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Drug-Induced Stuttering: Occurrence and Possible Pathways

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Official websites use. Share sensitive information only on official, secure websites. This article was submitted to Psychopharmacology, a section of the journal Frontiers in Psychiatry. The use, distribution or reproduction in other forums is permitted, provided the original author s and the copyright owner s are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Background: Stuttering is a well-known condition that affects mainly children. Often, they recover as they get older. However, a drug-induced form of stuttering may occur at any age. The aim of the present study was to detect drugs that have been associated with stuttering and discuss the mechanisms involved. Method: A descriptive study based on reports submitted to the global pharmacovigilance database VigiBase of the WHO was conducted. Results: A total of 3, reports of dysphemia were retrieved from VigiBase. These reports were contributed by 51 countries. Antiepileptics, antidepressants, immunosuppressants, antipsychotics, and centrally acting sympathomimetics were among the most frequently implicated drugs. Conclusion: A wide variety of drugs has been linked to the occurrence or recurrence of stuttering. Several mechanisms, such as increased dopamine levels, reduction of GABA, anticholinergic properties of drugs, or changes in serotonin levels, have been associated with the development of drug-induced stuttering. Paradoxically, agents known to reduce stuttering in some people may induce it in others. Keywords: stuttering, adverse drug reaction, antiepileptics, antipsychotics, antidepressants, dopamine, serotonin. Stuttering is defined as a disturbance in the normal fluency and time patterning of speech characterized by repetition of sounds, syllables, or words; prolongation of sounds; and interruptions in speech known as block s 1. Developmental stuttering is the most common form and usually has a gradual onset. It occurs most often in children between the ages of 2 and 6 years, when children are developing their language skills. Contrary to this developmental stuttering, another form, i. A sub-form of this, e. Stuttering has also been described as an adverse drug reaction ADR associated with a variety of drugs. Whether it pertains to recurrence of developmental stuttering in the past or a de novo form is not always known. In the literature, drug-induced stuttering has been associated with several drugs such as antiepileptics, antidepressants, antipsychotics, and methylphenidate 2 — 4. Evidence that several drugs may induce stuttering in humans is based on case series limited in size. The aim of the present study was to detect drugs that have been associated with stuttering be it newly occurring or a recurrence of recovered developmental stuttering by conducting a descriptive study based on reports submitted to the global pharmacovigilance database VigiBase of the WHO. Also, possible pathways are being discussed. This is the largest pharmacovigilance database in the world, with over 23 million reports of suspected adverse effects of medicines, submitted since by over countries 5. The dataset date was March 29, A PT is a distinct descriptor single medical concept for a symptom, sign, disease diagnosis, therapeutic indication, investigation, surgical or medical procedure, and medical social, or family history characteristic 6. In the ATC classification system, the active substances are classified in a hierarchy with five different levels. In this study, data of the fourth level therapeutical subgroup and fifth level chemical substance were used. The ROR represents the extent to which the association between the ADR and suspect drug stands out with respect to its background frequency in the database. It is the odds of a certain event occurring with your medicinal product compared to the odds of the same event occurring with all other medicinal products in the database. At least three reports have to be present in the database to compute a reliable ROR. The ROR is a measure of disproportionality, not of causality. It is important to note that the information in VigiBase originates from multiple sources different types of reporters and different countries , and the amount of information given as well as the likelihood that a drug caused the ADR may vary from case to case. In total, 3, reports of dysphemia were retrieved from VigiBase, dating from June 30, , to March 29, The mean reported age was 39 years median age 42 years. We found a significant disproportionality between drug use and stuttering for drugs at the fifth ATC level, the chemical substance. The top 20 drugs associated with dysphemia, ranked according to highest disproportionality in VigiBase, are shown in Table 1. A high disproportionality reported in Table 1 is not necessarily related to a high number of reports of dysphemia in the database. Table 2 shows the top 20 drugs associated with dysphemia, ranked according to the highest number of reports. In Table 3 , the top 10 ranking for highest number of reports is shown on the level of the chemical subgroup the fourth level. Top 10 drug groups at the fourth ATC level ranked