- Email: [email protected]
Green teeth resulting from neonatal hyperbilirubinemia: Report of a case
pediatria polska 90 (2015) 155–160
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.elsevier.com/locate/pepo
Case report/Kazuistyka
Green teeth resulting from neonatal hyperbilirubinemia: Report of a case Norma Suely Falcão de Oliveira Melo 1, Regina Paula Guimarães Vieira Cavalcante da Silva 2, Antonio Adilson Soares de Lima 1,* 1 2
Department of Stomatology, School of Dentistry, Universidade Federal do Paraná – UFPR, Curitiba-PR, Brazil Department of Pediatrics, School of Medicine, Universidade Federal do Paraná – UFPR, Curitiba-PR, Brazil
article info
abstract
Article history:
In general, cosmetic changes or painful disorders often lead parents to seek dental care
Received: 05.11.2014
for their children. Several systemic disorders in pediatric patients can produce dental
Accepted: 11.12.2014
alterations. One of the manifestations of these disorders is the elevated serum level of
Available online: 23.12.2014
bilirubin (hyperbilirubinemia), a product of hemoglobin degradation, which is deposited in mineralized and soft tissues. The aim of this article is to report a case of green teeth affecting all deciduous teeth in a 3-year-old girl. The patient was taken to see the dentist
Keywords: Hyperbilirubinemia
by their parents due to the presence of green pigmentation in the teeth. During birth, the
Dental enamel Deciduous teeth
mel pigmentation is permanent and occurred during the period of dental development.
Tooth discoloration
patient suffered a traumatic injury that resulted in hyperbilirubinemia. This kind of ena© 2015 Published by Elsevier Sp. z o.o. on behalf of Polish Pediatric Society.
Introduction Changes in the normal color of deciduous and permanent teeth may occur due to factors intrinsic or extrinsic. The intrinsic stains are changes in the color of the tooth related to systemic factors such as: genetic factors, birth defects, metabolic defects, prenatal care, infectious diseases, neurological disorders, endocrine, kidney, liver, nutritional deficiencies and poisoning that usually occurred during odontogenesis [1]. Moreover, the formation of the extrinsic stains on teeth occurs primarily from the remains of food, medicinal
substances and bacteria, which represent deposits, adhered to the enamel [2]. The intrinsic dental pigmentation is associated with a chemical active change in the tooth structure and it cannot be removed without changing the structure of the tooth. It can be caused by erythropoietic porphyria, fetal erythroblastosis, amelogenesis imperfecta, dental fluorosis, hyperbilirubinemia, decomposition of red blood cells and medications (tetracycline) [3]. Bilirubin, a breakdown product of heme, is normally excreted in the bile or further catabolized before excretion in the urine. Approximately 80% of bilirubin is derived from free hemoglobin resulting from hemocaterese. In this
* Corresponding author at: School of Dentistry – Department of Stomatology, Universidade Federal do Paraná – UFPR, Rua Prefeito Lothário Meissner 632, Jardim Botånico, 80170-210 Curitiba-PR, Brazil. Tel.: +55 41 33604050; fax: +55 41 33604134. E-mail address: [email protected] (A.A.S. de Lima). http://dx.doi.org/10.1016/j.pepo.2014.12.004 0031-3939/© 2015 Published by Elsevier Sp. z o.o. on behalf of Polish Pediatric Society.
156
pediatria polska 90 (2015) 155–160
physiological process, senescent red cells with approximately 120 days are destroyed by macrophages in the spleen, liver and bone marrow. Hyperbilirubinemia is a clinic condition characterized by an abnormal increase of bilirubin in the blood, which may result in jaundice. The jaundice is the clinical sign caused by the elevation of serum bilirubin levels and its deposition in the skin, sclera, mucous membranes and some organs (liver and kidneys). The deposition of this pigment in these tissues and organs produces a color ranging from yellow to black, passing through various shades of green [4]. All healthy neonates develop unconjugated hyperbilirubinemia during the first week of life, but 50% of these patients have jaundice, benign and transient in character [5]. Jaundice occurs when the liver fails to eliminate bilirubin produced by the body [6]. Severe neonatal hyperbilirubinemia carries a potential for permanent neurological impairment [7]. Furthermore, hyperbilirubinemia is associated with the development of changes in color of the teeth, known as green teeth [8]. These teeth do not show changes in their morphology. However, the green coloration considerably affects the esthetics of the affected tooth. The appearance of the dentition is of concern to a large number of people seeking dental treatment and the color of the teeth is of particular cosmetic importance [9]. The purpose of this report is to present a case of green teeth of the primary dentition in a 3-year-old Brazilian girl.
Fig. 2 – Lateral incisor, canine, and first primary molar with enamel hypoplasia and green pigmentation
A patient of 2 years was brought for consultation by the mother due to the presence of green teeth in the mouth. The intraoral examination showed the presence of anterior primary teeth with a green aspect. All deciduous teeth were affected. No other changes involving the oral soft tissues were observed. According to the story told by the mother, the teeth were erupting in the mouth with a discoloration. The pigment involved about 5/6 of the crown of the incisor teeth (Fig. 1). At 3 years of age, the child presented with the first primary molars with half of the crown pigmented (Fig. 2).
