Pathophysiology/Complications ORIGINAL ARTICLE

Prevalence and Risk Factors for Neuropathy in a Canadian First Nation Community

1 SHARON G. BRUCE, PHD Limited information exists on diabe- 2 T. KUE YOUNG, MD, DPHIL tes foot complications in Canadian First Nation populations. Depending on case definition, estimates of neuropathy range OBJECTIVE — The purpose of this study was to determine the prevalence of and risk factors from 12% among a pediatric population for diabetic neuropathy in a Canadian First Nation population. to 46% among adults (9–12). Hanley et al. (10) reported the prevalence of neu- RESEARCH DESIGN AND METHODS — This was a community-based screening ropathy to be 46% among adult members study of 483 adults. Measures included glucose, A1C, cholesterol, triglycerides, homocysteine, of the Sandy Lake First Nation (northern hypertension, waist circumference, height, weight, and foot examinations. Neuropathy was Ontario), with neuropathy being defined defined as loss of protective sensation determined through application of a 10-g monofilament. as a score of Ն2 on a modified Michigan RESULTS — Twenty-two percent of participants had a previous diagnosis of diabetes, and Neuropathy Screening Instrument. Reid 14% had new diabetes or impaired fasting glucose (IFG). The prevalence of neuropathy in- et al. (11) performed foot examinations, creased by glucose level: 5% among those with normal glucose levels, 8% among those with new interviews, and chart reviews on a sample IFG and diabetes, and 15% among those with established diabetes (P Ͻ 0.01). Those with (139 of 322) of individuals with diabetes neuropathy were more likely to have foot deformities (P Ͻ 0.01) and callus (P Ͻ 0.001) than in one northern First Nation those without neuropathy. Among those with dysglycemia (Ն6.1 mmol/l), the mean number of community and found that 82% had foot problems for those with insensate feet was 3 compared with 0.3 among those with sensation some form of diabetes-related foot prob- Ͻ (P 0.001). In multivariate logistic regression female sex, low education, A1C, smoking, and lem. The average number of foot prob- homocysteine were independently associated with neuropathy, after controls for age. lems per individual was three. CONCLUSIONS — Neuropathy prevalence is high, given the young age of our participants Neuropathy was found among 24% of (mean 40 years) and was present among those with undiagnosed diabetes. The high number and participants, past or present foot ulcer in type of foot problems places this population at increased risk for ulceration; the low level of foot 15%, and 3% had had an amputation. care in the community increases the risk. Homocysteine is a risk factor that may be related to Chuback et al. (12) completed chart re- lifestyle and requires further investigation. views, interviews, and examinations on 110 Aboriginal attendees at an urban pe- Diabetes Care 31:1837–1841, 2008 diatric diabetes clinic in Manitoba and found a high prevalence of foot abnormal- iabetes-related foot complications foot ulcer (6). Of these, the most impor- ities (age range of participants was 12–17 are an increasingly common yet tant contributory factor for foot ulcer- years). Neuropathic symptoms (numb- D understudied problem (1) and ation is peripheral neuropathy; when ness, aching, and tingling) were found in include conditions such as neuropathy, neuropathy is absent, ulceration is rare 12% of participants. These results are foot deformities, ulcers, and lower- (5,7). It is estimated that 80% of foot ul- especially disturbing, considering the extremity amputation. The impact of cers may be prevented through early de- short duration of diabetes in this pediat- diabetes-related foot complications on tection (5). Screening for neuropathy has ric population. quality of life and health care costs is therefore been identified as an effective The study community reported in significant, especially for ulcers and strategy in the prevention process (8). this article belongs to a tribal council for amputation (2–4). The lifetime risk for The purpose of this research was to deter- which the rate of diabetes-related ampu- foot ulceration among those with diabe- mine the prevalence and determinants of tation (6.2 per 1,000) is twice as great as