Efficacy of MRI and Mammography for Breast-Cancer Screening in Women with a Familial or Genetic Predisposition
Mieke Kriege, M.Sc., Cecile T.M. Brekelmans, M.D., Ph.D., Carla Boetes, M.D., Ph.D., Peter E. Besnard, M.D., Ph.D., Harmine M. Zonderland, M.D., Ph.D., Inge Marie Obdeijn, M.D., Radu A. Manoliu, M.D., Ph.D., Theo Kok, M.D., Ph.D., Hans Peterse, M.D., Madeleine M.A. Tilanus-Linthorst, M.D., Sara H. Muller, M.D., Ph.D., Sybren Meijer, M.D., Ph.D., Jan C. Oosterwijk, M.D., Ph.D., Louk V.A.M. Beex, M.D., Ph.D., Rob A.E.M. Tollenaar, M.D., Ph.D., Harry J. de Koning, M.D., Ph.D., Emiel J.T. Rutgers, M.D., Ph.D., Jan G.M. Klijn, M.D., Ph.D., for the Magnetic Resonance Imaging Screening Study Group
Background The value of regular surveillance for breast cancerin women with a genetic or familial predisposition to breastcancer is currently unproven. We compared the efficacy of magneticresonance imaging (MRI) with that of mammography for screeningin this group of high-risk women.
Methods Women who had a cumulative lifetime risk of breast cancerof 15 percent or more were screened every six months with aclinical breast examination and once a year by mammography andMRI, with independent readings. The characteristics of the cancersthat were detected were compared with the characteristics ofthose in two different age-matched control groups.
Results We screened 1909 eligible women, including 358 carriersof germ-line mutations. Within a median follow-up period of2.9 years, 51 tumors (44 invasive cancers, 6 ductal carcinomasin situ, and 1 lymphoma) and 1 lobular carcinoma in situ weredetected. The sensitivity of clinical breast examination, mammography,and MRI for detecting invasive breast cancer was 17.9 percent,33.3 percent, and 79.5 percent, respectively, and the specificitywas 98.1 percent, 95.0 percent, and 89.8 percent, respectively.The overall discriminating capacity of MRI was significantlybetter than that of mammography (P<0.05). The proportionof invasive tumors that were 10 mm or less in diameter was significantlygreater in our surveillance group (43.2 percent) than in eithercontrol group (14.0 percent [P<0.001] and 12.5 percent [P=0.04],respectively). The combined incidence of positive axillary nodesand micrometastases in invasive cancers in our study was 21.4percent, as compared with 52.4 percent (P<0.001) and 56.4percent (P=0.001) in the two control groups.
The cumulative lifetime risk of breast cancer among Dutch womenis approximately 11 percent.1 A family history of breast canceror the presence of a germ-line mutation of the BRCA1 or BRCA2gene increases this risk considerably and is often associatedwith a diagnosis at a young age.2,3 Among high-risk women, therisk of breast cancer can be reduced by prophylactic mastectomy,4,5prophylactic oophorectomy,6,7 or chemoprevention.8 Early diagnosisas a result of intensive surveillance may also decrease therate of death from breast cancer.
Randomized trials have shown that mammographic screening ofall women who are between 50 and 70 years of age can reducemortality from breast cancer by about 25 percent.9 Althoughthese findings were recently disputed,10 there is a consensusamong clinicians that breast-cancer screening of women in thisage group is effective. Screening is one of the main factorscontributing to the decrease in mortality associated with breastcancer in the Netherlands.11 However, there is no consensusabout the value of breast-cancer screening among women who are40 to 49 years old.12,13,14One of the reasons for the lackof agreement is the difficulty in detecting tumors by mammographicscreening in younger women, who have denser breasts than postmenopausalwomen.15,16 Although screening is frequently offered to womenwith a genetic predisposition to breast cancer who are underthe age of 50 years, the efficacy of this approach is unproven.Preliminary results of surveillance by mammography and clinicalbreast examination in such women showed that mammographic screeninghas a low sensitivity for detecting tumors, especially in carriersof a BRCA mutation.17,18,19,20,21 Possible reasons, apart fromthe high rate of growth of tumors in women with such mutations,include the atypical changes seen on screening mammograms andspecific histopathological characteristics in carriers of BRCAmutations, as compared with noncarriers of the same age.22,23,24
The design of our MRI screening study, in which six subcommitteesin different disciplines were involved, has been described previously.28Between November 1, 1999, and October 1, 2003, 1952 women witha genetic risk of breast cancer were recruited for the studyby six familial-cancer clinics in the Netherlands. The six centerswere Erasmus Medical Center–Daniel den Hoed Cancer Center,Rotterdam; the Netherlands Cancer Institute, Amsterdam; UniversityMedical Center Nijmegen, Nijmegen; Leiden University MedicalCenter, Leiden; University Hospital Groningen, Groningen; andFree University Medical Center, Amsterdam. The study was approvedby the ethics committees of all the centers. All the women whoparticipated gave written informed consent.
