Catatonia: A Narrative Review

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1 Catatonia: A Narrative Review Central Nervous System Agents in Medicinal Chemistry, 2011, 11, Michele Fornaro* Department of Neurosciences, Section of Psychiatry, University of Genova, Genova, Italy Abstract: Catatonic syndromes involve a complex mixture of motor, behavioral, and systemic manifestations that are derived from unclear mechanisms. What is clear is that neurotransmitters, such as dopamine (DA), gamma-aminobutyric acid (GABA), and glutamate (GLU), are of major importance in the pathogenesis of catatonia and Neuroleptic Malignant Syndrome (NMS) and that serotonin (5-hydroxytryptamine [5-HT]) is crucial to the development of Serotonin Syndrome (SS). As medications with potent effects on modulation of monoamines proliferate, the diagnosis and management of these complex disorders become even more important. Without question, these syndromes have signs, symptoms and treatments that overlap, thus, considering the symptomatological load and the associated clinical burden (including potentially life-threatening conditions), the need for a better knowledge of the hypothesized biological mechanisms and pharmacological management is imperative. Although the search for a unique, conclusive approach to the management of catatonia is futile, stating the heterogeneity of the clinical pictures and the wide range of effective treatment choices (including non-pharmacological interventions), clinicians should not disregard an accurate, critical therapeutic approach to such a relevant, yet often disregarded, topic. The aim of this narrative review is to provide both clinicians and pharmacologists with a narrative, panoramic review on catatonia and associated clinical pictures, focusing on its general pharmacological management. Keywords: Catatonia, neuroleptic malignant syndrome (NMS), serotonin syndrome (SS). 1. INTRODUCTION AND HISTORICAL BACK- GROUND Catatonias, including Catatonic Syndrome (CS), Neuroleptic Malignant Syndrome (NMS) and Serotonin Syndrome (SS) are severe neuropsychiatric conditions due to a complex mixture of motor, behavioral and systemic manifestations from unclear mechanisms [1]. Nonetheless, despite their clinical heterogeneity, these syndromes have signs and symptoms that overlap, with same neurotransmitters being involved. Among others, Dopamine (DA), gammaaminobutyric acid (GABA) and glutamate (GLU) play a major role in CS and NMS, while Serotonin (5-hydroxytryptamine, 5-HT) is essential to the genesis of SS [2]. Catatonia may be due to different causes, including structural brain diseases (e.g. epilepsy, toxic, metabolic or infectious diseases), systemic disorders involving the brain and psychiatric disorders including both schizophrenic and affective psychoses [3]. Although the concept of catatonic features was already familial since many centuries, across different cultures Figs. (1a and 1b), the first clinical accurate description dates back just to 1847, when Karl Kahlbaum (Driesen Görlitz 1899) first used the term catatonia, from the ancient Greek katateinein (to stretch tight) to describe an illness characterized by 4 phases according to the contemporary Neumann vision (1849) of Unitary psychosis : a short stage of immobility with waxy flexibility and posturing, a second *Address correspondence to this author at the Largo R. Benzi n.16, Ospedale San Martino, Clinica Psichiatrica Universitaria, Genova, ZIP 16132, Italy; Tel: ; Fax: ; stage of stupor or melancholy, a third stage of mania with pressure to speech and hyperactivity, and, after repetitive cycles of stupor and excitement, a final stage of dementia [4]. Remarkably, the course of illness was episodic and progressively more severe (as for the actual conceptualization of affective and anxious disorders) rather than chronicprocessual (usually associated to worsen outcome, as schizophrenia is generally considered). Frequently associated to catatonic pictures, the term catalepsy, from ancient Greek catalepsis ( interruption, stop ) indicated a condition characterized by rigidity and hypoesthesia, sometime referred to with the Latin flexibilitas cerea to indicate a possibility to induce the patient to acquire discomfort positions even for a long period of time, in the presence of a plastic muscular tone. Catalepsy may also be frequently associated to severe pictures of schizophrenia, psycho-organic syndromes (e.g. Parkinson s disease or epilepsy) or severe anxious states/emotive shocks - as the patient would be petrified from shock or scared tiff [5]. Kahlbaum also introduced the German terms spannungsirrsein (catatonia) or katatonische verrucktheit (catatonic insanity) in a short monography about 21 patients ( Die klinisch-diagnostischen Gesichtspunkte der Psychopathologie ) referring to a mental disorder, thus an organic disorder, including all the psychoses with prominent psychomotor symptomatology characterized by prominent dystonia, tension and choreic-like movements. Kahlbaum was also among the firsts at using a the Sydenham symptom based approach to diagnoses disorders without a known etiopathogenesis and distinguished catatonia in three forms according to severity: mitis, gravis and protracta [4] /11 $ Bentham Science Publishers Ltd.

