Thanatophoric dysplasia

Ana M. Bircher M.D., Fernando Heredia M.D., Philippe Jeanty M.D., Ph.D.

Women"s Health Alliance, Nashville, TN.

Definition
Thanatophoric dysplasia is the most common skeletal dysplasia that is lethal in neonatal period1, 2, 4, 5, 6,16.
The name "thanatophoric" derives from the Greek meaning "death bearing" or "death bringing", and was given by Maroteaux et al in 1967.2
It is characterized by extreme rhizomelia, and a very narrow thorax, (which leads to respiratory distress and respiratory acidosis), normal trunk length, macrocephalia and polyhydramnios.3 19

Synonyms
Thanatophoric dwarfism3

Classification
Two subtypes can be recognized by the presence or absence of curved femurs.4
1. Thanatophoric dysplasia type 1, the most common subtype, characterized by curved and short femurs (shaped like a french telephone receiver), platyspondyly (35 per cent or less of the adjacent disk space in the lumbar spine). Very few type I cases have cloverleaf skull, and it is always mild.5, 7.
2. Thanatophoric dysplasia type II, presenting longer and straighter femurs, taller vertebral bodies and almost always associated with severe cloverleaf skull.6,14,19 Rarely, the cloverleaf skull is absent7.

Incidence:
The estimated frequency is approximately 0.5:10,000 births12 .This makes it the most common lethal skeletal dysplasia at birth.3 The relative incidence of the 2 subtypes are: Type I: 86 % and type II 14 %. Male to female ratio is 1:1.

Etiology:
Thanatophoric dysplasia is an autosomal dominant disorder caused by specific mutations in the fibroblast growth factor receptor 3 (FGFR3) gene.13 This gene is located on the short arm of chromosome 414.

Pathophysiology:
Fibroblast growth factors are structurally related proteins associated with cell growth, differentiation, migration, wound healing and angiogenesis. They are also described as being oncogenes that contribute the tumor progression in cases or myeloma multiple
Transmembrane tyrosinekinase receptors located in the cells mediate their functions, and are called fibroblast growth factor receptors. There are 4 genes encoding these receptors, and the mutation of three of them, FGFR1, FGFR 2 and FGFR 3, can cause different congenital, autosomal dominant disorders affecting the craniofacial and skeletal development, producing craniosynostosis and chondrodysplasias.15,16

The craniosynostosis syndromes, like Apert syndrome, Pfeiffer syndrome, Crouzon syndrome, Muenke syndrome, are caused by mutations in either FGFR 1, FGFR2 or FG FR3. The chondrodysplasias: chondrodysplasia, hypochondroplasia and thanatophoric dysplasia are caused only by mutations in FG FR3.16,17
FG FR3 is a negative regulator of bone growth. Binding of fibroblast growth factors to the FG FR3 receptor stimulates its tyrosine kinase activity in the cell. This activates a signal pathway that regulates endochondral ossification by inhibition of cell division and stimulation of cell maturation and differentiation.
Mutations in the FG FR3  gene gives rise to activation of the receptor in the absence of growth factors, causing abnormal bone development. The type of mutation is what determines the severity and type of the anomaly.18

Chondral and osseous histopathology
At the level of the growth plate, normal cartilage and bone tissue coexist alongside very abnormal and poorly organized regions of cartilage and bone. This combination of almost normal cartilage and bone distributed among altered tissue is the reason for the differences between Type I and Type II9

Thanatophoric dysplasia type I

The epiphyseal cartilage in the long bones does not differ from the normal controls.
The trabeculae in the metaphysis show disorganization, with regions of markedly altered light chondrocytes with decreased or absent maturation. These are not arranged in columns but distributed irregularly, surrounded with tufts of fibrous tissue, specially at the periphery of the growth plate.3, 7,19 .

Thanatophoric dysplasia  type II

There are similarities in the disorganization pattern of the growth plate. The difference is the presence of partial ossification around the cartilage canals, which penetrate to the physis. The trabeculae are much more regular and perpendicularly oriented to the growth plate than in type I. Nevertheless, the same tufts of fibrous tissue with atypical ossification are seen7 .
The most accepted hypotheses to explain this tissue mosaicism seen inTthanatophoric dysplasia type I and Thanatophoric dysplasia type II is that they do not represent two different entities, but the same entity with varying features due to mutational events occurring at different times7.