The inclusion criteria for participation were a cumulative lifetimerisk of breast cancer of 15 percent or more owing to a familialor genetic predisposition, according to the modified tablesof Claus et al.,29 and an age of 25 to 70 years. Women couldbe tested at an age younger than 25 if they had a family historyof breast cancer diagnosed before the age of 30 years, sincetesting began at an age 5 years younger than that at which theyoungest family member was found to have breast cancer. Womenwith symptoms that were suggestive of breast cancer or womenwho had a personal history of breast cancer were excluded.
Surveillance
Surveillance consisted of a clinical breast examination performedby an experienced physician every six months and imaging studiesperformed annually by experienced radiologists. The imagingincluded a mammographic study (oblique and craniocaudal viewsand, if necessary, compression views or magnifications) anda dynamic breast MRI with gadolinium-containing contrast mediumaccording to a standard protocol.25 Whenever possible, bothimaging investigations were performed on the same day or inthe same time period, between day 5 and day 15 of the menstrualcycle. The results of mammography and MRI were scored in a standardizedway, according to the Breast Imaging Reporting and Data System(BI-RADS) classification,30,31 and the results were blindedso that the two examinations were not linked. When one of theexaminations was scored as either BI-RADS category 3 ("probablybenign [i.e., uncertain] finding") or category 0 ("need additionalimaging evaluation"), further investigation by ultrasonographywith or without fine-needle aspiration was advised, or mammographyor MRI was repeated. When one of the two examinations was scoredas BI-RADS category 4 ("suspicious abnormality") or category5 ("highly suggestive of malignancy"), a cytologic or histologicevaluation of a biopsy specimen was performed. When the resultsof mammography and MRI were negative but the findings on clinicalbreast examination were rated as uncertain or suspicious, additionalinvestigation was also performed. The diagnosis of malignanttumors was based on the results of a histologic examination.One of the investigators, an expert pathologist, reviewed allthe biopsy specimens that formed the basis for the diagnosisof breast cancer.
The rates of detection of breast cancer for the group as a wholeand for each of the three risk groups were calculated, and aPoisson distribution was assumed in order to calculate the 95percent confidence intervals. Person-years at risk were calculatedfrom the date of the first examination, irrespective of thetype of examination, to the date of detection of breast cancer,bilateral prophylactic mastectomy, or death; the date that apatient stopped surveillance; or the cutoff date for this analysis(October 1, 2003). An "interval cancer" was defined as a carcinomadetected between two rounds of screening after initially negativefindings on screening. In our analysis, we defined as positivea mammographic or MRI study with a BI-RADS score of 0, 3, 4,or 5 and a clinical breast examination that was classified as"uncertain" or "suspicious," because those were the resultsthat triggered an additional examination.
To compare the three different screening methods, we calculatedthe sensitivity, specificity, and positive predictive valueof each. The sensitivity used is that of one screening methodrelative to the others, meaning that a test result is a falsenegative when a proven cancer (diagnosed on the basis of a histologicexamination) is detected in the interval or by one of the othermethods. Receiver-operating-characteristic (ROC) curves forthe two imaging methods were generated. The area under the curvewas used as an index in evaluating the inherent capacity ofa screening method to discriminate between "positive" and "negative"cases. We used a z-test to compare the area under the curvefor the results of mammography and MRI. For the analysis ofthe screening variables, we used only the screening data thatincluded the results of both mammography and MRI.