tes is 15% (5,6), and foot ulceration pre- diabetic neuropathy in a Canadian First that for other people in the cedes amputation in 80% of patients (5). Nation community that has a significantly province (3.1 per 1,000) and 30 times The major risk factors for diabetic foot greater rate of diabetes-related amputa- greater than the rate for non–First Nations ulceration are peripheral neuropathy, pe- tion than that for the general population people in the province (0.19 per 1,000) ripheral vascular disease, and previous (9). (9). Thus, diabetes-related foot problems are emerging as a serious complication of ●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●● diabetes among First Nations people of From the 1Department of Community Health Services, University of Manitoba, Winnipeg, Manitoba, Can- . We undertook a screening study ada; and the 2Department of Public Health Services, University of Toronto, Toronto, Ontario, Canada. Corresponding author: Sharon Bruce, [email protected]. in a community with a high rate of ampu- Received 6 February 2008 and accepted 19 May 2008. tation to determine the burden of neurop- Published ahead of print at http://care.diabetesjournals.org on 28 May 2008. DOI: 10.2337/dc08-0278. athy and to initiate secondary prevention © 2008 by the American Diabetes Association. Readers may use this article as long as the work is properly strategies. cited, the use is educational and not for profit, and the work is not altered. See http://creativecommons. The data for this article are from a org/licenses/by-nc-nd/3.0/ for details. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby larger screening study for diabetes and di- marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. abetes complications conducted in 2003

DIABETES CARE, VOLUME 31, NUMBER 9, SEPTEMBER 2008 1837 Neuropathy in a First Nation community among adult members of the Sandy Bay cholesterol was measured by a direct en- RESULTS — Table 1 contains demo- First Nation. Sandy Bay First Nation is zymatic method (Boehringer Mannheim). graphic and health risk information. Men located in Manitoba, Canada. The com- LDL was calculated via the following for- and women were equally represented. munity is located about 200 km from mula but not on samples that had visible The sample was representative of the eli- Winnipeg, the nearest major urban cen- chylomicrons or triglycerides Ͼ4.52 gible adult community population for age ter, and is accessible by road year-round. mmol/l: and sex (Table 2). The level of employ- The on-reserve population as of Decem- ment is low for both sexes. Women were ber 2001 was 2,968, of which 35% are ϭ significantly more likely than men to re- aged Ͻ18. LDL cholesterol total cholesterol port having completed at least grade 9. Ϫ HDL cholesterol Ϫ (0.46 The majority of participants were current RESEARCH DESIGN AND smokers. Mean pack-years smoked was METHODS — As part of a larger ϫ triglycerides) about 8 for both sexes. Approximately screening study for diabetes and diabetes 40% of men and women have hyperten- complications, all nonpregnant commu- sion. Although obesity is a major problem Ն Apolipoproteins A and B were mea- nity members aged 18 years were in- sured by the Beckman APA and APB tests, in both men and women, the problem is vited to participate. A total of 483 respectively (Beckman Array Systems). significantly greater among women (15). community members participated, 36% Of the participants, 29% had diabetes; 7% ϭ Quantitative determination of APA and of all eligible adults (n 1,356). Full foot APB was completed by rate nephelome- (35 of 483) were new diagnoses, and 22% examinations were completed for 467 try. Total fasting homocysteine was de- (105 of 483) had a previous diagnosis of participants. termined by high-performance liquid diabetes upon entry to the study. A fur- chromatography with fluorometric ther 7% were found to have IFG. No sig- Assessment of neuropathy detection. nificant differences in glycemic status Neuropathy was defined as the loss of Hypertension. Hypertension was de- were found between men and women. protective sensation determined through Ͼ The mean age of those with dysglycemia fined systolic blood pressure 140 Ϯ application of the 10-g Semmes- mmHg or diastolic blood pressure