The presence or absence of visible third molars negatively influences periodontal Outcomes. More subjects had at least 1 visible molar (62%) as compared with subjects with no visible. Visible third molars were more likely to be significantly older, to be receiving medical assistance, to have used tobacco before pregnancy.
Original Description:
Original Title
The Presence of Visible Third Molars Negatively Influences Periodontal Outcomes in the Maternal Oral Therapy to Reduce Obstetric Risk Study
The presence or absence of visible third molars negatively influences periodontal Outcomes. More subjects had at least 1 visible molar (62%) as compared with subjects with no visible. Visible third molars were more likely to be significantly older, to be receiving medical assistance, to have used tobacco before pregnancy.
The presence or absence of visible third molars negatively influences periodontal Outcomes. More subjects had at least 1 visible molar (62%) as compared with subjects with no visible. Visible third molars were more likely to be significantly older, to be receiving medical assistance, to have used tobacco before pregnancy.
Negatively Inuences Periodontal Outcomes in the Maternal Oral Therapy to Reduce Obstetric Risk Study Kevin L. Moss,* Steven Offenbacher, DDS, PhD,y James D. Beck, PhD,z and Raymond P. White Jr, DDS, PhDx Purpose: To assess the relationship between the presence or absence of visible third molars and out- comes for periodontal inammatory disease. Methods: Obstetric subjects, at enrollment in an institutional review boardapproved, multisite study, Maternal Oral Therapy to Reduce Obstetric Risk (N = 1,798), were divided into 2 groups, those with no visible third molars (n = 692) and those with at least 1 visible third molar (n = 1,106), the predictor vari- ables for this study. The principal outcome variables were the patient-level periodontal status of the rst/second molars: mean periodontal probing depths, mean attachment levels, and mean extent scores. Periodontal disease severity also was assessed by criteria from the Oral Conditions and Pregnancy trial and the Centers for Disease Control and Prevention/American Academy of Periodontology. Outcomes accord- ing to the presence or absence of third molars were compared with c 2 statistics and multivariable analyses. Signicance was set at P < .05. Results: Signicantly more subjects had at least 1 third molar (62%) as compared with subjects with no visible third molar (38%) (P < .01). Ethnic characteristics of the 2 groups were similar. Overall, more subjects were white (61%), with most identifying their ethnicity as Latino. African-American subjects were well represented (37%). Subjects with a visible third molar were more likely to be signicantly older, to be receiving medical assistance, and to have used tobacco before pregnancy. If subjects had at least 1 visible third molar, the mean rst/second molar probing depths, attachment levels, and scores for bleed- ing on probing were signicantly greater even after adjustment for covariates. On the basis of either Oral Conditions and Pregnancy criteria or Centers for Disease Control and Prevention/American Academy of Periodontology criteria, subjects were signicantly more likely to have moderate or severe periodontal dis- ease if a third molar was detected. Conclusion: If at least 1 visible third molar was detected in subjects in the Maternal Oral Therapy to Reduce Obstetric Risk study at enrollment as compared with no detected third molars, periodontal out- comes were signicantly worse. 2013 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 71:988-993, 2013 Received from the School of Dentistry, University of North Carolina, Chapel Hill, NC. *Research Applications Specialist. yChair and OraPharma Distinguished Professor, Department of Periodontology. zKenan Distinguished Professor, Department of Dental Ecology, and Executive Associate Dean. xDalton L. McMichael Distinguished Professor, Department of Oral and Maxillofacial Surgery. Funding was provided by the Oral and Maxillofacial Surgery Foun- dation and American Association of Oral and Maxillofacial Surgeons, as well as oral and maxillofacial surgery departmental funds fromthe Dental Foundation of North Carolina. Conict of Interest Disclosures: None of the authors reported any disclosures. