Postepy Hig Med Dosw. (online), 2010; 64: 659-664
Original Article
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Selected aspects of the oral environment in cleft palate patients - a problem evidently beyond dentists' scope
Wybrane aspekty środowiska jamy ustnej pacjentów z rozszczepem podniebienia - problem ewidentnie nie tylko stomatologiczny
Joanna AntoszewskaABCD, Beata KawalaD, Liwia MinchDEF
Department of Maxillofacial Ortopeadics and Orthodontics Wrocław
Corresponding author
Dr. Liwia Minch, Department of Maxillofacial Ortopeadics and Orthodontics, ul. Krakowska 26, 50-425 Wrocław; e-mail: liwiaminch@tlen.pl

Authors' Contribution:
A - Study Design, B - Data Collection, C - Statistical Analysis, D - Data Interpretation, E - Manuscript Preparation, F - Literature Search, G - Funds Collection

Received:  2010.09.17
Accepted:  2010.11.30
Published:  2010.12.27

Streszczenie
Wstęp: Jama ustna człowieka jest wyspecjalizowanym ekosystemem złożonym z uzębienia oraz błony śluzowej, poddawanych działaniu śliny i płynu dziąsłowego. Budowa tych struktur stwarza ko­rzystne warunki do osiedlania się różnych rodzajów drobnoustrojów zarówno tlenowych pacior­kowców jak i beztlenowych pałeczek. Dynamiczna równowaga ekosystemu jamy ustnej może być zagrożona różnymi czynnikami. Przykładem mogą być rozszczepy wargi i podniebienia - naj­częstsze zaburzenia w rozwoju embriologicznym twarzy. Celem pracy było ustalenie czy pozio­my bakterii Streptococcus mutans i Lactobacillus acidophilus oraz higiena jamy ustnej pacjentów z rozszczepem podniebienia leczonych ortodontycznie są istotnie różne niż w przypadku pacjen­tów bez tej wady rozwojowej.
Materiał/Metody:
Do badań wybrano 250 pacjentów w wieku 6-21 roku życia, których podzielono na grupy w za­leżności od występowania rozszczepu podniebienia i techniki leczenia. Grupę C (kontrolną) stanowiło 50 pacjentów z zaburzeniami zgryzowo-zębowymi nieleczonymi ortodontycznie. Przeprowadzone badania składały się z części kliniczno-laboratoryjnej i analizy statystycznej.
Wyniki:
Wewnątrzgrupowo duże stężenia bakterii Streptococcus mutans i Lactobacilus acidophilus w śli­nie badanych występowały porównywalnie często, natomiast istotne statystycznie różnice doty­czyły porównań międzygrupowych.
Wnioski:
Ponieważ leczenie ortodontyczne zmienia środowisko jamy ustnej, kontrola nawyków higienicz­nych jest podstawowym elementem w edukacji zdrowotnej. Niezwykle ważne jest też wprowa­dzanie programów prewencyjnych.
Słowa kluczowe: wskaźnik PI • wskaźnik GI • rozszczep wargi • rozszczep podniebienia


Summary
Introduction: The oral cavity is a specialized ecosystem composed of dentition and mucosa exposed to the ef­fects of saliva and gingival liquid. Its structure provides advantageous conditions for various mi­croorganisms, both aerobic streptococci and anaerobic bacilli. The dynamic balance of the oral cavity ecosystem can be threatened by various factors. Lip and palatal clefts are the most fre­quent disorders in embryonic facial development. The aim of the study was to evaluate whether Streptococcus mutans and Lactobacillus acidophilus and oral cavity hygiene in patients with cleft palate treated orthodontically are significantly different compared with patients without these con­genital malformations.
Material/Methods: The study group consisted of 200 patients aged 6-21 who were divided into two groups depen­ding on the presence of cleft palate and treatment method. Group C (control) consisted of 50 or­thodontically untreated patients with occlusal dental defects. The performed studies consisted of 2 parts: the clinical-laboratory part and statistical analysis. Clinical-laboratory part
Results: High bacteria levels of Streptococcus mutans and Lactobacillus acidophilus in saliva of patients were comparably frequent between groups, but there were statistically significant differences in inter-group comparisons.
