British Journal of Neurosurgery, 2015; Early Online: 1–5 © 2015 The Neurosurgical Foundation ISSN: 0268-8697 print / ISSN 1360-046X online DOI: 10.3109/02688697.2015.1012047
REVIEW ARTICLE
Sinking skin flap syndrome (or Syndrome of the trephined): A review Mariam Annan1,2, Bertrand De Toffol1,2,4, Caroline Hommet2,3,4 & Karl Mondon2,3,4
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1Department of Neurology, University Hospital Center of Tours, Tours, France, 2Université François Rabelais, Tours, France, 3Department of Geriatric Medicine and Memory Center, University Hospital Center of Tours, Tours, France,
and 4INSERM U930, Tours, France Abstract Background. Bone defects of the skull are observed in various pathological conditions, including head trauma and conditions requiring surgery of the skull. Independent of the consequences of the original aetiology that necessitated the craniectomy, the bone defect alone may be the cause of the symptoms, called ‘trephined syndrome’ or ‘sinking skin flap syndrome’. Despite the early recognition of neurological symptoms directly linked to craniectomy, the description of this syndrome has often relied on a small series or single clinical case reports. Objectives. To list the previously reported symptoms of SSFS. Data sources. We selected the references for this review by searching PubMed, focusing on articles published prior to June 2013 and using references from relevant articles. Study eligibility criteria. We used the following search terms: ‘trephined syndrome’, ‘syndrome of the trephined’, ‘Sinking skin flap’, and ‘sinking skin flap syndrome’. There were no language restrictions. The final reference list was generated on the basis of its relevance to the topics covered in this review. Conclusions. Clinicians need to be aware of sinking skin flap syndrome and to look for abnormal neurological developments in patients with craniectomy in order to avoid unnecessary testing and to prevent its occurrence. Accordingly, cranioplasty can be undertaken as soon as necessary.
a feeling of apprehension and insecurity, mental depression, and intolerance to vibration’ which they suggested would resolve following a bone replacement procedure.2 Nevertheless, from both their own investigations and other previous research that they cited in their comprehensive study, the following additional symptoms were recognised: seizures, weakness or paralysis, headaches, numbness and other sensory changes, visual disturbances (e.g., field defects, blurred vision, and diplopia), mental changes, and speech disturbances. During the next half-century, these findings were confirmed by several studies that described patients whose neurological status improved after cranioplasty. In 1977, Yamaura et al3,4 reported on a large series of patients who suffered from reversible symptoms after bone replacement and coined the term ‘sinking skin flap syndrome’ (SSFS). If the SSFS and ‘trephined syndrome’ are considered synonymous in the literature, then the clinical picture of symptom improvement following cranioplasty widely exceeds the initial description from 1939. However, the precise meaning of these two terms is not clear. Some papers include in the definition any instance of neurologic deterioration occurring secondary to a craniectomy,3,5 whereas others add some characteristics to the definition, such as the association with a sinking skin flap or ‘paradoxical herniation’,6 or the reversibility of the symptoms after cranioplasty, which has been documented by many reports. Regardless of the definition behind those terms, the range of symptoms presented by the patients is extensive. The aim of this article was to clarify the clinical picture of SSFS according to published studies on the topic.
Keywords: decompressive craniectomy; neurorehabilitation; review; trauma
Bone defects of the skull are observed in various pathological conditions, including head trauma (comminuted fractures) and conditions requiring surgery of the skull (e.g., bone tumours, infections, decompressive craniectomy after trauma, strokes, cerebral thrombophlebitis, tumours, encephalitis).1 Independent of the original aetiology that necessitated the craniectomy, the bone defect alone may be the cause of the symptoms. In 1939, Grant and Norcross defined the ‘syndrome of the trephined’ by a cluster of symptoms that included ‘dizziness, undue fatigability, vague discomfort at the site of the defect,
Search strategy and selection criteria We selected the references for this review by searching PubMed for articles published prior to June 2013 and by consulting the references contained within relevant articles. We used the search terms ‘trephined syndrome’, ‘syndrome of the trephined’, ‘Sinking skin flap’, and ‘sinking skin flap syndrome’. No language restrictions were applied to our article
Correspondence: Dr Mariam Annan, Department of Neurology, University Hospital Center of Tours, Tours 37044, France. Tel: 33 2 47 47 86 45. Fax: 33 2 47 47 82 81. E-mail: [email protected] Received for publication 25 February 2014; accepted 18 January 2015
1
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2 M. Annan et al. search. The final reference list was generated on the basis of its relevance to the topics covered in this review. Of the 51 papers selected according to the search criteria, 42 directly concerned the topic of this review.3,4,6–17,5,18–44 The majority of the papers were in English with the exception of one that was published in Spanish14 and 4 that were in Japanese.4,8,22,29 For the purposes of our study, we only used the authors’ translated abstract in the four articles written in Japanese. We excluded three papers that consisted of general reviews of SSFS without any clinical case description,7,15,17 six that concerned craniectomy or cranioplasty without any specific focus on SSFS9,34,37,40,42,43 and one that did not include any clinical data.39 As a result, we retained 32 articles that contained a description of the clinical picture of the patients.3,4,6,8,10–14,16,5,18–33,35,36,38,41,44 A careful scrutiny of these articles and their references allowed us to identify 11 supplementary papers that were relevant to our aims.45–55 Consequently, our study group consisted of 43 published articles. Dramatic improvement of neurological symptoms after bone replacement is considered to be a core feature of the syndrome (see below) and papers with lacking description of neurological recovery after cranioplasty were excluded from analysis.
Data collection process In each article, we looked for demographic data, including the age and sex of the patients, and the indication for which craniectomy was performed. The following data were also collected: all symptoms that appeared secondary to the craniectomy and those that were relieved after the cranioplasty, the time between the craniectomy and the neurological aggravation, and the time between the cranioplasty and clinical improvement.