To determine whether breast cancer was diagnosed by screeningat a stage more favorable to treatment, the characteristicsof breast tumors detected in the study group were compared withthose in two control groups. The first control group was derivedfrom all women who had breast cancers diagnosed in 1998 in theNetherlands. These data were obtained from the National CancerRegistry. The second control group consisted of unselected patientswho had received a diagnosis of primary breast cancer in Leidenor Rotterdam between 1996 and 2002 and who were participatingin a prospective study of the prevalence of gene mutations.32Subjects in both control groups were matched for age with thepatients in the study group (in five-year categories). Fromthis series of consecutive patients in the second control group,we chose all the unscreened patients who were between 25 and60 years old and whose cumulative lifetime risk of breast cancerwas more than 15 percent because of a family history of thedisease — information that was routinely recorded in thisdatabase. The differences in tumor characteristics between thestudy group and the control groups were tested with the useof Pearson's chi-square test or the chi-square test for trend.A two-sided P value of less than 0.05 was considered to indicatestatistical significance. All statistical analyses were performedwith the use of SPSS software (version 9.0).
Results
Study Population
Of the women who were invited to participate in the study, 90percent agreed. Initially, 1952 women were included; 8 withdrewfrom the study before their first screening visit and another35 were excluded because they ultimately proved not to be carriersin a family with a proven mutation and therefore had less thana 15 percent cumulative lifetime risk of breast cancer. Of the1909 remaining women, 88 (4.6 percent) left the study or werelost to surveillance before October 1, 2003; 65 of these 88women underwent prophylactic mastectomy. Another 89 women (4.7percent) remained under surveillance but later refused screeningby MRI, because of claustrophobia or for other reasons.
Table 1 lists the characteristics of the 1909 women accordingto risk category. The mean age at entry was 40 years (range,19 to 72). Within the group of 358 carriers of pathogenic mutations,276 had a BRCA1 mutation, 77 had a BRCA2 mutation, 1 had botha BRCA1 and a BRCA2 mutation, 2 had a PTEN mutation, and 2 hada TP53 mutation.
Table 1. Characteristics of Participating Women at Study Entry, According to Risk Group.
Breast Cancers
From November 1, 1999, to October 1, 2003, 51 malignant tumors(44 invasive breast cancers, 6 ductal carcinomas in situ, and1 non-Hodgkin's lymphoma) were detected (Figure 1), during amedian follow-up period of 2.9 years (mean 2.7, range, 0.1 to3.9 years); 1 lobular carcinoma in situ was also found. Table 2shows the detection rate for the whole group and separatelyfor the different risk groups. The overall rate of detectionfor all breast cancers (invasive plus in situ) was 9.5 per 1000woman-years at risk (95 percent confidence interval, 7.1 to12.3), with the highest rate (26.5 per 1000) in the group ofwomen who were carriers of the BRCA1, BRCA2, PTEN, and TP53mutations.
Table 2. Detection of Cases of Breast Cancer (Including Ductal Carcinoma in Situ) According to Risk Group.
Performance of the Screening Methods
Table 3 shows the results with the three screening methods.Of the 50 breast cancers that were detected, 5 were excludedfrom the analysis (Table 3). The 45 cancers that were evaluatedin the comparison of the methods included 4 interval cancers(i.e., cancers detected between two episodes of screening).The first was symptomatic (30 mm in diameter, node-negative),detected seven months after screening by imaging and clinicalbreast examination and one month after screening by clinicalbreast examination only. The second (4 mm, node-negative) wasdetected in a specimen from a prophylactic mastectomy. The thirdwas symptomatic (45 mm, node-negative) and was detected sevenmonths after screening by imaging; the fourth, also symptomatic(13 mm, with isolated tumor cells in a lymph node), was detectedthree months after screening by imaging.
Table 3. Sensitivity, Specificity, and Positive Predictive Value (PPV) of the Three Screening Methods.
Overall, 32 breast cancers were found by MRI (22 of these werenot visible on mammography), whereas 13 were missed by MRI (8of the 13 were visible on mammography, including 5 ductal carcinomasin situ; 4 were interval cancers; and 1 tumor was detected onlyby clinical breast examination). In this group of 45 breastcancers, mammographic screening detected 18 tumors (10 of thesewere visible by MRI) and missed 27 tumors (including the 22that were visible on MRI, the 4 interval cancers, and the 1that was detected only by clinical breast examination).