Conclusions: As the orthodontic treatment changes the oral environment, control of proper hygienic behavior is an essential element of health education. Introduction of preventive programs is also very im­portant.
Key words: PI index • GI index • cleft palate • cleft lip




Introduction
The oral cavity is a specialized ecosystem composed of dentition and mucosa exposed to the effects of saliva and gingival liquid. Its structure provides advantageous condi­tions for various microorganisms, both aerobic streptococci existing in natural dentition grooves, and anaerobic bacil­li. Present knowledge about methods of intraoral micro­flora colonization in humans is rather limited. However, it is known that a few days after birth in the infant's oral ca­vity Streptococcus salivarius appears while Streptococcus sanguis correlates with the eruption of primary dentition. Their hard, non-scaling surfaces are conducive to coloni­zation of Streptococcus mutans, which plays a significant role in caries initiation. Streptococcus mutans colonizes the human oral cavity at the age of 7 to 24 months, i.e. during the eruption and presence of deciduous dentition (first in­fection period), and at the age from 6 to 12 years, i.e. du­ring the period of eruption and presence of permanent den­tition (second infection period). Thus a time of the child's life stands out when a child is less subject to colonization of the oral cavity by Streptococcus mutans, that is betwe­en eruption of the last deciduous tooth and the first perma­nent tooth. Transverse and review studies prove that mo­thers - Streptococcus mutans carriers - play a significant role in transferring these bacteria to the oral cavity of of­fspring and in caries development [1]. The main sites of colonization are the grooves and depressions of masticato­ry surfaces, seldom the facet [23]. Other places of micro­organisms' location in the oral cavity are contiguous surfa­ces and buccal/lingual surfaces of dental crowns, gingival clefts and the papilliform lingual surface.
In the oral cavity ecosystem, when functioning properly, pa­thogens are weakened by bacteriostatic and bactericidal pro­perties of salivary gland secretions. Saliva not only plays a mechanical role in microorganism removal but also it fights them actively with defensive factors (specific and non-speci­fic) such as: leucocytes, lysozyme, peroxidase and y-globulin. Saliva buffer (phosphate, carbonate and albumin) neutrali­zes acid products of bacterial metabolism, which allows the proper pH to be maintained for non-pathogenic, permanent microflora of the oral cavity. Local lowering of pH is a factor conducive to acid precipitation of saliva protein and organic stroma for bacterial plate formation. There are two types of saliva flow: highway and byway. The first type concerns fast, abundant saliva flow through the lingual surfaces of the lo­wer molars. The second type involves slow, scant saliva flow through the labial surfaces of the upper incisors. Slow saliva flow is conducive to localization of dental plaque, and incre­ased - in inflammatory gingival state - secretion rich with limestone ion of gingival pouch liquid can cause dental de­posits, forming another layer of organic matrix for future bac­terial colonization. Accumulation of polysaccharide - both bacterial (dextran) and nutritive (saccharose) - causes incre­ased concentration of microorganisms: Streptococcus mutans (Sm) and Lactobacillus acidophilus (Lb) with their proteoly­tic enzyme. Concretion is a source and place of varied bio­chemical processes whose products - with diminished sali­va secretion and a change of its natural composition or with supply of saccharic substratum [8,16,17] - induce caries and periodontal disease which retard the digestive system effect.
Knowledge of the presented physiological mechanisms, both bacterial colonization and immunological ones, allowed the creation of effective prophylactic methods for systemic dise­ases - contemporary rules of oral cavity hygiene. However, the dynamic balance of the oral cavity ecosystem can be threatened by various factors which most often act synergi­cally. Lip and palatal clefts are the most frequent disorders in embryonic facial development which arise in the first tri­mester, once in every 600-800 neonates. Disconnection of tissue continuity in alveolar and palatal clefts not only re­tards suction, swallowing and breathing function but also allows pathological migration of bacterial colonies betwe­en the oral and the nasal cavity. The risk to oral cavity mi­croflora balance is intensified by the necessity of occlusal disturbance treatment in patients with cleft palate because better developed appliances give more room for bacterial plate retention and block main saliva flow [15]. Alarming data from the literature show the scale of risk, with reten­tion of bacterial plaque in more than 50% of patients with cleft palates regardless of monthly tooth brushing training and detailed hygienic recommendations [2,3,18,19].