Results Type of articles, number of patients, and demographic characteristics The largest series of SSFS, which included the study of 22 patients, was published in 1984 by Fodstad et al.5 Six publications only contained a restricted number of case reports: 10,41 7,6 6,18 5,33 4,4 and 2 patients.24 The remaining 27 papers consisted of single case reports.3,8,10–15,19–23,25–32,35,36,38,44–47 In total, we identified only 83 patients in the published literature who had SSFS. The mean age of the patients was 45 / 14 years, and the range was 1718 to 77 years.25 The M/F sex ratio was 1.56.
Indications for craniectomy The indications for craniectomy were various and corresponded to the usual clinical indications1: stroke (n 116,18,20,36), traumatic brain injury (n 913,14,18,21,24,30,31), sub- or epidural haematoma (n 712,18,19,25,29,47), meningioma (n 627,33), subarachnoid haemorrhage (n 58,10,26,28,32), assault (n 111), or not available (n 43).
Diagnosis of SSFS In all the cases studied, the patients presented with a skin flap depression (clinically or radiologically) following craniectomy. The clinical status of six patients remained unchanged, and the diagnosis was based solely on the aspect of the skin flap.6,18
Delay in neurological progression The mean time before the appearance of neurological decline was 50 weeks, but the range was considerable (138 weeks). Four case reports described the appearance of neurological decline only a few days after craniectomy: Joseph and Reilly25 reported positional sensory impairment in a 77-year-old man 9 days following craniectomy. Three other case reports described early SSFS that appeared within a few days in patients with craniectomy after the following contributing factors: removal of the bone flap,12 lumbar puncture,20 or ventricular derivation.33 A very delayed onset of SSFS was also reported for 5 patients: 2,30,32 7,33 158 and 6038 years. With the exception of these cases, SSFS usually occurs between 1 month and 1 year after craniectomy (mean time 13 weeks / 8).
Motor symptoms Motor symptoms are often observed in SSFS and most frequently consist of hemiparesis, 8,5,22,26,27,33,47 which was seen in 17 of the 22 patients studied by Fodstad et al.5 Additionally, Stiver40 mentioned ‘motor SSFS’. Other symptoms that have been reported in the literature include gait disturbances,32 akinetic mutism,22 and parkinsonian tremor.10 Babinski’s sign has also been observed.6
Cognitive syndrome A large variety of cognitive symptoms have been described in the literature, including bradypsychia,10 slowing of speech fluency,10 impaired naming and word finding scores,30 aboulia,11,24 dysphasia,5 dyspraxia,5 and astereognosis.33 Memory disturbances11,5 have also been reported, but to the best of our knowledge, the precise stage of memory processing (e.g., storage, retrieval) to be affected was never described.
Impaired vigilance The severity of the impairment of vigilance is variable, ranging from fatigue,19 drowsiness,6,24 low arousal23,24,29,33 to lethargy18,33 and coma.11,27 Vigilance can be normal in SSFS.33
Headaches Fodstad et al. observed headaches in 10 of 22 cases of their series.5 These may be accompanied by vomiting, and positional aggravation has also been described.6
Other neurological symptoms Some authors have reported the following sensory impairments: dysesthesia,26 hypoalgesia,33 hypoasthesia,33 and proprioceptive deficit.27,33
Sinking skin flap syndrome 3 Visual symptoms have also been described, including visual impairment,5 orthostatic diplopia,10 mydriasis,10 strabismus,19 elevation deficit,19 and quadranopsia.33 Dysarthria,10 vertigo,5 urinary incontinence,27 mood disturbances,24,30 and vomiting6 have also been reported. Epileptic seizures have also described and most frequently consist of partial motor seizures.6,47
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Clinical course after bone replacement Excluding instances when the diagnosis of SSFS is based on clear-cut radiological criteria,6,18,33 authors report the complete recovery from all symptoms following cranioplasty3,4,8,10,11,14,18–22,24–27,30–33,35,47; as an exception, recovery is described as partial.18,33 The delay before recovery is almost always described as being very short, typically between 24 h and 2 weeks.3,10,14,20,24,26,32,47 However, late recovery (6 months) is also possible.30
Positional worsening of symptoms A number of papers have described the positional worsening of symptoms, such as when the patient rises to the orthostatic position, and usually consists of headaches6,30 but visual impairment has also been reported.10
Discussion The term ‘trephined syndrome’ has long been present in the literature. Despite the fact that it has often been associated with craniectomy, the publications in the literature are usually limited to single case reports: fewer than one hundred cases have been reported, and the clinical characteristics of the symptoms presented were often poorly described. Progressively, the use of the term ‘sinking skin flap syndrome’ was preferred,4 but the limits of the clinical picture remain unclear. According to the literature, the syndrome widely exceeds the original description:2 ‘vague discomfort at the side of the defect, feeling of apprehension and insecurity, intolerance to vibration’ are not observed, and dizziness and undue fatigability are usually rare. In contrast, sensorimotor impairment, cognitive disturbances and disorders of vigilance, and headaches are often present. According to
the symptoms most frequently reported in the literature, the typical clinical picture of SSFS is represented by a male subject of any age who undergoes a craniectomy for one of many possible indications and 3 months later develops neurological complications that are not explained by another medical condition (e.g., epileptic seizures, hydrocephalus, metabolic-, or toxic disorder). The principal symptoms are sensorimotor and cognitive impairment and headaches. Visual symptoms may be observed. Postural changes are very suggestive. It is sometimes difficult to distinguish the symptoms related to the disorder that required the craniectomy from those solely due to the skin flap. Many researchers consider a progressive and rapid recovery to be key features for making the diagnosis of SSFS.5 The pathophysiology of SSFS remains unclear, and hypotheses have often been formulated based on single case reports. One hypothesis suggests a direct transmission of atmospheric pressure to the intracranial cavity through the skin flap3,47,48,56 and, subsequently, direct brain compression. In 1974, George et al. revealed a positive correlation between clinical improvement and the return of the skin flap to its normal position.57 Other authors postulate that differential changes between intracranial pressure and atmospheric pressure lead to hypovolemia and/or hypopressure in the CSF,49 similar to the abrupt onset of changes seen in intracranial hydrostatic pressure following CSF depletion (lumbar puncture, removal of the bone flap, ventriculoperitoneal shunt).18,21,33 The orthostatic position may aggravate this phenomenon.10,21 According to some authors, craniectomy may lead to substantial changes in the regulation of blood flow and consequently modify cerebral glucose metabolism.50 A vascular mechanism involving a reduction in regional cerebral blood flow has been suggested by findings from studies employing CT scans,51 CT perfusion imaging,32 and Xenon CT.23 Yoshida demonstrated a link between improved brain perfusion and cerebral metabolism,52 and additional studies have demonstrated a positive correlation between an improvement in perfusion and symptom regression.51–54 Cranioplasty has been shown to improve the neurological impairment by correcting the last mentioned abnormalities.9,55 The principal hypotheses for explaining the possible mechanisms of SSFS are summarised in Fig. 1.
