#302060 ICD+
  • SNOMEDCT: 297231002,
  • ICD10CM: E78.71
SNOMEDCT: 297231002, ICD10CM: E78.71
BARTH SYNDROME; BTHS

Alternative titles; symbols
CARDIOSKELETAL MYOPATHY WITH NEUTROPENIA AND ABNORMAL MITOCHONDRIA
3-METHYLGLUTACONIC ACIDURIA, TYPE II; MGCA2
MGA, TYPE II; MGA2

Phenotype Gene Relationships
Location Phenotype Phenotype
MIM number
Gene/Locus Gene/Locus
MIM number
Xq28 Barth syndrome 302060 TAZ 300394


TEXT
A number sign (#) is used with this entry because Barth syndrome, also known as 3-methylglutaconic aciduria type II (MGCA2) is caused by mutation in the tafazzin gene (TAZ; 300394).

For a phenotypic description and a discussion of genetic heterogeneity of 3-methylglutaconic aciduria, see MGCA type I (250950).

Clinical Features
Barth et al. (1981, 1983) described a large pedigree showing X-linked inheritance of a disorder characterized by dilated cardiomyopathy, neutropenia, skeletal myopathy, and abnormal mitochondria. By electron microscopy, the mitochondria showed concentric, tightly packed cristae and occasional inclusion bodies. Hodgson et al. (1987) thought that the same disorder was present in the family they reported. The family reported by Barth et al. (1981, 1983) was Dutch. Many males in at least 3 generations and 7 sibships connected through females died between ages 3 days and 31 months of sepsis due to agranulocytosis or of cardiac failure. Weakness of skeletal muscles with sparing of the extraocular and bulbar muscles was noted. Granulocytopenia was found as early as cord blood samples. Differentiation in the bone marrow was arrested at the myelocyte stage. By electron microscopy, mitochondrial abnormalities were demonstrated in granulocyte precursors. Neustein et al. (1979) reported a family that may have had the same disorder. They demonstrated abnormal mitochondria on electron microscopic examination of a transvascular endomyocardial biopsy from an infant with cardiomyopathy and chronic congestive heart failure. At autopsy, similar abnormal mitochondria were seen in skeletal muscle, liver, and kidneys. In 3 other males in 2 sibships related as first cousins or first cousins once removed, autopsy showed endocardial fibroelastosis and, by electron microscopy, abnormal mitochondria. A heterozygote showed no abnormality on skeletal muscle biopsy. No mention of neutropenia in the affected males was made. The family described by Hodgson et al. (1987) contained multiple cases of males who died of cardiac failure within the first 8 months of life. These males were related through healthy females in a pattern consistent with X-linked recessive inheritance. None of the boys had a gross structural cardiac abnormality. Endocardial fibroelastosis was documented in 2, and in 1 of these, electron microscopy demonstrated abnormality of mitochondria. Ino et al. (1988) also reported cases. Kelley et al. (1989) reported increased levels of urinary 3-methylglutaconic acid and 2-ethylhydracrylic acid and referred to the disorder as Barth syndrome.

Kelley et al. (1991) elaborated on the clinical picture of this disorder on the basis of 7 affected boys with dilated cardiomyopathy, growth retardation, neutropenia, and persistently elevated urinary levels of 3-methylglutaconate, 3-methylglutarate, and 2-ethylhydracrylate. The clinical course of the disorder was characterized by severe or lethal cardiac disease and recurrent infections during infancy and early childhood but relative improvement in later childhood. The initial presentation of the syndrome varied from congenital dilated cardiomyopathy to infantile congestive heart failure to isolated neutropenia without clinical evidence of heart disease. The excretion of 3-methylglutaconate and 3-methylglutarate appeared to be independent of the metabolism of leucine, the presumed precursor of these organic acids. Chitayat et al. (1992) referred to this form of 3-methylglutaconic aciduria as type II.

