SUPERNUMERARY PHANTOM LIMBS ASSOCIATED WITH LEFT HEMISPHERIC STROKE: CASE REPORT AND REVIEW OF THE LITERATURE Nobuhiko Miyazawa, M.D. Department of Neurosurgery, Akiyama Neurosurgical Clinic, Yamanashi, Japan Masataka Hayashi, M.D. Department of Neurology, Kofu City Hospital, Yamanashi, Japan Keiji Komiya, M.D. Department of Rehabilitation, Kofu Johnan Hospital, Yamanashi, Japan Iwao Akiyama, M.D. Department of Neurosurgery, Akiyama Neurosurgical Clinic, Yamanashi, Japan Reprint requests: Nobuhiko Miyazawa, M.D., Department of Neurosurgery, Akiyama Neurosurgical Clinic, 1330 Wakao Ohkusa-cho, Nirasaki City, Yamanashi 407-0037, Japan. Email: akinouge@crux.ocn.ne.jp Received, March 8, 2003. Accepted, August 28, 2003. OBJECTIVE AND IMPORTANCE: Supernumerary phantom limb (SPL) is extremely rare. Literature reports noted 17 cases that occurred after right cerebral hemispheric stroke and 2 cases that occurred after left cerebral hemispheric stroke, but without imaging diagnoses. CLINICAL PRESENTATION: A 45-year-old male patient complained of SPLs on the right side after recurrent left thalamic hemorrhage. Computed tomography and magnetic resonance imaging demonstrated the lesion causing the left hemispheric stroke. INTERVENTION: The patient was treated conservatively. Computed tomographic scans demonstrated that the lesion had disappeared by 15 days after admission. The sensation of SPLs disappeared after 28 days. CONCLUSION: SPL may occur among patients with left hemispheric stroke, especially those with lesions in the thalamus, spastic paresis on the right side immediately after stroke, and psychiatric disorders such as alcohol and tobacco intoxication. KEY WORDS: Cerebral infarction, Intracerebral hemorrhage, Supernumerary phantom limb Neurosurgery 54:228-231, 2004 DOI: 10.1227/01.NEU.0000097558.01639.F5 T he phantom limb phenomenon commonly occurs after surgical or traumatic amputations, in as many as 90 to 100% of cases (8, 16). In contrast, the equivalent phenomenon caused by cerebral lesions, which is called supernumerary phantom limb (SPL) (4) or phantom third limb (8, 16), is extremely rare; it was first noted after right hemispheric stroke (6) or left hemispheric stroke (18), but without imaging diagnoses. SPL may be caused by lesions in the right or left cerebral hemisphere (7), but a predominance of right hemispheric stroke has been reported (3, 10, 11). Here we describe a case of SPL after left hemispheric hemorrhage, which was identified on computed tomographic (CT) and magnetic resonance imaging scans, and we discuss the clinical and radiological features. CASE REPORT A 42-year-old man was hospitalized on March 20, 1999, because of right hemiparesis and dysarthria. His history included alcohol intoxication, excessive smoking, liver dysfunction attributable to alcohol consumption, hypertension, hyperuremia, diabetes mellitus, and hyperlipidemia. The patient had been 228 | VOLUME 54 | NUMBER 1 | JANUARY 2004 www.neurosurgery-online.com treated medically, but his compliance was unusually poor. A neurological examination revealed consciousness disturbances, motor aphasia, right hemiparesis involving the face (spastic paresis), and superficial sensory disturbances, including an absence of sensitivity to pain, temperature, and light touch (almost anesthesia). No profound sensory disturbances, such as positional sense deficits, vibrational sense deficits, hemianopia, or right-side neglect, were observed. CT scans obtained at the time of admission revealed an area of left putaminal hemorrhage measuring 3 ⫻ 3.5 cm (Fig. 1A). The patient was treated conservatively, with hyperbaric therapy. Two days after admission, the patient became alert and could report his hemiparesis. He experienced kinetic hallucinations (movement of the right extremities) and macrosomatagnosia (ballooning of the face and body on the right side, especially the face) 5 days after admission. These phenomena tapered and disappeared