
ORIGINAL ARTICLE

Evaluation of renal osteodystrophy in the dental clinic
by assessment of mandibular and phalangeal cortical indices

Bruna Corrêa Massahud1
• João César Guimarães Henriques1

• Reinhilde Jacobs2
•

Rafaela Rangel Rosa3
• Caio Vinı́cius Bardi Matai3

Received: 12 April 2017 / Accepted: 20 June 2017 / Published online: 4 September 2017

� Japanese Society for Oral and Maxillofacial Radiology and Springer Japan KK 2017

Abstract

Objectives Secondary hyperparathyroidism (SHPT) is a

disease that affects patients with chronic kidney disease,

and is characterized by mineral disturbance and bone loss,

known as renal osteodystrophy. The aim of this study was

to assess the validity of using intraoral phosphor storage

plates to take radiographs of the middle phalanges to

evaluate bone loss resulting from SHPT during follow-up

of these patients.

Methods The sample consisted of 24 patients with chronic

kidney disease, 12 with parathyroid hormone (PTH) levels

C500 pg/ml, and 12 with PTH levels \500 pg/ml, who

underwent hemodialysis weekly. For each patient, a

panoramic radiograph and digital radiographs of the ring,

index, and middle fingers of both hands were taken. The

Mandibular Cortical Index (MCI) and the Trabecular Bone

Pattern Index (TBP) were applied to the panoramic radio-

graphs, while the Phalangeal Cortical Index (PCI) was

applied to the digital radiographs of the phalanges. Three

evaluators performed all analyses.

Results Significant correlations were found between the

PTH levels and the MCI (p = 0.023), the PCI (p = 0.039)

and the TBP index (p = 0.032). These parameters were

also significantly interrelated (MCI 9 PCI = 0.001;

MCI 9 TBP = 0.004 and PCI 9 TBP = 0.009). The PCI

was shown to have the highest correlation with PTH levels.

Conclusion In patients with chronic renal disease, it is

clinically relevant to use panoramic and digital radiographs

using intraoral storage plates to assess a number of quan-

titative parameters that can be linked to PTH levels.

Keywords Chronic kidney disease � Secondary
hyperparathyroidism � Renal osteodystrophy � Dental
radiography � Phalanges of the fingers

Introduction

Secondary hyperparathyroidism (SHPT) is a disease char-

acterized by an increase in parathyroid hormone (PTH)

resulting from reduced excretion of phosphorous and

diminished secretion of the active form of vitamin D

(calcitriol), resulting in hypocalcemia in patients with

chronic renal disease [1–5]. Generalized bone loss and the

mineral imbalance of calcium and phosphorous culminate

in so-called renal osteodystrophies and metastatic calcifi-

cations in these individuals [6–12].

The middle phalanges of the middle and index fingers

are the first bone sites to undergo the osteoporotic pro-

cesses resulting from SHPT [9, 13–20]. Recently, a marked

correlation was demonstrated between PTH levels and the

state of resorption of the middle phalanges of the middle

and index fingers of the right and left hands, by means of

applying the Phalangeal Cortical Index (PCI) to hand and

wrist radiographs [7, 8]. Furthermore, a direct correlation

was demonstrated between the osteoporotic action of SHPT

in the cortical bone of the middle phalanges of the hands

& João César Guimarães Henriques

joaocesarhenriques@yahoo.com.br

1 Diagnosis and Stomatology Department, Universidade

Federal de Uberlândia, Avenida Pará, 1720. Bloco 2G, Sala

08. Bairro Umuarama, Uberlândia, Minas Gerais 38405-320,

Brazil

2 Oral Imaging Center, Katholieke Universiteit Leuven,

Kapucijnenvoer 7, 3000 Louvain, Belgium

3 Faculdade de Odontologia, Campus de São José dos Campos,

Universidade Estadual Paulista Julio de Mesquita Filho,

Avenida Engenheiro Francisco José Longo, No. 777-Bairro:

Jardim São Dimas, São Paulo 12245-000, Brazil

123

Oral Radiol (2018) 34:172–178

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and that occurring in the basal cortex of the mandible,

evaluated by means of the Mandibular Cortical Index

(MCI) [9–11].