A particularly important question arises at the present time of contamination and environmental disturbances: whether microbiology and thus ecosystem physiology of the oral ca­vity changes in the case of anatomical disorders accompa­nying cleft palate? It can be a serious medical problem: the development risk of alimentary canal disorders resulting in caries and periodontosis with an unknown pathomechanism.
The aim of the study was to evaluate whether caries initia­ting bacteria (Streptococcus mutans) and caries developing ones (Lactobacillus acidophilus) as well as the oral cavi­ty hygiene in patients with cleft palate treated orthodon­tically are significantly different compared with patients without such congenital malformations.
Material and Methods
Study material
The study group comprised 200 patients aged 6-21 years chosen consecutively, based on the type of orthodontic approach (fixed or removable appliances) and cleft pala­te presence. Additionally, the control group C (50 indivi­duals) consisted of untreated patients with malocclusion and no cleft palate (Tab. 1).
Table 1. Group comparison of study material

Study methodology
The performed studies consisted of 2 parts: the clinical-laboratory part and statistical analysis.
Clinical-laboratory part
During the clinical phase, apart from case history taking and diagnosis, stating cleft extension on the basis of the topographic classification by Bardach and the anatomical one by Kernahan and Stark, and malocclusion, in artifi­cial lighting, with the use of a mirror and calibrated pro­be, the dental plaque level was studied. The indirect and direct study included teeth surfaces being in contact with elements of the appliance: brackets, arch wires, retainers, coil-spring, acrylic plate. Oral hygiene state was described by an indirect method with the plaque index (PlI) accor­ding to Löe and Silness [14] and by a direct method using the gingival index (GI) according to Silness and Löe [21]. The plaque index was used to estimate the layer thickness of dental plaque on selected dental surfaces. Evaluation cri­teria were as follows: 0. lack of plate; 1. thin layer of plate adjacent to gingival margin and cervical zone but invisi­ble to the naked eye; 2. moderate plaque deposits on gin­gival edge and on tooth surface and gingival pouch visible to the naked eye; 3. abundant plaque deposits in a pocket and/or on gingival edge and tooth surface.
Qualitative changes of gingival state were assessed on a 4-grade scale, the gingival index (GI): 0. healthy gingiva, rose colored; 1. mild inflammation, slight change in gingival color, lack of bleeding on probing; 2. moderate inflamma­tion: redness, swelling, gloss and gingival overgrowth, ble­eding with pressure or on probing; 3. severe inflammation: considerable redness and gingival swelling, ulceration, ten­dency to independent bleeding. Common level values for both indices were stated: low - not exceeding 1, average - more than 1 and not exceeding 2, and high - more than 2.
In order to evaluate halitosis - unpleasant odor of the oral cavity made by bacteria metabolizing volatile sulfur com­pounds - deposits from the dorsum of the tongue were ta­ken with layer and were evaluated using a value scale as follows: 0. lack of odor, 2. mild odor (imperceptible from a distance of 3 cm), 3. strong odor (perceptible from a di­stance of 3 cm).
After performing clinical and survey studies, from patients with the highest and the lowest plaque index values, sali­va specimens were collected in order to determine the pre­sence of Streptococcus mutans (Sm) and Lactobacillus acidophilus (Lb). In total, saliva of 100 patients was taken. Saliva samples were taken after paraffin-stimulating saliva­tion had been administered. Material from the oral cavity was taken with a pipette on a selected basis in special test-tubes (CRT-bacteria test, Vivadent company) which were placed in a container with NaHCO3 and then transferred to an incubator. After 48 hours of growth at a temperature of 370C, colony-forming units (CFU) of bacteria Sm and Lb were observed and the company pattern attached to a test was used for visual assessment of bacterial growth. The level of Sm and Lb in stimulated saliva was evaluated as high in the case of CFU/ml >105 or low when CFU/ml <105.