Orstavik et al. (1993) reported 3 families with possible X-linked congestive cardiomyopathy associated with specific abnormalities of the mitochondria. The heart disorder presented as endocardial fibroelastosis with neonatal death in 2 brothers in 1 family and as heart failure and death in infancy in 2 brothers in the other 2 families. In 1 family, a maternal uncle may also have been affected. Pyodermia and neutropenia were reported in 1 of the boys. Electron microscopy of heart muscle showed increased numbers of mitochondria and abnormal mitochondrial crystal condensations and paracrystalline inclusions in all sibships.

Marziliano et al. (2007) reported a 12-year-old boy with Barth syndrome. The boy had left ventricular noncompaction and dilated cardiomyopathy, which was detected at 3 months, skeletal myopathy, recurrent oral aphthous ulcers, and cyclic neutropenia. Left ventricular function progressively improved since age 5 years and became subclinical and normal; he presented at age 11 with recurrent ulcers and signs of myopathy, including muscle weakness and atrophy. Molecular analysis identified a mutation in the TAZ gene (300394.0012) inherited from his unaffected mother. He was also heterozygous for a mutation in the LDB3 gene (605906), which is associated with left ventricular noncompaction. The patient's father and brother also carried the LDB3 mutation and had evidence of left ventricular trabeculation on imaging without dysfunction. The significance of the LDB3 mutation was unclear.

Female Carriers

Female carriers of the BTHS gene appear to be healthy. This could be due to a selection against cells that have the mutant allele on the active X chromosome. Orstavik et al. (1998) therefore analyzed X-chromosome inactivation in 16 obligate carriers of BTHS from 6 families, using PCR of a polymorphic CAG repeat in the first exon of the androgen receptor gene (AR; 313700). An extremely skewed X-inactivation pattern (equal to or more than 95:5), not found in 148 female controls, was demonstrated in 6 carriers. The skewed pattern in 2 carriers from 1 family was confirmed in DNA from cultured fibroblasts. Five carriers from 2 families had a skewed pattern, between 80:20 and less than 95:5, a pattern that was found in only 11 of 148 female controls. Of the 11 carriers with a skewed pattern, the parental origin of the inactive X chromosome was maternal in all 7 cases for which this could be determined. In 2 families, carriers with an extremely skewed pattern and carriers with a random pattern were found. The skewed X inactivation in 11 of 16 carriers is probably the result of a selection against cells with the mutated gene on the active X chromosome. Since BTHS also shows great clinical variation within families, additional factors are likely to influence the expression of the phenotype. Such factors may also influence the selection mechanism in carriers.

Barth et al. (2004) updated information on Barth syndrome. Following the prediction that the TAZ gene encodes one or more acyltransferases (Neuwald, 1997), lipid studies in patients with Barth syndrome showed a deficiency of cardiolipin, especially its tetralinoleoyl form (L4-CL) (Vreken et al., 2000). Deficiency of L4-CL was subsequently demonstrated in a variety of tissues from patients with Barth syndrome (Schlame et al., 2002), with determination in platelets or cultured skin fibroblasts being the most specific biochemical test. Barth syndrome was the first identified inborn error of metabolism that directly affects cardiolipin, a component of the inner mitochondrial membrane necessary for proper functioning of the electron transport chain. Barth et al. (2004) found that some patients with Barth syndrome have deficient docosahexaenoic acid and arachidonic acid. They pointed out that the initial impression of a uniformly lethal infantile disorder had to be modified. Age distribution in 54 living patients ranged from neonate to 49 years and peaked around puberty. Mortality was highest in the first 4 years. An update on a family with affected members in 3 successive generations and by inference in 2 earlier generations reported by Barth et al. (1983) was provided.

Diagnosis
Cantlay et al. (1999) identified 5 unrelated families within a 7-year period in 1 hospital in the area of Bristol, England, with BTHS. Mutations in the G4.5 gene were found in all of the cases. The authors questioned whether BTHS is underdiagnosed and suggested that all male infants or young children presenting with idiopathic dilated cardiomyopathy be carefully investigated for BTHS. They noted that associated neutropenia is variable, and urinary 3-methylglutaconic acid levels fluctuate. They advocated mutation analysis, if available.