With respect to all breast cancers (invasive and ductal carcinomain situ), the sensitivity of clinical breast examination, mammography,and MRI was 17.8 percent, 40.0 percent, and 71.1 percent, respectively,when the BI-RADS score was 3 or higher (Table 3). For invasivecancers only, the respective percentages were 17.9 percent,33.3 percent, and 79.5 percent. The specificity was 98.1 percentfor clinical breast examination, 95.0 percent for mammography,and 89.8 percent for MRI.
Of the 41 cancers found by screening, 22 were detected at thefirst imaging screening in the study; of the women in whom cancerwas detected, 16 had undergone mammographic screening beforethe start of the study. Two of the interval cancers were detectedafter the first imaging screening, and two others after a subsequentimaging screening. The sensitivity of mammography was 37.5 percentfor the first screening and 42.9 percent for subsequent screening(P=0.71). The sensitivity of MRI was 79.2 percent for the firstscreening and 61.9 percent for subsequent screening (P=0.20).
Among the 83 clinical breast examinations with findings thatwere judged as probably benign or suspicious, or highly suggestiveof cancer, 8 cases of malignant disease were confirmed, fora positive predictive value of 9.6 percent (Table 3). Amongthe 225 mammograms with findings categorized as BI-RADS 3 orhigher, 18 cases of malignant disease were confirmed, for apositive predictive value of 8.0 percent. A total of 32 cancerswere confirmed among 452 MRI screenings with such findings,for a positive predictive value of 7.1 percent (Table 3). Witha cutoff level of BI-RADS 4, the sensitivity for both imagingmethods decreased, whereas the specificity increased.
To evaluate the discriminating capacity of the imaging methods,we generated ROC curves (Figure 2). The area under the curvewas 0.686 for mammography and 0.827 for MRI; the differencebetween the areas was 0.141 (95 percent confidence interval,0.020 to 0.262; P<0.05).
Figure 2. Receiver-Operating-Characteristic Curves for Mammography and MRI.
The difference between the area under the curve (AUC) for mammography and the AUC for MRI was 0.141 (95 percent confidence interval, 0.020 to 0.262; P<0.05).
Additional Investigations
Ultrasonography was performed 889 times in 627 different womenaccording to the protocol. Fine-needle aspiration was carriedout 312 times: 267 times in combination with ultrasonographyand 45 times with palpation. Biopsy was performed 85 times in82 women and showed malignant disease in 50 cases and 1 lobularcarcinoma in situ, making the rate of positive histologic findings60.0 percent. Sixty-seven of these 85 biopsies were performedafter a screening visit at which both MRI and mammography wereperformed. Of the 25 biopsies in women who had mammographicfindings with a score of 3 or higher, 7 (28.0 percent) showedno cancer. Of the 56 biopsies in women who had MRI findingswith a score of 3 or higher, 24 (42.9 percent) showed no cancer(Table 3). One of the 51 tumors was found in a specimen froma prophylactic mastectomy.
Tumor Characteristics
Table 4 compares the characteristics of tumors found in thestudy group with those of tumors in the two age-matched controlgroups. In the study group, 19 of the 44 women with an invasivebreast cancer (43.2 percent) had a small tumor (10 mm in diameter)— a proportion that was significantly higher than thatin the first control group (14.0 percent, P<0.001) or thesecond control group (12.5 percent, P=0.04). Six of 42 invasivetumors (14.3 percent) with known axillary status in the studygroup were node-positive and 3 (7.1 percent) had micrometastases(combined total, 21.4 percent). This rate was significantlylower than those in both control groups, in which the ratesof node-positive cancer were 52.4 percent (P<0.001) and 56.4percent (P=0.001), respectively. There were no major differencesbetween the study and control groups with respect to histologicfeatures, with the exception of a relatively high incidenceof the medullary type in the study group (11.3 percent, vs.1.8 percent in the first control group). In the study group,a high proportion of grade 1 tumors were in women at high risk(68.8 percent) or moderate risk (75.0 percent); however, thegroup of women with BRCA1,BRCA2, or other mutations had a highpercentage of grade 3 tumors (63.2 percent), in addition toa high percentage of tumors that were negative for steroid receptors(Table 4).