by 10 days after admission. The symptoms gradually improved, and the patient became independent in daily life, with slight difficulty in the fine movements of the fingers of the right hand. He was referred to a rehabilitation hospital on May 22, 1999. www.neurosurgery-online.com SUPERNUMERARY PHANTOM LIMBS WITH HEMISPHERIC STROKE FIGURE 1. A, CT scan obtained at the time of the first admission, showing a left putaminal area of hemorrhage measuring 3 ⫻ 3.5 cm. B, CT scan obtained at the time of the second admission, revealing a left thalamic area of hemorrhage measuring 1.5 ⫻ 2 cm. C, coronal magnetic resonance imaging scan, showing left posteromedial thalamic hemorrhage. D, drawing of the SPLs by the patient. The abnormal upper and lower limbs emerged inside the original limbs, and the distal SPLs were not clearly drawn. The patient experienced an onset of anesthesia on the right side of the body and worsening of right hemiparesis after he was surprised by a fire surrounding his garden on November 24, 2001. He was transported to our clinic by ambulance and was immediately hospitalized. He was almost alert, with anisocoria. A neurological examination demonstrated motor aphasia, right hemiparesis (severe spastic paresis), right anesthesia to both superficial and deep sensations, and autotopagnosia (agnosia of his own body parts) on the right side of the body without anosognosia (agnosia of hemiparesis). Axial CT scans demonstrated a high-density area extending from the thalamus to the posterior limb of the internal capsule in the left hemisphere, measuring 1.5 ⫻ 2 cm (Fig. 1B), which was considered to represent thalamic hemorrhage. Two days after admission, the patient complained of complex visual hallucinations in his hemianoptic field (a number of flying objects). He also complained of severe spasticity in the right extremities. Three days after admission, he was alert and fully oriented, and the visual hallucinations and hemianopia had disappeared. However, the patient felt the presence of another set of right upper and lower extremities, inside the original extremities (Fig. 1D). He explained that he could clearly see another upper arm, forearm, upper leg, and lower leg but no hand or foot. He became upset when asked about NEUROSURGERY his phantom limbs. He did not feel the phantom limbs when he used the left extremities. Five days after admission, axial magnetic resonance imaging scans revealed a high-intensity area extending from the thalamus to the internal capsule, measuring 2.1 ⫻ 4 cm, and coronal and sagittal magnetic resonance imaging scans demonstrated that the core of high intensity was located in the ventroposterior medial and lateral nuclei (Fig. 1C). Magnetic resonance angiography demonstrated no vascular abnormalities, such as an arteriovenous malformation. Fifteen days after admission, CT scans demonstrated that the high-density area in the thalamus had completely disappeared. Seventeen days after admission, single-photon emission CT scans revealed hypoperfusion in the posterior thalamus, putamen, subcortical region, parietal cortex (including the sensory cortex and motor cortex), and corpus callosum in the left hemisphere and also indicated crossed cerebellar diaschisis. Cerebral blood flow in the middle cerebral artery territory was 52 ml/100 g/min in the right hemisphere and 45 ml/100 g/min in the left hemisphere. Although the phantom lower extremity had disappeared by 15 days after admission, the patient experienced severe pain in the phantom upper extremity 18 days after admission. The phantom upper extremity gradually tapered (telescoping), and it disappeared completely 28 days after admission. No impairments of the visual field and acuity or hearing were noted. Electroencephalography demonstrated no abnormalities. The patient was transferred to the rehabilitation hospital on December 22, 2001. After discharge from the rehabilitation hospital, the patient was treated