Valianpour et al. (2002) used high performance liquid chromatography-electrospray mass spectrometry to quantify total cardiolipin and molecular subclasses in fibroblasts from 5 patients with Barth syndrome and compared the values to those in a healthy control group and a group with other diseases. Patients with Barth syndrome had decreased total cardiolipins and cardiolipin subclasses, especially tetralineoyl-cardiolipin. They suggested use of this biochemical test for diagnosis, followed by mutation analysis.

Clinical Management
Ostman-Smith et al. (1994) described a case of type II X-linked 3-methylglutaconic aciduria in a male infant who was admitted to hospital with gross congestive heart failure at the age of 3 weeks. A metabolic cause for his dilated cardiomyopathy was suspected because of the development on the electrocardiogram of an unusual 'camel's hump' shape of the T waves and progressive thickening of the left ventricular wall with increasing echogenicity. Digitalis did not provide sustained improvement and supplementation with L-carnitine was associated with rapid deterioration in cardiac state and may be contraindicated in this condition. At a point when the patient was moribund, large doses of pantothenic acid, a precursor of coenzyme A, produced a dramatic and sustained improvement in myocardial function and in growth, neutrophil cell count, hypocholesterolemia, and hyperuricemia, which suggested that limited availability of coenzyme A was the fundamental pathologic process in this condition. After 13 months, the clinical improvement had been maintained, and myocardial function was nearly normal. Oral pantothenol, unlike pantothenic acid, was not efficacious. Since the specific enzyme defect in this disorder was then unknown, the suggested dietary treatment was entirely empirical.

Mapping
By means of linkage studies in the family reported by Barth et al. (1983), Bolhuis et al. (1991) demonstrated that the BTHS locus is located in Xq28. Multipoint linkage analysis resulted in a maximum lod score of 5.24, with DXS305 being the closest of the markers used. Bolhuis et al. (1991) commented on the large number of genes that have been mapped to Xq28, despite its relatively small physical size, which is estimated to be 5-6 Mb. Ades et al. (1991, 1993) found a maximum lod score of 2.8 at theta = 0.0 with Xq28 polymorphic marker DXS52.

Molecular Genetics
In patients with Barth syndrome, Bione et al. (1996) identified mutations in the tafazzin gene which introduced stop codons in the open reading frame, aborting translation of most of the putative proteins. Using mutation analysis on DNA samples from members of 4 families, 2 large families used by Ades et al. (1993) and Bolhuis et al. (1991) for linkage mapping of the gene and 2 smaller families with the diagnostic features of the disease, Bione et al. (1996) found unique mutations in all patients. In 1 case the mutation was in exon 7 (300394.0004), one of the alternative exons. The mutation was predicted to cause truncation of most of the tafazzin proteins, but some minor forms lacking exon 7 could still be synthesized. The other 3 mutations (300394.0001, 300394.0002, and 300394.0003) were in the second exon and in the 3-prime splice junction of intron 2.

D'Adamo et al. (1997) studied the G4.5 gene, which they found to be mutant in Barth syndrome in 11 additional familial cases of cardiomyopathy; 8 were diagnosed as affected with BTHS, and 3 as affected with X-linked dilated cardiomyopathy (300069).

Johnston et al. (1997) evaluated 14 Barth syndrome pedigrees and found mutations in the G4.5 gene in all, including 4 splice site mutations (e.g., 302060.0007), 3 deletions, 1 insertion, 5 missense mutations, and 1 nonsense mutation. Nine of the 14 mutations were predicted to disrupt significantly the protein products of G4.5. The occurrence of missense mutations in exons 3 and 8 suggested that these exons encode essential portions of the G4.5 proteins.

Pathogenesis
Schlame and Ren (2006) provided an overview of the molecular basis of Barth syndrome, suggesting that the acyl-specific remodeling of cardiolipin by tafazzin promotes structural uniformity and molecular symmetry among the cardiolipin molecular species, and that inhibition of this pathway leads to changes in mitochondrial architecture and function.