Statistical analysis
Test of significance and correlation coefficient were used to study the dependences of variables in analysis, appropria­tely to the applied measurement scale. In the case of stu­dy variables measured on nominal scales - Streptococcus mutans and Lactobacillus acidophilus - Pearson's chi-squ­ared independence test was applied. To study the distribu­tion of continuous variables (PlI and GI) the Kolmogorov-Smirnov test was used. In the case of compound force between ordinal quality and continuous with asymmetrical distributions Spearman's rank correlation coefficient was used and significance was assessed with Student's t-test.
Data were analyzed with the program SPSS for Windows, version 15.0 (SPSS Inc., Chicago, IL, USA) and Statistica v. 8.0 (StatSoft Inc, Tulsa, OK, USA). Significance level was established at p<0.05.
Results
High bacteria levels of Streptococcus mutans and Lactobacillus acidophilus in saliva of patients were com­parably frequent between groups, but statistically significant differences (p<0.05) were observed in intergroup compa­risons: A1 and B1 and A2 and B2 (Fig. 1). In patients wi­thout cleft palate a higher percentage of high Sm and Lb bacteria levels was noted than in the control group. High levels of Sm and Lb concerned respectively 75% and 80% of subgroup B1 and 80% and 85% of subgroup B2. Different results were obtained in patients with cleft palate (group A). High levels of Sm and Lb were observed respective­ly in 40% and 45% in subgroup A1 and 45% and 55% in subgroup A2. In group A percentages of high levels of Sm and Lb were lower than in the control group.
Figure 1. High levels of carious bacteria Sm and Lb percentage distribution in study material *p<0.05

The distribution of index value PlI in patients with cleft pa­late was different than in patients without a developmen­tal anomaly (Fig. 2), and the observed intergroup differen­ce was statistically significant, which was confirmed with the Kruskal-Wallis ANOVA by ranks. A low value range for PlI was noted in 59% of group A and 84% of group B. High values of PlI were observed in 54% of subgroup A2 (patients with cleft using removable appliances). In this subgroup 6% of patients had a plaque index with the ma­ximum value. Simultaneously, in every patient from sub­group A2 there was no PlI=0. In subgroup A1 the maximum value of index PlI was 2.07 and the percentage of patients with a medium or high value of PlI was 28%. In the sub­group without cleft but treated with fixed appliances (sub­group B1) the value of the PlI index was the highest (PlI=3) in 2% of patients but a low range of value of PlI was obse­rved in 88% of cases. The highest value of PlI in the sub­group of patients without cleft treated with removable ap­pliances (subgroup B2) was 1.88; at the same time in 80% of cases the value did not exceed 1.
Figure 2. Percentage distribution of index value ranges of PlI in study material * p<0.05

A statistically significant correlation of high PlI values with growth of Streptococcus mutans and Lactobacillus acidophilus bacteria colonization was observed.
GI values and halitosis did not differentiate patients sta­tistically significantly (p>0.05). A low value range of GI and halitosis value equal to 0 was found respectively in 94% and 99% of patients.
Discussion
The performed studies allowed us to assess oral cavity hy­giene in patients during orthodontic treatment. Poor hygie­nic state in the oral cavity was found.
Caries danger with regard to bacteria number (CFU ?106) was quite high and it concerned 59% of patients with re­ference to Sm and 66% with reference to Lb. According to the literature, Sm levels were higher in studies performed in Łódź, Poznań and Szczecin. Lisiecka et al. stated on the basis of studies on 12-year-old teenagers that Sm increase was accompanied by Lb increase in saliva, which was con­firmed in this study only in one group of patients without cleft. It was found that Lb colony numbers were much hi­gher in this study as well as in studies from Szczecin than in other reports: Lb occurred in 2.4% of children's saliva from Łódź [10,11,13]. A considerably lower percentage of patients with high levels of pathogenic bacteria was obse­rved in Warsaw. In these studies there was a high titer of Sm bacteria in 16.8% [7]. Proportional distribution of high Sm levels observed in patients without cleft treated with fixed appliances compared with the control group, and Sm colony number increase with age and eruption, were con­sistent with reports from foreign papers [1,4]. Rosenbloom and Tinanoff [20] reported that increased Sm level during orthodontic treatment could be a causative factor of macu­la cariosa, which is quite often observed during treatment. The most important aspect of their work was to reveal a fourfold reduction of Sm level after finishing orthodontic treatment and during long-term observations. Using ap­pliances can only temporarily disturb the oral cavity envi­ronment state [12].