medically at another clinic. His compliance with the medication regimen was poor. The patient drank volumes of alcohol similar to those consumed previously. He complained of severe pain in the right upper arm and the spastic paresis continued, but the muscle tone was more relaxed than at the time of the second admission. No more episodes of SPL occurred, but the patient clearly remembered the SPLs on the right side during the second admission. DISCUSSION The 20 cases of SPL attributable to cerebral stroke that have been reported in the past 70 years, including our case, are summarized in Table 1 (1–7, 9–15, 18–21). The 14 male and 6 female patients were 35 to 80 years of age (mean, 58.1 yr). Right cerebral hemispheric stroke was the cause in 17 cases (2–7, 9–15, 19–21), and left hemispheric stroke was the cause in only 3 cases (1, 18). A 69-year-old female patient experienced SPL on the right side after encephalomalacia at the left claustrum to the internal capsule (18). Her right arm lay on her chest, and her hallucination was that she lifted her right arm 20 cm. A 60-year-old male patient experienced SPL on the right side after a cerebral infarction in the left thalamohypothalamic region (1). The causative event, as demonstrated with neuroimaging, was subarachnoid hemorrhage in one case (12), ischemic VOLUME 54 | NUMBER 1 | JANUARY 2004 | 229 MIYAZAWA ET AL. TABLE 1. Reports of supernumerary phantom limbs attributable to cerebral strokea Side of stroke Left Right With imaging diagnosisb Without imaging diagnosis Series (ref. no.) Age (yr)/sex Pinéas, 1932 (18) 69/F Bogaert, 1934 (1) 60/M Ehrenwald, 1930 (6) Series (ref. no.) Age (yr)/sex Diagnosis Present case, 2002 45/M ICH 59/M Hohjoh et al., 1989 (14) 49/M ICH Hecaen et al., 1952 (13) 64/M Halligan et al., 1993 (11) 65/M ICH Gilliatt and Pratt, 1952 (9) 62/F Halligan and Marshall, 1995 (10) 80/M CI Critchley, 1953 (4) 52/M Sellal et al., 1996 (19) 77/M CI Unknown / M a b Weinstein et al., 1954 (20) 57/F Worthington and Beevers, 1996 (21) 72/F CI Brock and Merwarth, 1956 (2) 58/M Donnet et al., 1997 (5) 35/M ICH Fredericks, 1963 (7) 36/M Mazzoni et al., 1997 (15) 66/M CI Hari et al., 1998 (12) 37/F SAH Canavero et al., 1999 (3) 61/F ICH ICH, intracerebral hemorrhage; CI, cerebral infarction; SAH, subarachnoid hemorrhage. Based on computed tomographic and/or magnetic resonance imaging findings. stroke in four cases (10, 15, 19, 21), and intracerebral hemorrhage in four (3, 5, 11, 14). Our case was interesting because no SPL occurred after the first hemorrhagic episode, whereas the SPLs persisted for a rather short period after the second hemorrhagic episode. Alcohol intoxication was noted in the histories of four patients, including our patient (5, 11, 14). A 49-year-old male patient experienced SPL after right putaminal hemorrhage (14). He had a history of alcohol intoxication and was hospitalized and treated. A 65-year-old male patient experienced SPL after a right basal ganglia hematoma (11). He also had a history of excessive alcohol consumption, which had ceased 3 years before admission. A 35-year-old male patient experienced SPL after a right capsulolenticular hematoma (5). He also had a history of alcohol and tobacco intoxication. Our patient had demonstrated severe alcohol and tobacco intoxication for nearly 20 years and was drinking two bottles of whiskey every night and smoking 60 cigarettes every day. These psychiatric factors might have influenced the occurrence of SPL. Cases of SPL on the left may present with various degrees of sensory disturbances, such as sensory loss (11), impairment of sensitivity to light touch and proprioception (15), left hemisensory disturbances in all modalities (5), and tactile-pinprick anesthesia on the left (3). Previous cases of SPL on the right involved no precise description of sensory disturbances (1) and sensory disturbances less severe than anesthesia (18). In our case, severe anesthesia to superficial