Genotype/Phenotype Correlations
In the families studied by Johnston et al. (1997), no correlation between the location or type of mutation in any of the clinical or laboratory abnormalities of Barth syndrome was found, suggesting that additional factors modify the expression of the Barth phenotype. The clinical histories of most of the subjects investigated by Johnston et al. (1997) had been reported by Kelley et al. (1991) or by Christodoulou et al. (1994). The diagnosis of Barth syndrome was based on the triad of dilated cardiomyopathy, neutropenia, and increased 3-methylglutaconic aciduria in males.

Animal Model
Xu et al. (2006) generated homozygous Drosophila mutants that were unable to express full-length tafazzin and observed an 80% reduction of cardiolipin with diversification of its molecular composition, similar to the changes seen in Barth syndrome patients. Other phospholipids were not affected. Flies with the tafazzin mutation showed reduced locomotor activity, and their indirect flight muscles displayed frequent mitochondrial abnormalities, mostly in the cristae membranes. Xu et al. (2006) concluded that a lack of full-length tafazzin is responsible for cardiolipin deficiency, which is integral to the disease mechanism and leads to mitochondrial myopathy.

See Also:
Neustein et al. (1979)

REFERENCES
1. Ades, L. C., Gedeon, A. K., Latham, M., Partington, M., Sillence, D. O., Mulley, J. C. Confirmation of localisation of Barth syndrome to distal Xq28. (Abstract) Cytogenet. Cell Genet. 58: 2053, 1991.

2. Ades, L. C., Gedeon, A. K., Wilson, M. J., Latham, M., Partington, M. W., Mulley, J. C., Nelson, J., Lui, K., Sillence, D. O. Barth syndrome: clinical features and confirmation of gene localisation to distal Xq28. Am. J. Med. Genet. 45: 327-334, 1993. [PubMed: 8434619, related citations] [Full Text: Pubget]

3. Barth, P. G., Scholte, J. A., Berden, J. A., Van der Klei-Van Moorsel, J. M., Luyt-Houwen, I. E. M., Van't Veer-Korthof, E. T., Van der Harten, J. J., Sobotka-Plojhar, M. A. An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci. 62: 327-355, 1983. [PubMed: 6142097, related citations] [Full Text: Pubget]

4. Barth, P. G., Valianpour, F., Bowen, V. M., Lam, J., Duran, M., Vaz, F. M., Wanders, R. J. A. X-linked cardioskeletal myopathy and neutropenia (Barth syndrome): an update. Am. J. Med. Genet. 126A: 349-354, 2004. [PubMed: 15098233, related citations] [Full Text: John Wiley & Sons, Inc., Pubget]

5. Barth, P. G., Van't Veer-Korthof, E. T., Van Delden, L., Van Dam, K., Van der Harten, J. J., Kuipers, J. R. G. An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leukocytes.In: Busch, H. F. M.; Jennekens, F. G. I.; Schotte, H. R. : Mitochondria and Muscular Diseases. Beetsterzwaag, The Netherlands: Mefar (pub.) 1981. Pp. 161-164.

6. Bione, S., D'Adamo, P., Maestrini, E., Gedeon, A. K., Bolhuis, P. A., Toniolo, D. A novel X-linked gene, G4.5.(sic) is responsible for Barth syndrome. Nature Genet. 12: 385-389, 1996. [PubMed: 8630491, related citations] [Full Text: Nature Publishing Group, Pubget]

7. Bolhuis, P. A., Hensels, G. W., Hulsebos, T. J. M., Baas, F., Barth, P. G. Mapping of the locus for X-linked cardioskeletal myopathy with neutropenia and abnormal mitochondria (Barth syndrome) to Xq28. Am. J. Hum. Genet. 48: 481-485, 1991. [PubMed: 1998334, related citations] [Full Text: Pubget]

8. Cantlay, A. M., Shokrollabi, K., Allen, J. T., Lunt, P. W., Newbury-Ecob, R. A., Steward, C. G. Genetic analysis of the G4.5 gene in families with suspected Barth syndrome. J. Pediat. 135: 311-315, 1999. [PubMed: 10484795, related citations] [Full Text: Elsevier Science, Pubget]

