Mariana C. Sllos, Vera M. Soviero Department of Preventive and Community Dentistry, School of Dentistry, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil One of the purposes of diagnosing dental caries is to detect and classify the lesions, in order to select the most appropriate treatment for each tooth surface (1). Con- sidering the slower rate of dental caries progression in contemporary populations, the assessment of non- cavitated lesions is of great importance for measuring the eectiveness of preventive approaches in longitudinal studies (26). If caries detection is restricted to counting the number of tooth surfaces with cavities, the early stages of the disease process are not considered. There- fore, caries prevalence is underestimated and the behaviour of individual caries lesions cannot be moni- tored (7, 8). Many studies have conrmed that high interexaminer and intra-examiner agreement can be achieved even when precavitated lesions are recorded (812), and since the 1950s, the inclusion of non- cavitated lesions has been recommended (1318). However, the World Health Organization decided not to include enamel caries lesions in their caries index, mainly because the diagnosis may not be reliable when the diagnostic threshold is set at the non-cavitated level, just as it was considered that the inclusion of enamel caries lesions would make a comparison of the caries situation amongst countries worldwide more dicult (19). Besides the inclusion of lesions at the non-cavitated stage, the assessment of lesion activity is of major importance. The decision on clinical treatment will vary depending on the classication of the lesion as being active or inactive. Inactive or arrested lesions may not need any intervention, whereas active lesions have to be treated using non-operative procedures (such as oral hygiene improvement and topical uorides) or operative treatment (6, 7, 20). The Nyvad caries diagnostic system was the rst classication system to dene clear criteria for the activity assessment of both non-cavitated and cavitated lesions (8). Recently, an International Caries Detection and Assessment System (ICDAS) has been suggested (4). This system is focused on the estimation of lesion depth and does not include lesion activity in their primary caries codes. A second score system to assess activity has been suggested for use in combination with the primary ICDAS codes (21). Clinical studies have shown that the Nyvad classi- cation system has construct validity because activity assessment reected the expected eects of uoride toothpaste on caries lesions (11, 22). Moreover, it has also been observed that caries activity assessment has predictive validity because active non-cavitated lesions have a signicantly greater risk of progressing to cavity than do inactive lesions (22). With the diagnostic threshold set at active vs. inactive lesions, the criteria have also been shown to be reliable, with kappa coe- cient values in permanent teeth ranging between 0.68 and 0.80 for intra-examiner agreement and between 0.74 and 0.78 for interexaminer agreement (8). So far, the Nyvad caries classication system has been used successfully in clinical studies (11, 2224), but more studies on its reli- ability in both permanent and primary teeth are needed. The purpose of the present clinical study was to assess the interexaminer and intra-examiner reliability of the Sellos MC, Soviero VM. Reliability of the Nyvad criteria for caries assessment in primary teeth. Eur J Oral Sci 2011; 119: 225231. 2011 Eur J Oral Sci This study assessed the interexaminer and intra-examiner reliability of the Nyvad caries classication system in primary teeth and calculated the mean examination time. The criteria were based on visual and tactile examinations to dierentiate active and inactive lesions at cavitated and non-cavitated levels. Eighty children (37 yr of age) were examined under standardized conditions by calibrated examiners. At the tooth surface level, reliability was expressed as percentage agreement and kappa coecient, using four diagnostic thresholds: sound vs. diseased; sound or inactive lesion vs. active lesion; intact surface vs. surface discontinuity; and sound or non-cavitated lesion vs. cavitated lesion. Interexaminer and intra-examiner kappa values were, respectively: 0.82/0.86; 0.80/0.86; 0.90/0.94; and 0.95/0.98. At the individual level, reliability of estimates of the caries prevalence and of the decayed or lled surface (dfs) counts were assessed at three diagnostic thresholds: sound vs. diseased; sound or inactive lesion vs. active lesion; and sound or non-cavitated