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Meta-Analysis
. 2021 Mar 15;3(3):CD014545.
doi: 10.1002/14651858.CD014545.

Imaging modalities to inform the detection and diagnosis of early caries

Tanya Walsh  1 , Richard Macey  1 , Philip Riley  2 , Anne-Marie Glenny  1 , Falk Schwendicke  3 , Helen V Worthington  2 , Janet E Clarkson  4 , David Ricketts  5 , Ting-Li Su  1 , Anita Sengupta  1
Affiliations
Meta-Analysis

Imaging modalities to inform the detection and diagnosis of early caries

Tanya Walsh et al. Cochrane Database Syst Rev. .

Abstract

Background: The detection and diagnosis of caries at the earliest opportunity is fundamental to the preservation of tooth tissue and maintenance of oral health. Radiographs have traditionally been used to supplement the conventional visual-tactile clinical examination. Accurate, timely detection and diagnosis of early signs of disease could afford patients the opportunity of less invasive treatment with less destruction of tooth tissue, reduce the need for treatment with aerosol-generating procedures, and potentially result in a reduced cost of care to the patient and to healthcare services.

Objectives: To determine the diagnostic accuracy of different dental imaging methods to inform the detection and diagnosis of non-cavitated enamel only coronal dental caries.

Search methods: Cochrane Oral Health's Information Specialist undertook a search of the following databases: MEDLINE Ovid (1946 to 31 December 2018); Embase Ovid (1980 to 31 December 2018); US National Institutes of Health Ongoing Trials Register (ClinicalTrials.gov, to 31 December 2018); and the World Health Organization International Clinical Trials Registry Platform (to 31 December 2018). We studied reference lists as well as published systematic review articles.

Selection criteria: We included diagnostic accuracy study designs that compared a dental imaging method with a reference standard (histology, excavation, enhanced visual examination), studies that evaluated the diagnostic accuracy of single index tests, and studies that directly compared two or more index tests. Studies reporting at both the patient or tooth surface level were included. In vitro and in vivo studies were eligible for inclusion. Studies that explicitly recruited participants with more advanced lesions that were obviously into dentine or frankly cavitated were excluded. We also excluded studies that artificially created carious lesions and those that used an index test during the excavation of dental caries to ascertain the optimum depth of excavation.

Data collection and analysis: Two review authors extracted data independently and in duplicate using a standardised data extraction form and quality assessment based on QUADAS-2 specific to the clinical context. Estimates of diagnostic accuracy were determined using the bivariate hierarchical method to produce summary points of sensitivity and specificity with 95% confidence regions. Comparative accuracy of different radiograph methods was conducted based on indirect and direct comparisons between methods. Potential sources of heterogeneity were pre-specified and explored visually and more formally through meta-regression.

Main results: We included 104 datasets from 77 studies reporting a total of 15,518 tooth sites or surfaces. The most frequently reported imaging methods were analogue radiographs (55 datasets from 51 studies) and digital radiographs (42 datasets from 40 studies) followed by cone beam computed tomography (CBCT) (7 datasets from 7 studies). Only 17 studies were of an in vivo study design, carried out in a clinical setting. No studies were considered to be at low risk of bias across all four domains but 16 studies were judged to have low concern for applicability across all domains. The patient selection domain had the largest number of studies judged to be at high risk of bias (43 studies); the index test, reference standard, and flow and timing domains were judged to be at high risk of bias in 30, 12, and 7 studies respectively. Studies were synthesised using a hierarchical bivariate method for meta-analysis. There was substantial variability in the results of the individual studies, with sensitivities that ranged from 0 to 0.96 and specificities from 0 to 1.00. For all imaging methods the estimated summary sensitivity and specificity point was 0.47 (95% confidence interval (CI) 0.40 to 0.53) and 0.88 (95% CI 0.84 to 0.92), respectively. In a cohort of 1000 tooth surfaces with a prevalence of enamel caries of 63%, this would result in 337 tooth surfaces being classified as disease free when enamel caries was truly present (false negatives), and 43 tooth surfaces being classified as diseased in the absence of enamel caries (false positives). Meta-regression indicated that measures of accuracy differed according to the imaging method (Chi2(4) = 32.44, P < 0.001), with the highest sensitivity observed for CBCT, and the highest specificity observed for analogue radiographs. None of the specified potential sources of heterogeneity were able to explain the variability in results. No studies included restored teeth in their sample or reported the inclusion of sealants. We rated the certainty of the evidence as low for sensitivity and specificity and downgraded two levels in total for risk of bias due to limitations in the design and conduct of the included studies, indirectness arising from the in vitro studies, and the observed inconsistency of the results.