Neuropathologic changes
Many severe abnormalities.The most common is temporal lobe dysplasia. The anterior temporal lobe of the brain shows unussualy deep sulci arranged perpendicular to the neuraxis.Also, a peculiar shape of the ventricles can be found in association with dysgenetic changes in the hippocampus, dentate gyrus, amygdaloid body and periventricular white matter.

Others include: Brain stem hypoplasia, maldevelopment of the inferior olivary and the cerebellar dentate nuclei19,, abnormal sulci with polymicrogyria and neuronal heterotopia 3.

These findings indicate that lack of growth and overgrowth can coexist in the brain of affected individuals as well, suggesting that interactions between the mesenchyme and nervous tissue may play an important role in normal differentiation.20

Etiopathology of these two different types
The FG FR3 is a receptor comprised of three domains: an extracellular ligand-binding (consisting of three immunoglobulin-like sub domains), a transmembrane domain and an intracellular domain (consisting of two tyrosine kinase sub domains).
The inhibition of linear bone growth is caused by mutations in either intra or extracellular domains of FG FR3 .

In Thanatophoric dysplasia type I, cysteine replaces several amino acids in three separate regions in the extracellular domain21. These mutations cause the activation of the receptor. It is interesting to remark that, if cysteine replaces amino acids located in different places, this also causes different intensities of activation, producing less severe form of dwarfism, like achondroplasia. This suggests that the intensity of FGFR 3 activation is position-dependent.20, 22
In Thanatophoric dysplasia type II , lysine is substituted by glutamic acid in one of the intracellular sub domains of FG FR3 .23

Recurrence risk
A general empiric recurrence risk in sibs is estimated in 2%.24
Thanatophoric dysplasia  represents an example of disorders occurring as sporadic conditions due to autosomal dominant genes with "zero fitness. The concept of "fitness" means that the chief factor that determines if a mutation is lost immediately, becomes stable in a population, or even becomes, with time, the predominant allele at the locus concerned. In other words, fitness represents the measure of the number of offspring of affected persons who survive to reproductive age, in comparison with a control group. If an allele causes death or sterility, selection acts against it, and fitness equals 0. That is why the vast majority of cases are due to de novo mutations.16
The implications for genetic counseling is that the parents of a baby with this disorder, genetically lethal, have a low risk of recurrence, because the condition would require another independent mutation to occur again. 25

Diagnosis
Sonographic diagnosis is easily made in the second trimester, due to the characteristic abnormal configuration of the long bones and narrowness of the thorax.26
Although the diagnosis is usually made with 2D ultrasound, some authors consider that the three dimensional ultrasound is a helpful tool to make an accurate diagnosis. It helps to enhance the visualization of thickened, redundant folds and craniofacial and thoracic deformities.27 Three dimensional ultrasound using multiplanar and volume-rendered images is better than 2D in depicting abnormal spatial relationships such short ribs, splayed digits and absent bones. The achieving capabilities of 3D US allow to review and manipulate the images after the patient has left the clinic.28

Common findings
Type I 19, 23
Severe micromelia. Predominantly rhizomelic reduction of limbs. The limb bones are under the 3rd centile. These are also curved (particularly the femur), with a telephone receiver like shape( due to broadening of the metaphyseal ends). Also the fibulae appears shorter than the tibiae.
Narrow and small chest, "bell-shaped" or "pear-shaped". This can be suspected easily when the cardiac circumference is greater than 60 % of the thoracic circumference. Also, the abdomen appears protuberant in comparison with the chest.
Platyspondyly.

Type II 19, 29, 23

Cloverleaf shaped skull, with a trilobed appearance in coronal views (kleeblattschädel)30. These three lobes are represented by the prominent vertex of the calvarium in the middle and the two temporal bones on the sides.31This is caused by the extreme wideness of the frontal suture, that becomes wider superiorly, being then contiguous to a huge anterior fontanel.7 Synostosis occur along the sagittal and lambdoid sutures in such way that the sagittal suture is displaced posteriorly. The posterior fontanel is usually opened. Some authors consider the cloverleaf skull as the end point of all the craniosynostosis syndromes, if complete craniosynostosis of all the sutures is present.33
There are three explanations for the primary cause of the cloverleaf shape of he skull.