Furthermore, the tip of the cusp canine was also pigmented. The clinical crown of all teeth showed hypoplasia areas between the middle and incisal thirds (Fig. 2). The teeth of the lower arch also showed a green coloration on the crown (Fig. 3). At this time, the child has not had the eruption of the primary second molars. The upper and lower canines had green pigmentation in the incisal half of the crown. The pigmentation of the first primary molars reached ¾ of the crown. According to the presence of this green pigmentation in the crown of teeth, a diagnosis of green teeth associated with a systemic disorder has been established. The past medical history revealed that the child's mother was 28 years old and that she had consulted 4 times during the prenatal period. During pregnancy, the mother had a urinary tract infection that was treated with cephalexin. The mother was admitted in premature labor and premature rupture occurred an hour earlier. The child was born by cesarean section with difficult extraction. The indication for this type of delivery was due to dystocia progression. At birth, the child had been in gestation for 31 weeks and was weighing 1660 g. The cause of preterm birth was
Fig. 1 – Upper incisors showing discoloration and areas of enamel hypoplasia
Fig. 3 – Clinical appearance of green teeth in the lower arch
Report of a case
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premature rupture of membranes. After birth, the child proved to be hypotonic, cyanotic and did not cry. A cycle of positive-pressure ventilation and cardiac massage for recovery were made. In addition, she was intubated in the delivery room. The newborn had neonatal asphyxia and slow infusion. In addition, the child had tocotraumatism, anemia, bloating, and early sepsis. The child was treated with ampicillin, gentamicin, dopamine, furosemide, piperacillin, tazobactam, dopamine, dobutamine, fentanyl and metronidazole. A diagnosis of large lesion in subcapsular hepatic lobe was established and it was classified as grade II splenic laceration that was treated expectantly. Infection of the child was treated for 52 days and the child remained intubated (intubation) for 12 days due to apnea and surfactant administration. During her stay in the Intensive Care Unit, volume globular and bilirubin levels were investigated (Table I). Jaundice was diagnosed on the second day of life by yellowish discoloration of the skin during routine physical examination. The pathological jaundice was treated with phototherapy. The child had the same blood type (A positive) as the mother and received packed red blood cells. The child presented with hyperbilirubinemia for about 2 months. The mother was instructed on the importance of diet and oral hygiene was reinforced. As the green pigmentation affected the deciduous dentition and there was a possibility it could also occur in the permanent dentition, the child's mother was advised to return for follow-up dental. No cosmetic treatment has been established in affected tooth. As the child was premature, we observed a delayed eruption of deciduous teeth and consequently also in the permanent dentition.
Discussion Bilirubin is produced mainly by degradation of the hemoglobin of red blood cells, the final product of the catabolism of heme [6]. The clinical jaundice in newborns occurs when bilirubin levels in blood plasma reaches values between 5 and 7 mg/dL. Severe neonatal hyperbilirubinemia, when unmonitored or untreated, can progress to acute bilirubin encephalopathy [10]. Neonatal jaundice is one of the most common problems for newborn infants during the first weeks of life, affecting approximately 60–70% of term babies and almost all premature babies [11]. According to Shrestha et al. [13], the risk factors associated with preterm birth are: inadequate antenatal checkup (52%), maternal age <20 years (34.7%), antepartum hemorrhage (23.4%) and pregnancy induced hypertension (13.1%). Morbidities more commonly observed in preterm infants are: clinical sepsis (66.7%), hyperbilirubinemia (58.8%), birth asphyxia (26.8%) and hyaline membrane disease (23.5%) [12]. The patient in this case report showed the major health problems related to prematurity, especially sepsis, neonatal jaundice, and apnea. In this case, bilirubin was considered pathologic due to lesion in the subcapsular lobe resulting from tocotrauma. The levels of total bilirubin reached 30.58 mg/dL in the 18th day of life. According to Watanabe et al. [12], total bilirubin levels between 1.2 and 1.8 mg/dL are already capable of inducing pigmentation tooth. These authors have identified levels of bilirubin in deciduous teeth obtained from 2 patients with a history of severe liver dysfunction and hyperbilirubinemia. The teeth were histologically analyzed and bilirubin was extracted and quantified by spectrophotometry. Histological
Table I – Values of globular volume and levels of bilirubin of the patient Date
Globular volume
Direct bilirubin
Indirect bilirubin
Total bilirubin
June June June June June
18 19 20 21 22
16% 32.9% 33.6% 37.5% 35.2%
N N 9.29 mg/dL 9.29 mg/dL
N N 12.56 mg/dL 12.56 mg/dL
June 23 June 25 June 28 June 30 July 1 July 2 July 3 July 4 July 5 July 9 July 11 July 13 July 17 July 20 July 21 July 27
38.3% 32.2% 30.1% 41.0% 37.4% 36.0% 34.4% 34.0% 46.0% 43.9% 34.9% N 33.2% 30.9% N 26.0%
N N 3.27 mg/dL 3.27 mg/dL Absence of bilirubin in the partial examination of urine 11.97 mg/dL Jaundice++/4+ 11.55 mg/dL N N N N 20.25 mg/dL 21.12 mg/dL N N 10.6 mg/dL N N 9.14 mg/dL 10.46 mg/dL
8.11 mg/dL
20.08 mg/dL
23.25 mg/dL N N N N 8.08 mg/dL 9.46 mg/dL N N 4.02 mg/dL N N 1.67 mg/dL 5.35 mg/dL
11.70 mg/dL N N N N 28.33 mg/dL 30.58 mg/dL N N 14.68 mg/dL N N 10.81 mg/dL 15.18 mg/dL
N = sample not collected.