The main aim of this study was to assess the clinical

applicability and diagnostic value of using intraoral phos-

phor storage plates to take radiographs of the phalanges of

the hand to evaluate bone loss resulting from SHPT. In

countries with limited healthcare access, screening for

diseases with the use of digital radiographs in the dental

clinic may help in directing affected subjects to the

appropriate primary care.

Materials and methods

This research was approved by the Research Ethics Com-

mittee of Federal University of Uberlândia (Protocol

112.646).

Subjects were selected from the clinical charts of 400

patients with chronic kidney disease and secondary

hyperparathyroidism, who were undergoing hemodialysis

in the hospital nephrology clinic. One evaluator approa-

ched the patients during their hemodialysis sessions, and 24

patients aged between 27 and 66 years agreed to participate

in the research after providing informed consent. The

subjects agreed to attend the dental, oral, and maxillofacial

imaging department of the university to undergo the nec-

essary examinations.

The PTH values of the subjects were measured and 2

groups were formed: 12 individuals with PTH levels

\500 pg/ml and 12 considered to have severe secondary

hyperparathyroidism, with PTH levels C500 pg/ml.

All patients underwent the following imaging exami-

nations conducted by the same radiologist: one panoramic

radiograph (Orthopantomograph OP 200 D; Instrumentar-

ium Oy, Tuusula, Finland) and four radiographs of the

middle phalanges of the index and middle fingers of both

hands, using size 2 phosphor storage plates for intraoral

imaging (VistaScan, Dürr Dental GmbH & Co. KG, Bie-

tigheim-Bissingen, Baden-Württemberg, Germany).

After a 14-day training period with a radiologist with

15 years of professional experience, three researchers were

calibrated for the observational task. They independently

and randomly applied the following evaluations to the

digital radiological images acquired:

1. Panoramic radiographs (70 KVp, 10–16 mAs) were

used to assess the Mandibular Cortical Index (Fig. 1)

[12] and the Trabecular Bone Pattern Index (TBP), a

qualitative parameter used to classify the mandibular

trabecular bone pattern as dense, heterogeneous,

sparse, or sparse with ground glass appearance

[8, 10, 11] (Fig. 2). The presence of soft tissue

calcifications and brown tumors was also evaluated

in the panoramic radiographs.

2. Digital radiographs with size 2 phosphor storage plates

for intraoral imaging were used to assess the PCI

applied to the middle phalanges of the index and

middle fingers of both hands. This index is correlated

with the MCI and is used to evaluate the cortical

osseous loss on the hand phalanges [7] (Fig. 3). The

patient placed the palm of each hand on a smooth flat

surface, and the phosphor storage plate was placed

over the middle phalanx. A paralleling technique was

applied with the X-ray cylinder (Time-X 70, Gnatus

Equipamentos Médico-Odontológico LTDA, Ribeirão

Preto, Brazil) positioned perpendicular to the sensor

handset with exposure parameters of 70 KVp/7 mA

and at a distance of approximately 20 cm (Fig. 4).

The degree of resolution of the radiographic images

obtained with the use of the intraoral phosphor plate sensor

was verified for the purpose of applying the PCI. The intra-

and inter-examiner agreement were verified by means of

the kappa coefficient. The Spearman’s correlation was used

to evaluate the correlation of the PTH levels with the

indices applied, and to evaluate the correlation between

these indices.

In addition, the frequency distribution of the different

grades of these indices was evaluated for both groups (PTH

\500 and C500 pg/ml).

Results

Digital radiographs taken with size 2 intraoral phosphor

storage plates provided sufficient coverage for visualiza-

tion of the middle phalanges of the index and middle fin-

gers. The images were of high resolution and detail,

allowing excellent precision for evaluating the PCI

(Fig. 2).