according to the highest number of reports in VigiBase. In the top 20 drug-stuttering associations with the highest disproportionality Table 1 , five psychostimulants used for attention deficit hyperactivity disorder ADHD are present: dexmethylphenidate, lisdexamfetamine, dexamfetamine, atomoxetine, and methylphenidate. Furthermore, antiepileptics are frequently occurring in this top tiagabine, topiramate, brivaracetam, pregabalin, and gabapentin. The unexpected high ROR of natalizumab, fingolimod, as well as interferon beta-1a may relate to the here not further explored application in multiple sclerosis, a cerebral inflammation. Controlled studies of drug-induced stuttering are not available, and only case reports sometimes of larger size have been reported. When analyzing this dataset, searching for the PT dysphemia, one is struck with the variety of drugs reported to induce stuttering. Antiepileptics, antidepressants, immunosuppressants, antipsychotics, and centrally acting sympathomimetics are among the most frequently implicated drugs. In the literature, drug-induced stuttering is reported as an ADR as a result of a change in the use of drugs of a patient. Stuttering as an ADR of medication is expected to show characteristics of the acquired type 7. Several drug classes are associated with the development of stuttering, mostly antidepressants, antiepileptics, and antipsychotics. A study by Bar et al. In six of the seven patients, this recovered rapidly after drug withdrawal within 2—4 days. One patient had a medical history of stuttering. The other patients had no medical history of speech problems. Paradoxically, for olanzapine, also positive effects on stuttering have been reported. In a study of 23 patients, olanzapine proved to be better than placebo at reducing symptoms of stuttering Alaghband-Rad et al. Mancano 12 describes a case of pregabalin an antiepileptic interfering in the GABA pathway as well -induced stuttering in a year-old woman. Atay et al. Yadav 14 also describes a patient who began to stutter after taking risperidone. In this case, there was a clear dose-dependent effect of risperidone on stuttering. That risperidone causes stuttering is paradoxical, as risperidone is also used in the treatment of stuttering 15 , Furthermore, bupropion 7 , lithium 17 , and sertraline 18 — 20 have also been linked to the re occurrence of stuttering. Moreover, the antimuscarinic properties of tricyclic antidepressants TCAs have been related to provoking or aggravating stuttering 4. Hays 21 reported an increase in speech disorders in depressed patients who stuttered and were treated with TCAs. Based on this observation, he set up a study into the effect of bethanechol a cholinergic substance in two bipolar patients. Their speech became more fluent with the use of bethanechol. Kampman et al. Speech and language disorders are common in children with ADHD. Five drugs in the top 20 drug—stuttering associations with the highest disproportionality in VigiBase are drugs prescribed for the treatment of ADHD Table 1. The paradoxical usage of the very same drug methylphenidate acting via the dopamine pathway in experimental treatment of stuttering 25 is dealt with below. In the general population of developmental stutterers, men appear to stutter more frequently than women. This may indicate that most cases of drug-induced stuttering indeed are of the acquired type—in contrast to developmental stuttering, where a strong male predominance is found 1. Several mechanisms have been associated with the development of drug-induced stuttering. Increased dopamine levels, reduction of GABA, anticholinergic properties of drugs, or changes in serotonin levels are factors that may contribute to the development of stuttering. Because some studies found that stuttering symptoms can be reduced by dopamine antagonists \[e. A hyperdopaminergic state was observed in stuttering patients in the medial prefrontal cortex, ventral limbic cortical regions, subcortical regions, and temporal cortical regions including the auditory cortex As the medial prefrontal cortex is functionally connected to the supplementary motor area, which plays an important role in speech motor control circuits, some researchers have proposed a dopamine excess hypothesis of stuttering 10 , 27 — According to this hypothesis, stuttering is related to abnormal elevations of cerebral dopamine activity. However, further research on the anatomical and functional changes in the dopaminergic pathways in stuttering patients is needed However, this notion is not without controversy, as these effects by dopamine antagonistic antipsychotics might also be mediated by anticholinergic properties of antipsychotics 4. It was observed that antipsychotics can provoke and suppress stuttering. Relevant aspect in this paradoxical effect of the dopamine pathway in stuttering is the inverted U-shaped effect of dopamine in cognitive control, described by Cools and D'Esposito 31 in Optimum dopamine levels for cognitive functions vary within people as well as within tasks, and manipulating dopamine may have therefore paradoxical effects in different processes. This then may underlie the challenges seen in experimental therapeutical approaches the balance between effects and side