Dentomaxillofacial Radiographic Changes in a Group of Iranian Patients with End Stage Renal Disease Undergoing Hemodialysis

Discussion

A wide range of dentomaxillofacial complications have been reported as a result of chronic renal failure (CRF) or its treatment. Dental manifestations include delayed eruption of permanent teeth in children with CRF, enamel hypoplasia in primary and permanent teeth, loss of lamina dura, widening of periodontal ligament, severe periodontal destruction, tooth mobility, and calcification or narrowing of dental pulp. Oral malodor, dry mouth, taste change, increased caries incidence, calculus formation, and gingival bleeding are the common oral manifestations (12). A range of bony anomalies can develop in chronic renal disease, which reflects the defect in calcium metabolism including hyperphosphatemia, hypocalcemia and resultant secondary hyperparathyroidism. Up to 92% of patients receiving hemodialysis are involved with secondary hyperparathyroidism. Orofacial features of CRF due to hyperparathyroidism include bone demineralization, ground glass appearance of bone, decrease thickness of cortical bone, radiolucent giant cell lesions (brown tumours), abnormal bone healing after extraction, metastatic soft tissue calcifications, and jaw fracture (8). Very few studies have been done previously on the assessment of radiographic changes in the jawbones of ESRD patients and the data is limited (11).

Panoramic and/or periapical radiographs of seventy-four patients on permanent hemodialysis were evaluated in this study. The mandibular molar area was the best region for investigation of radiographic changes on panoramic radiograph, because of no superimposition of anatomic structures and more involvement of this area by osseous pathosis. Therefore, the three major changes including lamina dura, trabecular pattern and density changes were much more evident in the molar region, above the mandibular canal on panoramic image (3,10).

In the present study no brown tumor was found, which was similar to Rani's study (10). Medeiros Queiroz et al. also reported the brown tumor only in one of 154 hemodialysis patients (5).

In hemodialysis patients of this study, the frequency of pulpal calcifications was 40%. In the study of Galili et al. (13) a significant pulp narrowing was shown in chronic renal disease patients compared with healthy control group. There is conflicting literature regarding by the presence of pulpal calcification and systemic disturbance. In the study of Patil and Sinha, 33.92% of the ESRD patients had pulp stones, but no significant relationship was found between the presence of the pulpal calcification and carotid artery calcifications (CAC) in the ESRD patients who were on haemodialysis (14). Similar findings were observed in the Kansu et al. study (15). In fact, the diversity and complexity of etiological factors of pulpal calcification (like long-standing local irritants, aging, idiopathic factors, fluoride supplementation, hypervitaminosis D or a genetic predisposition) make it very difficult to determine the specific aetiology in any particular patient (15).

In this study, the frequency of partial loss of the lamina dura was 25.7 percent, and complete or nearly complete loss of lamina dura were observed in the 25.7 percent of reviewed cases (51.4% of patients revealed lamina dura changes). In a study by Kelly, 45% of people showed partial loss of lamina dura while a complete or nearly complete loss of lamina dura were observed in only 8% (53% of patients revealed lamina dura alterations) (3). However in Rani's study, these changes were seen in 70% of dialysis patients (10). Rivas in a study using 29 panoramic radiographs of dialysis patients stated that lamina dura completely disappeared in 74 percent (16). Amann and Uthman (18) in a review of 10 patients, reported the loss of lamina dura, in 60% of patients. These differences in the prevalence may be due to differences in the number of patients, underlying etiologic condition of renal failure, treatment modalities and duration of their treatment. Pugh considered this phenomenon as a manifestation of subperiosteal resorption that is an indicator of hyperparathyroidism when it occurs in the last phalange (19). Some authors considered that loss of lamina dura is a first detectable finding (19) while the others reported this as a late finding in renal osteodystorphy (20).

However, since the loss of lamina dura may occur in Paget's disease, Cushing's syndrome fibrous dysplasia, rickets and osteomalacia, it should not be considered pathognomonic feature of this disease (10). A similar change to the loss of lamina dura, is radiographic cortical loss in the inferior border of the mandible, mandibular canal, alveolar crest, palatal suture, nasal floor and sinus wall (21,22). In this study, we were not looking specifically for these changes.