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analysis revealed a green line parallel to the incremental lines of dentin. These authors analyzed the deciduous canine of a child with a history of biliary atresia and congenital hyperbilirubinemia at birth that showed that the tooth were colored brown in the middle of the crown to half of the root. The other case was a boy of 7 years of age with a history of hemolytic anemia and hyperbilirubinemia at 18 months of life showed total bilirubin levels 20–60 mg/dL. The upper central incisors and lateral incisors had a change of color of green. Furthermore, this color change reached half incisal of the dental crown. These findings were similar to those observed in primary teeth of children of this report. The normal color of teeth is determined by the shades of blue, green and pink of the enamel and is reinforced by shades of brown or yellow dentin below. Metabolic diseases and systemic factors can affect the development of teeth and cause tooth discoloration, such as: alkaptonuria, erythropoietic porphyria congenital, amelogenesis imperfecta, dentinogenesis imperfecta, tetracycline stain, and congenital hyperbilirubinemia. However, the teeth do not show morphological changes [9]. The patient in this case report had green teeth and areas of enamel hypoplasia. Despite these changes, the teeth remained preserved in its form. The areas of enamel hypoplasia observed in the crown of the anterior teeth may be associated with systemic factors and intubation, because the child remained intubated for 12 days. The literature reveals that tracheal intubation in the neonatal period can cause enamel hypoplasia [14, 15]. The occurrence of hyperbilirubinemia in childhood is an important fact because the consequences of this systemic disorder can seriously compromise the color of teeth. The first report of case about green teeth associated with jaundice was performed by Weyers [16] in 1956. Since then, the dental literature shows some reports of patients who developed green teeth associated to neonatal hyperbilirubinemia [17–28]. It is known that the location and extent of pigmentation tooth corresponds to the period of tooth formation [28]. In this case report, the patient presented dental pigmentation in the crown of all deciduous teeth. These dental changes corresponded to the period when she was admitted to the Intensive Care Unit. Normally, deciduous tooth calcification process begins in the 4th month of intrauterine life and finishes 11 months after birth. The dental crown of incisors is completely formed 1 month after birth and the canines and molars after 6 months [29]. According to current knowledge, enamel mineralization proceeds in 2 steps. At first, ameloblasts secrete a protein matrix in which hydroxyapatite crystals are deposited up to a concentration of about 25%. In a second step, the enamel maturation, enamel matrix proteins are degraded and resorbed almost completely, while hydroxyapatite crystals grow in thickness, until the enamel attains a mineral content of about 95%. Consequences of this formation in 2 stages are also evident in the wisdom teeth showing crown pigmentation [30]. Enamel formation can be disrupted during the course of a systemic disorder, and all the teeth that form in this period may be marked by bands of enamel malformed. After healing of illness, the formation of normal enamel is restored again. Disorders induced by tetracycline or
bilirubin showed clinically the time of injury to the tooth germ by the incorporation of these substances to the enamel [12, 31]. In this case, the patient report presented different levels of pigmentation of deciduous teeth. The crowns of the central and lateral incisors were more affected as half of their crowns were affected. The pigmentation was observed involving only half of the crown of the molars. Moreover, canine teeth were the least affected. As calcification of the permanent dentition has its beginning from birth, the possibility of dental pigmentation affecting the permanent teeth, especially the first molar, has not been ruled out. High serum bilirubin levels favor the deposition of the product of hemoglobin degradation in many tissues, including soft tissue and mineralized tissues. When hyperbilirubinemia occurs during dental development, the teeth can develop a green color due to the bilirubin deposition. This intrinsic pigment keeps teeth permanently pigmented. The blood vessels of the dental follicle are the source of nutrients for the ameloblasts to synthesize the tooth enamel [32]. Thus, the pigmentation of the tooth is most likely the result of the pigment passing through the bloodstream to ameloblasts and, then, to the tooth enamel. Bilirubin is a yellow pigment. However, when this pigment undergoes oxidation it becomes a green pigment otherwise called biliverdin. In the past, it was believed that the accumulation of this pigment was responsible for the green teeth associated with hyperbilirubinemia. However, a study developed by Shibata et al. [33] proved that the green color comes from the accumulation of bilirubin and not of biliverdin. The correct diagnosis for the cause of dental discoloration is important as, invariably, it has a profound effect on treatment outcomes. According to Shibata et al. [33], the diagnosis of bilirubin pigmentation is usually based on a clinical history of jaundice combined with the green coloration. Therefore, it would seem reasonable that health care providers have an understanding of the etiology of tooth discoloration in order to diagnose and recommend a more appropriate treatment. Actually, cosmetic