Introduction

Deglutition is essential for natural nourishment. Dysphagia and difficulty in swallowing are frequent symptoms found in clinical practice. Practitioners often struggle in identifying its etiopathological genesis as it can be the expression of a large number of different nosographic categories. Basic aetiology of dysphagia may be simplified as mechanical/obstructive or neurological/muscular and prevalence varies in different age groups. Furthermore, it could be classified based on the location of oral/pharyngeal or oesophageal phase impairment [1]. Identifying functional origin of swallowing disorders seems to be one of the most difficult challenges, frequently leading to invasive and as expensive as unnecessary diagnostic procedures involving many different consultants.

There seems to be a mutual relationship between dysphagia and psychiatric disorders. Many different organic diseases can certainly cause swallowing impairment, but it must be considered that it can also be worsened by psychiatric comorbidities, like affective or anxious disorders, which in turn negatively influence outcomes and prognosis. Finally, these kinds of symptoms can also be exclusively expressions of various psychiatric disorders which can be distinguished one from another in relation to different psychopathological processes at the origin. Even though this distinction can look sophisticated and specific, it can be useful to recognize focal points to plan an adequate treatment and obtain resolution or significative reduction of symptoms. Research in this area is limited and heterogeneous and the link between these distinct components is far from being clear [2]. It is likely that alterations of some neuronal circuits in common (cingulate cortex, amygdala, basal ganglia) could lead to both psychopathological and functional symptomatic expressions. Data emerging from the literature show that affective symptoms are very frequent in patients suffering from dysphagia [3,4,5,6,7]. Within this framework, it is also possible that the individual’s affective state could amplify his own perceptions, contributing to a wrong cognitive experience of the swallowing act.

In this review, we would like to reappraise and discuss the relationship between dysphagia and psychopathology, trying to provide a useful overview for specialists in different disciplines. Since specific guidelines are lacking, deeper knowledge of the topic can help practitioners disentangle complex pathological manifestations.

Methods

In this systematic review, the authors undertake a thorough analysis of recent literature on the topic. The PubMed and Psycharticles electronic databases were searched for literature published until December 2020, to comprehensively identify the most relevant publications available on dysphagia in eating disorders, according to the PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analysis) method [8]. Sequential combinations of the search terms “dysphagia OR swallowing disorder” and “anorexia nervosa”, “eating disorders” “avoidant/restrictive food intake disorder”, “bulimia nervosa”, “binge eating disorder”, “pica”, “rumination disorder” were used. Research articles, either theoretical or empirical-based, published in peer-reviewed journals and in English language, were included. Case reports were also considered in the analysis when it was appropriate for completeness purposes. Finally, the most relevant references were examined to obtain further important publications that may supplement the discussion. In total 260 studies were identified and 206 were screened after the removal of duplicates. The majority (167) were excluded bond on relevance or abstract or title content. Forty studies were finally included. No exclusion criteria or statistical methods were applied nor was an assessment of study-level or outcome-level bias applicable for our purpose. Once systematically investigated the correlation between dysphagia and eating disorders, we summarized the relationship with other many psychiatric disorders, briefly describing their etiopathological and psychopathological features for differential diagnosis, patients’ management suggestions and treatment options (Fig. 1).

Fig. 1
figure 1

“Dysphagia and eating disorders” research flow diagram

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This review represents an effort to approach such an interdisciplinary and poorly understood topic, trying to systematize an overview of the most considerable and clinically useful information.

Discussion

Dysphagia and eating disorders

The relationship between swallowing disorders and eating disorders is only apparently straightforward. Patients who suffer from eating disorders act dysfunctional eating behaviours, like restrictive, binge eating or purging conducts, consequently to dysmorphophobia: it is the expression of a disturbance in the way in which one’s body weight or shape is experienced [9, 10]. These patients fear the consequences of nutrition, as gaining weight or changing body shape. These features are absent in avoidant restrictive food Intake disorder [11] or in selective eating often found in patients with autistic spectrum disorder [12], which must be considered as a differential diagnosis during the initial assessment.