2 74 Central Nervous System Agents in Medicinal Chemistry, 2011, Vol. 11, No. 1 Michele Fornaro Fig. (1a and 1b). Examples of catalepsy from ancient Western cultures: the biblical depiction of Lot s wife becoming a pillar of salt as punishment for witnessing the terrifying destruction of Sodom and Gomorrah ( Lot and His Daughters - Albrecht Durer, oil on canvas, National Gallery of Art, Washington, USA) and the fearsome power of the Gorgon sisters in ancient Greek mythology to turn victims to stone ( Head of Gorgon, plate in golden bronze of the II century A.D., coming from the traian Dacia, modern Romania). Kraepelin (Neustrelitz, Meclemburgh 1856 Munich 1926), who was influenced by Kahlbaum, included catatonia into the group of deteriorating psychotic disorders named dementia praecox in 1893 [6]. Kraepelin used longitudinal approach as Kahlbaum already, yet he noted differences between catatonia associated to mood disorders and the one linked to chronic psychosis. Both symptoms, course and prognosis significantly differed. Remarkably, Kraepelin also refused the concept of melancholia attonita and catatonia gravis which is called delirious melancholia and associated to mixed manic-depressive states. Indeed, Kraepelin considered early-onset catatonia as nosologic entity on its own, dementia praecox, and the fact that he didn t evaluate older patient (which were followed in the same, today Estonian, unit by Alois Alzheimer), possibly lead to under evaluation of catatonia protracta, which might had been the most investigated by Kahlbaum. Again, different patients might had different catatonias. Eugen Bleuler (Zurich, ) in 1911 adopted Kraepelin view that catatonia was subsumed under severe idiopathic deteriorating psychoses, which he renamed schizophrenias, considering both motor and behavioral symptoms essential. Nonetheless, Bleuler didn t consider catatonic symptoms related each other nor to other psychotic symptoms. The symptomatological interpretation of catatonic symptoms was on a psychoanalytic basis, in the view of subconsciuos Freudian conflicts, although Bleuler didn t completely refuse the biological hypothesis of catatonia by Wernike (1900) and Kleist (1912). Kraepelin and Bleuler both belived that catatonic symptoms could emerge as part of mood disorders (either mania or depression) Fig. (2) or could result from neurologic, toxicmetabolic or infectious diseases. These states were considered phenomenically indistinguishable from primary psychogenic catatonias. Fig. (2). The Kahlbaum observation of cyclic occurrence of waxy posturing/melancholy and mania influenced most of his European contemporaries: The catatonic and the manic, allegoric statues at the Department of Neurology, University of Bologna, Italy. Nevertheless, catatonia was strongly associated to schizophrenia until the 1990s, when the work of Fink and Taylor [7] contributed to the inclusion of new criteria for mood disorders Fig. (3) with catatonic features (and for catatonic disorders due to general medical conditions) in addition to the catatonic type of schizophrenia proposed by the Diagnostic and Statistical Manual for Mental Disorders, Fourth Edition (DSM-IV) [8], waiting for future revisions in the next edition of the Manual, DSM-V, which anticipated release is June 2012 [9]. 2. CLINICAL FEAUTERS AND ASSESSMENT The clinical presentation of catatonias may sensibly vary depending of the phase of illness and predominant etiopathology. Also, signs and symptoms associated to catatonias

3 Catatonia: A Narrative Review Central Nervous System Agents in Medicinal Chemistry, 2011, Vol. 11, No may appear to have opposite polarity in the same patient at different times as the items outlined by the Bush-Francis Catatonia Rating Scale (BFCRS) indicate [10] (Table 1). Fig. (3). DSM-IV-TR criteria for a mood disorder with catatonic features. Also, the rate of catatonia in general psychiatric population varies according to study design and research criteria. Yet, catatonia is present in about 10% of acutely ill psychiatry patients, only a minority of whom have schizophrenia, thus requiring also different treatments [11] Research Directions Although no test can confirm the diagnosis of catatonia, accurate personal and familial history taking as well as some procedures (e.g. electroencephalogram [EEG], neuroimaging of the brain, optokinetic and caloring testing) may help identify the etiology [12-14]. Research on regional cerebral blood flow has shown