lesion vs. cavitated lesion. For caries prev- alence, interexaminer and intra-examiner kappa values were, respectively: 0.84/0.94; 0.69/0.74; and 0.95/0.97. The mean examination time was 226.5 s (SD = 128.5). The use of the Nyvad caries diagnostic criteria in primary teeth showed reliable results. The examination time was acceptable. Prof. Vera Mendes Soviero, Faculdade de Odontologia, Clnica de Odontopediatria, Universidade do Estado do Rio de Janeiro UERJ, Av. 28 de Setembro, 157 (2/ andar), Vila Isabel, 20511-030 Rio de Janeiro RJ, Brazil Telefax: +552128686372 E-mail: verasoviero@gmail.com Key words: dental caries; diagnosis; primary teeth; reliability Accepted for publication March 2011 Eur J Oral Sci 2011; 119: 225231 DOI: 10.1111/j.1600-0722.2011.00827.x Printed in Singapore. All rights reserved 2011 Eur J Oral Sci European Journal of Oral Sciences Nyvad caries classication system for caries assessment and classication in primary teeth and to calculate the mean examination time. Material and methods The study sample consisted of 80 children [45 boys and 35 girls; 37 yr of age (mean age 5.1 yr)], with a high caries experience, from a government school in Rio de Janeiro, Brazil. Children had to have at least four primary incisors remaining to be included in the study. All children in the study sample were born and raised in an urban area that had a uoridated water supply (0.41.5 mg l )1 of uoride). Informed consent was obtained from parents, and the study was approved by the Committee for Ethics in Research at the Rio de Janeiro State University. Dental examinations were carried out in a dental chair under standardized conditions (compressed air for 35 s, articial light, cotton rolls, a dental mirror, and a sharp probe) by two calibrated examiners (V.S. and M.S.), inde- pendently. Children had their teeth brushed by the rst examiner before the examination. Then, they were positioned in the dental chair and, if necessary, additional biolm was removed during the examination using a probe. Only primary teeth were recorded at the tooth sur- face level. The Nyvad criteria are based on visual and tactile diagnoses to assess caries lesion activity at three progression stages: the non-cavitated stage; the enamel discontinuity stage; and the cavitated stage (8, 25). The codes used to classify the criteria in primary teeth are shown in Fig. 1. In the event of doubt, examiners were instructed to choose the code representing the less severe status. However, in the presence of two or more caries lesions on the same tooth surface, the most severe caries lesion was registered according to the following severity scale: active lesion >inactive lesion, and cavitated lesion >surface discontinuity >non-cavitated lesion. Each child was examined on two dierent days. The examiner M.S. performed the rst examination, and the examination time was measured using a digital chronometer, which was started as soon as the dental mirror was placed in the childs mouth. Immediately following the rst examina- tion, V.S. carriedout the secondexamination. One weeklater, M.S. repeated the examination. The examiners were trained for 2 wk by two of the authors of the criteria (Drs B. Nyvad and V. Machiulskiene), with the training being based on clinical examinations and A-a B-a C-a A-b B-b F-a F-b G I H J C-b A-c E-a E-b E-c D-a D-b D-c Fig. 1. Clinical aspects of the Nyvad caries diagnostic codes in primary teeth. A-a, A-b, and A-c: code 0, sound surfaces; B-a and B-b: code 1, active non-cavitated lesions; C-a and C-b: code 2, active enamel discontinuity; D-a, D-b, and D-c: code 3, active cavitated lesions; E-a, E-b, and E-c: code 4, inactive non-cavitated lesions; F-a and F-b: code 5, inactive enamel discontinuity; G: code 6, inactive cavitated lesion; H: code 7, lling; I: code 8, lling associated with an active lesion; J: code 9, lling associated with an inactive lesion. 226 Sellos & Soviero discussions. Calibration was performed in a pilot study involving 30 children, which was carried out under the same conditions as the present study. Evaluation The agreement was rst analyzed at the tooth surface level. Interexaminer and intra-examiner reliability of the caries diagnostic codes (09) was assessed. Then, the codes were dichotomized at four category thresholds: (i) sound (code 0) vs. diseased (codes 19); (ii) sound or inactive lesion (codes 0, 4, 5, 6, 7, and 9) vs. active lesion (codes 1, 2, 3, and 8); (iii) intact surface (codes 0, 1, 4, 7, and 9) vs. surface disconti- nuity (codes 2, 3, 5, 6, and 8); and (iv) sound or non- cavitated lesion (codes 0, 1, 2, 4, 5, 7, and 9) vs. cavitated