Natural history of Wolcott-Rallison syndrome: A systematic review and follow-up study.
ER stress
acute liver failure
neonatal-onset diabetes
paediatric
skeletal dysplasia
Journal
Liver international : official journal of the International Association for the Study of the Liver
ISSN: 1478-3231
Titre abrégé: Liver Int
Pays: United States
ID NLM: 101160857
Informations de publication
Date de publication:
17 Jan 2024
17 Jan 2024
Historique:
revised:
19
12
2023
received:
16
11
2023
accepted:
22
12
2023
medline:
17
1
2024
pubmed:
17
1
2024
entrez:
17
1
2024
Statut:
aheadofprint
Résumé
To systematically review the literature for reports on Wolcott-Rallison syndrome, focusing on the spectrum and natural history, genotype-phenotype correlations, patient and native liver survival, and long-term outcomes. PubMed, Livio, Google Scholar, Scopus and Web of Science databases were searched. Data on genotype, phenotype, therapy, cause of death and follow-up were extracted. Survival and correlation analyses were performed. Sixty-two studies with 159 patients met the inclusion criteria and additional 30 WRS individuals were collected by personal contact. The median age of presentation was 2.5 months (IQR 2) and of death was 36 months (IQR 50.75). The most frequent clinical feature was neonatal diabetes in all patients, followed by liver impairment in 73%, impaired growth in 72%, skeletal abnormalities in 59.8%, the nervous system in 37.6%, the kidney in 35.4%, insufficient haematopoiesis in 34.4%, hypothyroidism in 14.8% and exocrine pancreas insufficiency in 10.6%. Episodes of acute liver failure were frequently reported. Liver transplantation was performed in six, combined liver-pancreas in one and combined liver-pancreas-kidney transplantation in two individuals. Patient survival was significantly better in the transplant cohort (p = .0057). One-, five- and ten-year patient survival rates were 89.4%, 65.5% and 53.1%, respectively. Liver failure was reported as the leading cause of death in 17.9% of cases. Overall survival was better in individuals with missense mutations (p = .013). Wolcott-Rallison syndrome has variable clinical courses. Overall survival is better in individuals with missense mutations. Liver- or multi-organ transplantation is a feasible treatment option to improve survival.
Sections du résumé
BACKGROUND AND AIMS
OBJECTIVE
To systematically review the literature for reports on Wolcott-Rallison syndrome, focusing on the spectrum and natural history, genotype-phenotype correlations, patient and native liver survival, and long-term outcomes.
METHODS
METHODS
PubMed, Livio, Google Scholar, Scopus and Web of Science databases were searched. Data on genotype, phenotype, therapy, cause of death and follow-up were extracted. Survival and correlation analyses were performed.
RESULTS
RESULTS
Sixty-two studies with 159 patients met the inclusion criteria and additional 30 WRS individuals were collected by personal contact. The median age of presentation was 2.5 months (IQR 2) and of death was 36 months (IQR 50.75). The most frequent clinical feature was neonatal diabetes in all patients, followed by liver impairment in 73%, impaired growth in 72%, skeletal abnormalities in 59.8%, the nervous system in 37.6%, the kidney in 35.4%, insufficient haematopoiesis in 34.4%, hypothyroidism in 14.8% and exocrine pancreas insufficiency in 10.6%. Episodes of acute liver failure were frequently reported. Liver transplantation was performed in six, combined liver-pancreas in one and combined liver-pancreas-kidney transplantation in two individuals. Patient survival was significantly better in the transplant cohort (p = .0057). One-, five- and ten-year patient survival rates were 89.4%, 65.5% and 53.1%, respectively. Liver failure was reported as the leading cause of death in 17.9% of cases. Overall survival was better in individuals with missense mutations (p = .013).
CONCLUSION
CONCLUSIONS
Wolcott-Rallison syndrome has variable clinical courses. Overall survival is better in individuals with missense mutations. Liver- or multi-organ transplantation is a feasible treatment option to improve survival.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Jubiläumsfonds der Österreichischen Nationalbank
Informations de copyright
© 2024 The Authors. Liver International published by John Wiley & Sons Ltd.