1.- a premature closure of the sutures.

2.- the promontory growth of a relatively normal cartilage-bone tissues at the skull base, resulting in an early synostosis and consecutive fusion of the cranial sutures.7, 32 .

3.- the primary developmental disorder in the brain, with secondary deformation of the bones.7

Severe micromelia. Limb bones under 3rd centile. Curved and short bones, although the femurs are straighter than in type I
Platyspondyly, with vertebral bodies taller than in type I.
Narrow thorax, with small ribs.
Low-set dysmorphic ears20

Common findings present in both types.14, 19, 23, 24

Central nervous system: megalencephaly, hydrocephaly.

Craniofacial: small foramen magnum and short skull base, frontal bossing, low nasal bridge, bulging eyes, small facies.

Limbs: abducted and externally rotated, (this can be due to the redundancy of the skin, that appears thick, preventing normal movements, and orienting the limbs in right angles compared with the body).22  Scapulae are small and squarish. Hands are very short with sausage-like fingers. Simian crease can also appear.

Polyhydramnios

Occasional abnormalities 14 19  23 24

Renal anomalies: horseshoe kidney, hydronephrosis.

Cardiovascular: Patent ductus arteriosus, auricular septal defect.

Other: irmperforate anus, radio-ulnar synostosis, agenesia of the corpus callosum.

Clinical findings in thanatophoric dysplasia variants
Extreme shortening of limbs and bossing of the forehead with depressed nasal bridge. But the trunk and neck are also short, unlike type 1 and 2.
Coarse facies. The phenotype resembles more the moderate-severe form of achondrogenesis type II.9

Differential diagnosis
Although the conjunction of a 2 D ultrasound with 3 D ultrasound using multiplanar and 3 D rendered images can reliably detect thanatophoric dysplasia, in some special cases it is very hard to reach an accurate diagnosis. These include those small fetuses with thanatophoric dysplasia type I with an onset before 20 weeks of gestational age20, 34
In those cases, only the molecular genetic analysis  from either cultured amniotic fluid cells, cord blood or fetal tissue can provide the definitive diagnosis.20, 26
The most important differential diagnosis is with achondroplasia, because it is the most frequent of the life-compatible short-limb skeletal dysplasia . The distinction is quantitative, with patients with achondroplasia having milder phenotypes than thanatophoric dysplasia.
Shortening of femoral length is the best parameter when stablishing a differential diagnosis.35 Mild shortening (greater than 80 % of the mean for gestational age) is often seen in achondroplasia, while severe shortening (30 to 60 %) is present in thanatophoric dysplasia . However, there is some overlap between these two malformations.
Other severe osteochondrodysplasias include achondrogenesis and osteogenesis imperfecta type II, although most of them are lethal. Observation of the fractures can suggest the diagnosis of OI type II, and extreme hypomineralization make the diagnosis of achondrogenesis.
The femur length / abdominal circumference ratio is useful for predicting a lethal fetal outcome when a skeletal dysplasia is diagnosed.36
Other differential diagnosys are Camptomelic dysplasia and trisomy 13.
The first can be ruled out by the acute angulation of the midshaft bowing of the long bones.
Trisomy 13 does not usually produce such short limbs.

Prognosis
By definition, this malformation is uniformly lethal before or shortly after birth. The main cause for this is lung hypoplasia (due to the small thorax) which lead to immediate postnatal asphyxia.1, 2, 3, 4, 5, 15, 19, 20, 25,

Management
For the reasons explained above, the option of pregnancy termination can be offered at any time during gestation.

Case report

A 30 year old woman was refered for a second opinion at 25-week gestation. The following images were obtained at that time.

The fetal head (2D and 3D reconstructions) showed moderate hydrocephalus probably due to compression of foramen magnum.

The following coronal plane 3D reconstructions show the typical Kleeblattschädel or Cloverleaf skull.

Transverse mid face plane clearly show exophtalmos, and the facial profile show frontal bossing and low nasal bridge.

Further 3D surface rendering mode images show further details:

c4
c2

The following coronal plane 3D reconstructions show the typical Kleeblattschädel or Cloverleaf skull.

c5
c1
c6
c3

Transverse mid face plane clearly show exophtalmos, and the facial profile show frontal bossing and low nasal bridge.