9. Chitayat, D., Chemke, J., Gibson, K. M., Mamer, O. A., Kronick, J. B., McGill, J. J., Rosenblatt, B., Sweetman, L., Scriver, C. R. 3-Methylglutaconic aciduria: a marker for as yet unspecified disorders and the relevance of prenatal diagnosis in a 'new' type ('type 4'). J. Inherit. Metab. Dis. 15: 204-212, 1992. [PubMed: 1382150, related citations] [Full Text: Pubget]

10. Christodoulou, J., McInnes, R. R., Jay, V., Wilson, G., Becker, L. E., Lehotay, D. C., Platt, B.-A., Bridge, P. J., Robinson, B. H., Clarke, J. T. Barth syndrome: clinical observations and genetic linkage studies. Am. J. Med. Genet. 50: 255-264, 1994. [PubMed: 8042670, related citations] [Full Text: Pubget]

11. D'Adamo, P., Fassone, L., Gedeon, A., Janssen, E. A. M., Bione, S., Bolhuis, P. A., Barth, P. G., Wilson, M., Haan, E., Orstavik, K. H., Patton, M. A., Green, A. J., Zammarchi, E., Donati, M. A., Toniolo, D. The X-linked gene G4.5 is responsible for different infantile dilated cardiomyopathies. Am. J. Hum. Genet. 61: 862-867, 1997. [PubMed: 9382096, related citations] [Full Text: Elsevier Science, Pubget]

12. Hodgson, S., Child, A., Dyson, M. Endocardial fibroelastosis: possible X linked inheritance. J. Med. Genet. 24: 210-214, 1987. [PubMed: 3585935, related citations] [Full Text: HighWire Press, Pubget]

13. Ino, T., Sherwood, W. G., Cutz, E., Benson, L. N., Rose, V., Freedom, R. M. Dilated cardiomyopathy with neutropenia, short stature and abnormal carnitine metabolism. J. Pediat. 113: 511-514, 1988. [PubMed: 3411399, related citations] [Full Text: Pubget]

14. Johnston, J., Kelley, R. I., Feigenbaum, A., Cox, G. F., Iyer, G. S., Funanage, V. L., Proujansky, R. Mutation characterization and genotype-phenotype correlation in Barth syndrome. Am. J. Hum. Genet. 61: 1053-1058, 1997. [PubMed: 9345098, related citations] [Full Text: Elsevier Science, Pubget]

15. Kelley, R. I., Cheatham, J. P., Clark, B. J., Nigro, M. A., Powell, B. R., Sherwood, G. W., Sladky, J. T., Swisher, W. P. X-linked dilated cardiomyopathy with neutropenia, growth retardation, and 3-methylglutaconic aciduria. J. Pediat. 119: 738-747, 1991. [PubMed: 1719174, related citations] [Full Text: Pubget]

16. Kelley, R. I., Clark, B. J., Morton, D. H., Sherwood, W. G. X-linked cardiomyopathy, neutropenia, and increased urinary levels of 3-methylglutaconic and 2-ethylhydracrylic acids. (Abstract) Am. J. Hum. Genet. 45 (suppl.): A7, 1989.

17. Marziliano, N., Mannarino, S., Nespoli, L., Diegoli, M., Pasotti, M., Malattia, C., Grasso, M., Pilotto, A., Porcu, E., Raisaro, A., Raineri, C., Dore, R., Maggio, P. P., Brega, A., Arbustini, E. Barth syndrome associated with compound hemizygosity and heterozygosity of the TAZ and LDB3 genes. Am. J. Med. Genet. 143A: 907-915, 2007. [PubMed: 17394203, related citations] [Full Text: John Wiley & Sons, Inc., Pubget]

18. Neustein, H. B., Lurie, P. R., Dahms, B., Takahashi, M. An X-linked recessive cardiomyopathy with abnormal mitochondria. Pediatrics 64: 24-29, 1979. [PubMed: 572031, related citations] [Full Text: Pubget]

