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Allgrove Syndrome): Improving Outcomes with a Multidisciplinary Approach Pediatric Health, Medicine and Therapeutics Dovepress open access to scientific and medical research Open Access Full Text Article REVIEW Triple A syndrome (Allgrove syndrome): improving outcomes with a multidisciplinary approach This article was published in the following Dove Press journal: Pediatric Health, Medicine and Therapeutics Myrto Eleni Flokas Abstract: Allgrove syndrome or triple A (3A) syndrome is a multisystem disorder which Michael Tomani classically involves the triad of esophageal achalasia, alacrima, and adrenal insufficiency due Levon Agdere to adrenocorticotropin hormone insensitivity. It follows an autosomal recessive pattern of – – Brande Brown inheritance and is associated with mutations in the AAAS (achalasia addisonianism alacrima syndrome) gene. Since its first description in 1978, the knowledge on clinical and genetic Department of Pediatrics, NewYork- characteristics has been expanding; however, the current literature is limited to case reports Presbyterian Brooklyn Methodist Hospital, Brooklyn, NY, USA and case reviews. Early recognition of the syndrome is challenging, given the rarity of the condition and high phenotypic heterogeneity even among members of kin. The coordination of care for these patients requires a multidisciplinary team of specialists, including endocri- nologists, neurologists, gastroenterologists, ophthalmologists, developmental specialists, dentists, geneticists, and surgeons. In this review, we aim to summarize the current recom- mendations for the diagnosis, management, and follow-up of patients with 3A syndrome. For personal use only. Keywords: AAA, guidelines, alacrima, achalasia, adrenal failure Introduction Triple A (3A) syndrome or Allgrove syndrome is a multisystem disorder first described in 1978, which classically involves the triad of esophageal achalasia, alacrima, and adrenocorticotropin hormone (ACTH)-resistant adrenal insufficiency.1 While the complete triad is present in approximately 70% of patients,2 dysfunction of the autonomic nervous system is also seen in about one-third of the patients,3 leading some authors to use the term 4A syndrome (achalasia, alacrima, adrenal insufficiency, and autonomic abnormalities).4 Additional symptoms reported in the literature include other neurological and dermatological manifestations,5 short stature, micro- Pediatric Health, Medicine and Therapeutics downloaded from https://www.dovepress.com/ by 54.70.40.11 on 07-Sep-2019 cephaly, osteoporosis, and dysmorphic features.6 Given this wide array of phenotypes (Table 1), a genotype–phenotype correlation consequently is yet to be established.6 The exact burden of this disease is unknown. 3A syndrome has an estimated prevalence of 1 in 1 million, though it has been suggested to be very underreported due to missed diagnosis.7 This rare autosomal recessive disorder has been linked with mutations in the AAAS (achalasia–addisonianism–alacrima syndrome) gene. The AAAS gene product is a 546-amino acid protein called alacrima–achalasia–adrenal insufficiency neurologic disorder (ALADIN), which belongs to the WD-repeat Correspondence: Brande Brown 8 Department of Pediatrics, NewYork- family of proteins and exhibits wide functional diversity. Allgrove syndrome fea- Presbyterian Brooklyn Methodist tures great variability in presentation with discordance between phenotypes and Hospital, 506, 6th Street, Brooklyn, NY 9 11215, USA genotypes even among members of the same family. Although genetic testing is Tel +1 718 780 5260 essential in revealing the final diagnosis, DNA studies are not useful in the prediction Fax +1 718 780 3266 10 Email [email protected] of phenotype or prognosis of this disorder. submit your manuscript | www.dovepress.com Pediatric Health, Medicine and Therapeutics 2019:10 99–106 99 DovePress © 2019 Flokas et al. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms. php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the http://doi.org/10.2147/PHMT.S173081 work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php). Powered by TCPDF (www.tcpdf.org) 1 / 1 Flokas et al Dovepress Table 1 Manifestations of triple A syndrome* Table 1 (Continued). Neurologic Dysmorphic Decreased muscle tone Narrow face Muscle weakness Long plithrum Hyperreflexia Down-turned mouth Extensor plantar responses Ataxia/clumsiness Oral and dental Pes cavus Xerostomia Gait disturbances Fissured tongue Dysarthria/nasal speech Dental caries Parkinsonism/extrapyramidal symptoms Edentulism Dysautonomia Fungal infections Postural