and profound stimuli 230 | VOLUME 54 | NUMBER 1 | JANUARY 2004 was present; therefore, whether any sensory disturbance is characteristic of SPL remains unknown. All three patients with left hemispheric stroke experienced severe spastic right hemiparesis. Previous patients exhibited spastic paralysis of the right arm (18) and left spastic hemiplegia (1). Our patient exhibited severe spastic paresis in the right arm and leg, which continued during the episode of SPL. The development of SPL may be determined more by motor loss than by sensory loss (3, 11, 19). Therefore, spastic hemiparesis may be involved in SPL. The main site of damage was the lenticular nucleus in cases with right hemispheric hemorrhage causing left SPL (5, 11, 14) and the middle cerebral artery territory in cases with right hemispheric infarction (10, 15, 19, 21). Thalamic damage as the cause of left SPL was rare (3, 10, 11). In contrast, autopsies in two cases of left hemispheric stroke causing right SPL revealed that the main sites of damage were the thalamus and internal capsule (1, 18). In our case, the first episode of hemorrhage (in the putamen) was not associated with SPL, whereas the second episode of hemorrhage (in the thalamus) resulted in SPL. The reason why SPL is more likely to be associated with right hemispheric stroke than left hemispheric stroke remains unclear. This association may occur partly because of the functional differences between the right and left hemispheres and partly because of the prevalence of right hemispheric stroke. The right hemisphere seems to be involved in controlling sensorimotor integration (3) and is dominant in maintain- www.neurosurgery-online.com SUPERNUMERARY PHANTOM LIMBS WITH HEMISPHERIC STROKE ing the internal representation of the body state (3). The attentional network may also be controlled by the right hemisphere (5). The incidence of right thalamic hemorrhage is significantly higher than that of left thalamic hemorrhage (17). Our case illustrates some possible causative factors of SPL among patients with left hemispheric stroke, including lesions located in the thalamus, spastic paresis immediately after stroke, and psychiatric disorders, such as alcohol and tobacco intoxication. SPL may be more common than reported (7, 8, 10, 11); therefore, thorough examinations are essential for the care of stroke patients. REFERENCES 1. Bogaert LV: Sur la pathologie de l’image de soi. Ann Med Psychol 92:519– 536, 1934. 2. Brock S, Merwarth HR: The illusory awareness of body parts in cerebral disease. Arch Neurol Psychiatry 77:366–370, 1956. 3. Canavero S, Bonicalzi V, Castellano G, Perozzo P, Massa-Micon B: Painful supernumerary phantom arm following motor cortex stimulation for central poststroke pain: Case report. J Neurosurg 91:121–123, 1999. 4. Critchley M: The Parietal Lobes. New York, Hafner, 1953, pp 243–244. 5. Donnet A, Schmitt A, Poncet M, Graziani N, Grisoli F: Hallucinations of supernumerary limbs, left hemineglect and hypersexuality in a case of right capsulo-lenticular hematoma [in French]. Rev Neurol (Paris) 153:587–590, 1997. 6. Ehrenwald H: Verändertes Erleben des Körperbildes mit konsekutiver Wahnbildung bei linkseitiger Hemiplegie. Monatsschr Psychiatr Neurol 75:89–97, 1930. 7. Fredericks J: Occurrence and nature of phantom limb phenomena following amputation of body parts and following lesions of the central and peripheral nervous system. Psychiatr Neurol Neurochir 66:73–97, 1963. 8. Fredericks J: Phantom limb and phantom limb pain, in Fredericks J (ed): Handbook of Clinical Neurology: Clinical Neuropsychology. Amsterdam, Elsevier, 1985, vol 1, pp 373–393. 9. Gilliatt R, Pratt R: Disorders of perception and performance in a case of right-sided cerebral thrombosis. J Neurol Neurosurg Psychiatry 15:264–271, 1952. 10. Halligan PW, Marshall JC: Supernumerary phantom limb after right hemispheric stroke. J Neurol Neurosurg Psychiatry 59:341–342, 1995. 