19. Neustein, H. B., Lurie, P. R., Fugita, M. Endocardial fibroelastosis found on transvascular endomyocardial biopsy in children. Arch. Path. Lab. Med. 103: 214-219, 1979. [PubMed: 582252, related citations] [Full Text: Pubget]

20. Neuwald, A. F. Barth syndrome may be due to an acyltransferase deficiency. Curr. Biol. 7: 465-466, 1997.

21. Orstavik, K. H., Orstavik, R. E., Naumova, A. K., D'Adamo, P., Gedeon, A., Bolhuis, P. A., Barth, P. G., Toniolo, D. X chromosome inactivation in carriers of Barth syndrome. Am. J. Hum. Genet. 63: 1457-1463, 1998. [PubMed: 9792874, related citations] [Full Text: Elsevier Science, Pubget]

22. Orstavik, K. H., Skjorten, F., Hellebostad, M., Haga, P., Langslet, A. Possible X linked congenital mitochondrial cardiomyopathy in three families. J. Med. Genet. 30: 269-272, 1993. [PubMed: 8487269, related citations] [Full Text: HighWire Press, Pubget]

23. Ostman-Smith, I., Brown, G., Johnson, A., Land, J. M. Dilated cardiomyopathy due to type II X-linked 3-methylglutaconic aciduria: successful treatment with pantothenic acid. Brit. Heart J. 72: 349-353, 1994. [PubMed: 7833193, related citations] [Full Text: HighWire Press, Pubget]

24. Schlame, M., Ren, M. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett. 580: 5450-5455, 2006. [PubMed: 16973164, related citations] [Full Text: Elsevier Science, Pubget]

25. Schlame, M., Towbin, J. A., Heerdt, P. M., Jehle, R., DiMauro, S., Blanck, T. J. J. Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome. Ann. Neurol. 51: 634-637, 2002. [PubMed: 12112112, related citations] [Full Text: John Wiley & Sons, Inc., Pubget]

26. Valianpour, F., Wanders, R. J. A., Overmars, H., Vreken, P., van Gennip, A. H., Baas, F., Plecko, B., Santer, R., Becker, K., Barth, P. G. Cardiolipin deficiency in X-linked cardioskeletal myopathy and neutropenia (Barth syndrome, MIM 302060): a study in cultured skin fibroblasts. J. Pediat. 141: 729-733, 2002. [PubMed: 12410207, related citations] [Full Text: Elsevier Science, Pubget]

27. Vreken, P., Valianpour, F., Nijtmans, L. G., Grivell, L. A., Plecko, B., Wanders, R. J. A., Barth, P. G. Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem. Biophys. Res. Commun. 279: 378-382, 2000. [PubMed: 11118295, related citations] [Full Text: Elsevier Science, Pubget]

28. Xu, Y., Condell, M., Plesken, H., Edelman-Novemsky, I., Ma, J., Ren, M., Schlame, M. A Drosophila model of Barth syndrome. Proc. Nat. Acad. Sci. 103: 11584-11588, 2006. [PubMed: 16855048, related citations] [Full Text: HighWire Press, Pubget]

Contributors: Marla J. F. O'Neill - updated : 3/5/2010
Cassandra L. Kniffin - updated : 7/17/2007
Marla J. F. O'Neill - updated : 10/3/2006
Marla J. F. O'Neill - updated : 6/19/2006
Natalie E. Krasikov - updated : 7/14/2004
Victor A. McKusick - updated : 5/11/2004
Cassandra L. Kniffin - reorganized : 5/10/2002
Victor A. McKusick - updated : 1/15/2002
Victor A. McKusick - updated : 12/7/2001
Wilson H. Y. Lo - updated : 2/1/2000
Victor A. McKusick - updated : 10/26/1998
Victor A. McKusick - updated : 11/26/1997
Victor A. McKusick - updated : 11/11/1997
Victor A. McKusick - updated : 10/24/1997
Creation Date: Victor A. McKusick : 4/8/1991
Edit History: carol : 08/15/2011
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