Evaluation of oral hygiene state in patients treated ortho­dontically consisted of proportional distribution assessment of the PlI index value, which was higher in patients with cleft than in patients without this defect. Dental plaque qu­antity was in accordance with previous reports from the Lower Silesia region. 84% of patients were without cleft but with a PlI index value from 0 to 1; thus their number was almost 50% higher than in the group with cleft, al­though the percentage of patients with PlI=0 was simi­lar in both groups (in group A - 14%, in group B - 16%). Patients with cleft using removable unimaxillary applian­ces (subgroup A2) showed bigger problems with effective dental plaque elimination, which was proved by the high percentage of subgroup A2 (54%) with PlI index values over 1 and the biggest in the whole study material, and the percentage (6%) with PlI=3. It corresponded with the results of the study conducted for 10 years in the Medical Academy in Wrocław [2,6]. Kościukiewicz-Michewicz et al. [9] mentioned that these results may be a consequen­ce of appliance plate construction in which the appliance­'s acrylic shaft is thickened with a plastic mass penetra­ting the cleft slot. A much better hygiene state shown by the PlI index was observed in patients of group A, treated with fixed appliances. In this case, the percentage of pa­tients with PlI>1 decreased almost twofold compared with subgroup A2 and it was 28%.
This can be explained by the greater risk awareness with fixed appliances and more careful elimination of risk fac­tors for development of caries or paradontosis.
Higher PlI values in the group of patients without cleft tre­ated with removable appliances may indicate higher suscep­tibility of appliance material to dental plaque deposition.
The presented results confirm another working hypothe­sis and support the conclusion that hygiene teaching with subsequent monitoring should be an integral element of the proper orthodontic treatment process [5]. This main­ly concerns patients with cleft, using removable applian­ces (PlI=3 in 6% of subgroup A2), but it cannot be omit­ted in any case, because both groups were not free from dental plaque.
The observed lack of gingivitis symptoms concomitant with high values of PlI may show accidental dental pla­que accumulation. Studies confirmed earlier reports con­cerning significantly less gingival reactivity in children [8,22]. This fact results from the different bacterial flora composition compared with adults, lack of some compo­nents necessary for bacteria existence, and less reactivity of parodontium blood vessels.
A fundamental issue is oral cavity hygiene maintenan­ce in patients with cleft while malocclusion correction is performed. After a long orthodontic treatment and seve­ral procedures a patient is convinced that the therapy is becoming out of control. Therefore if appliance wearing is not preceded with oral cavity hygiene teaching and pa­rodontium recovery, this false idea will be preserved in a patient's mind. Effective help in the quality of oral cavity hygiene improvement requires time, patience and toleran­ce. The lip after corrective surgery can be thinner, which hampers proper toothbrush application to the anterior and lateral teeth, and a thin alveolar process can be revealed as a shallow vestibule in the cleft region. When recom­mending a new toothbrush we should take these circum­stances into consideration and if necessary we should re­commend to children a toothbrush with a short head. It is difficult to offer the whole range of instruments without taking into account individual needs, which is emphasized by Benington et al. [3].
Conclusions
The presented research clearly proves that the levels of ca­ries initiating bacteria (Streptococcus mutans) and develo­ping ones (Lactobacillus acidophilus), as well as oral hy­giene level, differ in patients with and without cleft palate. The latter, despite evidently worse PlI, display significantly lower carious bacteria level. Considering that orthodontic treatment additionally changes the oral environment, me­ticulous supervision of caries development and its overall consequences may be challenging, especially in individu­als with cleft palate. Therefore, since caries is a problem evidently beyond dentists' scope, proper oral hygiene se­ems to be an essential element of pro-health education, definitely requiring the introduction of programs of gene­ral disease prevention.
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The authors have no potential conflicts of interest to declare.