Patients suffering from eating disorders often complain about gastrointestinal and oesophageal symptoms to justify the avoidance of food intake, leading to unnecessary invasive and expensive further investigations and interfering with rehabilitation programmes [13, 14]. According to a recent review of the literature, most gastrointestinal symptoms reported seem to meet criteria for functional disorders, while structural, immunological disorders or food intolerances showed prevalence rates comparable to general population. In the studies considered, functional oesophageal disorders, like dysphagia, functional heartburn and retrosternal pain, displayed a prevalence rate of 23–51% in patients with eating disorders [15, 16]. Correlations among these symptoms, underweight, restrictive/binging behaviours or psychological traits were not found [15,16,17]. They seem to be characterized by marked instability and high turn-over, with prevalent persistence in a 12-month follow-up [17]. Another Italian study failed in finding a correlation between the improvement of oesophageal symptoms and psychopathological distress scores after treatment [13]. Furthermore, many symptoms, included dysphagia, showed different improving responses after weight rehabilitation in various studies [13, 16]. Hence, it is still difficult to assume predictive or causal factors for functional gastrointestinal symptoms onset in eating disorders [15].

Moreover, it should be kept in mind that gastrointestinal symptoms may represent the expression of severe organic complications [14, 18]. Weight loss experienced by patients who suffer from Anorexia Nervosa (AN) could lead to severe swallowing muscle hyposthenia which may or may not be associated with chronic gastrointestinal reflux and gastrointestinal muscle atrophy caused by self-induced vomit [18]. Oropharyngeal dysphagia seems to be related to lower BMI in more compromised patients, as the result of the severe underweight status, and longer length of hospitalization [18]. In a recent case report, a case of oesophageal dysphagia due to oesophageal ulcers probably induced by autophagic mechanisms secondary to starvation and malnutrition is described [19].

Studies describing swallowing difficulties in AN with instrumental examinations are lacking. Though several alterations are found in severe stages of the disease as a likely consequence of physical decay, these seem not to be frequent in early stages, when it could be hypothesized that psychological factors play a pivotal role. Unfortunately, few studies are found, with several limitations and small sample sizes, so it is difficult to characterize the swallowing process in patients with AN [20].

Unfortunately, literature is scarce when other eating disorders are considered. Gastrointestinal symptoms are frequent in patients suffering from Bulimia Nervosa (BN) and are often misdiagnosed or misinterpreted. Only an older study carried out in 1989 considered characteristics of oral motor and swallowing function in BN, finding some abnormalities in a limited group of patients (absence of pharyngeal and velar gag reflex, inhibition of tactile pharyngeal stimulation, mucosal structural and sensitive alterations, abnormal oesophageal motor patterns) [21]. Delayed gastric emptying and impaired contractile antrum function seem to be quite frequent in BN. Their aetiology is not clear, and the literature is lacking, but some authors hypothesized muscular atrophy and electrolytes imbalance resulting from self-induced vomit as possible causes [22]. Frequent acid exposure of the upper gastrointestinal tract due to recurrent induced vomiting could lead to swallowing impairment and severe complications as oesophageal irritation, esophagitis, oesophageal strictures, Barrett’s oesophagus and adenocarcinoma [23, 24], even though the association between BM and gastroesophageal reflux is controversial [25].

Finally, it could be reasonable to consider an individualized approach to refractory symptoms in patients with eating disorders [24].

Patients diagnosed with Binge Eating Disorder (BED) could complain of upper and lower gastrointestinal symptoms. According to data resulting from a study by Cremonini et al., BED could lead to gastrointestinal morbidity. Acid reflux could be the condition underlying dysphagic symptoms, but according to available data, the relationship between gastrointestinal symptoms and BED has still to be cleared [26].

For completeness, few cases are described of sudden dysphagia developed after ingestion of foreign bodies due to Pica, a rare eating disorder consisting in eating non-nutritive or non-food substances inappropriately to developmental level or cultural believes [9] that could reveal itself as a possible consequence of iron deficiency [27, 28].