Fig. 1. Summary of possible mechanisms of SSFS.
4 M. Annan et al.
Conclusion
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Despite the early recognition of neurological symptoms directly linked to craniectomy, the description of this syndrome has often relied on a small series or single clinical case reports. Using a comprehensive review of the literature, we listed the previously reported symptoms of SSFS. Clinicians need to be aware of SSFS and look for abnormal neurological developments in patients with craniectomy in order to avoid unnecessary testing and prevent its occurrence. Accordingly, cranioplasty can be undertaken as soon as necessary. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Kolias AG, Kirkpatrick PJ, Hutchinson PJ. Decompressive craniectomy: past, present and future. Nat Rev Neurol 2013;9: 405–15. 2. Grant FC, Norcross NC. Repair of cranial defects by cranioplasty. Ann Surg 1939;110:488–512. 3. Yamaura A, Makino H. Neurological deficits in the presence of the sinking skin flap following decompressive craniectomy. Neurol Med Chir (Tokyo) 1977;17:43–53. 4. Yamaura A, Sato M, Meguro K, Nakamura T, Uemura K. [Cranioplasty following decompressive craniectomy–analysis of 300 cases (author’s transl)]. No Shinkei Geka 1977;5:345–53. 5. Fodstad H, Love JA, Ekstedt J, Fridén H, Liliequist B. Effect of cranioplasty on cerebrospinal fluid hydrodynamics in patients with the syndrome of the trephined. Acta Neurochir (Wien) 1984;70:21–30. 6. Sarov M, Guichard J-P, Chibarro S, et al. Sinking skin flap syndrome and paradoxical herniation after hemicraniectomy for malignant hemispheric infarction. Stroke J Cereb Circ 2010;41:560–2. 7. Akins PT, Guppy KH. Sinking skin flaps, paradoxical herniation, and external brain tamponade: a review of decompressive craniectomy management. Neurocrit Care 2008;9:269–76. 8. Anei R, Uemori G, Orimoto R, et al. [A case of brain herniation due to delayed bone flap sinking]. No Shinkei Geka 2010;38:923–6. 9. Archavlis E, Carvi Y, Nievas M. The impact of timing of cranioplasty in patients with large cranial defects after decompressive hemicraniectomy. Acta Neurochir (Wien) 2012;154:1055–62. 10. Bijlenga P, Zumofen D, Yilmaz H, Creisson E, de Tribolet N. Orthostatic mesodiencephalic dysfunction after decompressive craniectomy. J Neurol Neurosurg Psychiatry 2007;78:430–3. 11. Carota A, Pintucci M, Zanchi F, D’Ambrosio E, Calabrese P. “Cognitive” sinking skin flap syndrome. Eur Neurol 2011;66:227–8. 12. Chalouhi N, Teufack S, Fernando Gonzalez L, Rosenwasser RH, Jabbour PM. An extreme case of the syndrome of the trephined requiring the use of a novel titanium plate. Neurologist 2012;18:423–5. 13. Choi JJ, Cirivello MJ, Neal CJ, Armonda RA. Paradoxical herniation in wartime penetrating brain injury with concomitant skull-base trauma. J Craniofac Surg 2011;22:2163–7. 14. de Quintana-Schmidt C, Clavel-Laria P, Asencio-Cortes C, Vendrell-Brucet JM, Molet-Teixido J. [Sinking skin flap syndrome]. Rev Neurol 2011;52:661–4. 15. Dujovny M, Aviles A, Agner C, Fernandez P, Charbel FT. Cranioplasty: cosmetic or therapeutic? Surg Neurol 1997;47: 238–41. 16. Dujovny M, Fernandez P, Alperin N, Betz W, Misra M, Mafee M. Post-cranioplasty cerebrospinal fluid hydrodynamic changes: magnetic resonance imaging quantitative analysis. Neurol Res 1997;19:311–16. 17. Dujovny M, Agner C, Aviles A. Syndrome of the trephined: theory and facts. Crit Rev Neurosurg 1999;9:271–8. 18. Gadde J, Dross P, Spina M. Syndrome of the trephined (sinking skin flap syndrome) with and without paradoxical herniation: a series of case reports and review. Del Med J 2012;84:213–18.