basal ganglia asymmetry (with left-sided hyper-perfusion), hypo-perfusion in the left medial temporal area and decreased perfusion in the right parietal cortex [15]. During work memory tasks and with emotional-memory activation, the orbitofrontal cortex appears to be altered in several cases studied with functional magnetic resonance (fmri) [14]. Yet, again, there are several subtypes of catatonias which may lead to different clinical presentation and eventually account to a high number of false positive results in neuroimaging studies due to the heterogeneity of the investigated sample. Specifically, similar considerations should be taken into account for genetic studies. In fact, while genetic studies should be independent on the phase of the illness (catatonic withdrawal characterized by psychomotor hypo-activity may alternate catatonic excitement associated to hyperactivity resembling what Kraepelin called periodic catatonia ), actual diagnostic criteria may involuntary confound genetic researchers giving inhomogeneous samples (with catatonic pictures hypothetically due to different etiologies) [16]. Nonetheless, actual genetic studies pointed out a dominant gene effect in families with periodic catatonia, with more parents than siblings being afflicted [17]. The disease locus maps onto chromosome 15q15 in families with periodic catatonia [17]. However, in one family the locus was on chromosome 22q13, with WKL1 as the associated gene [18] rather than 15q14 localization [19] or 1q21 [20]. Nonetheless, genetic investigations suggested the implication of cation channel proteins found in limbic and dorsal striatum, suggesting a mesolimbic and nigrostriatal change in periodic catatonia [18] Pathophysiology and Treatment Implications Catatonia is thought to reflect a basal ganglia disruption at the thalamocortical traits (including motor circuit [rigidity], the anterior cingulate/medial orbitofrontal circuit [akinetic mutism and, perhaps, through lateral hypothalamic connections, hyperthermia and dysautonomia], and the lateral orbitofrontal circuit [imitative and repetitive behaviors]) [15, 21] Fig. (4). Such disruptions may lead to a relative state of hypodopaminergia in these circuits through reduced flow in the medial forebrain bundle and the nigrostriatal and tuberoinfundibular tracts. DA activity in the dorsal striatum and in the ventral striatum and paralimbic cortex is thus reduced eventually due to reduced GABA A inhibition of GABA B at the substantia nigra (SN) and Ventral Tegmental Area (VTA) interneurons [21]. This would lead to a dampening of DA outflow, whereas activation at GABA A through the use of agonists such as Benzodiazepines (BDZs) (e.g. lorazepam), would indirectly disinhibit DA cell activity [22-24]. Another possible site of pathophysiology involves reduced GABA A inhibition of frontal corticostriatal tracts leading to N-Methyl-D-aspartic acid (NMDA) changes in the dorsal striatum and, indirectly, in the SN and VTA, thus suggesting the use of NMDA antagonists (e.g. amantadine) [25]. Since different causes may concur to neurotransmitter alterations at the basal ganglia, thalamus, paralimbic or frontal cortices, multiple etiologies could determine similar pictures of catatonia, with treatment potentially overlap Treatment of Catatonia Since catatonia is associated to significant morbidity and mortality rates, timely diagnosis and treatment are mandatory. While an appropriate management of catatonia should be oriented to the resolution of the determining (somatic) factors, psychiatric drugs should also play a role in the acute management of associated behavioral manifestations when due to a medical illness. For example, BDZs, especially lorazepam, have proven to be effective in the treatment of catatonia, regardless of its origin and actually represents the first-line pharmacological management in most of the cases [22]. Non pharmacological interventions, especially Electroconvulsive Therapy (ECT), are even more effective than pharmacological interventions in most of catatonic cases, especially when already refractory to pharmacological interventions [26]. Among others, ECT has been used for catatonia associated to lupus [27], Lyell syndrome [28] and encephalitis [29] as well psychiatric disorders as Gilles de la Tourette [30] or autism [31]. Non BDZs may also play a role in the management of catatonia as this seems to be the case of intravenous (IV) amobarbital, a barbiturate derivate, although their effect appears to be just transient [32]. Concerning first generations neuroleptics, they have been frequently used for catatonia although they could also worsen the clinical picture and precipitate the catatonic reactions associated to the Neuroleptic Malignant Syndrome (NMS) [33]. In fact, while higher doses of antipsychotics may reduce the eventual psychotic symptoms, they may worsen malignant catatonia and increase mortality rates