Table 4. Characteristics of Women with Breast Cancer and Breast Cancers Detected in the Three Risk Groups and in the Two Control Groups.
Disease-free and Overall Survival
In the study group, none of the 50 patients with breast cancer(44 with invasive cancer and 6 with ductal carcinoma in situ)died before the end of the study period; the total follow-upafter diagnosis was 87.6 woman-years for these 50 patients (median,1.5 years). Contralateral breast cancer occurred in one patient.The patient with non-Hodgkin's lymphoma died.
Discussion
In this prospective study, we compared the efficacy of mammographicand MRI screening for breast cancer in women with a family historyof the disease or a genetic predisposition to breast cancer.Among the women examined by both methods at the same screeningvisit, we detected 45 breast cancers (including 6 ductal carcinomasin situ): 32 by MRI (sensitivity, 71.1 percent) and 18 by mammography(40.0 percent); five other patients were excluded from thiscomparison for various reasons (Table 3). Thus, the sensitivityof MRI was higher than that of mammography, but both the specificityand positive predictive value of MRI were lower.
In our sensitivity and specificity calculations, we definedlesions that were in BI-RADS category 3 and higher as positive,but most other authors have included in their calculations onlylesions in BI-RADS categories 4 and 5 as positive.21,33,34 Ifwe had followed that policy, the sensitivity would have been24.4 percent for mammography and 46.6 percent for MRI, in accordwith the higher sensitivity previously reported for MRI.21,33,35,36However, the previous studies enrolled small groups of women,included some retrospective data,35 evaluated heterogeneousgroups that included women with previous breast cancers,21,33,36or had a plan for follow-up after a suspicious finding on MRIthat differed from the follow-up plan for a suspicious mammographicfinding.33 All these factors might have artificially increasedthe sensitivity of MRI. We also investigated sensitivity inrelation to specificity as determined by ROC curves, showingthat the area under the curve was significantly higher for MRIthan for mammography; this means that MRI screening could betterdiscriminate between malignant and benign cases.
To investigate whether screening improves the chance of diagnosingbreast cancer at an early stage, we compared the distributionof tumor stages in our study with the distribution in two externalcontrol groups. The first group consisted of age-matched womenin a database of all breast cancers diagnosed in 1998 in theNetherlands. A drawback of this group is that we had no informationabout whether or not they had been screened or the family history.Therefore, we added a second control group from a prospectivepopulation-based study of the prevalence of mutations in patientswith breast cancer. From this group, we selected all patientswith an age and a family history of breast cancer that weresimilar to the women in our surveillance study. The tumors inour study group were significantly smaller and were less likelyto be node-positive than those in the two control groups. Mostscreening studies (without MRI) in high-risk women have showna higher incidence of positive nodes (30 to 45 percent) thanwe found (21 percent).17,18,37 Moreover, Kollias et al.38 foundno significant differences in the size or grade of invasivetumors or in lymph-node status between women who had symptomsof cancer and women whose cancers had been found on screeningby mammography. So we may conclude that MRI screening did indeedcontribute to the early detection of hereditary breast cancer.
Supported by a grant (OG 98-03) from the Dutch Health InsuranceCouncil.
We are indebted to Petra Bos, Titia van Echten, Irene Groot,Marijke Hogenkamp, Arjan Nieborg, Angelique Schlief, and ManitaVerhoeven for data collection; to Leon Aronson for computerassistance; and to Truuske de Bock and Ronald Damhuis for helpin selecting the control groups.
* Other investigators in the Magnetic Resonance Imaging Screening(MRISC) study are listed in the Appendix.
Source Information
From the Rotterdam Family Cancer Clinic, Department of Medical Oncology (M.K., C.T.M.B., J.G.M.K.), and the Departments of Radiology (I.M.O.) and Surgery (M.M.A.T.-L.), Erasmus Medical Center–Daniel den Hoed Cancer Center, Rotterdam; the Department of Radiology (C.B.) and the Department of Medical Oncology and Family Cancer Clinic (L.V.A.M.B.), University Medical Center Nijmegen, Nijmegen; the Departments of Radiology (P.E.B., S.H.M.), Pathology (H.P.), and Surgery (E.J.T.R.), Netherlands Cancer Institute, Amsterdam; the Departments of Radiology (H.M.Z.) and Surgery (R.A.E.M.T.), Leiden University Medical Center, Leiden; the Departments of Radiology (R.A.M.) and Surgery (S.M.), Free University Medical Center, Amsterdam; the Departments of Radiology (T.K.) and Clinical Genetics (J.C.O.), University Hospital Groningen, Groningen; and the Department of Public Health, Erasmus Medical Center, Rotterdam (H.J.K.) — all in the Netherlands.