Références
Wolcott CD, Rallison ML. Infancy-onset diabetes mellitus and multiple epiphyseal dysplasia. J Pediatr. 1972;80:292-297.
Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89-102.
Julier C, Nicolino M. Wolcott-Rallison syndrome. Orphanet J Rare Dis. 2010;5:29.
Senée V, Vattem KM, Delépine M, et al. Wolcott-Rallison syndrome: clinical, genetic, and functional study of EIF2AK3 mutations and suggestion of genetic heterogeneity. Diabetes. 2004;53:1876-1883.
Ozbek MN, Senée V, Aydemir S, et al. Wolcott-Rallison syndrome due to the same mutation (W522X) in EIF2AK3 in two unrelated families and review of the literature. Pediatr Diabetes. 2010;11:279-285.
Goumy P, Maroteaux P, Stanescu V, Stanescu R, Labbe A, Menut G. A syndrome of congenital diabetes with disordered epiphyseal growth with autosomal recessive inheritance (author's transl). Arch Fr Pediatr. 1980;37:323-328.
Habeb AM, Deeb A, Johnson M, et al. Liver disease and other comorbidities in Wolcott-Rallison syndrome: different phenotype and variable associations in a large cohort. Horm Res Paediatr. 2015;83:190-197.
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
World Medical Association Declaration of Helsinki. Ethical principles for medical research involving human subjects. JAMA. 2013;310:2191-2194.
Squires JE, Alonso EM, Ibrahim SH, et al. North American Society for pediatric gastroenterology, hepatology, and nutrition position paper on the diagnosis and management of pediatric acute liver failure. J Pediatr Gastroenterol Nutr. 2022;74:138-158.
R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Satistical Computing; 2010.
Ioannidis NM, Rothstein JH, Pejaver V, et al. REVEL: an ensemble method for predicting the pathogenicity of rare missense variants. Am J Hum Genet. 2016;99:877-885.
Jagadeesh KA, Wenger AM, Berger MJ, et al. M-CAP eliminates a majority of variants of uncertain significance in clinical exomes at high sensitivity. Nat Genet. 2016;48:1581-1586.
Vaser R, Adusumalli S, Leng SN, Sikic M, Ng PC. SIFT missense predictions for genomes. Nat Protoc. 2016;11:1-9.
Vogel GF, Mozer-Glassberg Y, Landau YE, et al. Genotypic and phenotypic spectrum of infantile liver failure due to pathogenic TRMU variants. Genet Med. 2023;25:100314.
Schröter J, Dattner T, Hüllein J, et al. aRgus: multilevel visualization of non-synonymous single nucleotide variants & advanced pathogenicity score modeling for genetic vulnerability assessment. Comput Struct Biotechnol J. 2023;21:1077-1083.
Juneja A, Sultan A, Bhatnagar S. Wolcott-Rallison syndrome. J Indian Soc Pedod Prev Dent. 2012;30:250-253.
Davoodi MA, Karamizadeh Z, Ghobadi F, Shokrpour N. Wolcott-Rallison syndrome with different clinical presentations and genetic patterns in 2 infants. Health Care Manag (Frederick). 2018;37:354-357.
Asl SN, Vakili R, Vakili S, et al. Wolcott-Rallison syndrome in Iran: a common cause of neonatal diabetes. J Pediatr Endocrinol Metab. 2019;32:607-613.
Marafie MJ, Redha MA, Al-Naggar RL. Wolcott-Rallison syndrome in a Bedouin boy. Ann Saudi Med. 2004;24:476-479.
Huang A, Wei H. Wolcott-Rallison syndrome due to the same mutation in EIF2AK3 (c.205G>T) in two unrelated families: a case report. Exp Ther Med. 2019;17:2765-2768.
Valamparampil JJ, Shanmugam N, Rela M. Wolcott-Rallison syndrome- endocrinopathy with recurrent acute liver failure. Indian Pediatr. 2019;56:1055-1056.
Zhang HJ, Wang SB, Guo XF, Weng B, Lin L, Hao Y. A case report of EIF2AK3-related Wolcott-Rallison syndrome and literature review. Zhongguo Dang Dai Er Ke Za Zhi. 2019;21:176-179.