4 76 Central Nervous System Agents in Medicinal Chemistry, 2011, Vol. 11, No. 1 Michele Fornaro Dorsolateral prefrontal cortex, Anterior cingulate/medial orbitofrontal: akinetic mutism and dysautonomia. Lateral orbitofrontal cortex: imitative and repetitive behaviors. Supplementary motor/posterior parietal cortex: rigidity, initiation and termination of movements. Striatum: striatal regions support movement selection, preparation and execution/planning. Ventral Tegmental Area (VTA): this area contributes (also) in regulation of affect, goal directed thinking and positive reinforcement (reward). Substantia Nigra (SN): this region is also involved in movement initiation and regulation. Fig. (4). Basal ganglia thalamocortical putative circuits and catatonia. Red arrows refer to the striatum or substantia negra and ventral tegmental area while blue arrows refer to cortical structures. GABA, GLU and DA play major roles at these regions and are the candidate targets of most drugs used for CS, including Benzodiazepines - BDZs (e.g. lorazepam) cortex/mesocorticolimbic terminal zones; GABA-ergic (too)/nmda blockers (e.g. memantine and amantadine) striatum; GABA A and DA modulators (e.g. valproate and other antiepileptics, lorazepam or even amantadine, bromocriptine and levodopa) SN/VTA. (78% vs. 60%) as observed by Mann and colleagues [34]. Attentive case-by-case evaluation should be made even for the prescription of newer, second generations antipsychotics in course of catatonia. In fact, while there are indications that atypical antipsychotics may be useful in non-malignant catatonia, reducing the risk for Extrapyramidal Syndromes (EPS) and enhancing certain brain functions, Randomized Controlled Trials (RCTs) are lacking, and caution advisable since cases of NMS have been linked to the treatment with second generation antipsychotics [35]. Generally speaking, the prescription of atypical antipsychotics may be preferred for those patients having an history of affective disorders associated to non-malignant catatonic features ( periodic catatonia ) [36]. Apart from the acute management, which may also require administration of myorelaxant drugs as sodic dantrolene or calcium channel-blockers [37], some periodic catatonic cases may also benefit from lithium preventive therapy [38] although it may could also precipitate it when at toxic levels [39]. Carbamazepine, valproic acid, anticholinergics, thyroid medications, stimulants and corticosteroids have each anecdotally been reported to be effective in some catatonic cases [11]. As general pharmacological indication, BDZ (e.g. lorazepam) still constitute the most effective, yet substantially safe, drug management for most acute phases of catatonic states, with longer half-life agents generally preferred to short ones. Specifically, a switch from IV administration of lorazepam to oral or nasogastric administrations (in a daily dose of 6-20 mg) [40], diazepam (10-50 mg/day) [41] or clonazepam (1 to 5 mg/day) [42] usually maintains the therapeutic effect; if lorazepam is ineffective, ECT should be considered [26]. Two or three ECT applications are usually effective to lyse the catatonic state in routine cases, though four to six treatments are advised for recurrence prevention and ten to twenty administrations could be needed in some resistant cases [43]. While long-term prognosis is good in almost half of the catatonic cases, especially those related to personal or familial history for affective disorders, neuromedical catatonias tend to have higher mortality rates [44]; thus, whatever the choice of the (integrative too) treatment intervention, it should be quick. 3. CATONIC-RELATED SYNDROMES Neuroleptic Malignant Syndrome (NMS) and Serotonin Syndrome (SS) are two forms of catatonia with a psychiatric iatrogenic etiology. NMS is a form of malignant catatonia a rare condition that develops quickly and fulminantly and is fatal within a few days if untreated, thought to be due to a

