic lesions can be observed given their indolent, multifocal nature, yet some advocate earlier resection of accessible dorsal lesions before they enlarge. The decision balances cumulative operative morbidity against the risk of symptomatic progression.

Prophylactic fusion or laminoplasty. Whether to fuse or perform laminoplasty to prevent post-laminectomy kyphosis, particularly in children and after multilevel exposure, is not settled by trial evidence; age, sagittal alignment and the extent of facet preservation guide it.

Molecular reclassification. WHO CNS5 (2021) increasingly defines spinal ependymoma and glioma by molecular markers, for example MYCN amplification in spinal ependymoma, which carries a poor prognosis. How molecular subtype should modify surgical aggressiveness and adjuvant strategy is still evolving.

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2. Halvorsen CM, Kolstad F, Hald J, et al. Long-term outcome after resection of intraspinal ependymomas: report of 86 consecutive cases. Neurosurgery. 2010;67(6):1622-1631. doi:10.1227/NEU.0b013e3181f96d41. PMID 21107192.

3. Lonser RR, Weil RJ, Wanebo JE, DeVroom HL, Oldfield EH. Surgical management of spinal cord hemangioblastomas in patients with von Hippel-Lindau disease. J Neurosurg. 2003;98(1):106-116. doi:10.3171/jns.2003.98.1.0106. PMID 12546358.

4. Cannizzaro D, Mancarella C, Nasi D, et al. Intramedullary spinal cord tumors: the value of intraoperative neurophysiological monitoring in a series of 57 cases. J Neurosurg Sci. 2022;66(5):447-455. doi:10.23736/S0390-5616.19.04758-1. PMID 31565906.

5. Siller S, Szelenyi A, Herlitz L, Tonn JC, Zausinger S. Spinal cord hemangioblastomas: significance of intraoperative neurophysiological monitoring for resection and long-term outcome. J Neurosurg Spine. 2017;26(4):483-493. doi:10.3171/2016.8.SPINE16595. PMID 27982764.

6. McGirt MJ, Goldstein IM, Chaichana KL, et al. Extent of surgical resection of malignant astrocytomas of the spinal cord: outcome analysis of 35 patients. Neurosurgery. 2008;63(1):55-60. doi:10.1227/01.NEU.0000335070.37943.09. PMID 18728568.

7. Innocenzi G, Salvati M, Cervoni L, Delfini R, Cantore G. Prognostic factors in intramedullary astrocytomas. Clin Neurol Neurosurg. 1997;99(1):1-5. doi:10.1016/s0303-8467(96)00555-0. PMID 9107459.

8. Samartzis D, Gillis CC, Shih P, O'Toole JE, Fessler RG. Intramedullary spinal cord tumors: part I--epidemiology, pathophysiology, and diagnosis. Global Spine J. 2015;5(5):425-435. doi:10.1055/s-0035-1549029. PMID 26430598.

9. Samartzis D, Gillis CC, Shih P, O'Toole JE, Fessler RG. Intramedullary spinal cord tumors: part II--management options and outcomes. Global Spine J. 2016;6(2):176-185. PMID 26933620.

Every card below carries its PMID and DOI.