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Mucopolysaccharidosis IVB and sensorineural deafness associated with the CDH23 gene: A unique clinical case
- Authors: Kenis V.M.1, Gorobets L.V.2, Dimitrieva A.Y.1, Zhmurova-Kriventsova A.A.3, Bychkov I.O.4, Baydakova G.V.4, Markova T.V.4, Zakharova E.Y.4
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Affiliations:
- H. Turner National Medical Research Center for Children’s Orthopedics and Trauma Surgery
- Clinical and diagnostic center “Zdorovoe detstvo”
- Clinic of the evidence-based medicine “Umka Family”
- Research Centre for Medical Genetics
- Issue: Vol 10, No 3 (2022)
- Pages: 285-294
- Section: Clinical cases
- URL: https://journals.eco-vector.com/turner/article/view/108730
- DOI: https://doi.org/10.17816/PTORS108730
- ID: 108730
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Abstract
BACKROUND: Mucopolysaccharidoses are a group of lysosomal storage diseases belonging to orphan diseases. Certain types of mucopolysaccharides have a typical musculoskeletal findings and radiological changes. The mucopolysaccharidosis IVB is a rare type. Thus, >95% of cases of the mucopolysaccharidosis IV are subtype A.
CLINICAL CASE: Сlinical and radiological changes and genetic examination were performed to a 9-year-old patient with sensorineural deafness who applied to a medical institution with complaints of right hip pain and limping.
DISCUSSION: Based on complaints and radiological changes of the hip joints, the patient was initially diagnosed with Legg–Calve–Perthes disease. The presence of a symmetrical bilateral process, pathognomonic changes in the acetabulum and femoral heads, and an atypical clinic of Legg–Calve–Perthes disease made us suspect mucopolysaccharidos. Enzymatic analysis revealed a significant decrease in the beta-D-galactosidase enzyme activity. In addition, two compound heterozygous variants in the GLB1 gene were identified: the pathogenic variant c.808T>G, inherited from the father, and an insertion of a mobile genetic element, inherited from the mother. Only one variant in the GLB1 gene was detected in the brother (born in 2009), and none of the above GLB1 variants was detected in the older brother (born in 2003). Moreover, the proband (with clinical mucopolysaccharidos IVB) and his brother (born in 2009) (without mucopolysaccharidos IVB) inherited pathogenic CDH23 variants (c.6992T>C and c.805C>T) from their mother and father, respectively, which is consistent with their having sensorineural hearing loss.
CONCLUSIONS: The uniqueness of this clinical case is the presence of the rare type of mucopolysaccharidos and the separate genetic cause of sensorineural hearing loss in a single patient. The diagnosis of mucopolysaccharidos IVB in the proband was confirmed by biochemical and molecular genetic tests, and the diagnosis of CDH23-associated sensorineural deafness in the proband and brother (born in 2009) was confirmed by molecular genetic testing.
Full Text
BACKGROUND
Mucopolysaccharidoses (MPS) are lysosomal storage diseases. Currently, seven types of MPS are known, which are caused by a deficiency of one of the eleven enzymes involved in the degradation of glycosaminoglycans.
- Type I is associated with alpha-L-iduronidase deficiency. It is subdivided into subtypes, namely, Hurler syndrome, Hurler–Scheie syndrome, and Scheie syndrome, which do not differ in such a pronounced clinical presentation [1].
- Type II (Hunter’s syndrome) is caused by iduronate-2-sulfatase deficiency [2].
- Type III (Sanfilippo syndrome) is subdivided into subtypes: subtype A is caused by heparan-N-sulfatase deficiency, subtype B by alpha-N-acetylglucosaminidase deficiency, subtype C by acetyl-CoA-alpha-glucosaminide acetyltransferase deficiency, and subtype D by N-acetylglucosamine-6-sulfatase deficiency [3].
- Type IV (Morquio’s syndrome) is subdivided into subtypes, where subtypes A and B are caused by N-acetylgalactosamine-6-sulfate-sulfatase deficiency and beta-galactosidase deficiency, respectively [4].
- Type VI (Maroteaux–Lamy syndrome) is associated with arylsulfatase B deficiency [5].
- Type VII (Sly’s syndrome) develops with glucuronidase deficiency [1].
- Type IX occurs in hyaluronidase deficiency [6].