19. Gottlob I, Simonsz-Tòth B, Heilbronner R. Midbrain syndrome with eye movement disorder: dramatic improvement after cranioplasty. Strabismus 2002;10:271–7. 20. Gschwind M, Michel P, Siclari F. Life-threatening sinking skin flap syndrome due to CSF leak after lumbar puncture - treated with epidural blood patch. Eur J Neurol 2012;19:e49. 21. Han PY, Kim JH, Kang HI, Kim JS. “Syndrome of the sinking skin-flap” secondary to the ventriculoperitoneal shunt after craniectomy. J Korean Neurosurg Soc 2008;43:51–3. 22. Hodozuka A, Takebayashi S, Nakai H, Hashizume K, Tanaka T. [A case of the syndrome of the sinking skin flap: case report]. No Shinkei Geka 2000;28:245–9. 23. Isago T, Nozaki M, Kikuchi Y, Honda T, Nakazawa H. Sinking skin flap syndrome: a case of improved cerebral blood flow after cranioplasty. Ann Plast Surg 2004;53:288–92. 24. Janzen C, Kruger K, Honeybul S. Syndrome of the trephined following bifrontal decompressive craniectomy: implications for rehabilitation. Brain Inj 2012;26:101–5. 25. Joseph V, Reilly P. Syndrome of the trephined. J Neurosurg 2009;111:650–2. 26. Kemmling A, Duning T, Lemcke L, et al. Case report of MR perfusion imaging in sinking skin flap syndrome: growing evidence for hemodynamic impairment. BMC Neurol 2010;10:80. 27. Kumar GS, Chacko AG, Rajshekhar V. Unusual presentation of the “syndrome of the trephined”.Neurol India 2004;52:504–5. 28. Kwon SM, Cheong JH, Kim JM, Kim CH. Reperfusion injury after autologous cranioplasty in a patient with sinking skin flap syndrome. J Korean Neurosurg Soc 2012;51:117–19. 29. Mizumaki Y, Oka N, Itoh K, Endo S. [A case of the traumatic hydrocephalus after large craniectomy for acute subdural hematoma]. No Shinkei Geka 2003;31:201–6. 30. Mokri B. Orthostatic headaches in the syndrome of the trephined: resolution following cranioplasty. Headache 2010;50:1206–11. 31. Ng D, Dan NG. Cranioplasty and the syndrome of the trephined. J Clin Neurosci Off J Neurosurg Soc Australas 1997;4:346–8. 32. Sakamoto S, Eguchi K, Kiura Y, Arita K, Kurisu K. CT perfusion imaging in the syndrome of the sinking skin flap before and after cranioplasty. Clin Neurol Neurosurg 2006;108:583–5. 33. Schiffer J, Gur R, Nisim U, Pollak L. Symptomatic patients after craniectomy. Surg Neurol 1997;47:231–7. 34. Schmidt JH III, Reyes BJ, Fischer R, Flaherty SK. Use of hinge craniotomy for cerebral decompression. Technical note. J Neurosurg 2007;107:678–82. 35. Schneck MJ, Origitano TC. Hemicraniectomy and durotomy for malignant middle cerebral artery infarction. Neurol Clin 2006;24:715–27. 36. Schorl M. Sinking skin flap syndrome (SSFS) – clinical spectrum and impact on rehabilitation. Cent Eur Neurosurg 2009;70:68–72. 37. Sinclair AG, Scoffings DJ. Imaging of the post-operative cranium. Radiogr Rev Publ Radiol Soc North Am Inc 2010;30:461–82. 38. Singh FB, Khosla VK, Gupta SK, Prasad KS. Growing fracture of the skull: report of an unusual case. Surg Neurol 1994;42:165–7. 39. Staykov D, Huttner HB, Kollmar R, et al. When decompressive craniectomy does not lead to decompression: sinking skin flap syndrome after intracerebral hemorrhage. Eur Neurol 2010;64:319. 40. Stiver SI. Complications of decompressive craniectomy for traumatic brain injury. Neurosurg Focus 2009;26:E7. 41. Stiver SI. Wintermark M, Manley GT. Reversible monoparesis following decompressive hemicraniectomy for traumatic brain injury. J Neurosurg 2008;109:245–54. 42. Stula D. The problem of the “sinking skin-flap syndrome” in cranioplasty. J Maxillofac Surg 1982;10:142–5. 43. Takumi I, Akimoto M. Catcher’s mask cranioplasty for extensive cranial defects in children with an open head trauma: a novel application of partial cranioplasty. Childs Nerv Syst 2008;24:927–32. 44. Yang XF, Wen L, Shen F, et al. Surgical complications secondary to decompressive craniectomy in patients with a head injury: a series of 108 consecutive cases. Acta Neurochir (Wien) 2008;150:1241–7; discussion 1248. 45. Yamaura A, Makino H. Neurological deficits following craniectomy. Neurosurg Forum 1976;45:362. 46. Richaud J, Boetto S, Guell A, Lazorthes Y. [Effects of cranioplasty on neurological function and cerebral blood flow]. Neurochirurgie 1985;31:183–8. 47. Tabaddor K, LaMorgese J. Complication of a large cranial defect. Case report. J Neurosurg 1976;44:506–8. 48. Nakamura T, Takashima T, Isobe K, Yamaura A. Rapid neurological alteration associated with concave deformity of the skin flap in a
Sinking skin flap syndrome 5
49.
50.
51.
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52.
craniectomized patient. Case report. Neurol Med Chir (Tokyo) 1980;20:89–93. Oyelese AA, Steinberg GK, Huhn SL, Wijman CA. Paradoxical cerebral herniation secondary to lumbar puncture after decompressive craniectomy for a large space-occupying hemispheric stroke: case report. Neurosurgery 2005;57:E594; discussion E594. Winkler PA, Stummer W, Linke R, Krishnan KG, Tatsch K. Influence of cranioplasty on postural blood flow regulation, cerebrovascular reserve capacity, and cerebral glucose metabolism. J Neurosurg 2000;93:53–61. Suzuki N, Suzuki S, Iwabuchi T. Neurological improvement after cranioplasty. Analysis by dynamic CT scan. Acta Neurochir (Wien) 1993;122:49–53. Yoshida K, Furuse M, Izawa A, Iizima N, Kuchiwaki H, Inao S. Dynamics of cerebral blood flow and metabolism in patients with
53. 54. 55. 56. 57.
cranioplasty as evaluated by 133Xe CT and 31P magnetic resonance spectroscopy. J Neurol Neurosurg Psychiatry 1996;61:166–71. Stiver SI, Wintermark M, Manley GT. Reversible monoparesis following decompressive hemicraniectomy for traumatic brain injury. J Neurosurg 2008;109:245–54. Maeshima S, Kagawa M, Kishida Y, et al. Unilateral spatial neglect related to a depressed skin flap following decompressive craniectomy. Eur Neurol 2005;53:164–8. Segal DH, Oppenheim JS, Murovic JA. Neurological recovery after cranioplasty. Neurosurgery 1994;34:729–31; discussion 731. Langfitt TW. Increased intracranial pressure. Clin Neurosurg 1969;16:436–71. George AE, Morantz RA, Abad RM, Rovit RL, Chase N. Neuroradiology of the posthemicraniectomy patient with special emphasis on the radiology of unilateral atrophy. Radiology 1974;111:627–31.