dentistry is presented as a source to meet the esthetic and functional wishes of patients and professionals. The tooth whitening is a technique used to solve the esthetics of discolored teeth. It can be performed for both vital and non-vital teeth. Various chemicals such as 35% hydrogen peroxide, carbamide peroxide and sodium perborate and others are employed [34]. In general, the esthetic result of whitening of natural teeth has a better result when compared to the restoration or resin crowns. In this case, the natural appearance of the enamel is more esthetic in relation to restorative materials. The first reports of tooth whitening in primary teeth indicate the use of carbamide peroxide 10% for treatment of dental fluorosis. This technique requires a high level of adherence of the patient and the esthetic result does not always guarantee long treatment time due to the limited life of these teeth [35]. Moreover, some adverse effects of the tooth whitening may occur, such as: the external root resorption and dentin sensitivity [36]. According to Lee et al. [37], the use in children and adolescents of some dental bleaching agents
pediatria polska 90 (2015) 155–160
containing carbamide shows that: (1) 1 in every 2–3 patients may experience tooth sensitivity and/or gingival irritation after bleaching treatment, which may be more traumatic an experience for children than adults; (2) depending on dose, duration, frequency, and route, studies indicate excessive exposure to peroxide can be potentially harmful; (3) degree of potential toxicity and harmful outcomes increases in those who overuse whiteners – a concern in teenagers; (4) careful case selection using stringent criteria is suggested for primary teeth whitening; (5) whitening in healthy adolescents is a case-by-case determination that must include the weighing of risks (oral health and age) vs benefits (improved esthetic perception). However, there are some options of treatment for green teeth in the permanent dentition, such as: composite veneers, crowns, esthetic facets and possibly bleaching [18, 19, 27].
[6]
[7]
[8]
[9]
[10]
[11]
Authors' contributions/Wkład autorów According to order.
Conflict of interest/Konflikt interesu
[12]
[13]
None declared. [14]
Financial support/Finansowanie None declared.
[15]
Ethics/Etyka [16]
The work described in this article has been carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans; EU Directive 2010/63/EU for animal experiments; Uniform Requirements for manuscripts submitted to Biomedical journals.
[17]
[18]
[19]
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bilirubinometry in newborns stratified by gestation age Arch Venez Pueric Pediatr 2007;70(2):39–46. McDonagh AF, Lightner DA. Like a shrivelled blood orange' – bilirubin, jaundice, and phototherapy. Pediatrics 1985;75 (3):443–455. Cheng SW, Chiu YW, Weng YH. Etiological analyses of marked neonatal hyperbilirubinemia in a single institution in Taiwan. Chang Gung Med J 2012;35(2):148–154. Sommer S, Magagnin K, Kramer PF, Tovo MF, Bervian J. Green teeth associated with neonatal hyperbilirubinemia caused by biliary atresia: review and case report. J Clin Pediatr Dent 2010;35(2):199–202. Watts A, Addy M. Tooth discolouration and staining: a review of the literature. Br Dent J 2001;190(6): 309–316. Hameed NN, Na' Ma AM, Vilms R, Bhutani VK. Severe neonatal hyperbilirubinemia and adverse short-term consequences in Baghdad, Iraq. Neonatology 2011;100 (1):57–63. American Academy of Pediatrics Subcommittee on Hyperbilirubinemia. Management of hyperbilirubinemia in the newborn infant 35 or more weeks of gestation. Pediatrics 2004;114(1):297–316. Watanabe K, Shibata T, Kurosawa T, Morisaki I, Kinehara M, Igarashi S, et al. Bilirubin pigmentation of human teeth caused by hyperbilirubinemia. J Oral Pathol Med 1999;28 (3):128–130. Shrestha S, Dangol SS, Shrestha M, Shrestha RP. Outcome of preterm babies and associated risk factors in a hospital. J Nepal Med Assoc 2010;50(180):286–290. Seow WK, Brown JP, Tudehope DI, O'Callagan M. Developmental defects in the primary dentition of low birth-weight infants: adverse effects of laryngoscopy and prolonged endotracheal intubation. Pediatric Dent 1984;6 (1):28–31. Johnsen D, Krejci C, Hack M, Fanaroff A. Distribution of enamel defects and the association with respiratory distress in very low birthweight infants. J Dent Res 1984;63:59–64. Weyers H. Development of green teeth (chlorodontia) in children with icterus gravis. Kinderarztl Prax 1956;24 (7):289–293. Zizlavský V, Tichá B. Green teeth as consequence of hyperbilirubinemia. Cesk Pediatr 1974;29(2): 102–103. Rosenthal P, Ramos A, Mungo R. Management of children with hyperbilirubinemia and green teeth. J Pediatr 1986;108 (1):103–105. Herbert FL, Delcambre TJ. Unusual case of green teeth resulting from neonatal hyperbilirubinemia. ASDC J Dent Child 1987;54(1):54–56. Guimarães LP, Silva TA. Green teeth associated with cholestasis caused by sepsis: a case report and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;95(4):446–451. Alto LA, Pomarico L, Souza IP, Janini ME. Green pigmentation of deciduous teeth: report of two cases. J Dent Child (Chic) 2004;71(2):179–182. Tjon A, Ten WE, Houwen RH. Green teeth. Arch Dis Child 2007;92(3):250. Amaral TH, Guerra CS, Bombonato-Prado KF, Silva FWGP, Queiroz AM. Tooth pigmentation caused by bilirubin: a case report and histological evaluation. Spec Care Dentist 2008;28(6):254–257. Naudi AB, Ammari AB, Fung DE. A report of 2 cases of green pigmentation in the primary dentition associated with cholestasis caused by sepsis. J Dent Child (Chic) 2008;75 (1):91–94.