Literature offers many examples, mainly through case reports, of primary oesophageal dysmotility disorders misdiagnosed as eating disorders [29,30,31,32,33,34,35,36,37,38]. An organic condition showing significant symptomatic overlap seems to be achalasia [39]. Achalasia is a rare oesophageal motor disorder with unknown aetiology, often starting with dysphagia and many other upper gastrointestinal symptoms. It is characterized by altered oesophageal peristalsis and increased/normal resting pressure of the lower oesophageal sphincter without complete relaxation during swallowing [39]. This condition shares numerous physical, behavioural and psychological features with eating disorders, leading to delayed diagnosis and treatment [39, 40]. It should be considered primarily in case of atypical presentation of the disorder, like the absence of imperative drive to lose weight or body image distortion as well as uncontrollable vomiting (during sleep), regurgitation of non-digested food, frequent and persistent swallowing difficulties occurring after liquid intake, at night or in public, stereotyped behaviours during meals, history of aspiration pneumonia [39] or change in symptoms characteristics, frequency and severity [41, 42]. There are many case reports of patients of different ages initially diagnosed with AN and finally identified as suffering from achalasia after a specific diagnostic assessment. Oesophageal manometry represents a “gold standard” [39]. Some authors stated that eating disorders could represent a risk factor for achalasia through decreased gastric motility and myenteric plexus damage due to recurrent vomiting [41]. Differential diagnosis could be challenging, above all in prepuberal age children, always considering that a comorbidity between the two conditions could always be possible [29,30,31,32,33,34,35,36,37,38,39, 41, 43]. Only a case report was found about the misdiagnosis of juvenile Alexander Disease, a rare sporadic leukoencephalopathy that can mimic AN in the early stages [44].

Since distinguishing between the conditions described could be challenging, a standardized assessment approach could be recommended, aiming to select only the more severely ill patients that really need invasive diagnostic exams and, at the same time, to avoid a superficial management [45]. The diagnostic approach to patients with eating disorders complaining gastrointestinal symptoms should be guided primarily by clinical history (onset of symptoms, history of purging or restrictive behaviours, kind of food selected) and by the quality of symptoms, while a general screening for some disturbances, such as irritable bowel syndrome, celiac disease, food allergies or intolerances, cannot be recommended according to available current literature [16]. Only more severely ill patients should be screened for signs and symptoms of oropharyngeal dysphagia, like the incidence of previous aspiration pneumonia episodes, coughing or choking with food and liquid or complaints about difficulty in swallowing, trying to identify patients at high risk of aspiration. A speech-language pathologist evaluation could be useful and, if needed, patients could be addressed to a more in-depth examination through additional instrumental tests to detect functional or structural abnormalities in oropharyngeal or oesophageal swallowing phase. For this aim, a cluster of standardized questions could be an advantageous tool. In patients suffering from oropharyngeal dysphagia, traditional swallowing therapy may help to improve nutritional and hydration status and reduce the risk of aspiration [18, 46, 47].

Differential diagnosis

Dysphagia and anxiety disorders

Dysphagia or swallowing difficulties can be found in Post-traumatic Stress Disorder or Anxiety Disorders, such as Panic Disorder, Social Phobia or Specific Phobia. Although these symptoms are not the most frequently reported, they revealed a remarkable rate: some studies found that swallowing complaints occurred nearly in 40% of patients suffering from Panic Disorder, with little differences between females and men [48,49,50]. Anxiety or intense fear arising when the patient is exposed to the phobic object (i.e. social situation in which the subject is exposed to others’ judgment, a situation that caused vomit/suffocation) is the common element among all these psychopathological categories [51]. Some authors define this set of symptoms as “swallowing anxiety” and recognize them as a potential worsening factor, since it leads to inconsistency in drug use, negatively affecting patients’ functionality and heightening the risk of relapses [52]. The common behavioural response consists in avoiding the phobic object or situation (“phagophobia”): the subjects develop symptoms that imitate oral apraxia with intact pharyngoesophageal, neurologic functions and linguistic abilities [53, 54]. Deglutition-related traumatic experiences seem to have a correlation with phagophobia, which may also be associated to panic disorder, obsessive compulsive disorder and separation anxiety symptoms [52]. It seems also to share some characteristics and similar comorbidities with functional dysphagia, a psychologically based swallowing problem not associated with clinically relevant fear and anxiety symptoms, and globus pharyngeus [52]. Some authors found such a strong relationship between the two syndromes, that they defined them as parts of a psychopathological continuum [51]. Intensity of anxious symptoms can condition the type of food they avoid, and, in some cases, cause severe consequences on both the organic (weight loss, metabolic ad hydro-electrolytic alterations) and psychosocial side (social withdrawal, depression, anxiety and panic attacks) becoming extremely difficult to treat [7, 52, 55].