Authors' conclusions: The design and conduct of studies to determine the diagnostic accuracy of methods to detect and diagnose caries in situ are particularly challenging. Low-certainty evidence suggests that imaging for the detection or diagnosis of early caries may have poor sensitivity but acceptable specificity, resulting in a relatively high number of false-negative results with the potential for early disease to progress. If left untreated, the opportunity to provide professional or self-care practices to arrest or reverse early caries lesions will be missed. The specificity of lesion detection is however relatively high, and one could argue that initiation of non-invasive management (such as the use of topical fluoride), is probably of low risk. CBCT showed superior sensitivity to analogue or digital radiographs but has very limited applicability to the general dental practitioner. However, given the high-radiation dose, and potential for caries-like artefacts from existing restorations, its use cannot be justified in routine caries detection. Nonetheless, if early incidental carious lesions are detected in CBCT scans taken for other purposes, these should be reported. CBCT has the potential to be used as a reference standard in diagnostic studies of this type. Despite the robust methodology applied in this comprehensive review, the results should be interpreted with some caution due to shortcomings in the design and execution of many of the included studies. Future research should evaluate the comparative accuracy of different methods, be undertaken in a clinical setting, and focus on minimising bias arising from the use of imperfect reference standards in clinical studies.

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Conflict of interest statement

Tanya Walsh: none known. I am Statistical Editor with Cochrane Oral Health. Richard Macey: none known. Philip Riley: none known. I am Deputy Co‐ordinating Editor of Cochrane Oral Health. Anne‐Marie Glenny: none known. I am Joint Co‐ordinating Editor of Cochrane Oral Health. Falk Schwendicke: I have a conflict of interest when it comes to artificial intelligence (AI)‐based diagnostics. This, however, is beyond the remit of this review. Helen V Worthington: none know. I am Emeritus Co‐ordinating Editor of Cochrane Oral Health. Janet E Clarkson: none known. I am Joint Co‐ordinating Editor of Cochrane Oral Health. David Ricketts: none known. Ting‐Li Su: none known. Anita Sengupta: none known.