 

N
O

Further 3D surface rendering mode images show further details:

ca1
ca3
ca5
ca4
ca2

Note the "bell-shaped"  thorax seen on the images below.

M

B

The upper limbs were short, mostly rhizomelic and mantained a right angle throughout all examinations.

l3
l5
brazos1

Lower limbs were as well very short and rhizomelic. The femurs in these next images show the typical "telephone receiver" shape.

l1
l2
l4

Probably the most striking feature this fetus showed during its examination was the cloverleaf skull which is clearly shown on this video clip.

Within these, the most probable one is Thanatophoric dysplasia (type II) with cloverleaf skull.

These are postmortem images of this fetus:

pat1
pat4
pat3
pat2

And the radiology.

rx1
rx3
rx2

References


1 Orioli, I.M.; Castilla, E. E.; Barbosa-Neto, J.G. : The birth prevalence rates for the skeletal dysplasias. J. Med. Genet.  23: 328-332, 1986.
2 Maroteaux, P.;Lamy, M.;Robert, JM.:Le nanisme thanatophore. Presse Med. 75: 2519-2524, 1967.
3 Taybi, H., Langman R : Radiology of Syndromes, Metabolic disorders, and Skeletal Dysplasias . Third edition  Chicago, London , 1990.
4 Wilcox WR, Tavormina PL, Krakov D, Kitoh H, Lachman RS, Wasmuth JJ, Thompson LM, Rimoin DL. Molecular, radiologic, and histopathologic correlations in thanatophoric dysplasia. Am. J. Med. Genet 1998Jul 7;78(3):274-81.
5 Escobar LF, et al.: Quantitation of craniofacial anomalies in utero: fetal alcohol and Crouzon síndromes and thanatophoric dysplasia. Am. J. Med. Genet. 1993 Jan 1;45(1):25-9.
6 Langer, L . O., Jr.; Yang, S.S.; Hall, J.G.; Sommer, A.; Kottamasu, S. R.; Golabi, M.; Kressikoff, N.: Thanatophoric dysplasia and cloverleaf skull. Am. J. Med. Genet. Suppl. 3: 167-179, 1987.
7 Brons, J., van der Harten, H.; Skeletal dysplasias. Pre- and postnatal identification.1988. 111-142.
8 Brodie SG, Kitoh H, Lachman RS, Nolasco LM, Mekikian PB, Wilcox WR. Platyspondylic lethal skeletal dysplasia, San Diego type, is caused by FGFR3 mutations. Am J Med Genet 1999 Jun 11;84(5):476-80
9 van der Harten HJ, Brons JT, Dijkstra PF, Barth PG, Niermeyer MF, Meijer CJ, van Geijn HP, Arts NF  Some variants of lethal neonatal short-limbed platyspondylic dysplasia: a radiological ultrasonographic, neuropathological and histopathological study of 22 cases. Clin Dysmorphol 1993 Jan;2(1):1-19
10 Kitoh H, Lachman RS, Brodie SG, Mekikian PB, Rimoin DL, Wilcox WR. Extra pelvic ossification centers in thanatophoric dysplasia and platyspondylic lethal skeletal dysplasia-San Diego type Pediatr Radiol 1998 Oct;28(10):759-63 
11 http://www.csmc.edu/genetics/skeldys/default.html
12 Orioli, I.M.; Castilla, E.E.; Barbosa-Neto, J.G.: The birth prevalence rates for the skeletal dysplasias. J.Med. Genet. 23:328-332, 1986.
13 Wilcox  WR, Tavormina PL, Krakov D, Kitoh H, Lauchman RS, Wasmuth JJ, Thompson LM, Rimoin DL. Molecular, radiologic, and histopathologic correlartions in thanatophoric dysplasia. AM J Med Genet 1998 Jul 7;78(3):274-81.
14 Yuce, MA., Yardim, T, Kurtul, M., Durkan, S., Gucer, F. Prenatal diagnosis of thanatophoric dwarfism in second trimester. A case report. Clin Exp Obstet Gynecol 1990;25(4):149-50.
15 Chesi, M., Brents, LA., Eli, SA., Bais, C., Robbiani, DF., Mesri, EA., Kuel, WM., Bergsagel, PL. Activated fibroblast growth factor receptor 3 is an oncogene that contributes to tumor progression in multiple myeloma. Blood 2001Feb1;97(3):729-36.