Unfortunately, this condition has not been extensively evaluated and data often is limited to case reports and affected by the heterogeneity of the definitions used. Thus, is not possible to describe a univocal evidence-based treatment strategy. Cognitive-Behavioural Therapy seems to be a common useful treatment approach. It is combined in many cases with other techniques (psychoeducation, exposure therapy, muscle relaxation, group therapy, hypnosis, Eye Movement Desensitization and Reprocessing—EMDR) and pharmacological treatment. This one seems confined to antidepressants and benzodiazepines [53].

Dysphagia and functional disorders

Functional Neurologic Disorders (DSM 5) [9] or Conversion Disorder shows a great impact on clinical practice. It consists of sensitive or motor symptoms, usually under voluntary control, that are not explained by any neurological syndrome and lead to significant impairment of individual’s global functioning. They are classified as “Somatic Symptoms and Related Disorders” and it can be specified if it shows “with swallowing symptoms” [9]. Functional dysphagia is, in the end, defined by Roma III criteria for gastroenterological functional symptoms [56]. Three symptoms during at least three of the six months preceding diagnosis must be present: feeling of difficulty in bolus pharyngo-oesophageal transit, no evidence of previous gastroesophageal reflux disease, no histopathological evidence of oesophagus motility disease. “Globus pharyngis” or “globus hystericus” is a subjective feeling of a lump or foreign body in the throat when one attempts to swallow [52]. Patients use to describe their feeling as a lump, foreign body, “ball-like”, “hair”, itching, swelling, scratching sensation in the throat and is often followed by pharyngeal irritation symptoms, like throat cleaning and chronic cough [57, 58]. Classically it improves with eating and it is not associated with odynophagia or dysphagia [59]. It seems to be related to a multifactorial aetiology and some studies found a correlation with psychological distress, especially anxiety and depression. Mostly it is a benign disorder, even though it is long-lasting, recurrent and difficult to treat. That’s why explanation and reassurance are pivotal in patients’ management. The nosographic translation from “hysteria/psychogenic disorder” (DSM, DSM II) to “functional disorder” [9] reflects the focus transition from a psychologic aetiology to a bio-psycho-social interpretation model [60,61,62], other than appearing more suitable for a medical context [63]. It is important to point out that conversion disorder should not be an exclusion diagnosis, but a result of a multidisciplinary diagnostic-therapeutic process. Patients often show high levels of frustration because specialists remain sceptical towards them and sometimes they take into account “simulation” of symptoms. Identifying this population has important implications on clinical practice, as it is one of the most frequent conditions observed by neurologists [63, 64]. This population often shows the same discomfort and subjective disability as patients who suffer from neurological diseases. Second, they present higher levels of unemployment and use more disability-related state financial benefits than neurological population [65]. They have often psychiatric comorbidities (like Anxiety Disorders, Panic Disorder, Depression, Obsessive–Compulsive Disorder, Eating Disorders, Post-traumatic Stress Disorder) that condition each other and show common risk factors (adverse experience in infancy and stressful life events, among others). There is not enough knowledge about the pathophysiological mechanisms of these functional disturbances [57]. There are not even evidence-based guidelines on this topic. Treatment should be personalized and based on a good risk–benefit assessment [66]. Primarily, specialists should recognize cases at high risk of malignancies, focusing their attention on symptoms which need further evaluation (dysphagia, odynophagia, throat pain, lateralization, weight loss), reflux symptoms or psychological distress. A clinical evaluation of the neck should follow. The use of instrumental evaluation routinely is controversial since most patients do not need further investigations. An empirical Proton-Pump Inhibitors treatment could be a useful strategy to save instrumental examinations to non-responders. In case of negative clinical investigations and persistence of bolus sensation patients could be addressed to speech therapy, cognitive–behavioural therapy or treatment with antidepressants [59]. One of the essential elements of an efficient management is the foundation of a solid therapeutic alliance, starting from an extensive anamnestic record. It may lead to a reduction of “doctor shopping” practice, costs and risks of invasive diagnostic procedures. Clinicians should guide patients to understand symptoms and, if it is not possible, to act interpersonal/behavioural strategies [67], even with the help of caregivers.