Figures

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1
Keystones of the International Caries Classification and Management System (ICCMS™).
Copyright© 2018 Ismail AI, Pitts NB, Tellez M. The International Caries Classification and Management System (ICCMS™) an example of a caries management pathway. BMC Oral Health 2015;15(Suppl 1):S9. Reproduced with permission.
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Study flow diagram.
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Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study.
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Risk of bias and applicability concerns graph: review authors' judgements about each domain presented as percentages across included studies.
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Forest plot of 104 datasets from 77 studies.
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Summary receiver operating characteristic (SROC) plot of 104 datasets from 77 studies.
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Forest plot of different imaging: analogue, digital, cone beam computed tomography (CBCT).
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Summary receiver operating characteristic (SROC) plot of different imaging: analogue, digital, cone beam computed tomography (CBCT).
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Forest plot of in vivo/in vitro (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Summary receiver operating characteristic (SROC) plot of in vivo/in vitro (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Forest plot of dentition (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Summary receiver operating characteristic (SROC) plot of dentition (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Forest plot of reference standard (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Summary receiver operating characteristic (SROC) plot of reference standard (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Forest plot of tooth surface (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Summary receiver operating characteristic (SROC) plot of tooth surface (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Forest plot of caries into dentine prevalence category (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Summary receiver operating characteristic (SROC) plot of caries into dentine prevalence category (97 non‐cone beam computed tomography (non‐CBCT) datasets).
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Summary receiver operating characteristic (SROC) plot of within‐person analysis analogue and digital radiographs.
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Summary receiver operating characteristic (SROC) plot of within‐person analysis digital radiographs and cone beam computed tomography (CBCT).
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Summary receiver operating characteristic (SROC) plot of within‐person analysis analogue radiographs and cone beam computed tomography (CBCT).
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Analogue
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CBCT
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All non‐CBCT
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Soviero 2012 {published data only}
    1. Soviero VM, Leal SC, Silva RC, Azevedo RB. Validity of MicroCT for in vitro detection of proximal carious lesions in primary molars. Journal of Dentistry 2012;40(1):35-40. - PubMed
Svanaes 2000 {published data only}
    1. Svanaes DB, Moystad A, Larheim TA. Approximal caries depth assessment with storage phosphor versus film radiography. Evaluation of the caries-specific Oslo enhancement procedure. Caries Research 2000;34(6):448-53. - PubMed
Tarim 2014 {published data only}
    1. Tarim Ertas E, Kucukyilmaz E, Ertas H, Savas S, Yircali Atici M. A comparative study of different radiographic methods for detecting occlusal caries lesions. Caries Research 2014;48(6):566-74. - PubMed
Tonkaboni 2019 {published data only}
    1. Tonkaboni A, Saffarpour A, Aghapourzangeneh F, Fard MJK. Comparison of diagnostic effects of infrared imaging and bitewing radiography in proximal caries of permanent teeth. Lasers in Medical Science 2019;34(5):873-9. - PubMed
Virajsilp 2005 {published data only}
    1. Virajsilp V, Thearmontree A, Aryatawong S, Paiboonwarachat D. Comparison of proximal caries detection in primary teeth between laser fluorescence and bitewing radiography. Pediatric Dentistry 2005;27(6):493-9. - PubMed
Wenzel 2002 {published data only}
    1. Wenzel A, Hintze H, Kold LM, Kold S. Accuracy of computer-automated caries detection in digital radiographs compared with human observers. European Journal of Oral Sciences 2002;110(3):199-203. - PubMed
Xavier 2011 {published data only}
    1. Xavier CRG, Araujo-Pires AC, Poleti ML, Rubira-Bullen IRF, Ferreira Jr O, Capelozza ALA. Evaluation of proximal caries in images resulting from different modes of radiographic digitalization. Dento Maxillo Facial Radiology 2011;40(6):338-43. - PMC - PubMed
Zangooei 2010 {published data only}
    1. Zangooei Booshehry M, Davari A, Ezoddini Ardakani F, Rashidi Nejad MR. Efficacy of application of pseudocolor filters in the detection of interproximal caries. Journal of Dental Research, Dental Clinics, Dental Prospects 2010;4(3):79-82. - PMC - PubMed