5 Catatonia: A Narrative Review Central Nervous System Agents in Medicinal Chemistry, 2011, Vol. 11, No Table. 1. According to the 23-Item Bush-Francis Catatonia Rating Scale (BFCRS), here Partially Modified and Partially Reported, the Severity of Catatonia is Assessed Through 23 Signs on a 0-3 Continuum for Each Sign. The first 14 Signs Combine to Form the Bush-Francis Catatonia Screening Instrument (BFCSI), which Only Measures the Presence or Absence of the First 14 Signs, and is Used for Case Detection. Item Definitions on the Two Scale are Equal. Note that Most of the Sign May have Opposite Polarity 1) Excitement Extreme hyperactivity and constant motor unrest, which is apparently non purposeful. 2) Immobility and stupor Extreme hypoactivity, immobility or minimal response to stimuli. 3) Mutism Verbal non responsiveness or minial responsiveness. 4) Staring Fixed gaze, little or no visual scanning of environment and decreased blinking. 5) Posturing/.catalepsy Spontaneous maintenance of posture(s). 6) Grimacing Maintenance of odd facial expressions. 7) Eschopraxia/echolalia Mimiking of an examiner s movements/speech 8) Stereotype Repetitive, non goal directed, motor activity. 9) Mannerism Odd, purposeful movements. 10) Verbigerations Repetition of phrases (like a scratched record). 11) Rigidity Maintenance of a rigid position despite efforts to be moved. Excled if cogwheel or tremor is present. 12) Negativism Motiveless resistance to instructions. Contrant behavior (one does the exact opposite of the instruction). 13) Waxy flexibility During reposturing of the patient, he offers initial resistance before allowing repositioning. 14) Withdrawal Refusal to eat, drink or make eye contact. 15) Impulsivity Sudden inappropriate behavior without provocation. 16) Automatic obidience Exaggered cooperation with the examiner request of spontaneous continuation of the requested movement. 17) Mitgehen Anglepoise lamp arm raising in response to light pressure of finger despite opposite instruction. 18) Gegenhalten Resistance to passive movement proportional to the strength of the stimulus. 19) Ambitendency The appearance to be stuck in indecisive hesitant movement. 20) Grasp reflex Per neurologic examination. 21) Perseveration Repeatedly returns to the same topic or persistence of movement. 22) Combativeness Usually aggressive in an undirected manne, with no or just partial explanation afterward. 23) Autonomic abnormal Abnormal temperature, blood pressure, pulse or respiratory rate and diaphoresis. severely decreased central dopaminergic activity due to a toxic-pharmacologic or idiopathic origin [45]. SS is also a potentially life-threatening condition which also characterizes for a iatrogenic origin (usually very high doses of serotonergic drugs) and for neurovegetative impairments [46] Neuroleptic Malignant Syndrome Estimated of NMS have varied widely depending on the diagnostic criteria, population susceptibility and prescribing habits, with prevalence rates ranging between 0.02 to 3% [47, 48]. While NMS could occur in association to any disorder treated with neuroleptics, a history of catatonia, schizophrenia, EPS susceptibility, mood disorders especially postpartum depression [49] -, organic disorders, organic brain disorders, alcoholism or substance abuse disorder, as well male gender (but not ethnicity of sociodemographic factors) may increase the risk for development of the syndrome [50, 51]. The period of withdrawal from alcohol or sedative hypnotics may increase the risk for NMS due to aberrant thermoregulation and autonomic dysfunction. Agitation, dehydration and exhaustion may also increase the risk for NMS. Basal ganglia disorders (e.g. Parkinson s disease, Wilson s disease, Huntington s disease and Tardive Dystonia [TD]) further increase the risk for NMS [52]. Low serum iron in course of catatonia appears to be a statespecific finding predicting increased risk for NMS when neuroleptic medications are prescribed [53]. Remarkably, while higher potency D2 DA-ergic blockers may be at higher risk for induction of NMS vs. atypical antipsychotics (especially clozapine), these latter have also been associated to NMS [54], as well sudden withdraw form anti-parkinson medications or lorazepam in vulnerable subjects [55]. While catatonia may manifest with a constellation of symptoms, and these latter could even acquire opposite