16 Hertz JM, Junker I, Christensen L. Ostergaard JR, Jensen PK: The molecular genetic background of hereditary craniosynostosis and chondrodysplasias. Ugeskr Laeger.2001 Sep 3; 163(36):4862-7.  Review. Danish.
17 Wilkie, AO. Fibroblast growth factor receptor mutations and craniosynostosis: three receptors, five syndromes. Indian J Pediatr 1996May-June;63(3):351-6.
18 van Ravenswaaij-Arts CM.; Losekoot M. From gene to disease; achondroplasia and other skeletal dysplasias due to an activating mutation in the fibroblast growth factor. Ned Tijdschr Geneeskd 2001 Jun2;1454(22):1056-9
19 Jones K.L MD: Smith"s Recognizable Patterns of Human Malformation. 5th edition. Philadelphia, London, 1997.
20 Yamaguchi, K., Honma, K.. Autopsy case of thanatophoric dysplasia : observations on the serial sections of the brain. Neuropathology.2001Sep;21(3):222-8.
21 Adar R, Monsonego-Ornan E, David P, Yayon A.: Differential activation of cysteine-substitution mutants of fibroblast growth factor receptor 3 is determined by cysteine localization: J Bone Miner Res 2002 May;17(5):860-8
22 Bellus GA, Spector EB, Speiser PW, Weaver CA, Garber AT, Bryke CR, Israel J, Rosengren SS, Webster MK, Donoghue DJ, Francomano CA.: Distinct missense mutations of the FGFR3 lys650 codon modulate receptor kinase activation and the severity of the skeletal dysplasia phenotype. Am J Hum Genet 2000 Dec;67(6):1411-21
23 Pediatric database (PEDBASE). Last updated: 11/15/97
24 Pena, S.D. J.; Goodman, H.O.: The genetics of thanatophoric dwafism. Pediatrics 51: 104-109, 1973.
25 Thompson & Thompson. Genetics in Medicine. Sixth edition.2001. 102.
26 Benacerraf, B MD: Ultrasound of Fetal Syndromes. New York, Edinburg. 1998.
27 Chen, CP; Chern,Sr; Shih JC; Wang, W; Yeh, LF; Chang, TY; Tzen, CY. Prenatal diagnosis and genetic analysis of type I and type II thanatophoric dysplasia. Prenat. Diagn 2001 Feb;21(2):89-95
28 Garjian, KV., Pretorius, DH., Budorick, NE., Cantrell, CJ., Johnson, DD., Nelson, TR. Fetal skeletal dysplasia: three-dimensional US-initial experience. Radiology2002 Mar;214(3):717-23.
29 Callen, P.:Ultrasonography in Obstetrics and Gynecology. 4th. Edition. Philadelphia, London. 2000.
30 Budorik, N E., The fetal musculoskeletal System. Callen P. W. Ultrasonography in Obstetric and Gynecology  4th edition 2000; 343-45.
31 Romero R., Pilu G., Jeanty P. Prenatal diagnosis of congenital anomalies.  Norwalk, Connecticut 1988:335-39.
32Weber M, Johanhisson R, Cartens C, Pauschert R, Niethard FU. Thanatophoric dysplasia type II: new entity? J Pediatr Orthop B 1999 Jan;7(1):10-22.
33 Winter, RM., Knowles, SAS., Bieber, FR., Baraitser, M.: the Malformed Fetus and Stillbirth. A diagnostic approach. Chichester, New York.1988.
34 Sawai, H., Komori, S., Ida, A., Henmi T., Besho T., Koyama K.: Prenatal Diagnosis of Thanatophoric Dysplasia by Mutational Analysis of the fibroblast Growth Factor Receptor 3 Gene and a Proposed Correction of Previously Published PCR Results. Prenat. Diagnost.19: 21-24(1999).
35 Goncalves, L., Jeanty, P.: Fetal biometry of skeletal dysplasias; a multicentric study.J. Ultrasound Med. 13: 167-175(1996).
36 Rahemtullah , A., Mc Guillivray, B., Wilson, RD.: Suspected skeletal dysplasia: femur length to abdominal circumference ratio can be used in ultrasonographic prediction of fetal outcome. Am. J. Obstet. Ginecol. 177:864-869(1997).

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