effects is not easily met and may explain the abovementioned paradoxes in provoking or suppressing stuttering with the very same drugs, for instance, methylphenidate. Quite a lot of reports involved selective serotonin reuptake inhibitors SSRIs as suspect drugs. This suggests that serotonergic mechanisms might play a role. Also, akathisia is commonly present in cases of drug-induced stuttering. The SSRIs are more prone to produce akathisia than most other antidepressants 4. Serotonin might bring about akathisia by the inhibition of dopamine pathways in the nigrostriatal. A similar mechanism may be operating in serotonin-induced stuttering 4. Stuttering is a rare side effect of theophylline therapy, what may also give insight into the mechanisms involved in stuttering. Theophylline-induced stuttering is hypothesized to involve the disruption of the optimal balance between excitatory and inhibitory neurotransmission throughout the brain by inhibiting GABA receptors. This may lead to hyperexcitation of the motor cortex that may mimic the motor cortex hyperexcitability that exists in developmental stuttering Market et al. Within that total number, drug-induced stuttering was found in 6. Generally, one would try to remove or adjust the putative causal drug. Therapy remains a process of trial and error. This is a study of drug-induced stuttering, searching for the effect of the totality of drugs, as reported in the worldwide VigiBase. These results are very similar but not totally identical, possibly caused by a slightly different search strategy. This is the case when the number of reports for the association is low. Therefore, it is important to keep in mind that the ROR is a measure of disproportionality, not of causality. Acquired stuttering can be hard to distinguish from related speech and language disorders, such as dysarthria 8. This may result in misclassification when coding these speech disorders for inclusion in the database. No distinction between the development of stuttering and aggravation of stuttering could be made based on the coded information on the reports, since there are no separate MedDRA terms to code this. Furthermore, in-depth information as reported in the narrative was not available to the authors. Another limitation is the lack of information on many of the reports in VigiBase. Missing data means that it may be difficult to make a clinical judgment regarding case relevance Obviously, these VigiBase data cannot be used to give an indication as to the frequency of side effects here stuttering in relation with the drugs used. Usually, such quantitative relationships are being found in prospective studies or controlled clinical studies. Based on a search via the international pharmacovigilance database VigiBase, a wide variety of drugs have been linked to the occurrence or recurrence of stuttering. Case reports were discussed, taking into account the mechanisms of the pharmacologic agents being used. Different neurotransmitter systems seem to play a role in the development of stuttering. Examples pertaining to some of the drugs mentioned in the tables are quoted here: duloxetine 35 , pregabalin 36 , methylphenidate and amphetamine 37 , and bupropion These data are discussed, taking into account both qualitative and quantitative aspects of neurotransmitters and interfering substances. The inverted U-shaped effect of dopamine in cognitive control, described by Cools and D'Esposito 31 in , may be crucial in this paradoxical effect. These adverse drug reactions mostly seen in psychopharmacotherapy may help to study the pharmacological pathways of normal speech as well as of stuttering. Increased knowledge in these pathways seems to be required before devising productive pharmacological interference with stuttering. The VigiBase datasets generated and analysed during the current study are not publicly available due to agreements between contributors of data to the database used VigiBase and the custodian of this database. CE and FH organized the database. All authors contributed to the manuscript revision, read, and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. Lucie Gattepaille is kindly acknowledged for her contribution to the data extraction. Thea Heeren is kindly acknowledged for her stimulating discussion. This section collects any data citations, data availability statements, or supplementary materials included in this article. As a library, NLM provides access to scientific literature. Front Psychiatry. Find articles by Corine Ekhart. Find articles by Florence van Hunsel. Find articles by Peter van Harten. Find articles by Jeanette van Baarsen. Find articles by Tan Yingying. Find articles by Bert Bast. Received Apr 8; Accepted Jul 16; Collection date Open in a new tab. Drug Number of reports Other antiepileptics Selective immunosuppressants Other antidepressants Diazepines, oxazepines, thiazepines, and oxepines Selective serotonin reuptake inhibitors Interferons Centrally acting sympathomimetics Tumor necrosis factor alpha inhibitors Other antipsychotics Other immunosuppressants ATC, anatomical therapeutic chemical. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel. Diazepines, oxazepines, thiazepines, and oxepines.

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