Welters A, Meissner T, Konrad K, et al. Diabetes management in Wolcott-Rallison syndrome: analysis from the German/Austrian DPV database. Orphanet J Rare Dis. 2020;15:100.
Rubio-Cabezas O, Patch AM, Minton JA, et al. Wolcott-Rallison syndrome is the most common genetic cause of permanent neonatal diabetes in consanguineous families. J Clin Endocrinol Metab. 2009;94:4162-4170.
Al Kaissi A, Ganger R, Roetzer KM, Schwarzbraun T, Klaushofer K, Grill F. Re-alignment-procedures for skeletal dysplasia in three patients with genetically diverse syndromes. Orthop Surg. 2013;5:33-39.
Anne RP, Vasikarla M, Oleti TP. Wolcott-Rallison syndrome affecting three consecutive conceptions of a consanguineous couple. Indian Pediatr. 2021;58:80-81.
Habeb AM. Frequency and spectrum of Wolcott-Rallison syndrome in Saudi Arabia: a systematic review. Libyan J Med. 2013;8:21137.
Bonthron DT, Dunlop N, Barr DG, El Sanousi AA, Al-Gazali LI. Organisation of the human PAX4 gene and its exclusion as a candidate for the Wolcott-Rallison syndrome. J Med Genet. 1998;35:288-292.
Brickwood S, Bonthron DT, Al-Gazali LI, et al. Wolcott-Rallison syndrome: pathogenic insights into neonatal diabetes from new mutation and expression studies of EIF2AK3. J Med Genet. 2003;40:685-689.
Deeb A, Al-Zidgali F, Ofoegbu BN. Multicystic dysplastic kidney: a new association of Wolcott-Rallison syndrome. Endocrinol Diabetes Metab Case Rep. 2017;2017:17-0090.
Lundgren M, De Franco E, Arnell H, Fischler B. Practical management in Wolcott-Rallison syndrome with associated hypothyroidism, neutropenia, and recurrent liver failure: a case report. Clin Case Rep. 2019;7:1133-1138.
Gürbüz F, Yüksel B, Topaloğlu AK. Wolcott-Rallison syndrome with novel EIF2AK3 gene mutation. J Clin Res Pediatr Endocrinol. 2016;8:496-497.
Sreeramaneni PGA, Ambula SRV. Ketoacidosis in neonatal diabetes mellitus, part of Wolcott-Rallison syndrome. Am J Case Rep. 2017;18:719-722.
Tzakis AG, Nunnelley MJ, Tekin A, et al. Liver, pancreas and kidney transplantation for the treatment of Wolcott-Rallison syndrome. Am J Transplant. 2015;15:565-567.
Uçar A, Aydemir Y, Doğan A, Tunçez E. Relative hypoaldosteronism in a patient with Wolcott-Rallison syndrome. Diabet Med. 2016;33:e13-e16.
Mihci E, Türkkahraman D, Ellard S, Akçurin S, Bircan I. Wolcott-Rallison syndrome due to a novel mutation (R491X) in EIF2AK3 gene. J Clin Res Pediatr Endocrinol. 2012;4:101-103.
Khare S, Goroshi MR, Budyal S, Bandgar T, Lila A, Shah N. Wolcott Rallison syndrome: a rare inherited diabetes mellitus. Indian J Pediatr. 2014;81:1225-1227.
Bejiqi R, Retkoceri R, Zeka N, Bejiqi R, Bejic S. An infant with neonatal diabetes and double outlet right ventricle-Wolcott-Rallison syndrome. Med Arch. 2018;72:289-291.
Søvik O, Njølstad PR, Jellum E, Molven A. Wolcott-Rallison syndrome with 3-hydroxydicarboxylic aciduria and lethal outcome. J Inherit Metab Dis. 2008;31(suppl 2):S293-S297.
Romera AC, Hervías M, López-Gil MT, Tranche I. Anaesthesia and orphan disease: a child with Wolcott-Rallison syndrome. Eur J Anaesthesiol. 2015;32:217-218.
Sümegi A, Hendrik Z, Gáll T, et al. A novel splice site indel alteration in the EIF2AK3 gene is responsible for the first cases of Wolcott-Rallison syndrome in Hungary. BMC Med Genet. 2020;21:61.