All MPS types are characterized by progressive changes in the osteoarticular system. The pathogenesis involves excessive accumulation of non-degraded glycosaminoglycans, which leads to the activation of pro-inflammatory cytokines, apoptosis of chondrocytes, and secondary hyperplasia of the synovial membrane of the joints [7–9]. These metabolic and inflammatory changes are manifested by a typical clinical and radiological presentation [10].
In MPS, X-ray images present multiple dysostoses characterized by an anomaly in the formation of the osteoarticular system over time. Macrocephaly, clavicular expansion, paddle-like costal deformity, hypoplasia of the odontoid process of the second cervical vertebra, atlanto-axial instability, vertebral ventral deformity with lumbar kyphosis, anisospondylia (uneven height of the vertebrae in the craniocaudal direction), epiphyseal flattening, metaphyseal zone expansion, acetabular dysplasia, insufficient ossification of the acetabular rim and femoral heads, a change in the proportions between the iliac wing width and body (“Mickey Mouse symptom”), and valgus deformity of the femoral necks are observed [11].
Orthopedic manifestations of MPS also include stenosis of the cervical and thoracolumbar spine, progressive scoliosis, multiple contractures, joint subluxations and dislocations, axial limb deformities, and carpal tunnel syndrome [12].
MPS type IVB is rare, and >95% of identified cases of MPS type IV are subtype A [13]. This is probably due to the more “mild” phenotypic forms of MPS type IV and the complexity of their clinical diagnostics [14].
This study presents the diagnostic results of a patient with a rare form of MPS type IVB and sensorineural deafness, which was not associated pathogenetically with storage disease.
CLINICAL CASE
Patient K., 9 years old.
Complaints. The parents with a child born in 2011 (9 years old at the time of the initial visit) presented to an orthopedist with complaints of pain in the right hip joint and gait disturbance, which appeared about 1 week before the visit. They denied having had injuries. Previously, the child was diagnosed with grade IV sensorineural hearing loss, and a cochlear implant was installed at the age of 8 months.
Anamnesis vitae. Obstetric and gynecological history was not complicated (delivery 3, timely). Psychomotor development corresponded to the patient’s age. The patient has two older brothers, born in 2009 and 2003. The brother born in 2009 was diagnosed with grade IV sensorineural hearing loss, and a cochlear implant was installed in 2011. The middle brother had no history of complaints of gait disturbance and pain. GJB2 mutations, which are the most common cause of hereditary hearing loss, were ruled out. The older brother (born in 2003) had hearing and musculoskeletal complaints and had no chronic diseases. The genealogy of the family is presented in Fig. 1 (the child born in 2011 is marked in the family tree as the proband).
Fig. 1. Family tree of the proband. Generation I, white square and circle indicate the father and the mother, respectively; generation II, square 1 is the older brother born in 2003 without hearing loss, square 2 is the older brother born in 2009 with hearing loss, and square 3 with a black arrow is the examined patient with hearing loss (proband). MPS, mucopolysaccharidosis
During examination, the child was of normosthenic physique and had increased nutrition. A cochlear implant on the right was noteworthy. There was no prominent facial dysmorphism.
The gait was antalgic, with limping on the right lower limb, rotating it outwards. On examination, no signs of inflammatory changes were observed. Due to the pain syndrome, the range of motion in the right hip joint was limited, with flexion on the right and left of 100° and 120°, extension on the right and left of 0°–5° and 5°–10°, abduction on the right and left of 20° and 50°, adduction on the right and left of 15° and 25°, internal rotation on the right and left of 0° and 10°, and external rotation on the right and left of 40° and 50°, respectively. The intensity of the pain syndrome corresponded to 7 of 10 points according to the visual analog scale. A diagnosis of Legg–Calve–Perthes disease was presumably established.
From the anamnesis, gait disturbance appeared at the age of 6 years 10 months after an acute respiratory viral infection. There were no complaints of pain. By the time of treatment, the gait visually worsened, and pain was felt in the right hip joint, for which they turned to an orthopedist.
Diagnosis. The plain radiograph of the pelvic bones presented bilateral acetabular dysplasia and deformed femoral heads. According to the study, bilateral Legg–Calve–Perthes disease was confirmed.