Inter-observer agreement was assessed by comparing

the results obtained by each of the three evaluators. Kappa

values (j) were 0.80 (p\ 0.01) for the MCI, 0.80

(p\ 0.01) for the PCI, and 0.81 (p\ 0.01) for the TBP.

Therefore, inter-examiner agreement was very favorable.

For the intra-examiner agreement, the j value was 0.90

(p\ 0.01).

The PTH levels of the subjects were significantly cor-

related with the MCI, PCI, and TBP (Table 1).

The frequency distribution tables for the MCI, PCI, and

TBC showed that the group with PTH values C500 pg/ml

had higher concentrations in the more severe classifications

of the indices when compared with the group with PTH

values\500 pg/ml (Tables 2, 3, 4).

Oral Radiol (2018) 34:172–178 173

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The results also showed a statistically significant cor-

relation (p\ 0.01) among the indices (Table 5).

In eight subjects (33%), additional calcified structures

were found on the panoramic radiographs. Panoramic

radiographic analysis revealed five subjects with carotid

atheromas (20%); six with tonsil calcifications (25%); three

with calcified lymph nodes (12.5%), and one with a

Monckeberg calcification (4%). Brown tumors were found

in two subjects (8%). All these abnormalities occurred in

patients with PTH values C500 pg/ml. Only one carotid

atheroma was found in the group with PTH values

\500 pg/ml. Only four patients (16%) with PTH values

C500 pg/ml had complete loss of the lamina dura, visual-

ized on the panoramic radiographs.

Fig. 1 The mandibular cortical

index (MCI) is a qualitative

parameter that classifies, by

bilateral inspection, the

morphological appearance of

the mandibular cortical bone

distal to the mental foramen as

normal cortex (C1), moderately

eroded cortex (C2), and severely

eroded cortex (C3)

Fig. 2 A subject presenting

with grade C3 Mandibular

Cortical Index (MCI) and a

Trabecular Bone Pattern Index

(TBP) qualitatively classified as

‘‘sparse with ground glass

appearance’’. Complete loss of

the lamina dura is also evident

174 Oral Radiol (2018) 34:172–178

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Discussion

Subperiosteal bone resorption of the middle phalanges of

the fingers has been recognized as the first radiographic

finding of bone loss resulting from hyperparathyroidism

and the marked increase in PTH levels [5, 8, 9, 18–21]. The

PCI uses hand and wrist radiographs to evaluate the

cortical morphology of the middle phalanges of patients

with chronic kidney disease and secondary hyperparathy-

roidism, and consists of three levels of severity (P1, P2, P3)

which correlate directly with increases in hormone levels

[7].

The present study is the first to substitute conventional

radiographs of the hand and wrist with size 2 digital

Fig. 3 The Phalangeal Cortical

Index (PCI): the left phalanx is

classified as P1 (normal cortex),

the central phalanx as P2

(moderately eroded cortex) and

the right phalanx as P3 (severely

eroded cortex)

Fig. 4 The size 2 intraoral phosphor storage plate covering the middle phalanx of the index finger (left). The same storage plate on the middle

finger (right)

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intraoral-computed radiographs of the finger phalanges,

resulting in better quality visualization of the details of

bone resorption resulting from the disease. In addition to

the improved quality of the digital intraoral films compared

with conventional radiographs of the hands and wrists,

dental health professionals have this radiographic equip-

ment readily available in the dental office environment.

Thus, this method is convenient and easy to perform in the

clinic. Additionally, when available, occlusal digital

intraoral film may be used with the advantage of requiring

a single exposure for irradiating the middle phalanges of

the index, middle, and ring fingers, reducing the need for a

second exposure (Fig. 5).

Our findings corroborate those of a previous study [7, 8]

that showed a high correlation of the PTH level with the

indices evaluated (MCI, PCI, and TBP), and good corre-

lation among these indices, showing how important are

these parameters to collaborate in the diagnosis process.