Dysphagia and psychotic disorders

Swallowing disorders are frequent in patients suffering from schizophrenia and other psychotic disorders. Since they show higher morbidity than general population and patients suffering from other psychiatric illnesses [68,69,70], at least an organic cause should be taken into consideration. Many types of dysphagia have been recognized in psychiatric patients, even though they often coexist in clinical practice, so a clear distinction might be difficult [71]. Two main aetiologic categories are found: antipsychotic treatments collateral effects (first extrapyramidal effects, even if sialorrhea and xerostomia play a significant role) and abnormal behaviours that may occur during a psychotic illness (e.g., PICA, fast-eating syndrome). Dysphagia and swallowing abnormalities can also be associated with low concentration and distractibility during meals [72]. Furthermore, in some cases, the hypothesis that dysphagic symptoms are part of a delusion of control or a somatic passivity phenomenon cannot be excluded [73]. Dysphagia could lead to malnutrition, aspiration and cause choking deaths more frequently in schizophrenia and organic psychotic illnesses, even independently to medication [74]. The fact that psychiatric patients could have low cognition of these problems and could show difficulties in expressing their distress adds more complexity to assessment and management [71]. There are no systematic studies focused on this condition, almost all publications found on the topic agreed about the necessity of a systematic approach to diagnosis through a multidimensional and multidisciplinary team to understand the nature of dysphagic symptoms in psychotic patients. The same is applied to treatment attitude, which includes adjustment of pharmacological therapy, avoiding medications that could worsen symptoms when possible, caregivers education and monitoring during meals, dietary modification, long-term speech (logopaedic) rehabilitation, screening for proper oral health to avoid edentulism [71, 75, 76]. This can lead to the development of active and passive strategies to reduce the incidence of aspiration episodes [72].

Dysphagia and psychotropic medications

A substantial number of patients suffering from dysphagia are taking psychotropic drugs according to the literature [77]; thus, it is necessary to consider the iatrogenic aetiology as a potential cause of the disorder [78]. Attention has been addressed to this theme since the second half of the last century [79] and has grown after the FDA warning published in 2005 (http://www.fda.gov/cder/drug/advisory/antipsychotics.htm) in relation to high number of patient deaths by pneumonia among those treated with neuroleptic drugs (haloperidol, chlorpromazine, perphenazine and others). In particular, elderly patients and patients with cognitive impairment seem to present the highest risk [1]. Neuroleptic drugs are not the only psychotropic category associated with risk of dysphagia: antiepileptic, anticholinergic drugs and benzodiazepines [1], which are frequently added to neuroleptic drugs in most severely ill patients [80], can also cause dysphagia adding further choking/aspiration risk, although their mechanism of action at the level of central nervous system is not clear [78]. The iatrogenic origin of dysphagia could be an effect directly derived from agents’ mechanism of action or their secondary side effect [78]. They can directly impair both deglutition phases, but also cause alterations of the state of consciousness, of the oesophageal motility and a reduction of the cough reflex probably via both sensory (afferent) and motor (efferent) components. Furthermore, side effects of antipsychotic drugs, because of their dopamine and histamine effects, such as parkinsonism, acute dystonic reactions and tardive dyskinesia, including their significant role in inducing hypersalivation, sedation and xerostomia, can lead to dysphagia episodes and severe consequences like choking and pneumonia. For an exhaustive overview of mechanisms and consequences of drug-induced dysphagia see Cicala et al. [1]. A systematic review regarding 18 studies published by Miarons Font and Rofes Salsench [77] shows that antipsychotic drugs that are associated with higher dysphagia incidence were haloperidol among first-generation antipsychotics (followed by thioridazine hydrochloride, sulpiride, chlorpromazine) and risperidone among second-generation antipsychotics (followed by clozapine, olanzapine, quetiapine). These data regarding second-generation antipsychotics suggest that dysphagia cannot be simply explained by nigrostriatal effects (extrapyramidal syndrome and tardive dyskinesia) by D2 receptors antagonism. Multiple receptor actions are probably involved: antihistaminergic (with sedation and cough reflex reduction), anticholinergic (xerostomia, impaired bolus transit), catecholaminergic (muscle tone). They all have a great impact on the first two phases of swallowing. Data from this review is discordant and heterogeneous, so more observational studies and randomized clinical trials are necessary. The authors lead to the conclusion that iatrogenic aetiology must be considered for both typical and atypical antipsychotic drugs [77]. Thus, it is particularly problematic to define a causality of drug reactions in patients at high basal risk of swallowing impairment, as elderly people with dementia or intellectual disability [1, 77]. Randomized clinical trials involving newer recently marketed antipsychotics do not include information on the prevalence of these effects, maybe because individuals involved seem to be relatively healthy [1]. Reducing or, when it is possible, discontinuing drugs with the strongest side effects, switching to a different antipsychotic with a more favourable side effects profile or adding anticholinergic drugs, depending on the situation could all be useful strategies to reduce antipsychotics’ impact on deglutition [1]. Providing an adequate caloric intake is pivotal to prevent malnutrition in patients who develop drug-induced dysphagic symptoms. A nutritionist consultation might be useful to elaborate a feeding program adequate to the type and degree of impairment and that fits the nutritional patient’s need, preventing the risk of aspiration at the same time. Nutritional parameters and weight should be regularly checked, and meals supervised. Patients showing severe tardive dyskinesia or parkinsonism should be directly and routinely asked about swallowing difficulties, to prevent late diagnosis due to their difficulty in reporting such symptoms and patient’s medication history should be evaluated to primarily determine the cause of these symptoms [81].