lesion (codes 3, 6, and 8). The results were expressed as percentage agreement and Cohens kappa coecient for each diagnostic threshold. At the individual level, the caries prevalence (the per- centage of children with caries) and the extent [the decayed or lled surface (dfs) count for each child] was estimated considering: (i) all caries lesions (codes 19); (ii) active caries lesions (codes 1, 2, 3, and 8); and (iii) cavitated caries lesions (codes 3, 6, and 8). For the dfs, interexaminer and intra-examiner agreement was assessed using the method described by Bland & Altman (26). In this analysis, the dierence between the dfs counts obtained in the rst and second examination is plotted against the mean count of both examinations. Based on the SD of the dierences, upper and lower limits of agreement are calculated, which results in an interval where 95% of the dierences between the examinations are found. For caries prevalence, agree- ment was assessed by percentage agreement and Cohens kappa coecient for each diagnostic threshold. The MannWhitney U-test was used to verify the inu- ence of the childrens age and caries experience on the mean examination time. The signicance level for all of the analyses was set at 5% (a = 0.05). Results A total of 6,400 tooth surfaces from 80 children were suitable for the study. Table 1 presents the intra- examiner and interexaminer percentage agreement and kappa values at the tooth-surface level. In general, kappa values were 0.80 or higher in all analyses, with the exception of a kappa value of 0.76 when considering all codes from 0 to 9. The percentage agreement varied from 0.96 to 0.99. The highest kappa values (0.95 and 0.98) were observed when a positive diagnosis was based on the presence of cavitation. Lower kappa values (0.80 and 0.86) were observed when a positive diagnosis was based on the presence of an active lesion. In all the analyses the intra-examiner agreement had slightly higher values than the interexaminer agreement. Among the 6,400 tooth surfaces examined, disagree- ments between examiners were observed in 242 (3.8%) cases. Most of these disagreements (65.3%; 158/242) concerned the dierentiation between sound surfaces and non-cavitated lesions, representing 2.5% (158/6,400) of all tooth surfaces. From the total number of disagree- ments, 33.5% (81/242) were related to the dierentiation between sound surfaces and inactive non-cavitated lesions, representing 1.3% (81/6,400) of all tooth sur- faces; 26.0% (63/242) concerned disagreement between Table 1 Percentage agreement, kappa coecient values, and respective 95% CIs for interexaminer (V.S. M.S. 1st) and intra-examiner (M.S. 1st M.S. 2nd) examinations considering all codes and four diagnostic thresholds (n = 6,400 tooth surfaces) Interexaminer (V.S. M.S. 1st) Intra-examiner (M.S. 1st M.S. 2nd) Nyvad criteria Percentage agreement = 96 Percentage agreement = 97 (codes 09) j = 0.76 j = 0.83 Diagnostic thresholds ) + ) + 1. Sound vs. diseased (n) ) 5794 91 5813 58 + 77 438 74 455 Percentage agreement (95% CI) 97 (9798) 98 (9798) Kappa (CI) 0.82 (0.800.85) 0.86 (0.840.86) 2. Sound or inactive lesions vs. active lesions (n) ) 6020 76 6031 35 + 46 258 53 281 Percentage agreement (95% CI) 98 (9798) 99 (9899) Kappa (95% CI) 0.80 (0.760.83) 0.86 (0.830.89) 3. Intact surface vs. surface discontinuity (n) ) 6090 35 6096 12 + 18 257 21 271 Percentage agreement (95% CI) 99 (9899) 99 (9999) Kappa (95% CI) 0.90 (0.880.93) 0.94 (0.920.96) 4. Sound or non-cavitated lesion vs. cavitated lesion (n) ) 6192 9 6198 5 + 11 188 3 194 Percentage agreement (95% CI) 99 (9999) 99 (9999) Kappa (95% CI) 0.95 (0.920.97) 0.98 (0.960.99) Code 0, sound surfaces; code 1, active non-cavitated lesions; code 2, active enamel discontinuity; code 3, active cavitated lesions; code 4, inactive non-cavitated lesions; code 5, inactive enamel discontinuity; code 6, inactive cavitated lesion; code 7, lling; code 8, lling associated with an active lesion; code 9, lling associated with an inactive lesion; +, positive diagnoses; ), negative diagnoses. Caries assessment in primary teeth 227 sound surfaces and active non-cavitated lesions, repre- senting 0.9% (63/6,400) of all tooth surfaces; and 5.8% (14/242) concerned disagreement between active non- cavitated lesions and inactive non-cavitated lesions, representing 0.2% (14/6,400) of all tooth surfaces. The remaining disagreements (34.7%; 84/242) were related to other combinations. The cross-tabulation showing the interexaminer agreement is available as supporting information (Table S1). Disagreements in intra-examiner examinations were observed