References to studies excluded from this review

Abdinian 2015 {published data only}
    1. Abdinian M, Razavi SM, Faghihian R, Samety AA, Faghihian E. Accuracy of digital bitewing radiography versus different views of digital panoramic radiography for detection of proximal caries. Journal of Dentistry (Tehran, Iran) 2015;12(4):290-7. - PMC - PubMed
Abdinian 2017 {published data only}
    1. Abdinian M, Nazeri R, Ghaiour M. Effect of filtration and thickness of cross-sections of cone beam computed tomography images on detection of proximal caries. Journal of Dentistry (Tehran, Iran) 2017;14(4):223-30. - PMC - PubMed
Abdinian 2018 {published data only}
    1. Abdinian M, Ghaiour M. Effect of filtration and slice thickness of cone-beam computed tomography images on occlusal caries detection: an ex vivo study. Journal of Dentistry (Tehran, Iran) 2018;15(5):283-93. - PMC - PubMed
Alomari 2014 {published data only}
    1. Alomari QD, Qudeimat MA, Ghayyath AA. Imaging of occlusal dentine caries: a comparison among conventional radiographs, digital radiographs, and cone-beam computed tomography images. Oral Radiology 2014;31(2):73-80.
Alomari 2015 {published data only}
    1. Alomari QD, Qudeimat MA, Khalaf ME, Al-Tarakemah Y. The effect of combining radiographs and DIAGNOdent with visual examination on detection and treatment decisions of non-cavitated occluso-dentinal caries. Operative Dentistry 2015;40(3):313-21. - PubMed
Arslan 2014 {published data only}
    1. Arslan U, Karaağaoğlu E, Özkan G, Kanlı A. Evaluation of diagnostic tests using information theory for multi-class diagnostic problems and its application for the detection of occlusal caries lesions. Balkan Medical Journal 2014;31(3):214-8. - PMC - PubMed
Berkhout 2007 {published data only}
    1. Berkhout WE, Verheij JG, Syriopoulos K, Li G, Sanderink GC, Stelt PF. Detection of proximal caries with high-resolution and standard resolution digital radiographic systems. Dento Maxillo Facial Radiology 2007;36(4):204-10 [Erratum appears in Dento Maxillo Facial Radiology 2007;36(6):374-5]. - PubMed
Blazejewska 2016 {published data only}
    1. Blazejewska A, Dacyna N, Niesiobedzki P. Comparison of the detection of proximal caries in children and youth using DIAGNOcam and bitewing radiovisiography. Dental and Medical Problems 2016;53(7):468-75.
Bussaneli 2015c {published data only}
    1. Bussaneli DG, Restrepo M, Boldieri T, Albertoni TH, Santos-Pinto L, Cordeiro RCL. Proximal caries lesion detection in primary teeth: does this justify the association of diagnostic methods? Lasers in Medical Science 2015;30(9):2239-44. - PubMed
Chawla 2012 {published data only}
    1. Chawla N, Messer LB, Adams GG, Manton DJ. An in vitro comparison of detection methods for approximal carious lesions in primary molars. Caries Research 2012;46:161-9. - PubMed
Cortes 2000 {published data only}
    1. Cortes DF, Ekstrand KR, Elias-Boneta AR, Ellwood RP. An in vitro comparison of the ability of fibre-optic transillumination, visual inspection and radiographs to detect occlusal caries and evaluate lesion depth. Caries Research 2000;34(6):443-7. - PubMed
Coutinho 2014 {published data only}
    1. Coutinho TC, daRocha Costa C. An in vivo comparison of radiographic and clinical examination with separation for assessment of approximal caries in primary teeth. European Journal of Paediatric Dentistry 2014;15(4):371-4. - PubMed
da Silva Neto 2008 {published data only}
    1. da Silva Neto JM, dos Santos RL, Sampaio MC, Sampaio FC, Passos IA. Radiographic diagnosis of incipient proximal caries: an ex-vivo study. Brazilian Dental Journal 2008;19(2):97-102. - PubMed
Dehghani 2017 {published data only}
    1. Dehghani M, Barzegari R, Tabatabai H, Ghanea S. Diagnostic value of conventional and digital radiography for detection of cavitated and non-cavitated proximal caries. Journal of Dentistry (Tehran, Iran) 2017;14(1):21-30. - PMC - PubMed
Diniz 2016 {published data only}
    1. Diniz MB, Cordeiro RC, Ferreira-Zandona AG. Detection of caries around amalgam restorations on approximal surfaces. Operative Dentistry 2016;41(1):34-43. - PubMed
Espelid 1994 {published data only}
    1. Espelid I, Tveit AB, Fjelltveit A. Variations among dentists in radiographic detection of occlusal caries. Caries Research 1994;28(3):169-75. - PubMed