Conclusion

Deglutition is a complex sensorimotor behaviour and its impairment could lead to severe consequences on the organic side. Dysphagia should be a relevant concern for clinicians and should not be overlooked in patients’ assessment, considered its frequency in clinical practice and its implications in patients’ morbidity, mortality and quality of life. Not only psychologists and psychiatrists might show particular interest in this topic, but it also could be useful for all specialists outside mental health, considering the overlap between organic and psychopathologic symptomatology. It is generally difficult to identify causal or predictive factors for gastrointestinal manifestations in eating disorders; thus, studies involving imaging or instrumental examinations are lacking at any phase of the disease course. Therefore, swallowing impairment in other mental disorders is less documented, but still common (see Table 1).

Table 1 Psychiatric disorders associated with dysphagia
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Special attention should be paid to mentally ill patients, who might display complex and multiple comorbidities with additional choking risk factors such as poor eating habits, impaired dentition, comorbid neurological diseases [1], as well as consequences of abnormal eating behaviours, occasionally exacerbated by psychotropic medications. Furthermore, psychiatric comorbidity is a potential contributing factor to swallowing symptoms, which has an established negative impact on course, management and compliance to treatment of organic diseases. The literature concerning this topic is scanty, generally recent and lacking in international guidelines. Despite this, published knowledge agreed on the need of multidisciplinary management of patients displaying swallowing disorders, from the diagnostic assessment to the implementation of treatment and rehabilitation strategies.

It should be important to proceed with a detailed study of swallowing symptoms with more clinical trials, to better understand the aetiopathogenesis of functional manifestations, avoiding direct and indirect management costs, and clear the role of psychopathological manifestation as well as psychopharmacotherapy, especially in high-risk populations.

What is already known on this subject?

Dysphagia is a condition frequently detected in clinical practice, whose diagnostic assessment and treatment management often involve several consultants. Identifying the aetiology of swallowing disorders is indeed challenging, due to the complexity of potentially involved causal processes, including psychopathology. Increasing awareness on the topic might have many implications in resource management, clinical outcomes, and impact on patients’ quality of life.

What does this study add?

This review aimed at providing a systematic overview of psychopathology associated with dysphagia for all consultants, especially outside mental health. It might help enlightening some usually overlooked issues, clarifying some key points, and underlying the importance of a multidisciplinary approach finally entailing an optimization of patients’ management.

Strengths and limits

The main strength of this review is its purpose to systematize the heterogeneous and fragmented data on psychopathological implications of dysphagia, trying to provide some key points, which might be useful in clinical practice.

Some limitations are related to the heterogeneity of available data itself, mainly lacking in systematic approach or recent clinical studies. The topic is vast and research bias could not be excluded. It is hoped that further studies would help to deepen what already emerged from this review. It would be especially interesting to clarify mechanisms underlying dysphagic symptoms in eating disorders through more clinical studies involving instrumental as well as psychometric evaluations.