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[25] Sommer S, Kramer PF, Magagnin K, Tovo MF. Unusual case of green pigmentation in human teeth resulting from neonatal hyperbilirubinemia. Gen Dent 2008;56(5):e21–e23. [26] Fernandes KS, Magalhães M, Ortega KL. Green Teeth. J Pediatr 2011;158(3):510. [27] Range H, Camy S, Cohen J, Colon P, Bouchard P. Dental treatment of an adult patient with a history of biliary atresia. Quintessence Int 2012;43(4):337–341. [28] Morisaki I, Abe K, Tong LS, Kato K, Sobue S. Dental findings of children with biliary atresia: report of seven cases. ASDC J Dent Child 1990;57(3):220–223. [29] Lunt RC, Law DB. A review of the chronology of eruption of deciduous teeth. J Am Dental Assoc 1974;89:872–879. [30] Schroeder HE. Orale Strukturbiologie. Entwicklungsgeschichte, Struktur und Funktion normaler Hart und Weichgewebe der Mundhöhle und des Kiefergelenks, 5th ed., Stuttgart: Thieme; 2000. [31] Franco KMD, Line SRP, Moura-Ribeiro MVL. Prenatal and neonatal variables associated with enamel hypoplasia in
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deciduous teeth in low birth weight preterm infants. J Appl Oral Sci 2007;15(6):518–523. Nanci A. Ten Cate's oral histology: development, structure, and function, 8th ed., St. Louis: Elsevier; 2008. Shibata T, Watanabe K, Oda H, Arisue M, Kurosawa T, Tohma M, et al. Experimental bilirubin pigmentation of rat dentine and its detection by a qualitative analytical method. Arch Oral Biol 1996;41(5):509–511. Campos SFF, Silva CRG, Cesar ICR, Rego MA. Technique of evaluation of darkening deciduous teeth by reflectance. Cienc Odontol Bras 2005;8(4):49–55. Brantley DH, Barnes KP, Haywood VB. Bleaching primary teeth with 10% carbamide peroxide. Pediatr Dent 2001;23 (6):514–516. Fugaro JO, Nordahl I, Fugaro OJ, Matis BA, Mjör IA. Pulp reaction vital bleaching. Oper Dent 2004;29(4):363–368. Lee SS, Zhang W, Lee DH, Li Y. Tooth whitening in children and adolescents: a literature review. Pediatr Dent 2005;27:362–368.
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.elsevier.com/locate/pepo
Case report/Kazuistyka
Green teeth resulting from neonatal hyperbilirubinemia: Report of a case Norma Suely Falcão de Oliveira Melo 1, Regina Paula Guimarães Vieira Cavalcante da Silva 2, Antonio Adilson Soares de Lima 1,* 1 2
Department of Stomatology, School of Dentistry, Universidade Federal do Paraná – UFPR, Curitiba-PR, Brazil Department of Pediatrics, School of Medicine, Universidade Federal do Paraná – UFPR, Curitiba-PR, Brazil
article info
abstract
Article history:
In general, cosmetic changes or painful disorders often lead parents to seek dental care
Received: 05.11.2014
for their children. Several systemic disorders in pediatric patients can produce dental
Accepted: 11.12.2014
alterations. One of the manifestations of these disorders is the elevated serum level of
Available online: 23.12.2014
bilirubin (hyperbilirubinemia), a product of hemoglobin degradation, which is deposited in mineralized and soft tissues. The aim of this article is to report a case of green teeth affecting all deciduous teeth in a 3-year-old girl. The patient was taken to see the dentist
Keywords: Hyperbilirubinemia
by their parents due to the presence of green pigmentation in the teeth. During birth, the
Dental enamel Deciduous teeth
mel pigmentation is permanent and occurred during the period of dental development.
Tooth discoloration
patient suffered a traumatic injury that resulted in hyperbilirubinemia. This kind of ena© 2015 Published by Elsevier Sp. z o.o. on behalf of Polish Pediatric Society.