REVIEW ARTICLE
Sinking skin flap syndrome (or Syndrome of the trephined): A review Mariam Annan1,2, Bertrand De Toffol1,2,4, Caroline Hommet2,3,4 & Karl Mondon2,3,4
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1Department of Neurology, University Hospital Center of Tours, Tours, France, 2Université François Rabelais, Tours, France, 3Department of Geriatric Medicine and Memory Center, University Hospital Center of Tours, Tours, France,
and 4INSERM U930, Tours, France Abstract Background. Bone defects of the skull are observed in various pathological conditions, including head trauma and conditions requiring surgery of the skull. Independent of the consequences of the original aetiology that necessitated the craniectomy, the bone defect alone may be the cause of the symptoms, called ‘trephined syndrome’ or ‘sinking skin flap syndrome’. Despite the early recognition of neurological symptoms directly linked to craniectomy, the description of this syndrome has often relied on a small series or single clinical case reports. Objectives. To list the previously reported symptoms of SSFS. Data sources. We selected the references for this review by searching PubMed, focusing on articles published prior to June 2013 and using references from relevant articles. Study eligibility criteria. We used the following search terms: ‘trephined syndrome’, ‘syndrome of the trephined’, ‘Sinking skin flap’, and ‘sinking skin flap syndrome’. There were no language restrictions. The final reference list was generated on the basis of its relevance to the topics covered in this review. Conclusions. Clinicians need to be aware of sinking skin flap syndrome and to look for abnormal neurological developments in patients with craniectomy in order to avoid unnecessary testing and to prevent its occurrence. Accordingly, cranioplasty can be undertaken as soon as necessary.
a feeling of apprehension and insecurity, mental depression, and intolerance to vibration’ which they suggested would resolve following a bone replacement procedure.2 Nevertheless, from both their own investigations and other previous research that they cited in their comprehensive study, the following additional symptoms were recognised: seizures, weakness or paralysis, headaches, numbness and other sensory changes, visual disturbances (e.g., field defects, blurred vision, and diplopia), mental changes, and speech disturbances. During the next half-century, these findings were confirmed by several studies that described patients whose neurological status improved after cranioplasty. In 1977, Yamaura et al3,4 reported on a large series of patients who suffered from reversible symptoms after bone replacement and coined the term ‘sinking skin flap syndrome’ (SSFS). If the SSFS and ‘trephined syndrome’ are considered synonymous in the literature, then the clinical picture of symptom improvement following cranioplasty widely exceeds the initial description from 1939. However, the precise meaning of these two terms is not clear. Some papers include in the definition any instance of neurologic deterioration occurring secondary to a craniectomy,3,5 whereas others add some characteristics to the definition, such as the association with a sinking skin flap or ‘paradoxical herniation’,6 or the reversibility of the symptoms after cranioplasty, which has been documented by many reports. Regardless of the definition behind those terms, the range of symptoms presented by the patients is extensive. The aim of this article was to clarify the clinical picture of SSFS according to published studies on the topic.
Keywords: decompressive craniectomy; neurorehabilitation; review; trauma
Bone defects of the skull are observed in various pathological conditions, including head trauma (comminuted fractures) and conditions requiring surgery of the skull (e.g., bone tumours, infections, decompressive craniectomy after trauma, strokes, cerebral thrombophlebitis, tumours, encephalitis).1 Independent of the original aetiology that necessitated the craniectomy, the bone defect alone may be the cause of the symptoms. In 1939, Grant and Norcross defined the ‘syndrome of the trephined’ by a cluster of symptoms that included ‘dizziness, undue fatigability, vague discomfort at the site of the defect,
Search strategy and selection criteria We selected the references for this review by searching PubMed for articles published prior to June 2013 and by consulting the references contained within relevant articles. We used the search terms ‘trephined syndrome’, ‘syndrome of the trephined’, ‘Sinking skin flap’, and ‘sinking skin flap syndrome’. No language restrictions were applied to our article
Correspondence: Dr Mariam Annan, Department of Neurology, University Hospital Center of Tours, Tours 37044, France. Tel: 33 2 47 47 86 45. Fax: 33 2 47 47 82 81. E-mail: [email protected] Received for publication 25 February 2014; accepted 18 January 2015
1
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2 M. Annan et al. search. The final reference list was generated on the basis of its relevance to the topics covered in this review. Of the 51 papers selected according to the search criteria, 42 directly concerned the topic of this review.3,4,6–17,5,18–44 The majority of the papers were in English with the exception of one that was published in Spanish14 and 4 that were in Japanese.4,8,22,29 For the purposes of our study, we only used the authors’ translated abstract in the four articles written in Japanese. We excluded three papers that consisted of general reviews of SSFS without any clinical case description,7,15,17 six that concerned craniectomy or cranioplasty without any specific focus on SSFS9,34,37,40,42,43 and one that did not include any clinical data.39 As a result, we retained 32 articles that contained a description of the clinical picture of the patients.3,4,6,8,10–14,16,5,18–33,35,36,38,41,44 A careful scrutiny of these articles and their references allowed us to identify 11 supplementary papers that were relevant to our aims.45–55 Consequently, our study group consisted of 43 published articles. Dramatic improvement of neurological symptoms after bone replacement is considered to be a core feature of the syndrome (see below) and papers with lacking description of neurological recovery after cranioplasty were excluded from analysis.
Data collection process In each article, we looked for demographic data, including the age and sex of the patients, and the indication for which craniectomy was performed. The following data were also collected: all symptoms that appeared secondary to the craniectomy and those that were relieved after the cranioplasty, the time between the craniectomy and the neurological aggravation, and the time between the cranioplasty and clinical improvement.
Results Type of articles, number of patients, and demographic characteristics The largest series of SSFS, which included the study of 22 patients, was published in 1984 by Fodstad et al.5 Six publications only contained a restricted number of case reports: 10,41 7,6 6,18 5,33 4,4 and 2 patients.24 The remaining 27 papers consisted of single case reports.3,8,10–15,19–23,25–32,35,36,38,44–47 In total, we identified only 83 patients in the published literature who had SSFS. The mean age of the patients was 45 / 14 years, and the range was 1718 to 77 years.25 The M/F sex ratio was 1.56.