6 78 Central Nervous System Agents in Medicinal Chemistry, 2011, Vol. 11, No. 1 Michele Fornaro trends within different phases of illness, NMS clinical pictures are usually more characterized. NMS is usually associated to prominent autonomic dysfunctions, including tachycardia, hyperthermia, elevate blood pressure and also rigidity, mutism and stupor and creatine phosphokinase (CPK) elevation with risk for myoglobinuric renal failure [56]. Specifically, hyperthermia is reported in 98% of the cases is usually life-threatening [57]. Emergency treatment of NMS require sudden withdraw of antipsychotics harmful medications and introduction of DA-agonists as bromocriptine [58], dantrolene [59] and lifesupportive therapy prior evaluation of lorazepam and/or ECT [60] Serotonin Syndrome SS has been associated to hyper-dose of serotonergic medications, including, among others, toxic doses of Tricyclic, Selective Serotonin Reuptake Inhibitors (SSRIs) of other serotonergic drugs. Nonetheless, most of SS cases (actual prevalence rates are imprecise) are due to hazardous (or accidental) association of Monoaminoxidase Inhibitors (MAOIs) and serotonergic medications, with subsequent Central Nervous System (CNS) Serotonin (5-HT) hypertone and potentially fatal consequences [61]. Signs of SS include confusion, anxiety, irritability, euphoria and dysphoria, gastrointestinal symptoms (e.g. nausea, vomiting, diarrhea and incontinence), behavioral manifestations (e.g. restlessness and agitation) and neurological findings (e.g. ataxia or incoordination, tremor, myoclonus, hyperreflexia ankle clonus and muscle rigidity) as well nervous autonomic abnormalities (e.g. hyper- or hypotension, tachycardia, diaphoresis, shivering sialorrhea, mydriasis tachypnea or hyperthermia) [62, 63]. Treatment of SS generally require sudden withdraw of offending medication, life-supportive interventions for respiratory and cardiovascular system, hydration to prevent renal failure and use of BDZs for management of agitation [64]. Specific 5-HT receptor antagonists as ciproheptadine (a 5- HT2A blocker antihistaminic) and mirtazapine (5-HT3 and 5-HT2 antagonist, Noradrenergic and specific serotonergic antidepressant [NaSSA]) have also been proposed for SS [62] although being not a firs line choice. 4. SUMMING UP From a clinical perspective, it should be bared in mind that search for a unique (pharmacological or nonpharmacological) treatment for catatonias is futile. This is essentially due to different etiologies which may lead to heterogeneous clinical presentations. On the contrary, when different etiologies are supposed to give similar clinical pictures, no matter about the hypothesized origin of catatonia, at least not in an acute setting. In fact, as for many of actual psychiatric disorders, actual nosologic boundaries due to a categorical classification proposed by DSM-IV reduce the chance of a dimensional therapeutic approach, which on turn appears to be pivotal for the management of catatonia. Thus, from a clinical perspective, the choice of the appropriate treatment, especially for drug agents, should not leave apart an accurate anamnesis of personal and familial clinical history. Patients with affective disorders, especially (soft) bipolar hints [65], may benefit from ECT, GABA-ergic antiepileptics and perhaps lithium or atypical antipsychotics, while patients with prominent Anxiety disorders (e.g. very severe Obsessive-Compulsive Disorder [OCD], Post-Traumatic Stress Disorder [PTDS]) may preferentially respond to high doses of BDZs and/or even high doses of TCAs as clomipramine. Conversely, schizophrenic patients or patients with prominent psychotic features or severe cognitive impairment may require ECT and/or neuroleptics. Nonetheless, these directions should be considered merely indicative: most patients have comorbid features and mixed states [66], thus at least for the acute phase, treatment of catatonias should be focused on the sudden resolution of the hypothesized harmful etiopathology rather than recovery from what remains a puzzling home of its own of clinical psychiatry [67]. ACKNOWLEDGEMENTS The author has no acknowledgement to state. REFERENCES [1] Conti, N. A. From alienation to mental illnesses in Germany: Karl Kahlbaum and his thought of change. Vertex, 2008, 19(80), [2] Carroll, B. T.; Ramirez, J.; Faiz, K.; Kirkhart, R.; Thomas, C. Regarding catatonia. Psychiatry (Edgmont), 2007, 4(5), [3] Kay, S.R.; Kanofsky, D.; Lindenmayer, J.P.; Opler, L.A. The changing presentation of catatonia. Am. J. Psychiatry, 1987, 144 (6), [4] Morrison, J.R. 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