The child was consulted in absentia by the staff of the H.I. Turner National Medical Research Center for Сhildren’s Orthopedics and Trauma Surgery due to the symmetry of the lesion and clinical presentation atypical for Legg–Calve–Perthes disease. The diagnosis of MPS was suggested. Radiography of the spine in the lateral view and hands and knee joints in the frontal view was recommended.
Lateral radiograph of the thoracolumbar spine showed changes in the shape of the vertebral bodies according to the type of tongue-shaped deformity, anisospondylia, paddle-like costal deformity, as well as hypoplasia of the odontoid process of the second cervical vertebra, atlanto-axial instability, and deformity of the ventral parts of the cervical vertebrae (Fig. 2).
Fig. 2. Radiographs of the cervical and thoracic spine: a, white arrows indicate expansion of the intercostal spaces, paddle-like costal deformity, and deformity of the ventral vertebrae; blue-dotted line indicates anisospondylia with an uneven height of the vertebrae in the craniocaudal direction; b, white line indicates hypoplasia of the odontoid process of the second cervical vertebra, black arrows indicate signs of atlanto-axial instability, and white arrows indicate deformity of the ventral cervical vertebrae
Radiographs of the hands and knee joints without significant changes (Fig. 3).
Fig. 3. X-ray images of the hands and knee joints in the frontal view
Moreover, the radiograph of the hip joints presents typical signs, as shown in Fig. 4.
Fig. 4. X-ray image of the hip joints in the frontal view: flattening and impaired ossification of the epiphyses (blue arrow), expansion of the metaphyseal zones, acetabular dysplasia (blue angle), insufficient ossification of the edge of the acetabulum and femoral heads (red arrow), change in the proportions between the width of the wings and body of the ilium (Mickey Mouse sign) (black arrows), valgus deformity of the femoral necks (red line), and discontinuity of Shenton’s line (yellow lines)
In connection with the clinical and radiological presentation, enzymatic diagnostics (screening for lysosomal storage diseases) was performed at the Academician N.P. Bochkov Medical Genetic Research Center (Moscow). The results revealed a decrease in the activity of the enzyme beta-D-galactosidase, which is a biochemical marker of MPS type IVB. The results of repeated tests also revealed a decrease in the activity of beta-D-galactosidase. In the brothers of the proband, no data of a decrease in the activity of lysosomal enzymes were obtained (Table).
Table. Results of the study of beta-D-galactosidase activity
Patient | Enzyme activity | Beta-D-galactosidase reference value | |
09.11.2020 | 24.02.2021 | ||
Proband born in 2011 | 0.72 | 0.4 | 2–30 nM/mL/h |
Brother born in 2009 | 3.43 | Not tested | |
Brother born in 2003 | 5.57 | Not tested | |
Owing to a decrease in beta-D-galactosidase activity, the proband underwent a complete analysis of GLB1 (NM_000404.3) by direct automatic sequencing and exome sequencing. In both cases, in exon 8 of GLB1, only one pathogenic variant c.808T>G (p.Tyr270Asp) in the heterozygous state was detected, which, given the autosomal recessive type of MPS type IVB inheritance, is not sufficient to establish a molecular genetic diagnosis. Genome sequencing was performed to search for the pathogenic variant 2 in the gene, and the analysis of GLB1 at the mRNA level was also conducted. According to the results of the genome sequencing in GLB1, in addition to the c.808T>G (p.Tyr270Asp) variant in the heterozygous state, data confirmed the insertion of a mobile genetic element from the class of retrotransposons. Subsequent functional analysis revealed that the insertion leads to impaired splicing of GLB1 and is probably a pathogenic variant [15]. The identified variants in the proband and its relatives were validated by direct automatic sequencing. The proband’s parents, as well as his brother (born in 2009), are heterozygous carriers of the detected variants (Fig. 1), whereas the proband has these variants in the compound heterozygous state.
Thus, the diagnosis of MPS type IVB in the proband was confirmed by biochemical and molecular genetic methods.
Since the proband and his brother (born in 2009) have grade IV sensorineural hearing loss, but type IVВ MPS was ruled out in the brother based on the results of biochemical and molecular genetic studies, additional analysis of exome sequencing data was performed to identify rare variants in the genes associated with isolated hearing loss.