in 171 (2.7%) of the 6,400 tooth surfaces and the majority (70.7%; 121/171) were again related to the dierentiation between sound surfaces and non-cavitated lesions. The cross-tabulation showing the intra-examiner agreement is available as supporting information (Table S2). Comparison between examinations was also made based on caries prevalence (Table 2) and dfs count (Table 3), which are variables at the individual level. Considering the presence of at least one surface with caries (codes 19) or with cavitated lesions (scores 3, 6, or 8), the percentage agreement on caries prevalence was high, ranging from 93.8% to 98.7% with corresponding kappa values ranging from 0.84 to 0.97. The lowest agreement was observed when caries diagnosis at the individual level was based on the presence of at least one surface with an active lesion (codes 1, 2, 3, or 8). In this case, the interexaminer percentage agreement was 85% (j = 0.69) and the intra-examiner percentage agreement was 87.5% (j = 0.74). Table 3 shows the mean dfs (i.e. the number of tooth surfaces aected by caries per subject) for both examin- ers according to three diagnostic thresholds. In no situ- ation was the mean dfs statistically signicantly dierent among examinations. Table 4 shows the data related to the analysis of the interexaminer and intra-examiner agreement on dfs counts. The mean dfs dierence between examinations was below 1 in all situations, indicating a high level of agreement for the three diag- nostic thresholds. The limits of agreement denote the interval which holds 95% of the dierence: the smaller the range between the limits, the higher the agreement. The narrowest interval was observed when the diagnostic threshold was set at the cavity level (from )0.72 to 0.67 surfaces for intra-examiner analysis, and from )1.40 to 1.60 surfaces for interexaminer analysis), indicating very high agreement. The wider interval (from )4.90 to 4.60 surfaces) was seen for interexaminer agreement when all types of lesions were included in the dfs counts. When only active caries lesions were included in the dfs counts, the limits of agreement ranged from )3.90 to 3.20 surfaces for interexaminer analysis and from )3.20 to 3.60 surfaces for intra-examiner analysis. The mean examination time was 226.5 s (SD = 128.5 s) and was not inuenced by the childrens age, whereas it was inuenced by their caries experience (Table 5). Discussion This study assessed the interexaminer and intra-examiner agreement on caries diagnosis in primary teeth using the Nyvad classication system. Usually, agreement in caries Table 2 Interexaminer (V.S. M.S. 1st) and intra-examiner (M.S. 1st M.S. 2nd) reliability in the assessment of caries prevalence (percentage of children with caries) according to three diagnostic thresholds (n = 80 subjects) Diagnostic thresholds Interexaminer estimate Intra-examiner estimate V.S. M.S. 1st Agreement j M.S. 1st M.S. 2nd Agreement j At least one surface aected by caries (codes 19) 72.5 73.8 93.8 0.84 73.8 73.8 97.5 0.94 At least one surface with active caries lesions (codes 1, 2, 3, or 8) 58.8 61.3 85.0 0.69 61.3 61.3 87.5 0.74 At least one surface with cavitated caries lesions (codes 3, 6, or 8) 40.0 37.5 97.5 0.95 37.5 38.8 98.7 0.97 Code 0, sound surfaces; code 1, active non-cavitated lesions; code 2, active enamel discontinuity; code 3, active cavitated lesions; code 4, inactive non-cavitated lesions; code 5, inactive enamel discontinuity; code 6, inactive cavitated lesion; code 7, lling; code 8, lling associated with an active lesion; code 9, lling associated with an inactive lesion. Table 3 Mean decayed or lled surface (dfs) and SD for examiners V.S. and M.S (1st and 2nd examinations) according to three diagnostic thresholds (n = 80 children) Diagnostic thresholds Mean dfs (SD) V.S. M.S. 1st M.S. 2nd Tooth surfaces aected by caries (codes 19) 6.59 (8.57) 6.71 (8.44) 6.53 (8.33) Tooth surfaces with active lesions (codes 1, 2, 3, or 8) 3.80 (5.85) 4.18 (5.99) 3.95 (5.86) Tooth surfaces with cavitated lesions (codes 3, 6, or 8) 2.55 (4.63) 2.46 (5.53) 2.49 (4.53) Code 0, sound surfaces; code 1, active non-cavitated lesions; code 2, active enamel discontinuity; code 3, active cavitated lesions; code 4, inactive non-cavitated lesions; code 5, inactive enamel discontinuity; code 6, inactive cavitated lesion; code 7, lling; code 8, lling associated with an active lesion; code 9, lling associated with an inactive lesion. 