Hietala‐Lenkkeri 2014 {published data only}
    1. Hietala-Lenkkeri AM, Tolvanen M, Alanen P, Pienihäkkinen K. The additional information of bitewing radiographs in the detection of established or severe dentinal decay in 14-year olds: a cross-sectional study in low-caries population. ScientificWorldJournal 2014;2014:175358. - PMC - PubMed
Holtzman 2010 {published data only}
    1. Holtzman J, Pharar J, Lee K, Ahn YC, Tucker T, Sabet S, et al. Ability of optical coherence tomography to detect caries beneath commonly used dental sealants. Lasers in Surgery and Medicine 2010;42:49. - PMC - PubMed
Holtzman 2014 {published data only}
    1. Holtzman JS, Ballantine J, Fontana M, Wang A, Calantog A, Benavides E, et al. Assessment of early occlusal caries pre- and post-sealant application - an imaging approach. Lasers in Surgery and Medicine 2014;46(6):499-507. - PMC - PubMed
Jan 2016 {published data only}
    1. Jan J, Wan Bakar WZ, Mathews SM, Okoye LO, Ehler BR, Louden C, et al. Proximal caries lesion detection using the Canary Caries Detection System: an in vitro study. Journal of Investigative and Clinical Dentistry 2016;7(4):383-90. - PubMed
Kamburoglu 2012 {published data only}
    1. Kamburoglu K, Kolsuz E, Murat S, Yuksel S, Ozen T. Proximal caries detection accuracy using intraoral bitewing radiography, extraoral bitewing radiography and panoramic radiography. Dento Maxillo Facial Radiology 2012;41(6):450-9. - PMC - PubMed
Katge 2016 {published data only}
    1. Katge F, Wakpanjar M, Rusawat B, Shetty A. Comparison of three diagnostic techniques for detecting occlusal dental caries in primary molars: an in vivo study. Indian Journal of Dental Research 2016;27(2):174-7. - PubMed
Kavvadia 2008 {published data only}
    1. Kavvadia K, Lagouvardos P. Clinical performance of a diode laser fluorescence device for the detection of occlusal caries in primary teeth. International Journal of Paediatric Dentistry 2008;18(3):197-204. - PubMed
Kavvadia 2012 {published data only}
    1. Kavvadia K, Lagouvardos P, Apostolopoulou D. Combined validity of DIAGNOdentTM and visual examination for in vitro detection of occlusal caries in primary molars. Lasers in Medical Science 2012;27(2):313-9. - PubMed
Kim 2017 {published data only}
    1. Kim ES, Lee ES, Kang SM, Jung EH, Josselin de Jong E, Jung HI, et al. A new screening method to detect proximal dental caries using fluorescence imaging. Photodiagnosis and Photodynamic Therapy 2017;20:257-62. - PubMed
Kordic 2003 {published data only}
    1. Kordic A, Lussi A, Luder HU. Performance of visual inspection, electrical conductance and laser fluorescence in detecting occlusal caries in vitro. Schweizer Monatsschrift fur Zahnmedizin 2003;113(8):852-9. - PubMed
Krzyzostaniak 2015 {published data only}
    1. Krzyzostaniak J, Kulczyk T, Czarnecka B, Surdacka A. A comparative study of the diagnostic accuracy of cone beam computed tomography and intraoral radiographic modalities for the detection of non-cavitated caries. Clinical Oral Investigations 2015;19(3):667-72. - PMC - PubMed
Kuhnisch 2009 {published data only}
    1. Kuhnisch J, Ifland S, Tranaeus S, Heinrich-Weltzien R. Comparison of visual inspection and different radiographic methods for dentin caries detection on occlusal surfaces. Dento Maxillo Facial Radiology 2009;38(7):452-7. - PubMed
Laitala 2017 {published data only}
    1. Laitala ML, Piipari L, Sampi N, Korhonen M, Pesonen P, Joensuu T, et al. Validity of digital imaging of fiber-optic transillumination in caries detection on proximal tooth surfaces. International Journal of Dentistry 2017;2017:8289636. - PMC - PubMed
Lara‐Capi 2017 {published data only}
    1. Lara-Capi C, Cagetti MG, Lingström P, Lai G, Cocco F, Simark-Mattsson C, et al. Digital transillumination in caries detection versus radiographic and clinical methods: an in vivo study. Dento Maxillo Facial Radiology 2017;46(4):20160417. - PMC - PubMed
Matalon 2003 {published data only}
    1. Matalon S, Feuerstein O, Kaffe I. Diagnosis of approximal caries: bitewing radiology versus the Ultrasound Caries Detector. An in vitro study. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 2003;95(5):626-31. - PubMed
Menem 2017 {published data only}