Two rare variants not previously described in the literature were found in CDH23 (NM_022124.6). The variant 1 c.6992T>C (p.Val2331Ala) is absent from population databases, is in a highly conserved position, and according to the ACMG classification is regarded by the laboratory that conducted the study as a variant of undefined value. Variant 2 c.805C>T (p.Arg269Trp) is present in databases, with a very low frequency, and is regarded as an undefined value variant. Pathogenic variants in CDH23 can be homozygous and compound heterozygous in patients with autosomal recessive deafness type 12 and in patients with Usher syndrome type 1D. Moreover, the patient did not have retinitis pigmentosa, which is characteristic of Usher syndrome, but had severe preverbal hearing loss, which confirmed the diagnosis.
During the validation of these variants by direct automatic sequencing, these variants were noted in the compound heterozygous state in the proband and his brother (born in 2009) and in the heterozygous state in their parents. Having received additional criteria for pathogenicity for these variants, we classified them according to ACMG as probably pathogenic and established a molecular genetic diagnosis of autosomal recessive deafness type 12 associated with CDH23.
Thus, detailed molecular genetic, clinical, radiological, and biochemical studies enabled us to diagnose two rare genetic diseases, MPS type IVB and CDH23-associated neurosensory deafness.
DISCUSSION
Mucopolysaccharidoses are a group of rare diseases related to lysosomal storage diseases. The first case of MPS was described by Charles Hunter in 1917 [16].
The epidemiology of MPS demonstrates racial and ethnic characteristics in relation to the predominance of one type or another in the population [17]. Thus, in a study conducted from 1984 to 2004 in Taiwan, the total prevalence of MPS was 2.04 per 100,000 live births. Moreover, MPS type II occurred in 52% of cases, type I in 6.0%, type III in 19.0%, type IV in 16%, and type VI in 7.0%. In a Chinese study of 2006–2012 data, type II was also the most common (47.4%), followed by type IVA (26.8%) and type I (16.3%) [18, 19].
According to an American study of 1995–2005 data, MPS type I accounts for 31.7% of cases, type II for 28.3%, type III for 24.2%, type IV for 7.5%, and type VI for 4.2% [20]. In a Canadian study (1969–1996), the proportion of MPS type I was 30%; type IV, 20%; type VI, 15%; type III, 15%; and type II, 5% [21].
Quite often, different MPS types are associated with sensorineural and conductive hearing loss. Thus, MPS type I is characterized by hearing loss in 76.2%–100% of patients [22]. Progressive sensorineural and mixed-type hearing loss has been described in 67.3%–94.0% of patients with MPS type II [23]. Few studies have been conducted regarding the analysis of hearing in patients with MPS type III (A, B, C, and D). This is due to the complexity of audiological screening in this category of patients due to severe cognitive impairment [24]. The degree of hearing loss correlates with the disease subtype, as with MPS type IIID, hearing loss was registered in 25% of patients and in 100% of cases with subtype B [25, 26]. In MPS type IV, hearing loss is associated with subtype A (67.0%–94.0% of patients) [27–29]. Patients with type VI are characterized by conductive hearing loss due to recurrent acute otitis media [30]. In one study, which included 56 patients with MPS type VII, sensorineural hearing loss was detected in 41% of the cases [31]. To date, only four patients with MPS type IX have been described, and none of them had hearing loss [6, 32].
The uniqueness of this clinical case is related to the presence of grade IV sensorineural hearing loss, which is not associated with lysosomal storage diseases. According to the literature, MPS type IVB has not been associated with hearing loss; therefore, another cause of hearing loss in the patient was suspected. Moreover, the proband’s brother also has grade IV sensorineural hearing loss; however, he had no clinical and laboratory data of MPS.
In our case, the pathogenic variant c.808T>G in GLB1 was obtained from the father, and the insertion in the same gene was inherited from the mother, i.e., these variants were detected in the proband in the compound heterozygous state, which determined the clinical presentation of MPS type IVB. Regarding hearing loss, the proband and his brother (born in 2009) inherited both variants, c.6992T>C (p.Val2331Ala) and c.805C>T (p.Arg269Trp) from their mother and father, respectively, which is consistent with the clinical presentation.
Differential diagnostics was primarily performed in bilateral Legg–Calve–Perthes disease. Symmetrical bilateral process, pathognomonic changes in the acetabulum and femoral heads [acetabular dysplasia, insufficient ossification of the acetabular rim and femoral heads, disproportion between the width of the wings and body of the ilium (Mickey Mouse symptom), and valgus deformity of the femoral necks], and a clinical presentation atypical for of Legg–Calve–Perthes disease enabled us to suspect MPS [33].