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC 27599-7450; e-mail: ray_white@dentistry.unc.edu 2013 American Association of Oral and Maxillofacial Surgeons 0278-2391/13/00093-1$36.00/0 http://dx.doi.org/10.1016/j.joms.2013.01.012 988 Population or clinical trial data from third molars re- main limited because third molars are often missing in those aged over 30 years without data on the reasons for removal, and third molar data fromyoung and older subjects often have not been collected or have been ex- cluded in the analyses. 1-4 Moss et al 5 have shown that periodontal probing measures could be assessed as accurately on third molars as on other teeth. Subse- quently, third molar periodontal data have been re- ported more often from both clinical and population studies. 6-8 On the basis of the high prevalence of increased peri- odontal probing depths (PDs) in molar regions of the mouth associated with retained third molars, White et al 9 suggested that inyoung adults the presence of a vis- ible third molar alone may be a risk indicator for more se- vere periodontal inammatory disease requiring clinical assessment for conrmation. Data from 1,020 subjects at enrollment in the Oral Conditions and Pregnancy (OCAP) trial conducted at a single clinical academic cen- ter supported this association. 10 Visible third molars were detected in 405 subjects at enrollment. Subjects with visible third molars were signicantly more likely to have moderate/severe periodontal disease and less likely to be periodontally healthy. If at least 1 third molar was visible, the odds for more severe periodontal inam- matory disease were more than double as compared with subjects with no visible third molars, withthe inves- tigators controlling for covariates such as tobacco use or low socioeconomic status. The specic aims of these analyses were to assess the relationship between the presence of visible third molars and clinical indicators at the rst/second mo- lars of periodontal inammatory disease in a multisite study of obstetric subjects, the Maternal Oral Therapy to Reduce Obstetric Risk (MOTOR) study. In addition, subjects level of periodontal disease according to the presence or absence of third molars was categorized by the recently promulgated Centers for Disease Con- trol and Prevention (CDC)/American Academy of Peri- odontology (AAP) classication system. Methods SAMPLE The MOTORstudy was an institutional reviewboard approved, National Institutes of Healthsupported trial enrolling pregnant subjects with clinically de- tected periodontal disease to assess the impact of periodontal treatment on obstetric outcomes, preterm birth, and low birth weight. 8 Subjects at 3 academic clinical centers and afliated clinics (Duke University, University of Alabama at Birmingham, and The Uni- versity of Texas at San Antonio) were enrolled over a 4-year period beginning in 2003 and randomized to periodontal treatment before ultrasound conrmed 23 weeks of gestation or delayed treatment until after delivery. Treatment at the stated intervals for both study groups consisted of mechanical debridement of supragingival and subgingival biolm accompanied by oral hygiene instructions. DATA COLLECTION To be eligible for the MOTORstudy, pregnant subjects had to have at least 20 teeth in total and a minimum of 3 teeth with a clinical attachment level (AL) of at least 3 mm, the inclusion criteria for the study. We excluded subjects with criteria that might impact periodontal out- comes, conditions suchas diabetes mellitus, or a require- ment for antibiotic prophylaxis as part of periodontal assessment. Conducted by trained, calibrated dental ex- aminers, subjects periodontal examinations included periodontal PDs, 6 sites per tooth on all visible teeth in- cluding the third molars. PDs were rounded to the low- est whole number (eg, a measured PD of 4.8 mm was recorded as a PD of 4 mm). No radiographs were avail- able to complement the clinical examinations. The arti- cle by Offenbacher et al 8 provides additional details on the design and conduct of the MOTOR study. DATA ANALYSES Specic to our assessment, all obstetric subjects at enrollment were divided into 2 groups, those with no visible third molars and those with at least 1 visible third molar, the principal predictor variables for the analyses. Covariates included study center, race/ethnic- ity, age, smoking before pregnancy, body mass index (BMI), and medical assistance status. Because molar teeth were more affected than teeth more anterior in subjects in the OCAP trial, outcome variables chosen for these analyses were the patient-level periodontal status of the rst/second molar teeth categorized by the following clinical indicators: mean periodontal PDs, mean ALs, and mean percentage of rst or second molars with bleeding on probing (BOP). 