Indications for craniectomy The indications for craniectomy were various and corresponded to the usual clinical indications1: stroke (n 116,18,20,36), traumatic brain injury (n 913,14,18,21,24,30,31), sub- or epidural haematoma (n 712,18,19,25,29,47), meningioma (n 627,33), subarachnoid haemorrhage (n 58,10,26,28,32), assault (n 111), or not available (n 43).
Diagnosis of SSFS In all the cases studied, the patients presented with a skin flap depression (clinically or radiologically) following craniectomy. The clinical status of six patients remained unchanged, and the diagnosis was based solely on the aspect of the skin flap.6,18
Delay in neurological progression The mean time before the appearance of neurological decline was 50 weeks, but the range was considerable (138 weeks). Four case reports described the appearance of neurological decline only a few days after craniectomy: Joseph and Reilly25 reported positional sensory impairment in a 77-year-old man 9 days following craniectomy. Three other case reports described early SSFS that appeared within a few days in patients with craniectomy after the following contributing factors: removal of the bone flap,12 lumbar puncture,20 or ventricular derivation.33 A very delayed onset of SSFS was also reported for 5 patients: 2,30,32 7,33 158 and 6038 years. With the exception of these cases, SSFS usually occurs between 1 month and 1 year after craniectomy (mean time 13 weeks / 8).
Motor symptoms Motor symptoms are often observed in SSFS and most frequently consist of hemiparesis, 8,5,22,26,27,33,47 which was seen in 17 of the 22 patients studied by Fodstad et al.5 Additionally, Stiver40 mentioned ‘motor SSFS’. Other symptoms that have been reported in the literature include gait disturbances,32 akinetic mutism,22 and parkinsonian tremor.10 Babinski’s sign has also been observed.6
Cognitive syndrome A large variety of cognitive symptoms have been described in the literature, including bradypsychia,10 slowing of speech fluency,10 impaired naming and word finding scores,30 aboulia,11,24 dysphasia,5 dyspraxia,5 and astereognosis.33 Memory disturbances11,5 have also been reported, but to the best of our knowledge, the precise stage of memory processing (e.g., storage, retrieval) to be affected was never described.
Impaired vigilance The severity of the impairment of vigilance is variable, ranging from fatigue,19 drowsiness,6,24 low arousal23,24,29,33 to lethargy18,33 and coma.11,27 Vigilance can be normal in SSFS.33
Headaches Fodstad et al. observed headaches in 10 of 22 cases of their series.5 These may be accompanied by vomiting, and positional aggravation has also been described.6
Other neurological symptoms Some authors have reported the following sensory impairments: dysesthesia,26 hypoalgesia,33 hypoasthesia,33 and proprioceptive deficit.27,33
Sinking skin flap syndrome 3 Visual symptoms have also been described, including visual impairment,5 orthostatic diplopia,10 mydriasis,10 strabismus,19 elevation deficit,19 and quadranopsia.33 Dysarthria,10 vertigo,5 urinary incontinence,27 mood disturbances,24,30 and vomiting6 have also been reported. Epileptic seizures have also described and most frequently consist of partial motor seizures.6,47
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Clinical course after bone replacement Excluding instances when the diagnosis of SSFS is based on clear-cut radiological criteria,6,18,33 authors report the complete recovery from all symptoms following cranioplasty3,4,8,10,11,14,18–22,24–27,30–33,35,47; as an exception, recovery is described as partial.18,33 The delay before recovery is almost always described as being very short, typically between 24 h and 2 weeks.3,10,14,20,24,26,32,47 However, late recovery (6 months) is also possible.30
Positional worsening of symptoms A number of papers have described the positional worsening of symptoms, such as when the patient rises to the orthostatic position, and usually consists of headaches6,30 but visual impairment has also been reported.10
Discussion The term ‘trephined syndrome’ has long been present in the literature. Despite the fact that it has often been associated with craniectomy, the publications in the literature are usually limited to single case reports: fewer than one hundred cases have been reported, and the clinical characteristics of the symptoms presented were often poorly described. Progressively, the use of the term ‘sinking skin flap syndrome’ was preferred,4 but the limits of the clinical picture remain unclear. According to the literature, the syndrome widely exceeds the original description:2 ‘vague discomfort at the side of the defect, feeling of apprehension and insecurity, intolerance to vibration’ are not observed, and dizziness and undue fatigability are usually rare. In contrast, sensorimotor impairment, cognitive disturbances and disorders of vigilance, and headaches are often present. According to
the symptoms most frequently reported in the literature, the typical clinical picture of SSFS is represented by a male subject of any age who undergoes a craniectomy for one of many possible indications and 3 months later develops neurological complications that are not explained by another medical condition (e.g., epileptic seizures, hydrocephalus, metabolic-, or toxic disorder). The principal symptoms are sensorimotor and cognitive impairment and headaches. Visual symptoms may be observed. Postural changes are very suggestive. It is sometimes difficult to distinguish the symptoms related to the disorder that required the craniectomy from those solely due to the skin flap. Many researchers consider a progressive and rapid recovery to be key features for making the diagnosis of SSFS.5 The pathophysiology of SSFS remains unclear, and hypotheses have often been formulated based on single case reports. One hypothesis suggests a direct transmission of atmospheric pressure to the intracranial cavity through the skin flap3,47,48,56 and, subsequently, direct brain compression. In 1974, George et al. revealed a positive correlation between clinical improvement and the return of the skin flap to its normal position.57 Other authors postulate that differential changes between intracranial pressure and atmospheric pressure lead to hypovolemia and/or hypopressure in the CSF,49 similar to the abrupt onset of changes seen in intracranial hydrostatic pressure following CSF depletion (lumbar puncture, removal of the bone flap, ventriculoperitoneal shunt).18,21,33 The orthostatic position may aggravate this phenomenon.10,21 According to some authors, craniectomy may lead to substantial changes in the regulation of blood flow and consequently modify cerebral glucose metabolism.50 A vascular mechanism involving a reduction in regional cerebral blood flow has been suggested by findings from studies employing CT scans,51 CT perfusion imaging,32 and Xenon CT.23 Yoshida demonstrated a link between improved brain perfusion and cerebral metabolism,52 and additional studies have demonstrated a positive correlation between an improvement in perfusion and symptom regression.51–54 Cranioplasty has been shown to improve the neurological impairment by correcting the last mentioned abnormalities.9,55 The principal hypotheses for explaining the possible mechanisms of SSFS are summarised in Fig. 1.