CONCLUSION
Timely diagnosis of lysosomal storage diseases, including MPS, is necessary for early enzyme replacement therapy, which currently exists for MPS types I, II, IVA, VI, and VII. At an early disease stage, transplantation of hematopoietic stem cells (MPS types I, II, VI, and VII) is also used.
Orthopedic manifestations such as multiple ligamentitis of the hand joints, joint contractures, pathognomonic changes in the epiphyses, and an atypical form of bilateral Legg–Calve–Perthes disease should alert physicians about the presence of MPS.
The determination of enzyme activity in dried blood stains is the simplest and minimally invasive method for diagnosing these diseases, which does not require special training of the patient and medical personnel.
ADDITIONAL INFORMATION
Funding. The study had no external funding.
Conflict of interest. The authors declare no conflict of interest.
Ethical considerations. Written informed consent was obtained from the parents of the proband to conduct molecular genetic testing of blood samples and to publish anonymously the study results.
Author contributions. V.M. Kenis performed clinical diagnostics and edited the text. L.V. Gorobets and A.Yu. Dimitrieva performed clinical diagnostics, literature analysis, and wrote the text. A.A. Zhmurova-Kriventsova wrote the text. I.O. Bychkov performed molecular genetic and functional analysis and edited the text. G.V. Baydakova and E.Yu. Zakharova performed biochemical analysis and edited the text. T.V. Markova edited the text.
All authors made a significant contribution to the study and preparation of the article, read and approved the final version before its publication.
About the authors
Vladimir M. Kenis
H. Turner National Medical Research Center for Children’s Orthopedics and Trauma Surgery
Email: kenis@mail.ru
ORCID iD: 0000-0002-7651-8485
SPIN-code: 5597-8832
Scopus Author ID: 36191914200
ResearcherId: K-8112-2013
MD, PhD, Dr. Sci. (Med.), Professor
Russian Federation, Saint PetersburgLeonid V. Gorobets
Clinical and diagnostic center “Zdorovoe detstvo”
Email: gorobetsleonid@gmail.com
ORCID iD: 0000-0001-9424-3713
MD, traumatologist-orthopedist
Russian Federation, Rostov-on-DonAlena Yu. Dimitrieva
H. Turner National Medical Research Center for Children’s Orthopedics and Trauma Surgery
Author for correspondence.
Email: aloyna17@mail.ru
ORCID iD: 0000-0002-3610-7788
SPIN-code: 7112-8638
Scopus Author ID: 57194179597
ResearcherId: AGO-2659-2022
MD, PhD, Cand. Sci. (Med.)
Russian Federation, Saint PetersburgAlisa A. Zhmurova-Kriventsova
Clinic of the evidence-based medicine “Umka Family”
Email: alice.kriventsova@gmail.com
ORCID iD: 0000-0002-8257-2680
MD, neurologist
Russian Federation, Rostov-on-DonIgor O. Bychkov
Research Centre for Medical Genetics
Email: bychkov.nbo@gmail.com
ORCID iD: 0000-0002-6594-6126
Scopus Author ID: 57201638845
ResearcherId: J-6421-2018
MD, PhD, Cand. Sci. (Med.)
Russian Federation, MoscowGalina V. Baydakova
Research Centre for Medical Genetics
Email: labnbo@yandex.ru
ORCID iD: 0000-0001-8806-5287
Scopus Author ID: 25622266400
PhD, Cand. Sci. (Biol.)
Russian Federation, MoscowTatiana V. Markova
Research Centre for Medical Genetics
Email: markova@med-gen.ru
ORCID iD: 0000-0002-2672-6294
SPIN-code: 4707-9184
Scopus Author ID: 57204436561
ResearcherId: AAJ-8352-2021
MD, PhD, Cand. Sci. (Med.)
Russian Federation, MoscowEkaterina Yu. Zakharova
Research Centre for Medical Genetics
Email: doctor.zakharova@gmail.com
ORCID iD: 0000-0002-5020-1180
SPIN-code: 7296-6097
Scopus Author ID: 7102655877
ResearcherId: K-3413-2018
MD, PhD, Dr. Sci. (Med.), Professor
Russian Federation, MoscowReferences
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