Ersoy B, Özhan B, Kiremitçi S, Rubio-Cabezas O, Ellard S. Primary hypothyroidism: an unusual manifestation of Wolcott-Rallison syndrome. Eur J Pediatr. 2014;173:1565-1568.
Dias RP, Buchanan CR, Thomas N, et al. Os odontoideum in wolcott-rallison syndrome: a case series of 4 patients. Orphanet J Rare Dis. 2016;11:14.
Triantafyllou P, Vargiami E, Vagianou I, Badouraki M, Julier C, Zafeiriou DI. Early-onset diabetes mellitus and neurodevelopmental retardation: the first Greek case of Wolcott-Rallison syndrome. J Pediatr Endocrinol Metab. 2014;27:967-970.
Bahsi T, Unal A, Bakir A, Perçin EF. The 3rd W522X mutation in EIF2AK3 gene from Turkey: a new patient with Wolcott-Rallison syndrome. Genet Couns. 2016;27:411-418.
Jahnavi S, Poovazhagi V, Kanthimathi S, Gayathri V, Mohan V, Radha V. EIF2AK3 mutations in South Indian children with permanent neonatal diabetes mellitus associated with Wolcott-Rallison syndrome. Pediatr Diabetes. 2014;15:313-318.
Collardeau-Frachon S, Vasiljevic A, Jouvet A, Bouvier R, Senée V, Nicolino M. Microscopic and ultrastructural features in Wolcott-Rallison syndrome, a permanent neonatal diabetes mellitus: about two autopsy cases. Pediatr Diabetes. 2015;16:510-520.
Spehar Uroić A, Mulliqi Kotori V, Rojnić Putarek N, Kušec V, Dumić M. Primary hypothyroidism and nipple hypoplasia in a girl with Wolcott-Rallison syndrome. Eur J Pediatr. 2014;173:529-531.
Sang Y, Liu M, Yang W, Yan J, Chengzhu NG. A novel EIF2AK3 mutation leading to Wolcott-Rallison syndrome in a Chinese child. J Pediatr Endocrinol Metab. 2011;24:181-184.
Durocher F, Faure R, Labrie Y, Pelletier L, Bouchard I, Laframboise R. A novel mutation in the EIF2AK3 gene with variable expressivity in two patients with Wolcott-Rallison syndrome. Clin Genet. 2006;70:34-38.
Reis AF, Kannengiesser C, Jennane F, et al. Two novel mutations in the EIF2AK3 gene in children with Wolcott-Rallison syndrome. Pediatr Diabetes. 2011;12:187-191.
Rivera E, Gupta S, Chavers B, et al. En bloc multiorgan transplant (liver, pancreas, and kidney) for acute liver and renal failure in a patient with Wolcott-Rallison syndrome. Liver Transpl. 2016;22:371-374.
Biason-Lauber A, Lang-Muritano M, Vaccaro T, Schoenle EJ. Loss of kinase activity in a patient with Wolcott-Rallison syndrome caused by a novel mutation in the EIF2AK3 gene. Diabetes. 2002;51:2301-2305.
Fatani TH. EIF2AK3 novel mutation in a child with early-onset diabetes mellitus, a case report. BMC Pediatr. 2019;19:85.
Nayak S, Sarangi AN, Sahoo SK, et al. Neonatal diabetes mellitus: novel mutations. Indian J Pediatr. 2021;88:785-792.
Elsabbagh AM, Hawksworth J, Khan KM, Yazigi N, Matsumoto CS, Fishbein TM. World's smallest combined en bloc liver-pancreas transplantation. Pediatr Transplant. 2018;22.
Hawkes CP, McGlacken-Byrne SM, Murphy NP. Short stature in child with early-onset diabetes. Eur J Pediatr. 2013;172:1255-1257.
Deeb A, Habeb A, Kaplan W, et al. Genetic characteristics, clinical spectrum, and incidence of neonatal diabetes in the Emirate of AbuDhabi, United Arab Emirates. Am J Med Genet A. 2016;170:602-609.