11 We per- formed multivariate modeling with SAS Proc GLM (SAS Institute, Cary, NC) to calculate the least squares means, adjusting for the study outcome variables and covariates. Variables were selected for inclusion into the adjusted models based on a signicant (P < .05) bivariate association with outcome. In addition, race/ ethnicity was included because it is often a standard control variable. Signicance for reported outcomes was set at P < .05. It has been difcult to compare subjects periodontal severity among clinical and population studies because no single standard for periodontal pathology has been applied. For comparison purposes, we have reported outcomes for patient-level periodontal disease severity compared by presence or absence of third molars, based on denitions from the prior reported study of MOSS ET AL 989 obstetric subjects inthe OCAPtrial and the most current, recently derived classication fromthe combined efforts of the CDCand AAP. 10,12 In the OCAP trial, subjects were categorized as healthy/disease absence, mild disease, and moderate/severe disease. Healthy was dened as no periodontal probing site (PD) of 4 mm or greater and no probing sites greater than 3 mm with BOP; mild disease, at least 1 PD of 4 mm or greater or at least 1 PD of 3 mm or greater with BOP up to a maximum of 15 PD sites of 4 mm or greater; and moderate/severe disease, 15 or more PD sites of 4 mm or greater. On the basis of CDC/AAP criteria, subjects were categorized as healthy/mild disease, moderate disease, or severe disease. Healthy/mild disease was dened as neither moderate nor severe disease. Moderate disease was dened as at least 2 teeth with interproximal probing sites with clinical ALs of at least 4 mm or at least 2 teeth with interproximal PDs of at least 5 mm. Severe disease was dened as at least 2 teeth with interproximal probing sites with clinical ALs of at least 6 mm and at least 1 tooth with an interproximal PD of at least 5 mm. In addition, patient-level extent scoresthe number of probing sites with BOP (numerator) of all possible probing sites (denominator) for visible teethwere reported. Outcomes for the severity of disease based on the 2 classication systems by the presence or absence of third molars were compared by use of c 2 statistics. Signicance was set at P < .05. Results Data from 1,798 obstetric subjects at enrollment were available for analyses. Signicantly more subjects had at least 1 visible third molar (1,106 [62%]) as com- pared with subjects with no visible third molars (692 [38%]) (P < .01) (Table 1). Ethnic characteristics of the 2 groups were similar. Most subjects were white (61%), but African-American subjects were well repre- sented (37%). Latino was the reported ethnicity for 85% of the white subjects; fewer than 10% of subjects were non-Latino white. Subjects with a visible third mo- lar, as compared with those with no visible third molars, were more likely to be signicantly older, with a mean age of 26 years versus 24.3 years (P < .01); to have a higher mean BMI, 28.8 versus 27.7 (P < .01); to re- ceive medical assistance, 63% versus 37% (P = .03); and to have used tobacco before pregnancy, 56%versus 44% (P = .04). In subjects with at least 1 visible third molar, the mean rst/second molar PD was signicantly greater than that in subjects who did not have a third molar vis- ible, 3.74 mm versus 3.50 mm (P < .01) (Table 2). Simi- larly, for subjects with at least 1 visible third molar, the mean rst/second molar AL was signicantly greater compared with subjects with no visible third molars, 2.06mmversus 1.96mm(P<.01). Themeanpercentage of rst/second molars with BOP was greater if a third molar was visible as compared with no visible third mo- lars, 63.9% versus 53.9% (P < .01). These relationships continued to be signicantly different (P < .01) after we adjusted for the following covariates: study clinical center, race/ethnicity, age, smoking before pregnancy, BMI, and medical assistance status (Table 3). Table 1. SUBJECTS CHARACTERISTICS (N = 1,798) No Third Molar Visible (n = 692) $1 Third Molar Visible (n = 1,106) P Value Race/ethnicity .19 African American 240 (34.8%) 430 (39.1%) White including Latino 440 (63.9%) 655 (59.5%) Other 9 (1.3%) 15 (1.4%) Mean