Three radiographic trabecular patterns of facial bone are attributed to hyperparathyroidism although these facial skeletal changes are uncommon. The classic form is termed “osteitis fibrosacystica” including increased bone cell activity, peritrabecular fibrosis, and brown tumors. Radiographically, this form appears with a combination of cortical thinning of multiple bones, coarsened trabecular patterns, osteolytic lesions, and “salt-and-pepper” appearance of the skull, which is the result of mixed osteolytic and sclerotic bone. The second form is a classic ground glass pattern, similar to fibrous dysplasia. But unlike true fibrous dysplasia, this finding can be diffuse and generalized, with poor corticomedullary distinction, an imaging finding not present in fibrous dysplasia. The third and the rarest form is uremic leontiasisossea which is characterized by significant hypertrophy of the jaws with serpiginous tunneling or channeling within the bone and poor visualization of the cortical bone. The cause of this unusual structure is not known; and the radiographic findings could not be explained with any specific microscopic changes (23).

In the present study, trabecular changes were revealed in 40.6% of patients. Among these, 8.1% (n=6) had delicate and finely intertwined trabecular pattern, 3 patients (4.1%) represented complete loss of normal trabeculation, granular or almost homogeneous pattern, 19 patients (25.7%) showed some mild coarse trabeculae, and 2.7% (n=2) showed coarse whole trabecular pattern. In the Kelly study (3), thin, delicate and finely intertwined trabeculation was seen in 37% of patients, Among these 8% revealed complete loss of normal trabeculation, granular or almost homogeneous pattern. Differences in the reported percentages could be due to variation in the number of subjects, observer disagreement, and the differences in the study design.

It is notable that renal osteodystrophy is a range between low turnover bone disease such as osteomalacia, and high turnover bone disease, like severe secondary hyperparathyroidism. Patients at both ends of the spectrum of bone turnover in renal osteodystrophy may represent the same bone mineral density on densitometry. Low bone mineral density may reflect inadequate mineralization as seen in osteomalacia or increased peritrabecular fibrosis as seen in secondary hyperparathyroidism. High bone mineral density readings on densitometry may capture extraosseous calcifications, which are frequently seen in chronic renal disease (24).

About the relation of radiographic changes with serum parameters in the present study, we revealed a relation between trabecular bone changes and serum P, and also bone density changes and ALP. Alteration in lamina dura showed a relation with iPTH, P and ALP, but not with Ca. However, in Rani's study, the relation between the radiographic changes and Ca, P, and ALP levels did not show significance (10). In the study of Medeiros Queiroz et al. (5), no significant correlation was observed between dialysis duration and also biochemical changes with radiographic bone alterations in the patients with chronic kidney disease undergoing dialysis (5). However, the radiographic alterations that were evaluated in this article were different from our study, and consisted of calculus, tooth decay, bone loss, residual roots, impacted teeth, diffuse or circumscribed bone rarefaction and bone sclerosis. Furthermore, the differences in the study design, the patients' medications, their clinical and paraclinical status, and ethnic variations could be the factors of discrepancy between studies.

Although, an appropriate sampling method was considered for this study, our findings may be limited because of the difference in etiologic underlying conditions of renal failure in our patients, and also impossibility to perform drug assessment accurately. Some of our patients were given supplements of calcium, but the majority of them were from a low economic background, so their supplements use was irregular. This might be also one of the contributing factors for lack of a correlation between calcium levels and bone changes in this study. According to our results, we could not establish a definitive relation of radiographic manifestations in ESRD patients with the duration and frequency of dialysis. We suggest further longitudinal studies to assess the influence of hemodialysis state on maxillofacial radiographic features along with the biochemical serum markers over duration of time so as to validate the influence of duration of dialysis therapy on radiographic and dental health.

Conclusion

ESRD patients undergoing hemodialysis show various degrees of changes in jaw radiographic pattern. Nevertheless, none of these changes had relation with calcium level. Annual radiographic evaluation is recommended to assess the progress of the insufficiency or reversal of the changes after therapy.

Acknowledgement

The authors have no financial interests related to the materials in the manuscript. This study fully funded by Dental school of Hamadan University of Medical Sciences in Hamadan, Iran.