11. Halligan PW, Marshall JC, Wade DT: Three arms: A case study of supernumerary phantom limb after hemisphere stroke. J Neurol Neurosurg Psychiatry 56:159–166, 1993. 12. Hari R, Hanninen R, Makinen T, Jousmaki V, Forss N, Seppa M, Salonen O: Three hands: Fragmentation of human bodily awareness. Neurosci Lett 240:131–134, 1998. 13. Hecaen H, Ajuriaguerra J, Angelergues R: Délire centré sur un memberfantôme chez une hémiplégique gauche par lésion vasculaire avec anosognosie. Evol Psychiatr (Paris) 2:273–279, 1952. 14. Hohjoh T, Ohyama H, Watanabe S: Asomatognosia and anosognosia [in Japanese], in Yamadori S (ed): Neuropsychiatry and Image Diagnosis. Tokyo, Asakura Shoin, 1989, vol 2, pp 218–225. 15. Mazzoni M, Lucchini C, Meucci G, Vista M, Moretti P, Sartucci F: Replication: Supernumerary phantom limb after ischaemic stroke. Neurocase 3:223–230, 1997. 16. Melzack R: Phantom limbs and the concept of a neuromatrix. Trends Neurosci 13:88–92, 1990. 17. Nasreddine ZS, Saver JL: Pain after thalamic stroke: Right diencephalic predominance and clinical features in 180 patients. Neurology 48:1196–1199, 1997. 18. Pinéas H: Ein Fall von phantomähnlichen Erscheinungen (“Phantomarm”) bei hemiplegischer Lähmung. Nervenarzt 5:233–236, 1932. NEUROSURGERY 19. Sellal F, Renaseau-leclerc C, Labrecque R: The man with 6 arms: An analysis of supernumerary phantom limbs after right hemisphere stroke [in French]. Rev Neurol (Paris) 152:190–195, 1996. 20. Weinstein EA, Kahn RL, Malitz S, Rozanski J: Delusional reduplication of parts of the body. Brain 77:45–60, 1954. 21. Worthington A, Beevers L: Two arms, three hands: A supernumerary phantom phenomenon after right middle cerebral artery stroke. Neurocase 2:135–140, 1996. COMMENTS I n this report, the authors describe a rare case of supernumerary phantom limbs (SPLs) after left cerebral hemisphere stroke with imaging diagnosis. Computed tomography and magnetic resonance imaging demonstrated a left thalamic hemorrhage. Such lesions may occur in the right or the left cerebral hemisphere, but there is a predominance of right hemisphere strokes in association with SPL. The reason why SPL is more likely to be associated with right hemisphere stroke than left hemisphere stroke remains unclear. The fact that SPLs are experienced more frequently after right-sided brain stroke is closely akin to the higher proportion of central pain after right thalamic stroke: the right hemisphere seems to have a role in monitoring somatic states and a dominant role in processing somatic representation. In a recent article reporting the findings of a functional magnetic resonance imaging study, McGonigle et al. (1) suggested that activity within areas traditionally classified as parts of the motor system (supplementary motor area) can influence the conscious perception of the body under pathological conditions. Previously, only two cases of SPLs had been reported after left-sided brain stroke. As the first report of SPLs after left-sided brain stroke accompanied by neuroimaging, this article is unique and important. Akira Yamaura Chiba, Japan 1. McGonigle DJ, Hanninen R, Salenius S, Hari R, Frackowiak RS, Frith CD: Whose arm is it anyway? An fMRI case study of supernumerary phantom limb. Brain 125:1265–1274, 2002. I n this well-documented report, the authors provide interesting information about the neuroanatomic substrate of the rare phenomenon of SPLs after right and left hemisphere stroke. Right hemisphere damage with left-side SPL is most commonly observed. In the patient reported in this article (and in two patients in the literature) with left-sided stroke and right SPL, the stroke involved the thalamus and internal capsule, and the patients also exhibited spastic paresis of the right limbs. The authors hypothesize that the experience of SPL is related to motor impairment as well as sensory loss and psychotic states caused by toxins. Robert G. Grossman Houston, Texas VOLUME 54 | NUMBER 1 | JANUARY 2004 | 231