    1. Menem R, Barngkgei I, Beiruti N, Al Haffar I, Joury E. The diagnostic accuracy of a laser fluorescence device and digital radiography in detecting approximal caries lesions in posterior permanent teeth: an in vivo study. Lasers in Medical Science 2017;32(3):621-8. - PMC - PubMed
Milosavljevic 2016 {published data only}
    1. Milosavljevic A, Westerberg J, Hellen-Halme K. Diagnostic accuracy of carious lesions in digital radiographs at a public dental clinic - can it be improved by optimizing viewing conditions and further education? Swedish Dental Journal 2016;40(2):235-42. - PubMed
Nair 2001 {published data only}
    1. Nair MK, Nair UP. An in vitro evaluation of Kodak Insight and Ektaspeed Plus film with a CMOS detector for natural proximal caries: ROC analysis. Caries Research 2001;35(5):354-9. - PubMed
Nascimento 2018 {published data only}
    1. Nascimento EH, Gaêta-Araujo H, Vasconcelos KF, Freire BB, Oliveira-Santos C, Haiter-Neto F, et al. Influence of brightness and contrast adjustments on the diagnosis of proximal caries lesions. Dento Maxillo Facial Radiology 2018;47(8):20180100. - PMC - PubMed
Nikneshan 2015 {published data only}
    1. Nikneshan S, Abbas FM, Sabbagh S. Detection of proximal caries using digital radiographic systems with different resolutions. Indian Journal of Dental Research 2015;26(1):5-10. - PubMed
Ricketts 1997 {published data only}
    1. Ricketts DN, Whaites EJ, Kidd EA, Brown JE, Wilson RF. An evaluation of the diagnostic yield from bitewing radiographs of small approximal and occlusal carious lesions in a low prevalence sample in vitro using different film types and speeds. British Dental Journal 1997;182(2):51-8. - PubMed
Schaefer 2018 {published data only}
    1. Schaefer G, Pitchika V, Litzenburger F, Hickel R, Kühnisch J. Evaluation of occlusal caries detection and assessment by visual inspection, digital bitewing radiography and near-infrared light transillumination. Clinical Oral Investigations 2018;22(7):2431-8. - PubMed
Shwetha 2017 {published data only}
    1. Shwetha G, Chandra P, Anandakrishna L, Dhananjaya G, Shetty AK, Kamath PS. Validation of different diagnostic aids in detection of occlusal caries in primary molars: an in vitro study. Journal of the Indian Society of Pedodontics and Preventive Dentistry 2017;35(4):301-6. - PubMed
Sinanoglu 2014 {published data only}
    1. Sinanoglu A, Ozturk E, Ozel E. Diagnosis of occlusal caries using laser fluorescence versus conventional methods in permanent posterior teeth: a clinical study. Photomedicine and Laser Surgery 2014;32(3):130-7. - PubMed
Singh 2016 {published data only}
    1. Singh R, Tandon S, Rathore M, Tewari N, Singh N, Shitoot AP. Clinical performance of ICDAS II, radiovisiography, and alternating current impedance spectroscopy device for the detection and assessment of occlusal caries in primary molars. Journal of the Indian Society of Pedodontics and Preventive Dentistry 2016;34(2):152-8. - PubMed
Terry 2016 {published data only}
    1. Terry GL, Noujeim M, Langlais RP, Moore WS, Prihoda TJ. A clinical comparison of extraoral panoramic and intraoral radiographic modalities for detecting proximal caries and visualizing open posterior interproximal contacts. Dento Maxillo Facial Radiology 2016;45(4):20150159. - PMC - PubMed
White 1997 {published data only}
    1. White SC, Yoon DC. Comparative performance of digital and conventional images for detecting proximal surface caries. Dento Maxillo Facial Radiology 1997;26(1):32-8. - PubMed
Wojtowicz 2003 {published data only}
    1. Wojtowicz PA, Brooks SL, Hasson H, Kerschbaum WE, Eklund SA. Radiographic detection of approximal caries: a comparison between senior dental students and senior dental hygiene students. Journal of Dental Hygiene 2003;77(4):246-51. - PubMed
Yoon 2017 {published data only}
    1. Yoon HI, Yoo MJ, Park EJ. Detection of proximal caries using quantitative light-induced fluorescence-digital and laser fluorescence: a comparative study. Journal of Advanced Prosthodontics 2017;9(6):432-8. - PMC - PubMed
Young 2009 {published data only}
    1. Young SM, Lee JT, Hodges RJ, Chang TL, Elashoff DA, White SC. A comparative study of high-resolution cone beam computed tomography and charge-coupled device sensors for detecting caries. Dento Maxillo Facial Radiology 2009;38(7):445-51. - PubMed

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