The group with PTH C 500 pg/ml displayed greater

severity of resorption, highlighting the extent to which the

increased level of PTH acts on bone resorption of the

phalanges and maxillary bones in patients with chronic

kidney disease.

We also observed a significant number of calcifications

in the panoramic radiographs, resulting from disturbances

in the calcium levels of patients as the disease progresses,

and associated with calcium supplement treatment to

replace the lost calcium [22–25]. Most of the calcifications,

apart from the complete loss of lamina dura and brown

tumor lesions, were found in the group with PTH levels

C500 pg/ml. This is consistent with the finding that higher

hormone levels are associated with more severe symptoms

of the disease.

Dental health professionals should be aware of the

serious consequences to patients of secondary hyper-

parathyroidism, and should add the rapid and simple pro-

cedure of using intraoral radiographs of the phalanges to

evaluate the PCI in the environment of the dental office.

This will contribute to the prompt diagnosis of renal

osteodystrophy triggered by the increase in hormone levels

present in this disease.

Within the limitations of the sample, we conclude that

the digital dental radiographs taken with the occlusal and

size 2 intraoral phosphor storage plates are well suited for

the correct evaluation of the PCI from the index, middle,

and ring fingers of patients with chronic kidney disease

affected by severe secondary hyperthyroidism.

The MCI, PCI, and TBC correlated with each other and

with the plasma PTH levels that, in turn, were shown to

increase as the level of these parameters increased.

Table 1 Spearman’s

correlation between PTH and

MCI, PCI and TBP variables

Variable Correlation p value

MCI 0.462 0.023

PCI 0.424 0.039

TBC 0.439 0.032

PTH parathyroid hormone, MCI

Mandibular Cortical Index, PCI

Phalangeal Cortical Index, TBP

Trabecular Bone Pattern Index

Table 2 Frequency distribution of MCI in the two groups

Group C1 C2 C3

PTH\ 500 pg/ml 10 2 0

PTH C 500 pg/ml 7 1 4

MCI Mandibular Cortical Index

Table 3 Frequency distribution of PCI in the two groups

Group F1 F2 F3

PTH\ 500 pg/ml 5 7 0

PTH C 500 pg/ml 5 3 4

PCI Phalangeal Cortical Index

Table 4 Frequency distribution of TBC in the two groups

Group Dense Heterogeneous Sparse Sparse with

ground glass

appearance

PTH\ 500 pg/

ml

4 8 0 0

PTH C 500 pg/

ml

5 1 2 4

TBP Trabecular Bone Pattern Index

Table 5 Spearman’s correlation between MCI, PCI, and TBC

Correlation p value

MCI vs PCI 0.624 0.001

MCI vs TBP 0.570 0.004

PCI vs TBP 0.524 0.009

MCI Mandibular Cortical Index, PCI Phalangeal Cortical Index, TBP

Trabecular Bone Pattern Index

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Acknowledgements This research was conducted with financial

assistance from the Research Support Foundation of the State of

Minas Gerais—FAPEMIG.

Compliance with ethical standards

Conflict of interest Authors Bruna Corrêa Massahud, João César

Guimarães Henriques, Reinhilde Jacobs, Rafaela Rangel Rosa and

Caio Vinı́cius Bardi Matai declare that they have no conflict of

interest.

Human rights statements All procedures followed were in accor-

dance with the ethical standards of the responsible committee on

human experimentation (institutional and national) and with the

Helsinki Declaration of 1975, as revised in 2008.

Informed consent Informed consent was obtained from all patients

for being included in the study.

Animal rights statement This article does not contain any studies

with animal subjects performed by any of the authors.

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	Evaluation of renal osteodystrophy in the dental clinic by assessment of mandibular and phalangeal cortical indices
	Abstract
	Objectives
	Methods
	Results
	Conclusion

	Introduction
	Materials and methods
	Results
	Discussion
	Acknowledgements
	References