Fig. 1. Summary of possible mechanisms of SSFS.
4 M. Annan et al.
Conclusion
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Despite the early recognition of neurological symptoms directly linked to craniectomy, the description of this syndrome has often relied on a small series or single clinical case reports. Using a comprehensive review of the literature, we listed the previously reported symptoms of SSFS. Clinicians need to be aware of SSFS and look for abnormal neurological developments in patients with craniectomy in order to avoid unnecessary testing and prevent its occurrence. Accordingly, cranioplasty can be undertaken as soon as necessary. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Kolias AG, Kirkpatrick PJ, Hutchinson PJ. Decompressive craniectomy: past, present and future. Nat Rev Neurol 2013;9: 405–15. 2. Grant FC, Norcross NC. Repair of cranial defects by cranioplasty. Ann Surg 1939;110:488–512. 3. Yamaura A, Makino H. Neurological deficits in the presence of the sinking skin flap following decompressive craniectomy. Neurol Med Chir (Tokyo) 1977;17:43–53. 4. Yamaura A, Sato M, Meguro K, Nakamura T, Uemura K. [Cranioplasty following decompressive craniectomy–analysis of 300 cases (author’s transl)]. No Shinkei Geka 1977;5:345–53. 5. Fodstad H, Love JA, Ekstedt J, Fridén H, Liliequist B. Effect of cranioplasty on cerebrospinal fluid hydrodynamics in patients with the syndrome of the trephined. Acta Neurochir (Wien) 1984;70:21–30. 6. Sarov M, Guichard J-P, Chibarro S, et al. Sinking skin flap syndrome and paradoxical herniation after hemicraniectomy for malignant hemispheric infarction. Stroke J Cereb Circ 2010;41:560–2. 7. Akins PT, Guppy KH. Sinking skin flaps, paradoxical herniation, and external brain tamponade: a review of decompressive craniectomy management. Neurocrit Care 2008;9:269–76. 8. Anei R, Uemori G, Orimoto R, et al. [A case of brain herniation due to delayed bone flap sinking]. No Shinkei Geka 2010;38:923–6. 9. Archavlis E, Carvi Y, Nievas M. The impact of timing of cranioplasty in patients with large cranial defects after decompressive hemicraniectomy. Acta Neurochir (Wien) 2012;154:1055–62. 10. Bijlenga P, Zumofen D, Yilmaz H, Creisson E, de Tribolet N. Orthostatic mesodiencephalic dysfunction after decompressive craniectomy. J Neurol Neurosurg Psychiatry 2007;78:430–3. 11. Carota A, Pintucci M, Zanchi F, D’Ambrosio E, Calabrese P. “Cognitive” sinking skin flap syndrome. Eur Neurol 2011;66:227–8. 12. Chalouhi N, Teufack S, Fernando Gonzalez L, Rosenwasser RH, Jabbour PM. An extreme case of the syndrome of the trephined requiring the use of a novel titanium plate. Neurologist 2012;18:423–5. 13. Choi JJ, Cirivello MJ, Neal CJ, Armonda RA. Paradoxical herniation in wartime penetrating brain injury with concomitant skull-base trauma. J Craniofac Surg 2011;22:2163–7. 14. de Quintana-Schmidt C, Clavel-Laria P, Asencio-Cortes C, Vendrell-Brucet JM, Molet-Teixido J. [Sinking skin flap syndrome]. Rev Neurol 2011;52:661–4. 15. Dujovny M, Aviles A, Agner C, Fernandez P, Charbel FT. Cranioplasty: cosmetic or therapeutic? Surg Neurol 1997;47: 238–41. 16. Dujovny M, Fernandez P, Alperin N, Betz W, Misra M, Mafee M. Post-cranioplasty cerebrospinal fluid hydrodynamic changes: magnetic resonance imaging quantitative analysis. Neurol Res 1997;19:311–16. 17. Dujovny M, Agner C, Aviles A. Syndrome of the trephined: theory and facts. Crit Rev Neurosurg 1999;9:271–8. 18. Gadde J, Dross P, Spina M. Syndrome of the trephined (sinking skin flap syndrome) with and without paradoxical herniation: a series of case reports and review. Del Med J 2012;84:213–18.