hypotension Ophthalmologic Anisocoria/abnormal pupillary responses Alacrima/hypolacrima Increased/decreased sweating Optic atrophy Heart arrhythmias/abnormal heart responses Anisocoria/abnormal pupillary responses Sexual dysfunction Notes: *In only a minority of patients (<5 case reports): delayed puberty, lack of eyelashes, poor wound healing, cleft palate, multiple nasal polyps, scoliosis, long QT Sensory impairment syndrome, hyperlipoproteinemia type IIb. Color grading represents prevalence, with Sensorineural deafness darker shades representing increased frequency of clinical symptom. For personal use only. Microcephaly Given that the presence of 2 of the 3 cardinal clinical Mental retardation entities strongly suggests the diagnosis of 3A, the recogni- Dementia tion of the clinical syndrome is a challenge at the onset of Endocrine the disease, when only one presenting symptom is typically observed. Differential diagnosis includes other causes of Glucocorticoid deficiency adrenal insufficiency including familial glucocorticoid defi- fi Mineralocorticoid de ciency ciency. In adrenoleukodystrophy, similar to 3A, patients Osteoporosis may present with impaired glucocorticoid function with Short stature minimal or no dysfunction in mineralocorticoid production. Gastrointestinal Elevated levels of very-long-chain fatty acids in the plasma are pathognomonic. There is a broad differential for neuro- Achalasia “ ” Pediatric Health, Medicine and Therapeutics downloaded from https://www.dovepress.com/ by 54.70.40.11 on 07-Sep-2019 logical symptoms (see the section Neurology ). Finally, Dysphagia 3A syndrome is sometimes confused with Sjogren symptom Regurgitation when the presenting symptoms are alacrima and xerostomia Weight loss/failure to thrive (see the section “Oral Health”). Chronic respiratory symptoms/recurrent infections Long-term follow-up recommendations for patients with 3A are limited, as current literature consists mainly of case Dermatologic reports and case series. With no definitive treatment for the Hyperpigmentation condition, management focuses on individual presenting Palmoplantar hyperkeratosis signs and symptoms. The prognosis of 3A syndrome is highly dependent on early diagnosis in order to prevent Cutis anserine life-threatening adrenal crises—a challenging feat given the Incomplete dermatoglyphs rarity of the condition and its high phenotypic heterogeneity. (Continued) Early diagnosis may also prevent unnecessary investigations 100 submit your manuscript | www.dovepress.com Pediatric Health, Medicine and Therapeutics 2019:10 DovePress Powered by TCPDF (www.tcpdf.org) 1 / 1 Dovepress Flokas et al and inappropriate treatments.11 In this review, we present an 100,000 individuals.23 Esophageal achalasia in childhood is analytical, multidisciplinary approach for the diagnosis, rare, with less than 5% of patients presenting under the age of management, and follow-up of patients with 3A syndrome. 15 years.24 Symptoms of achalasia most often include regur- gitation, dysphagia, weight loss, and/or failure to thrive.25 Genetics Patients with achalasia may additionally present with pul- In 3A syndrome, approximately 90% of the mutations monary symptoms, including cough, aspiration, hoarseness, involve altered genetic modification, leading to a repeat dyspnea, wheezing, or sore throat in up to 40% of the cases.26 of the AAAS gene on chromosome 12q13.12 The AAAS In some cases, rare or recurrent pneumonias have alerted the gene encodes for a 546-amino acid polypeptide, known medical team, triggering further investigations and subse- – as ALADIN, which is involved with signal transduction, quent diagnosis of 3A syndrome.27 29 RNA processing, and transcription, as well as nuclear pore The exact mechanism of achalasia is not fully under- complex targeting.8,9 In addition, the ALADIN gene has stood. Achalasia present in 3A is caused by absent lower been reported to play a role in redox homeostasis in human esophageal sphincter relaxation and impaired esophageal adrenal cells and to inhibit steroidogenesis.13 Krumbholz motility, compared to also rare cricopharyngeal achalasia, et al have shown that most mutations cause mislocalization which is caused by isolated upper esophageal sphincter of the mutant ALADIN proteins in the cytoplasm, as a dysfunction. The gold standard of diagnosing achalasia is result of inhibition of the correct targeting of ALADIN to manometry25 and is established by the presence of aperis- nuclear pore complexes.14 High expression of this protein talsis in the distal two-thirds of the esophagus and incom- is seen in
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