Introduction Changes in the normal color of deciduous and permanent teeth may occur due to factors intrinsic or extrinsic. The intrinsic stains are changes in the color of the tooth related to systemic factors such as: genetic factors, birth defects, metabolic defects, prenatal care, infectious diseases, neurological disorders, endocrine, kidney, liver, nutritional deficiencies and poisoning that usually occurred during odontogenesis [1]. Moreover, the formation of the extrinsic stains on teeth occurs primarily from the remains of food, medicinal
substances and bacteria, which represent deposits, adhered to the enamel [2]. The intrinsic dental pigmentation is associated with a chemical active change in the tooth structure and it cannot be removed without changing the structure of the tooth. It can be caused by erythropoietic porphyria, fetal erythroblastosis, amelogenesis imperfecta, dental fluorosis, hyperbilirubinemia, decomposition of red blood cells and medications (tetracycline) [3]. Bilirubin, a breakdown product of heme, is normally excreted in the bile or further catabolized before excretion in the urine. Approximately 80% of bilirubin is derived from free hemoglobin resulting from hemocaterese. In this
* Corresponding author at: School of Dentistry – Department of Stomatology, Universidade Federal do Paraná – UFPR, Rua Prefeito Lothário Meissner 632, Jardim Botånico, 80170-210 Curitiba-PR, Brazil. Tel.: +55 41 33604050; fax: +55 41 33604134. E-mail address: [email protected] (A.A.S. de Lima). http://dx.doi.org/10.1016/j.pepo.2014.12.004 0031-3939/© 2015 Published by Elsevier Sp. z o.o. on behalf of Polish Pediatric Society.
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pediatria polska 90 (2015) 155–160
physiological process, senescent red cells with approximately 120 days are destroyed by macrophages in the spleen, liver and bone marrow. Hyperbilirubinemia is a clinic condition characterized by an abnormal increase of bilirubin in the blood, which may result in jaundice. The jaundice is the clinical sign caused by the elevation of serum bilirubin levels and its deposition in the skin, sclera, mucous membranes and some organs (liver and kidneys). The deposition of this pigment in these tissues and organs produces a color ranging from yellow to black, passing through various shades of green [4]. All healthy neonates develop unconjugated hyperbilirubinemia during the first week of life, but 50% of these patients have jaundice, benign and transient in character [5]. Jaundice occurs when the liver fails to eliminate bilirubin produced by the body [6]. Severe neonatal hyperbilirubinemia carries a potential for permanent neurological impairment [7]. Furthermore, hyperbilirubinemia is associated with the development of changes in color of the teeth, known as green teeth [8]. These teeth do not show changes in their morphology. However, the green coloration considerably affects the esthetics of the affected tooth. The appearance of the dentition is of concern to a large number of people seeking dental treatment and the color of the teeth is of particular cosmetic importance [9]. The purpose of this report is to present a case of green teeth of the primary dentition in a 3-year-old Brazilian girl.
Fig. 2 – Lateral incisor, canine, and first primary molar with enamel hypoplasia and green pigmentation
A patient of 2 years was brought for consultation by the mother due to the presence of green teeth in the mouth. The intraoral examination showed the presence of anterior primary teeth with a green aspect. All deciduous teeth were affected. No other changes involving the oral soft tissues were observed. According to the story told by the mother, the teeth were erupting in the mouth with a discoloration. The pigment involved about 5/6 of the crown of the incisor teeth (Fig. 1). At 3 years of age, the child presented with the first primary molars with half of the crown pigmented (Fig. 2).
Furthermore, the tip of the cusp canine was also pigmented. The clinical crown of all teeth showed hypoplasia areas between the middle and incisal thirds (Fig. 2). The teeth of the lower arch also showed a green coloration on the crown (Fig. 3). At this time, the child has not had the eruption of the primary second molars. The upper and lower canines had green pigmentation in the incisal half of the crown. The pigmentation of the first primary molars reached ¾ of the crown. According to the presence of this green pigmentation in the crown of teeth, a diagnosis of green teeth associated with a systemic disorder has been established. The past medical history revealed that the child's mother was 28 years old and that she had consulted 4 times during the prenatal period. During pregnancy, the mother had a urinary tract infection that was treated with cephalexin. The mother was admitted in premature labor and premature rupture occurred an hour earlier. The child was born by cesarean section with difficult extraction. The indication for this type of delivery was due to dystocia progression. At birth, the child had been in gestation for 31 weeks and was weighing 1660 g. The cause of preterm birth was
Fig. 1 – Upper incisors showing discoloration and areas of enamel hypoplasia
Fig. 3 – Clinical appearance of green teeth in the lower arch
Report of a case
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premature rupture of membranes. After birth, the child proved to be hypotonic, cyanotic and did not cry. A cycle of positive-pressure ventilation and cardiac massage for recovery were made. In addition, she was intubated in the delivery room. The newborn had neonatal asphyxia and slow infusion. In addition, the child had tocotraumatism, anemia, bloating, and early sepsis. The child was treated with ampicillin, gentamicin, dopamine, furosemide, piperacillin, tazobactam, dopamine, dobutamine, fentanyl and metronidazole. A diagnosis of large lesion in subcapsular hepatic lobe was established and it was classified as grade II splenic laceration that was treated expectantly. Infection of the child was treated for 52 days and the child remained intubated (intubation) for 12 days due to apnea and surfactant administration. During her stay in the Intensive Care Unit, volume globular and bilirubin levels were investigated (Table I). Jaundice was diagnosed on the second day of life by yellowish discoloration of the skin during routine physical examination. The pathological jaundice was treated with phototherapy. The child had the same blood type (A positive) as the mother and received packed red blood cells. The child presented with hyperbilirubinemia for about 2 months. The mother was instructed on the importance of diet and oral hygiene was reinforced. As the green pigmentation affected the deciduous dentition and there was a possibility it could also occur in the permanent dentition, the child's mother was advised to return for follow-up dental. No cosmetic treatment has been established in affected tooth. As the child was premature, we observed a delayed eruption of deciduous teeth and consequently also in the permanent dentition.