Ͼ90 (44.51 11.97 years) was significantly Weinstein monofilament wire system. greater than for those with normal glu- mmHg or a previous diagnosis with Ϯ Ͻ Using a standardized questionnaire, a reg- medications. cose values (34.01 10.77 years; P istered nurse ascertained experience of 0.001), with dysglycemia being defined Anthropometric measures. Height, Ն foot pain, numbness, and tingling and weight, and waist and hip circumferences as FBG 6.1 mmol/l or previous diagno- then completed a foot examination for de- were measured using standard tech- sis of diabetes. formities, calluses, preulcers, ulcers, toe- niques (14). nail integrity, and amputation. After this Smoking. Current and past smoking sta- examination, the nurse applied the mono- tus and number of cigarettes smoked per Neuropathy filament to 10 sites on the foot. Partici- day were determined using a standard- Neuropathic foot problems by glycemic pants who were unable to sense the ized questionnaire. Pack-years was calcu- status are listed in Table 3. Overall, 34 monofilament on one or more sites were lated as number of packs per day (one participants (7%) had neuropathy. A sig- defined as insensate (13). Individuals pack ϭ 20 cigarettes) multiplied by num- nificant progression in symptom occur- who had a previous foot ulcer (n ϭ 1) or rence is noted for all categories of ϭ ber of years smoked. toe amputation (n 3) were placed in the Demographic information. Standard neuropathic problems by glycemic status. neuropathy category. demographic information and diabetes Neuropathy was present in those with history were derived via questionnaire. normal glucose levels (5%), was increased Risk factors for neuropathy in those with newly discovered IFG or di- Glucose. Fasting samples were obtained abetes (8%), and was highest in those after an overnight 12-h fast. Glucose lev- Analysis with established diabetes (15%). Of the els were determined using the hexoki- Demographic, anthropomorphic, and participants, 34 (7%) reported numbness nase/glucose-6-phosphate dehydro- health risk characteristics were compared and tingling and 38 (8%) reported foot genase assay. A1C determination was by sex using ␹2 tests for categorical vari- pain; 6 participants reported both. based on the turbidimetric inhibition im- ables and Kruskal-Wallis nonparametric Women were more likely to report numb- munoassay for hemolyzed whole blood. tests for continuous variables. Means Ϯ ness and/or tingling (P Ͻ 0.05). Of the Participants with fasting glucose values SD are reported. ␹2 tests for linear associ- women, 9% (21 of 240) had insensate feet Ն5.8 mmol/l were requested to return for ation were used to assess differences in compared with 6% (13 of 227) of men. a second sample, with the average of the foot problems by glycemic status. ␹2 tests Significant differences in age were found two samples being used in analysis. Dia- were used to assess differences in foot between those with and without neurop- betes was defined as a fasting blood glu- problems by protective sensation. Tests athy. The mean age of those with neurop- cose (FBG) Ն7.0 mmol/l. Impaired were two-tailed with P Ͻ 0.05 taken as athy was 42.5 Ϯ 12.5 years, whereas the fasting glucose (IFG) was defined as FBG significant. Multivariate logistic regres- mean age of those without neuropathy of 6.1–6.9 mmol/l. sion was used to estimate odds ratios for was 36.7 Ϯ 11.9 years (P Ͻ 0.01). Among Lipids and amino acids. Total choles- the presence of neuropathy with 95% CIs. the participants who reported a previous terol and triglycerides were determined P values were two-tailed. Statistical anal- diagnosis of diabetes, no significant dif- via enzymatic colorimetric methods yses were performed using SPSS (version ferences in time since diagnosis were (CHOD-PAP and GPO-PAP; Boehringer 15; SPSS, Chicago, IL) and SAS (version found between those with and without Mannheim, Mannheim, Germany). HDL 8; SAS Institute, Cary, NC). neuropathy and only 22% had previously

1838 DIABETES CARE, VOLUME 31, NUMBER 9, SEPTEMBER 2008 Bruce and Young