maternal age (SD) (y) 24.3 (5.8) 26.0 (5.1) <.0001 Mean BMI at baseline (SD) 27.7 (6.8) 28.9 (6.8) .0007 Married .57 Yes 328 (47.4%) 509 (46.0%) No 364 (52.6%) 597 (64.0%) Medical assistance .03 Yes 405 (58.5%) 693 (64.5%) No 276 (41.5%) 381 (35.5%) Smoke before pregnancy .04 Yes 129 (18.7%) 166 (15.0%) No 562 (81.3%) 937 (85.0%) Note: Of white subjects, 85% identied their ethnicity as Latino (52% of the total number of subjects). Moss et al. Visible Third Molars and Periodontal Outcomes. J Oral Maxillofac Surg 2013. Table 2. PATIENT-LEVEL CLINICAL PERIODONTAL OUTCOMES FOR FIRST AND SECOND MOLARS AT ENROLLMENT First and Second Molar Measurement No Third Molar Visible (n = 667) $1 Third Molar Visible (n = 1,106) P Value Mean PD (SE) (mm) 3.50 (0.02) 3.74 (0.02) <.0001 Mean AL (SE) (mm) 1.96 (0.02) 2.06 (0.02) <.0001 Mean % BOP (SE) 53.9 (1.16) 63.9 (0.76) <.0001 Note: Signicance was set at P < .05. Moss et al. Visible Third Molars and Periodontal Outcomes. J Oral Maxillofac Surg 2013. 990 VISIBLE THIRD MOLARS AND PERIODONTAL OUTCOMES The mean PD for rst/second molars was greater if subjects had 4 third molars visible as compared with only 1 third molar visible, 3.83 mm versus 3.65 mm (data not shown). Similarly, the mean AL for rst/second molars was greater if subjects had4thirdmolars visible as comparedwithonly1thirdmolar visible, 2.07mmversus 1.98 mm. The mean percentage of rst/second molars with BOP followed the same pattern: if subjects had 4 third molars visible as compared with only 1 third molar visible, the extent for BOP was 66.6% versus 64.7%. Because subjects in the MOTOR study had to have evidence of at least mild periodontal disease as an in- clusion criterion, most subjects had at least 1 PD of at least 5 mm or a probing site with BOP, detected more often on molars. However, if subjects had at least 1 third molar visible, subjects were signicantly more likely to have at least 1 PD of 5 mm or greater as com- pared with subjects with no visible third molar, 96% versus 84% (P < .01) (Table 4). Similarly, subjects hav- ing an extent of BOP of at least 10% was signicantly more likely if a visible third molar was detected as com- pared with no visible third molar (P < .01). On the basis of either OCAP or CDC/AAP criteria for the absence or presence of periodontal disease, subjects were signicantly more likely to have moderate or se- vere disease if a third molar was detected (P < .01) (Table 4). For example, by CDC/AAP criteria, moderate or severe disease was detected in 61%MOTOR subjects if a third molar was visible compared with 41% of sub- jects with no third molar visible. Similarly, based on OCAP criteria, 93% of subjects had moderate or severe disease if a third molar was visible compared with 77% of subjects with no third molar visible. Discussion These analyses of data from a population of obstetric subjects enrolled in the rst trimester of pregnancy were designed to assess the relationship between the presence of visible third molars and clinical indicators of periodontal inammatory dis- ease. If subjects in the MOTOR study had at least 1 third molar visible at enrollment, clinical indicators of more severe periodontal inammatory disease for the rst and second molarsperiodontal PDs, ALs, and scores for BOPwere detected more often as compared with subjects with no visible third mo- lars. To be included in the MOTOR study, subjects could not be periodontally healthy. Having at least 20 teeth in total and 3 teeth with periodontal ALs of 3 mm or greater were important inclusion criteria for the principal aims of the MOTOR study. However, subjects with at least 1 visible third molar at enroll- ment in the MOTOR study were more likely to have moderate or severe periodontal disease detected throughout the entire mouth, as compared with sub- jects with no visible third molars, based on the clas- sication used in the OCAP trial or the more recently promulgated CDC/AAP classication. 