Discussion Bilirubin is produced mainly by degradation of the hemoglobin of red blood cells, the final product of the catabolism of heme [6]. The clinical jaundice in newborns occurs when bilirubin levels in blood plasma reaches values between 5 and 7 mg/dL. Severe neonatal hyperbilirubinemia, when unmonitored or untreated, can progress to acute bilirubin encephalopathy [10]. Neonatal jaundice is one of the most common problems for newborn infants during the first weeks of life, affecting approximately 60–70% of term babies and almost all premature babies [11]. According to Shrestha et al. [13], the risk factors associated with preterm birth are: inadequate antenatal checkup (52%), maternal age <20 years (34.7%), antepartum hemorrhage (23.4%) and pregnancy induced hypertension (13.1%). Morbidities more commonly observed in preterm infants are: clinical sepsis (66.7%), hyperbilirubinemia (58.8%), birth asphyxia (26.8%) and hyaline membrane disease (23.5%) [12]. The patient in this case report showed the major health problems related to prematurity, especially sepsis, neonatal jaundice, and apnea. In this case, bilirubin was considered pathologic due to lesion in the subcapsular lobe resulting from tocotrauma. The levels of total bilirubin reached 30.58 mg/dL in the 18th day of life. According to Watanabe et al. [12], total bilirubin levels between 1.2 and 1.8 mg/dL are already capable of inducing pigmentation tooth. These authors have identified levels of bilirubin in deciduous teeth obtained from 2 patients with a history of severe liver dysfunction and hyperbilirubinemia. The teeth were histologically analyzed and bilirubin was extracted and quantified by spectrophotometry. Histological
Table I – Values of globular volume and levels of bilirubin of the patient Date
Globular volume
Direct bilirubin
Indirect bilirubin
Total bilirubin
June June June June June
18 19 20 21 22
16% 32.9% 33.6% 37.5% 35.2%
N N 9.29 mg/dL 9.29 mg/dL
N N 12.56 mg/dL 12.56 mg/dL
June 23 June 25 June 28 June 30 July 1 July 2 July 3 July 4 July 5 July 9 July 11 July 13 July 17 July 20 July 21 July 27
38.3% 32.2% 30.1% 41.0% 37.4% 36.0% 34.4% 34.0% 46.0% 43.9% 34.9% N 33.2% 30.9% N 26.0%
N N 3.27 mg/dL 3.27 mg/dL Absence of bilirubin in the partial examination of urine 11.97 mg/dL Jaundice++/4+ 11.55 mg/dL N N N N 20.25 mg/dL 21.12 mg/dL N N 10.6 mg/dL N N 9.14 mg/dL 10.46 mg/dL
8.11 mg/dL
20.08 mg/dL
23.25 mg/dL N N N N 8.08 mg/dL 9.46 mg/dL N N 4.02 mg/dL N N 1.67 mg/dL 5.35 mg/dL
11.70 mg/dL N N N N 28.33 mg/dL 30.58 mg/dL N N 14.68 mg/dL N N 10.81 mg/dL 15.18 mg/dL
N = sample not collected.
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analysis revealed a green line parallel to the incremental lines of dentin. These authors analyzed the deciduous canine of a child with a history of biliary atresia and congenital hyperbilirubinemia at birth that showed that the tooth were colored brown in the middle of the crown to half of the root. The other case was a boy of 7 years of age with a history of hemolytic anemia and hyperbilirubinemia at 18 months of life showed total bilirubin levels 20–60 mg/dL. The upper central incisors and lateral incisors had a change of color of green. Furthermore, this color change reached half incisal of the dental crown. These findings were similar to those observed in primary teeth of children of this report. The normal color of teeth is determined by the shades of blue, green and pink of the enamel and is reinforced by shades of brown or yellow dentin below. Metabolic diseases and systemic factors can affect the development of teeth and cause tooth discoloration, such as: alkaptonuria, erythropoietic porphyria congenital, amelogenesis imperfecta, dentinogenesis imperfecta, tetracycline stain, and congenital hyperbilirubinemia. However, the teeth do not show morphological changes [9]. The patient in this case report had green teeth and areas of enamel hypoplasia. Despite these changes, the teeth remained preserved in its form. The areas of enamel hypoplasia observed in the crown of the anterior teeth may be associated with systemic factors and intubation, because the child remained intubated for 12 days. The literature reveals that tracheal intubation in the neonatal period can cause enamel hypoplasia [14, 15]. The occurrence of hyperbilirubinemia in childhood is an important fact because the consequences of this systemic disorder can seriously compromise the color of teeth. The first report of case about green teeth associated with jaundice was performed by Weyers [16] in 1956. Since then, the dental literature shows some reports of patients who developed green teeth associated to neonatal hyperbilirubinemia [17–28]. It is known that the location and extent of pigmentation tooth corresponds to the period of tooth formation [28]. In this case report, the patient presented dental pigmentation in the crown of all deciduous teeth. These dental changes corresponded to the period when she was admitted to the Intensive Care Unit. Normally, deciduous tooth calcification process begins in the 4th month of intrauterine life and finishes 11 months after birth. The dental crown of incisors is completely formed 1 month after birth and the canines and molars after 6 months [29]. According to current knowledge, enamel mineralization proceeds in 2 steps. At first, ameloblasts secrete a protein matrix in which hydroxyapatite crystals are deposited up to a concentration of about 25%. In a second step, the enamel maturation, enamel matrix proteins are degraded and resorbed almost completely, while hydroxyapatite crystals grow in thickness, until the enamel attains a mineral content of about 95%. Consequences of this formation in 2 stages are also evident in the wisdom teeth showing crown pigmentation [30]. Enamel formation can be disrupted during the course of a systemic disorder, and all the teeth that form in this period may be marked by bands of enamel malformed. After healing of illness, the formation of normal enamel is restored again. Disorders induced by tetracycline or