Table 1—Characteristics and health risk profile of the study population by sex nificantly greater than that among those with sensation (0.27), with foot problems Variable Male Female P value defined as pain, numbness, tingling, cal- lus, nail pathological changes, foot defor- n 230 (48) 253 (52) mity, preulcer, current or past ulcer, and Age (years) 37.3 Ϯ 12.5 38.2 Ϯ 12.1 0.373 amputation (P Ͻ 0.001). Age-group (years) Using multivariate logistic regression, 18–29 73 (32) 70 (28) 0.728 we sought to determine factors associated 30–39 65 (28) 79 (31) with neuropathy (Table 4). Variables in- 40–49 49 (21) 59 (23) cluded in the modeling process were 50ϩ 43 (19) 45 (18) those that were significantly associated Education with neuropathy in bivariate ␹2 testing. Grade 9 or higher 89 (39) 131 (54) Ͻ0.01 These variables were age (P Ͻ 0.01), ed- ϽGrade 9 138 (61) 111 (46) ucation (P Ͻ 0.01), employment status Employment status (P Ͻ 0.01), hypertension (P Ͻ 0.05), A1C Employed 60 (26) 77 (31) 0.265 (P Ͻ 0.01), apolipoprotein A (P Ͻ 0.05), Not employed 169 (74) 170 (69) homocysteine (P Ͻ 0.05), and pack-years Speak aboriginal language* smoked (P Ͻ 0.01). Backwards stepwise Yes 204 (89.5) 204 (83) 0.061 logistic regression was performed using No 24 (10.5) 41 (17) the preceding variables and sex. The final Current smoker logistic regression model for presence Yes 165 (73) 184 (75) 0.529 of neuropathy included sex (female No 62 (27) 60 (25) sex), education (completion of less than Pack-years smoked† 8.02 Ϯ 12.46 7.48 Ϯ 10.68 0.921 grade 9), A1C, pack-years smoked, and Hypertension‡ homocysteine. Yes 93 (41) 108 (44) 0.446 The odds of having neuropathy were No 135 (59) 136 (56) 2.7 times greater for women than for men BMI (kg/m2) 29.65 Ϯ 5.92 33.32 Ϯ 7.49 Ͻ0.001 and 3 times greater among those who Large waist§ completed less than grade 9 compared Yes 120 (53) 193 (81) Ͻ0.001 with those who completed grade 9 or No 106 (47) 45 (19) higher. The odds of neuropathy increase Glycemic status for each percent increase in A1C; the risk Normoglycemic 150 (65) 161 (64) 0.444 for neuropathy is twice as great for some- Impaired fasting glucoseʈ 18 (8) 14 (5) one with an A1C of 9 versus 6%. Neurop- Diabetes 62 (27) 78 (31) athy risk is three times greater for Data are n (%) or means Ϯ SD. *Local language is . †Number of packs per day (1 pack ϭ 20 someone who smoked 30 pack-years than cigarettes) ϫ number of years smoked. ‡Systolic Ͼ140 mmHg or diastolic Ͼ90 mmHg. §Men Ն102 cm; for someone who smoked 10 pack-years. Ն ʈ Ն women 88 cm. Fasting glucose 6.1–6.9 mmol/l. Fasting glucose 7.0 mmol/l or previous diagnosis. Finally, the risk of neuropathy is twice as great for participants with a homocysteine had their feet examined by a health care sate feet, 18% (6 of 34) had an abnormal level of 9 ␮mol/l versus those with a level provider before the screening study. foot shape versus 5% (20 of 427) of those of 13 ␮mol/l (hyperhomocysteinemia de- Participants with insensate feet were with sensation. Of those with insensate fined as Ͼ12 ␮mol/l) (16). significantly more likely to have foot de- feet, 41% (14 of 34) had plantar calluses formities (hallux valgus, hammer toes, versus 12% (52 of 433) of those with sen- CONCLUSIONS — Of the partici- claw toes, and bony protuberances) (P Ͻ sation. In addition, the mean number of pants with diabetes upon entry to the 0.01) and calluses (P Ͻ 0.001) than were foot problems among dysglycemic partic- study, 15% had neuropathy, a number those with sensation. Of those with insen- ipants with insensate feet (3.15) was sig- that is similar to recent estimates (17). However, the mean age of our partici- pants (40.7 years) is younger than that of Table 2—Eligible and study populations by sex and age-group the comparison populations, and the mean time since diabetes diagnosis is Eligible population* Study participants comparatively short (8.75 years). The Males Females Males Females prevalence of neuropathy increased sig- nificantly by glucose level, a finding that Age-group (years) is consistent with population-based stud- 18–29 258 (35) 191 (31) 73 (32) 70 (28) ies (17) and current understanding on the 30–39 195 (27) 187 (30) 65 (28) 79 (31) role of glycemic control in the develop- 40–49 148 (20) 131 (21) 49 (21) 59 (23) ment and progression of neuropathy (7). 50–59 84 (11) 67 (11) 29 (13) 32 (13) Of the individuals with new IFG or dia- 60ϩ 49 (7) 46 (7) 14 (6) 13 (5) betes diagnoses, 8% had evidence of neu- Total 734 622 230 253 ropathy. Thus, complications were Data are n (%). *Community members who met eligibility criteria (n ϭ 1,356). developing at the time of diagnosis. The