228 Sellos & Soviero diagnosis is analyzed at the tooth surface level when codes are assigned to each surface. Although this type of analysis is important to identify how reproducible the method is, it does not show the impact of agreement level on epidemiological data. No two examiners, and not even the same examiner, are expected to agree completely or give identical results in repeated examinations. However, it is most important to know whether this disagreement could cause problems in clinical practice (i.e. cause the clinician to choose an inappropriate treatment, or bring about a misleading conclusion to a clinical study) (26). The high reproducibility of the Nyvad caries classi- cation system in the present study was in accordance with results from studies carried out on permanent teeth in young individuals (8, 24). As also observed in previous studies (8), disagreements were concentrated on the dierentiation between sound surfaces (code 0) and non-cavitated lesions (codes 1 and 4). Therefore, non-cavitated stages still represent the major problem in clinical diagnosis. Despite its common usage, the Cohen kappa coe- cient is not always the most suitable indicator for assessing agreement. It was originally proposed to mea- sure agreement between two examiners when subjects are classied into two nominal categories. The extension of its application to multicategory data may result in mis- leading interpretations. When kappa is used for multi- category data, the categories should be grouped to become dichotomies. Even so, kappa values can be highly inuenced by the way in which multicategory classications are grouped. (27) A more comprehensive analysis should also focus on the disagreements and their possible impact on the - nal outcomes. Thereby, it would provide a better understanding of the diculties related to each level of diagnosis and allow for a more profound comparison between studies. A detailed analysis of disagreements may identify some of their eects on clinical research and practice. In the present study, most of the dis- agreements were between sound surfaces (code 0) and non-cavitated lesions (codes 1 and 4). In the case of inactive lesions, this would not result in any over- treatment in a clinical situation, because neither sound surfaces nor inactive lesions require any intervention. This disagreement has often been related to stained ssures on occlusal surfaces. In the case of active le- sions, it could be a relevant disagreement in terms of the clinical practice as it could change the treatment decision. Although total agreement is not expected, disagreements must be avoided as much as possible. It is important to reinforce that improvement in agree- ment is highly related to the quality of training and experience of the examiners (8, 10, 22, 23). Table 5 Mean examination time in seconds (s) according to age and number of aected tooth surfaces n Mean time (s) SD Min. Max. Age* 3650 months 24 203.29 a 136.17 47 601 5170 months 29 224.17 b 134.75 54 586 Older than 71 months 27 249.74 c 114.78 66 525 Number of aected tooth surfaces** 0 22 106.64 a 45.57 47 226 16 29 191.72 b 58.38 74 313 7 29 352.31 c 112.74 178 601 Max., longest examination time; Min., shortest examination time. *MannWhitney U-test (a b; a c; b c: P > 0.05). **MannWhitney U-test (a b; a c: P < 0.01); (b c: P = 0.01). Table 4 Interexaminer (V.S. M.S. 1st) and intra-examiner (M.S. 1st M.S. 2nd) agreement in the assessment of number of tooth surfaces aected by caries per subject [decayed or lled surface (dfs)] according to three dierent thresholds (n = 80 subjects) Diagnostic thresholds Examiners Mean dfs dierence per subject Limits of agreement Range of the dfs dierences between the two examinations Surfaces aected by caries (codes 19) V.S. M.S. 1st )0.13 [)4.90; 4.60] [)6; 14] M.S. 1st M.S. 2nd 0.20 [)3.50; 3.90] [)9; 6] Surfaces with active lesions (codes 1, 2, 3, or 8) V.S. M.S. 1st )0.40 [)3.90; 3.20] [)8; 6] M.S. 1st M.S. 2nd 0.22 [)3.20; 3.60] [)10; 6] Surfaces with cavitated lesions (codes 3, 6, or 8) V.S. M.S. 1st 0.03 [)1.01; 1.06] [)2; 5] M.S. 1st M.S. 2nd )0.03 [)0.72; 0.67] [)2; 1] Code 0, sound surfaces; code 1, active non-cavitated lesions; code 2, active enamel discontinuity; code 3, active cavitated lesions; code 4, inactive non-cavitated lesions; code 5, inactive enamel discontinuity; code 6, inactive cavitated lesion; code 7, lling; code 8, lling associated with an active lesion; code 9, lling associated with an inactive lesion. Caries assessment in primary teeth 229 For numerical variables, such as dfs counts, the Bland & Altman method (26) is considered an appropriate method with which to assess agreement between repeated measurements: the narrower the interval, the higher the agreement between measurements. As expected, the