10,12 Although similarities in the study of pregnant sub- jects enrolled in the OCAP trial and MOTOR study exist, important differences suggest that the periodontal out- comes that we detected are more than complementary. In both the OCAP trial and the MOTOR study, periodontal assessment by trained, calibrated exam- iners was based on full-mouth periodontal probing at Table 3. PATIENT-LEVEL CLINICAL PERIODONTAL OUTCOMES FOR FIRST AND SECOND MOLARS AT ENROLLMENT ADJUSTED FOR DIFFERENCES IN STUDY CLINICAL CENTER, RACE/ETHNICITY, AGE, SMOKING BEFORE PREGNANCY, BMI, AND MEDICAL ASSISTANCE First and Second Molar Measurement No Third Molar Visible (n = 667) $1 Third Molar Visible (n = 1,106) P Value Mean PD (SE) (mm) 3.54 (0.02) 3.72 (0.02) <.0001 Mean AL (SE) (mm) 1.95 (0.02) 2.06 (0.01) <.0001 Mean % BOP (SE) 55.2 (0.99) 62.6 (0.78) <.0001 Note: Signicance was set at P < .05. Moss et al. Visible Third Molars and Periodontal Outcomes. J Oral Maxillofac Surg 2013. Table 4. PREVALENCE OF SUBJECTS OVERALL CLINICAL PERIODONTAL CONDITIONS BY PRESENCE OF AT LEAST 1 VISIBLE THIRDMOLAR (N= 667) OR NO VISIBLE THIRD MOLARS (N = 1,106) No Third Molar Visible [n (%)] $1 Third Molar Visible [n (%)] P Value CDC/AAP criteria <.0001 Healthy/mild 394 (59.1) 432 (39.1) Moderate 263 (39.4) 632 (57.1) Severe 10 (1.5) 42 (3.8) OCAP criteria <.0001 Healthy 0 (0.0) 0 (0.0) Mild 153 (23.0) 80 (7.2) Moderate/severe 514 (77.0) 1,026 (92.8) PD <.0001 All PDs <5 mm 106 (15.9) 43 (3.9) $1 PD $5 mm 561 (84.1) 1,063 (96.1) Extent of BOP <.0001 <10% 117 62 $10% 550 1,044 Note: Patient-level extent scores for BOP were calculated as the number of probing sites with BOP (numerator) of all possible probing sites (denominator) for all teeth. Moss et al. Visible Third Molars and Periodontal Outcomes. J Oral Maxillofac Surg 2013. MOSS ET AL 991 6 designated sites for all visible teeth including the third molars. No radiographs were available in either study to complement clinical examinations. However, as com- pared with the OCAP trial, which was conducted at a single clinical center, more subjects were enrolled in the MOTOR study at multiple clinical centers, a third molar was detected more frequently in MOTOR sub- jects, the racial/ethnic mix was more diverse inMOTOR subjects, and more subjects in the MOTOR study were receiving medical assistance. Subjects in the MOTOR study (N = 1,798) were en- rolled at 3 clinical centers as compared with the single clinical center in the OCAP trial (N = 1,020). Subjects in the MOTOR study were more likely to have a third molar visible (62%) as compared with those in the OCAP trial (40%). Fewer subjects in the MOTOR study were African American (37%) compared with the OCAP trial (46%). Most white subjects in the MOTOR study (85%) reported their ethnicity as Latino, a popu- lation with limited data on third molar periodontal inammatory disease in the literature. Although eligi- bility differs by state, subjects in the MOTOR study were more likely to be receiving medical assistance (61%) than were those in the OCAP trial (18%). In summary, data from the OCAP trial and MOTOR add support to the possibility that in young adults the presence of a visible third molar alone may be a risk indicator for more severe periodontal inammatory disease, suggesting that a clinical examination is im- portant for conrmation. 9 Clinicians may question the clinical importance of the small differences in mean rst/second molar PDs between groups that we report and the relationship of these differences to periodontal pathology. As an ex- ample, the difference inrst/second molar mean PDbe- tween subjects with visible third molars and no visible third molars was 0.24 mm. If considered at only a single probing site, clinicians could dismiss this small differ- ence without reection. However, the 6 periodontal probing sites for each tooth approximate the total sur- face area of the biolm-gingival interface (BGI) around that tooth. For this analysis, the mean difference in PD for each probing site must be amplied by multiply- ing 6 probing sites measured for all rst/second molars in each patient, a total of 48 probing sites, yielding a mean increase in PD of 11.5 mm per patient. This dif- ference reects a substantial and clinically important in- creased surface area at the BGI as compared with subjects with no visible third molar. Any increase in PD is more often found at the deeper periodontal prob- ing sites. The overall greater surface area of the BGI for affected subjects contributes to an enhanced anaerobic clinical environment for possible colonization by sub- gingival pathogens and resulting increased expression of inammatory mediators in the gingival crevicular uid and blood. Clinicians should exercise some caution when apply- ing our ndings to individual subjects. Subjects in the MOTOR study and OCAP trial were enrolled for a study of obstetric outcomes, not a study of the association be- tween third molars and levels of periodontal inamma- tory disease. Although subjects in the MOTOR study were a diverse group, the subjects were not representa- tive of the US population. All subjects were pregnant; subjects in the same age range who were men or who were not pregnant may have different outcomes. Few Asians were included, non-Latino white subjects were under-represented, and Latino subjects were over- represented, comprising 52% of the study population. In both the MOTOR study and OCAP trial, 16% of sub- jects used tobacco before pregnancy, a marginally lower outcome than might be expected for this age group and socioeconomic status. 