DIABETES CARE, VOLUME 31, NUMBER 9, SEPTEMBER 2008 1839 Neuropathy in a First Nation community

Table 3—Neuropathic foot problems by glycemic status mocysteine was significantly associated with neuropathy. New IFG or The study is subject to limitations. Normoglycemia diabetes Previous diabetes P value* First, the sample is relatively small. It is possible that study participants are sys- Neuropathy† tematically different from those who did Present 14 (5) 5 (8) 15 (15) Ͻ0.01 not participate. However, the sample is Absent 286 (95) 61 (92) 86 (85) representative of the eligible community Pain population on demographic factors. Im- Present 18 (6) 6 (9) 14 (14) Ͻ0.05 portantly, we did not only screen the Absent 282 (94) 60 (91) 87 (86) “sickest” individuals in the community. Numbness, tingling When data were collected for this study, Present 14 (5) 8 (12) 12 (12) Ͻ0.01 there were 275 community members Absent 286 (95) 58 (88) 88 (88) with diabetes; 105 participated in the Previous foot examination study. In addition, 10 individuals had am- Yes NA NA 22 (22) NA putations, and 15 individuals had end- No 78 (78) stage renal disease. Three individuals with Data are n (%). *␹2 test for linear association. †Inability to sense 10-g monofilament on Ն1 site/10. NA, not amputations participated in the study, applicable. whereas none of the individuals with end- stage renal disease participated. The prev- short duration of disease before the onset socioeconomic status, which in turn may alence and pattern of neuropathy found of foot problems may indicate that diabe- be associated with poorer access to health in our study are similar to those in other tes complications occur more quickly care services and self-care practices. population-based studies. Thus, we have among this population and/or that diabe- Smoking has been found to be associated some confidence that our sample is repre- tes diagnoses are delayed. Participants with neuropathy incidence among those sentative of the eligible study population. with neuropathy were, on average, older with type 1 diabetes (18). Homocysteine, A second limitation is that we used than those without neuropathy. How- an amino acid that is produced from the fasting glucose to identify glucose intoler- ever, in multiple logistic modeling, glyce- metabolism of methionine (19), increased ance, similar to other population-based mic control was a stronger predictor of risk for neuropathy independent of age, epidemiologic studies. Had we completed neuropathy than age. sex, education level, A1C, and smoking. 2-h glucose tolerance tests, we probably Individuals with neuropathy were Homocysteine has been implicated in car- would have identified more glucose intol- more likely to have other foot problems dio- and cerebrovascular disease, primar- erance. It is possible that some individuals compared with those without neuropa- ily through impairment of endothelial we classified as normoglycemic may have thy. The presence of these foot problems functioning, leading to atherosclerosis been dysglycemic. However, the relation- increases the risk for foot ulceration and thrombosis (16,19–22). However, ship between glucose control and neu- among those with insensate feet, because the etiological role of homocysteine in ropathy was confirmed in the logistic of increased pressure loads and shearing cardio- and cerebrovascular disease has regression analyses. forces (7,8). Therefore, foot examinations not been established, so homocysteine A third limitation is that our defini- and treatment are a vital component of may be a marker for other factors or may tion of neuropathy may have high sensi- ulcer and amputation prevention (8). be related to other confounding factors tivity but lower specificity. Use of the 10-g In multivariate logistic regression, fe- (16). Ambrosch et al. (20) found a rela- monofilament is a validated procedure male sex, low education level, A1C, tionship between homocysteine and neu- that has demonstrated ability to predict smoking, and homocysteine were inde- ropathy among patients with type 2 risk for ulceration and amputation (8,23– pendently associated