19. Gottlob I, Simonsz-Tòth B, Heilbronner R. Midbrain syndrome with eye movement disorder: dramatic improvement after cranioplasty. Strabismus 2002;10:271–7. 20. Gschwind M, Michel P, Siclari F. Life-threatening sinking skin flap syndrome due to CSF leak after lumbar puncture - treated with epidural blood patch. Eur J Neurol 2012;19:e49. 21. Han PY, Kim JH, Kang HI, Kim JS. “Syndrome of the sinking skin-flap” secondary to the ventriculoperitoneal shunt after craniectomy. J Korean Neurosurg Soc 2008;43:51–3. 22. Hodozuka A, Takebayashi S, Nakai H, Hashizume K, Tanaka T. [A case of the syndrome of the sinking skin flap: case report]. No Shinkei Geka 2000;28:245–9. 23. Isago T, Nozaki M, Kikuchi Y, Honda T, Nakazawa H. Sinking skin flap syndrome: a case of improved cerebral blood flow after cranioplasty. Ann Plast Surg 2004;53:288–92. 24. Janzen C, Kruger K, Honeybul S. Syndrome of the trephined following bifrontal decompressive craniectomy: implications for rehabilitation. Brain Inj 2012;26:101–5. 25. Joseph V, Reilly P. Syndrome of the trephined. J Neurosurg 2009;111:650–2. 26. Kemmling A, Duning T, Lemcke L, et al. Case report of MR perfusion imaging in sinking skin flap syndrome: growing evidence for hemodynamic impairment. BMC Neurol 2010;10:80. 27. Kumar GS, Chacko AG, Rajshekhar V. Unusual presentation of the “syndrome of the trephined”.Neurol India 2004;52:504–5. 28. Kwon SM, Cheong JH, Kim JM, Kim CH. Reperfusion injury after autologous cranioplasty in a patient with sinking skin flap syndrome. J Korean Neurosurg Soc 2012;51:117–19. 29. Mizumaki Y, Oka N, Itoh K, Endo S. [A case of the traumatic hydrocephalus after large craniectomy for acute subdural hematoma]. No Shinkei Geka 2003;31:201–6. 30. Mokri B. Orthostatic headaches in the syndrome of the trephined: resolution following cranioplasty. Headache 2010;50:1206–11. 31. Ng D, Dan NG. Cranioplasty and the syndrome of the trephined. J Clin Neurosci Off J Neurosurg Soc Australas 1997;4:346–8. 32. Sakamoto S, Eguchi K, Kiura Y, Arita K, Kurisu K. CT perfusion imaging in the syndrome of the sinking skin flap before and after cranioplasty. Clin Neurol Neurosurg 2006;108:583–5. 33. Schiffer J, Gur R, Nisim U, Pollak L. Symptomatic patients after craniectomy. Surg Neurol 1997;47:231–7. 34. Schmidt JH III, Reyes BJ, Fischer R, Flaherty SK. Use of hinge craniotomy for cerebral decompression. Technical note. J Neurosurg 2007;107:678–82. 35. Schneck MJ, Origitano TC. Hemicraniectomy and durotomy for malignant middle cerebral artery infarction. Neurol Clin 2006;24:715–27. 36. Schorl M. Sinking skin flap syndrome (SSFS) – clinical spectrum and impact on rehabilitation. Cent Eur Neurosurg 2009;70:68–72. 37. Sinclair AG, Scoffings DJ. Imaging of the post-operative cranium. Radiogr Rev Publ Radiol Soc North Am Inc 2010;30:461–82. 38. Singh FB, Khosla VK, Gupta SK, Prasad KS. Growing fracture of the skull: report of an unusual case. Surg Neurol 1994;42:165–7. 39. Staykov D, Huttner HB, Kollmar R, et al. When decompressive craniectomy does not lead to decompression: sinking skin flap syndrome after intracerebral hemorrhage. Eur Neurol 2010;64:319. 40. Stiver SI. Complications of decompressive craniectomy for traumatic brain injury. Neurosurg Focus 2009;26:E7. 41. Stiver SI. Wintermark M, Manley GT. Reversible monoparesis following decompressive hemicraniectomy for traumatic brain injury. J Neurosurg 2008;109:245–54. 42. Stula D. The problem of the “sinking skin-flap syndrome” in cranioplasty. J Maxillofac Surg 1982;10:142–5. 43. Takumi I, Akimoto M. Catcher’s mask cranioplasty for extensive cranial defects in children with an open head trauma: a novel application of partial cranioplasty. Childs Nerv Syst 2008;24:927–32. 44. Yang XF, Wen L, Shen F, et al. Surgical complications secondary to decompressive craniectomy in patients with a head injury: a series of 108 consecutive cases. Acta Neurochir (Wien) 2008;150:1241–7; discussion 1248. 45. Yamaura A, Makino H. Neurological deficits following craniectomy. Neurosurg Forum 1976;45:362. 46. Richaud J, Boetto S, Guell A, Lazorthes Y. [Effects of cranioplasty on neurological function and cerebral blood flow]. Neurochirurgie 1985;31:183–8. 47. Tabaddor K, LaMorgese J. Complication of a large cranial defect. Case report. J Neurosurg 1976;44:506–8. 48. Nakamura T, Takashima T, Isobe K, Yamaura A. Rapid neurological alteration associated with concave deformity of the skin flap in a
Sinking skin flap syndrome 5
49.
50.
51.
Br J Neurosurg Downloaded from informahealthcare.com by SUNY State University of New York at Stony Brook on 03/13/15 For personal use only.
52.
craniectomized patient. Case report. Neurol Med Chir (Tokyo) 1980;20:89–93. Oyelese AA, Steinberg GK, Huhn SL, Wijman CA. Paradoxical cerebral herniation secondary to lumbar puncture after decompressive craniectomy for a large space-occupying hemispheric stroke: case report. Neurosurgery 2005;57:E594; discussion E594. Winkler PA, Stummer W, Linke R, Krishnan KG, Tatsch K. Influence of cranioplasty on postural blood flow regulation, cerebrovascular reserve capacity, and cerebral glucose metabolism. J Neurosurg 2000;93:53–61. Suzuki N, Suzuki S, Iwabuchi T. Neurological improvement after cranioplasty. Analysis by dynamic CT scan. Acta Neurochir (Wien) 1993;122:49–53. Yoshida K, Furuse M, Izawa A, Iizima N, Kuchiwaki H, Inao S. Dynamics of cerebral blood flow and metabolism in patients with
53. 54. 55. 56. 57.
cranioplasty as evaluated by 133Xe CT and 31P magnetic resonance spectroscopy. J Neurol Neurosurg Psychiatry 1996;61:166–71. Stiver SI, Wintermark M, Manley GT. Reversible monoparesis following decompressive hemicraniectomy for traumatic brain injury. J Neurosurg 2008;109:245–54. Maeshima S, Kagawa M, Kishida Y, et al. Unilateral spatial neglect related to a depressed skin flap following decompressive craniectomy. Eur Neurol 2005;53:164–8. Segal DH, Oppenheim JS, Murovic JA. Neurological recovery after cranioplasty. Neurosurgery 1994;34:729–31; discussion 731. Langfitt TW. Increased intracranial pressure. Clin Neurosurg 1969;16:436–71. George AE, Morantz RA, Abad RM, Rovit RL, Chase N. Neuroradiology of the posthemicraniectomy patient with special emphasis on the radiology of unilateral atrophy. Radiology 1974;111:627–31.