Furdela V, Pavlyshyn H, Korytskyi H, Filiuk A. permanent neonatal diabetes mellitus in a young Ukrainian child. Pediatr Endocrinol Diabetes Metab. 2016;22:134.
Zhao N, Yang Y, Li P, Xiong Q, Xiao H, Wu C. Identification of two novel compound heterozygous EIF2AK3 mutations underlying Wolcott-Rallison syndrome in a Chinese family. Front Pediatr. 2021;9:679646.
Shah N, Karguppikar MB, Khadilkar V, Khadilkar A. Long-term follow-up of a child with Wolcott-Rallison syndrome. BMJ Case Rep. 2021;14.
Maleki E, Baniasad A, Sepehran M, Davoudian N. The first presentation of Wolcott-Rallison syndrome in a four-month-old infant with diabetic ketoacidosis (DKA) precipitating by COVID-19: a case report. Clin Case Rep. 2021;9:e05096.
Korula S, Ravichandran L, Paul PG, et al. Genetic heterogeneity and challenges in the management of permanent neonatal diabetes mellitus: a single-centre study from South India. Indian J Endocrinol Metab. 2022;26:79-86.
Gupta A, Reddy C, Saini L, et al. Lissencephaly-pachygyria spectrum in a North Indian boy with Wolcott-Rallison syndrome due to homozygous deletion of exon 1 in the EIF2AK3 gene. Pediatr Endocrinol Diabetes Metab. 2021;27:287-290.
Memon F, Arif M, Kirmani S, Humayun K. Wolcott-Rallison syndrome: a case series of three patients. Pediatr Endocrinol Diabetes Metab. 2022;28:238-240.
Laimon W, El-Ziny M, El-Hawary A, et al. Genetic and clinical heterogeneity of permanent neonatal diabetes mellitus: a single tertiary Centre experience. Acta Diabetol. 2021;58:1689-1700.
Globa E, Zelinska N, Johnson MB, Flanagan SE, De Franco E. Neonatal and early-onset diabetes in Ukraine: atypical features and mortality. Diabet Med. 2023;40:e15013.
Al-Shawi M, Al Mutair A, Ellard S, Habeb AM. Variable phenotype in five patients with Wolcott-Rallison syndrome due to the same EIF2AK3 (c.1259delA) mutation. J Pediatr Endocrinol Metab. 2013;26:757-760.
Behnam B, Shakiba M, Ahani A, Razzaghy AM. Recurrent hepatitis in two Iranian children: a novel (Q166R) mutation in EIF2AK3 leading to Wolcott-Rallison syndrome. Hepat Mon. 2013;13:e10124.
Bin-Abbas B, Shabib S, Hainau B, Al-Ashwal A. Wolcott-Rallison syndrome: clinical, radiological and histological findings in a Saudi child. Ann Saudi Med. 2001;21:73-74.
Habeb AM, Al-Magamsi MS, Eid IM, et al. Incidence, genetics, and clinical phenotype of permanent neonatal diabetes mellitus in northwest Saudi Arabia. Pediatr Diabetes. 2012;13:499-505.
de Wit MC, de Coo IF, Julier C, et al. Microcephaly and simplified gyral pattern of the brain associated with early onset insulin-dependent diabetes mellitus. Neurogenetics. 2006;7:259-263.
Bin-Abbas B, Al-Mulhim A, Al-Ashwal A. Wolcott-Rallison syndrome in two siblings with isolated central hypothyroidism. Am J Med Genet. 2002;111:187-190.
al-Gazali LI, Makia S, Azzam A, Hall CM. Wolcott-Rallison syndrome. Clin Dysmorphol. 1995;4:227-233.
De Franco E, Flanagan SE, Houghton JA, et al. The effect of early, comprehensive genomic testing on clinical care in neonatal diabetes: an international cohort study. Lancet. 2015;386:957-963.
Alexander EC, Deep A. Therapeutic plasma exchange in children with acute liver failure (ALF): is it time for incorporation into the ALF armamentarium? Pediatr Nephrol. 2022;37:1775-1788.
Mann JP, Lenz D, Stamataki Z, Kelly D. Common mechanisms in pediatric acute liver failure. Trends Mol Med. 2023;29:228-240.