with neuropathy, diabetes. After addition of controls for 27). The protocol we followed has been shown to be associated with large-fiber after controls for age. Completion of less creatinine, vitamins B12 and B6, and folate than grade 9 may be a marker of lower (all confounders for homocysteine), ho- neuropathy and increased risk for ulcer- ation (27). Armstrong et al. (25) tested sensitivity and specificity of the 10-g Table 4—Multivariate logistic regression analysis of factors associated with neuropathy monofilament procedure and found that specificity increased without a decrease in ␤ (SEM) P value Exp (␤) (95% CI) sensitivity up to four imperceptible sites. Our use of one or more insensate sites Ϫ Age 0.016 (0.02) 0.411 0.984 (0.946–1.023) may have resulted in an overestimation of Sex neuropathy prevalence. However, as our Male 1.00 population is at high risk for ulceration Ͻ Female 0.989 (0.428) 0.05 2.689 (1.163–6.220) and amputation, we chose a protocol with Education high sensitivity. That our findings are Ͻ Grade 9 1.00 similar to those of recent population- Ն Ϫ Ͻ Grade 9 1.118 (0.466) 0.05 0.327 (0.131–0.0814) based studies provides confidence in the Ͻ A1C 0.267 (0.089) 0.01 1.306 (1.097–1.556) protocol. Ͻ Homocysteine 0.151 (0.045) 0.01 1.163 (1.064–1.271) Finally, we did not control for other Ͻ Pack-years smoked 0.048 (0.013) 0.001 1.049 (1.023–1.077) factors known to cause neuropathy (e.g.,

1840 DIABETES CARE, VOLUME 31, NUMBER 9, SEPTEMBER 2008 Bruce and Young vitamin B12 and folate deficiencies, hypo- F, Koulack J, Fong HM, Simonsen N, Geneva, World Health Org., 2000 thyroidism, and alcohol intake) (28) or Nicolle LE, Trepman E, Embil JM: Dis- 16. Kaul S, Zadeh AA, Shah PK: Homocys- ability and quality of life in Canadian Ab- teine hypothesis for atherothrombotic hyperhomocysteinemia (e.g., vitamin B6, chronic alcohol intake, smoking, caffeine, original and non-Aboriginal diabetic cardiovascular disease. J Am Coll Cardiol and certain medications) (16), so the re- lower-extremity amputees. Arch Phys Med 48:914–923, 2006 Rehabil 86:1594–1602, 2005 17. Gregg EW, Gu Q, Williams D, de Rek- lationship between homocysteine and 4. Jacobs P, Blanchard JF, James RC, Depew eneire N, Cheng YJ, Geiss L, Engelgau M: neuropathy requires further investiga- N: Excess costs of diabetes in the Aborig- Prevalence of lower extremity diseases as- tion. 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Winnipeg, Manitoba Centre risk factors on the ethnic-specific odds for 22% of those with diabetes had ever re- for Health Policy, 2002 peripheral arterial disease in the multi- ceived a foot examination. We increased 10. Hanley AJG, Harris SB, Mamakeesick M, ethnic study of atherosclerosis (MESA). community capacity to identify those at Goodwin K, Fiddler E, Hegele RA, Spence J Am Coll Cardiol 48:1190–1197 greatest risk. We continue to work with JD, House AA, Brown E, Schoales B, 23. Boyko E, Ahroni JH, Stensel V, Forsberg McLaughlin JR, Klein R, Zinman B: Com- RC, Davignon DR, Smith DG: A prospec- the community on secondary prevention plications of type 2 diabetes among Ab- tive study of risk factors for diabetic foot efforts. original Canadians. Diabetes Care 28: ulcer: the Seattle Diabetic Foot Study. Di- 2054–2057, 2005 abetes Care 22:1036–1042, 1999 11. Reid KS, Martin BD, Duerksen F, Nicolle 24. Pham H, Armstrong DG, Harvey C, Hark- Acknowledgments— This research was sup- LE, Garrett M, Simonsen JN, Trepman E, less LB, Giurini J, Veves A: Screening ported by the Canadian Institute for Health Embil JM: Diabetic foot complications in techniques to identify people at high risk Research and the Manitoba Health Research a northern Canadian Aboriginal commu- for diabetic foot ulceration: a prospective Council. nity. Foot Ankle 27:1065–1073, 2006 multicenter trial. Diabetes Care 23:606– We gratefully acknowledge the study par- 12. Chuback J, Embil JM, Sellers E, Trepman 611, 2000 ticipants, the Sandy Bay Diabetes Working E, Cheang M, Dean H: Foot abnormalities 25. Armstrong DG, Lavery LA, Vela SA, Group, and the Sandy Bay First Nation lead- in Canadian Aboriginal adolescents with Quebedeaux TL, Fleischli JG: Choosing a ership. We thank the anonymous reviewers type 2 diabetes. 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