13 Subjects knowledge about the risks of smoking while being pregnant may account for the lower prevalence of tobacco use. However, the data we report do suggest that the association between third molars and periodontal inammatory disease should be studied further with a population more representative of the US population. How might clinicians apply our data to their subjects? Once third molars are exposed to the oral cavity and can be probed, oral ora colonize on the surfaces in a non- sheddable biolm. 14 Because the third molars are the most posterior teeth in each jaw, erupting most often af- ter jawgrowth is complete, individuals are likely to have deeper periodontal PDs, harboring anaerobic pathogens that are difcult to eradicate by mechanical debridement alone. 15,16 The data from subjects in the MOTOR study suggest again that in young adults, retained third molars require careful monitoring for the presence of deeper periodontal PDs as potential sources for the initiation of periodontal inammatory disease. If periodontal PDs of at least 4 mm are detected, removal of the third molars should be considered as the only current treatment available to effectively reduce the local and systemic inammatory immune response to pathogenic bacteria. References 1. Hugoson A, Kugelberg CF: The prevalence of third molars in a Swedish population, an epidemiological study. Commun Dent Health 5:121, 1988 2. Thomson WM, Broadbent JM, Welch D, et al: Cigarette smoking and periodontal disease among 32-year-olds: Aprospective study of a representative birth cohort. J Clin Periodontol 34:828, 2007 3. Tanner ACR, Kent R Jr, Van Dyke T, et al: Clinical and other risk in- dicators for early periodontitis in adults. J Periodontol 76:573, 2005 4. Elter JR, Cuomo C, Slade GD, et al: Relationship of third molars to periodontal health in NHANES III. J Oral Maxillofac Surg 62: 440, 2004 5. Moss KL, Mauriello SM, Ruvo AT, et al: Reliability of third molar probing measures and the systemic impact of periodontal pa- thology. J Oral Maxillofac Surg 64:652, 2006 6. Moss KL, Beck JD, Mauriello SM, et al: Risk indicators for third molar caries and periodontal disease in senior adults. J Oral Max- illofac Surg 65:958, 2007 992 VISIBLE THIRD MOLARS AND PERIODONTAL OUTCOMES 7. Garaas R, Moss K, Fisher E, et al: Prevalence of third molars in middle-aged and older Americans with no caries experience or periodontal pathology. J Oral Maxillofac Surg 69:463, 2011 8. Offenbacher S, Beck JD, Jared HL, et al: Effects of periodontal ther- apy on rate of preterm delivery. Obstet Gynecol 114:551, 2009 9. White R, Fisher E, Phillips C, et al: Visible third molars as a risk indicator for increased periodontal probing depths. J Oral Max- illofac Surg 69:92, 2011 10. Moss KL, Serlo AD, Offenbacher S, et al: The oral and systemic impact of third molar periodontal pathology. J Oral Maxillofac Surg 65:1739, 2007 11. Moss KL, Beck JD, Offenbacher S: Clinical risk factors associated with incidence and progression of periodontal conditions in pregnancy. J Clin Periodontal 32:493, 2005 12. Page RC, Eke PI: Case denitions for use in population-based sur- veillance of periodontitis. J Periodontol 78:1387, 2007 13. Centers for Disease Control and Prevention (CDC): Vital signs: Current cigarette smoking among adults aged $18 yearsUnited States 2005-2010. MMWR Morb Mortal Wkly Rep 60:1207, 2011 14. Socransky SS, Haffajee AD, Cugini MA, et al: Microbial com- plexes in subgingival plaque. J Clin Periodontol 25:134, 1998 15. Rantanen AV: The age of eruption of the third molar teeth. A clin- ical study based on Finnish university students. Acta Odontol Scand Suppl 48:1, 1967 16. Fisher E, Blakey G, Offenbacher S, et al: The clinical impact of mechanical debridement of sub-gingivalbiolm on third molar periodontal pathology. J Oral Maxillofac Surg 71:467, 2013 MOSS ET AL 993