narrowest interval of agreement was found to be when the cut-o point was set at cavitated lesions. However, for the other two cut-o points, considering all codes or only active lesions, the limits of agreements were not excessively wide and the nal mean dfs count did not dier signicantly between examiners or within an examiner (Tables 4 and 5). These results encourage the use of more comprehensive assessment of carious lesions in clinical studies. In our opinion, the main advantage of the Nyvad caries classication systemis the ability to assess the progression stage and activity of the lesions simultaneously, using a very straightforward code system. In addition, the dierentiation between enamel discontinuity and a dentin cavity provides important information for monitoring caries progression. The theoretical underpinning of the Nyvad caries classication system is to provide a dis- cernible link between the diagnosis and the best treatment option. Although dental biolm has to be removed from the tooth surfaces to allow proper visualization of early carious lesions, professional cleaning of the teeth is not recommended before examination using the Nyvad sys- tem. Most of the biolm is usually removed during toothbrushing, and only those surfaces where the patient does not usually clean eectively will remain covered by biolm. In the present study, children were assisted by the examiner during toothbrushing because they were very young. When visual examination combining surface features (opacity, roughness, colour, and location of the lesion) is not enough to classify activity, tactile examination using a probe is recommended (8). For a proper understanding of the surface texture, the probe must be sharp. However, the intention is not to test whether the probe catches irregularities on the enamel, but rather to feel the texture or the consistency of the lesion. For enamel lesions, the tip of the probe must be placed at an angle of about 30 to the tooth surface and be moved gently across the lesion, so that the dierence between the smooth texture of a sound surface or inactive lesion and the rough texture of an active lesion can be felt. For dentin lesions, tactile examination, using slight pressure, dierentiates hard tissue from soft tissue or a leathery consistency. In fact, surface texture has been considered as a better indicator of activity than colour (7, 20). That is why activity assessment may not be based only on the colour of the lesion, especially for dentin lesions. Many dark-brown dentin lesions have a leathery consistency, indicating that they are still active. As the transition between active and inactive stages does not occur instantaneously, mixed lesions must be considered as active. We believe that all these considerations on activity assessment were of great importance for the high levels of agreement achieved on activity assessment in the present study. Disagreement on the dierentiation between active and inactive lesions was very infrequent, indicating a good reproducibility of activity assessment when a consensus on the presence of the lesion was reached. For proper detection of non-cavitated lesions, tooth surfaces must be dried and visualized under good illumination. The requirement of compressed air and articial light is therefore a prerequisite for the Nyvad caries classication system, as well as for other caries classication systems that aim to detect initial carious lesions; otherwise, non-cavitated lesions are underesti- mated. The mean examination time is not frequently men- tioned in reliability studies in the literature. In the present study, the mean time needed for the examina- tion was less than expected. The average examination time for each child was 3 min and 46 s. In a previous study, with older children and adolescents, the exami- nation time was estimated to be between 5 and 8 min (8). This dierence was probably because more tooth surfaces are present in mixed or permanent dentitions compared with the primary dentition. We expected that younger children would need more time for examina- tion because it is often more dicult to control their behaviour in the dental chair. However, age did not inuence examination time. Probably, behaviour con- trol was not a problem in the present study because both examiners were specialized in paediatric dentistry. On the other hand, the more the tooth surfaces were aected by caries the longer the examination took be- cause, if a tooth surface was not sound, examiners needed additional time to reect and assign a code to that surface. 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