bilirubin showed clinically the time of injury to the tooth germ by the incorporation of these substances to the enamel [12, 31]. In this case, the patient report presented different levels of pigmentation of deciduous teeth. The crowns of the central and lateral incisors were more affected as half of their crowns were affected. The pigmentation was observed involving only half of the crown of the molars. Moreover, canine teeth were the least affected. As calcification of the permanent dentition has its beginning from birth, the possibility of dental pigmentation affecting the permanent teeth, especially the first molar, has not been ruled out. High serum bilirubin levels favor the deposition of the product of hemoglobin degradation in many tissues, including soft tissue and mineralized tissues. When hyperbilirubinemia occurs during dental development, the teeth can develop a green color due to the bilirubin deposition. This intrinsic pigment keeps teeth permanently pigmented. The blood vessels of the dental follicle are the source of nutrients for the ameloblasts to synthesize the tooth enamel [32]. Thus, the pigmentation of the tooth is most likely the result of the pigment passing through the bloodstream to ameloblasts and, then, to the tooth enamel. Bilirubin is a yellow pigment. However, when this pigment undergoes oxidation it becomes a green pigment otherwise called biliverdin. In the past, it was believed that the accumulation of this pigment was responsible for the green teeth associated with hyperbilirubinemia. However, a study developed by Shibata et al. [33] proved that the green color comes from the accumulation of bilirubin and not of biliverdin. The correct diagnosis for the cause of dental discoloration is important as, invariably, it has a profound effect on treatment outcomes. According to Shibata et al. [33], the diagnosis of bilirubin pigmentation is usually based on a clinical history of jaundice combined with the green coloration. Therefore, it would seem reasonable that health care providers have an understanding of the etiology of tooth discoloration in order to diagnose and recommend a more appropriate treatment. Actually, cosmetic dentistry is presented as a source to meet the esthetic and functional wishes of patients and professionals. The tooth whitening is a technique used to solve the esthetics of discolored teeth. It can be performed for both vital and non-vital teeth. Various chemicals such as 35% hydrogen peroxide, carbamide peroxide and sodium perborate and others are employed [34]. In general, the esthetic result of whitening of natural teeth has a better result when compared to the restoration or resin crowns. In this case, the natural appearance of the enamel is more esthetic in relation to restorative materials. The first reports of tooth whitening in primary teeth indicate the use of carbamide peroxide 10% for treatment of dental fluorosis. This technique requires a high level of adherence of the patient and the esthetic result does not always guarantee long treatment time due to the limited life of these teeth [35]. Moreover, some adverse effects of the tooth whitening may occur, such as: the external root resorption and dentin sensitivity [36]. According to Lee et al. [37], the use in children and adolescents of some dental bleaching agents
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containing carbamide shows that: (1) 1 in every 2–3 patients may experience tooth sensitivity and/or gingival irritation after bleaching treatment, which may be more traumatic an experience for children than adults; (2) depending on dose, duration, frequency, and route, studies indicate excessive exposure to peroxide can be potentially harmful; (3) degree of potential toxicity and harmful outcomes increases in those who overuse whiteners – a concern in teenagers; (4) careful case selection using stringent criteria is suggested for primary teeth whitening; (5) whitening in healthy adolescents is a case-by-case determination that must include the weighing of risks (oral health and age) vs benefits (improved esthetic perception). However, there are some options of treatment for green teeth in the permanent dentition, such as: composite veneers, crowns, esthetic facets and possibly bleaching [18, 19, 27].
[6]
[7]
[8]
[9]
[10]
[11]
Authors' contributions/Wkład autorów According to order.
Conflict of interest/Konflikt interesu
[12]
[13]
None declared. [14]
Financial support/Finansowanie None declared.
[15]
Ethics/Etyka [16]
The work described in this article has been carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans; EU Directive 2010/63/EU for animal experiments; Uniform Requirements for manuscripts submitted to Biomedical journals.
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