Address reprint requests to Dr. Klijn at Erasmus Medical Center–Daniel den Hoed Cancer Center, Groene Hilledijk 301 3075 EA, Rotterdam, the Netherlands, or at j.g.m.klijn{at}erasmusmc.nl.
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Appendix
In addition to the authors, the following investigators participatedin the MRISC Study: Erasmus Medical Center, Rotterdam —C.C.M. Bartels, A. Ciurea, A.N. van Geel, E.J. Meijers-Heijboer,M. Menke, A.J. Rijnsburger, C. Seynaeve, D. Urich; Leiden UniversityMedical Center, Leiden — C. van Asperen, M.N.J.M. Wasser;Netherlands Cancer Institute, Amsterdam — R. Kaas, W.Koops, M. Piek-den Hartog, M. van de Vijver; University HospitalGroningen, Groningen — C. Dorbritz, S. van Hoof, A.M.van der Vliet, J. de Vries; University Medical Center Nijmegen,Nijmegen — J.O. Barentsz, H. Brunner, J.H.C.L. Hendriks,R. Holland, N. Hoogerbrugge, M. Stoutjesdijk, A.L.M. Verbeek,T. Wobbes; Free University Medical Center, Amsterdam —F. Menko, A. Taets van Amerongen.
MRI in Breast Cancer
Altundag K., Morandi P., Altundag O., Gur D., Kriege M., Brekelmans C. T.M., Klijn J. G.M.
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Gorechlad, J. W., McCabe, E. B., Higgins, J. H., Likosky, D. S., Lewis, P. J., Rosenkranz, K. M., Barth, R. J. Jr
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Hoogerbrugge, N., Kamm, Y. J. L., Bult, P., Landsbergen, K. M., Bongers, E. M. H. F., Brunner, H. G., Bonenkamp, H. J., de Hullu, J. A., Ligtenberg, M. J. L., Boetes, C.
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Bigenwald, R. Z., Warner, E., Gunasekara, A., Hill, K. A., Causer, P. A., Messner, S. J., Eisen, A., Plewes, D. B., Narod, S. A., Zhang, L., Yaffe, M. J.
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Bollet, M. A., Servant, N., Neuvial, P., Decraene, C., Lebigot, I., Meyniel, J.-P., De Rycke, Y., Savignoni, A., Rigaill, G., Hupe, P., Fourquet, A., Sigal-Zafrani, B., Barillot, E., Thiery, J.-P.
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(2007). Genetic Testing in Diverse Populations: Are Researchers Doing Enough to Get Out the Correct Message?. JAMA
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Tilanus-Linthorst, M. M.A., Obdeijn, I.-M., Hop, W. C.J., Causer, P. A., Leach, M. O., Warner, E., Pointon, L., Hill, K., Klijn, J. G.M., Warren, R. M.L., Gilbert, F. J.
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Lehman, C. D., Isaacs, C., Schnall, M. D., Pisano, E. D., Ascher, S. M., Weatherall, P. T., Bluemke, D. A., Bowen, D. J., Marcom, P. K., Armstrong, D. K., Domchek, S. M., Tomlinson, G., Skates, S. J., Gatsonis, C.
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10 mm in diameter) — a proportion that was significantly higher than that in the first control group (14.0 percent, P<0.001) or the second control group (12.5 percent, P=0.04). Six of 42 invasive tumors (14.3 percent) with known axillary status in the study group were node-positive and 3 (7.1 percent) had micrometastases (combined total, 21.4 percent). This rate was significantly lower than those in both control groups, in which the rates of node-positive cancer were 52.4 percent (P<0.001) and 56.4 percent (P=0.001), respectively. There were no major differences between the study and control groups with respect to histologic features, with the exception of a relatively high incidence of the medullary type in the study group (11.3 percent, vs. 1.8 percent in the first control group). In the study group, a high proportion of grade 1 tumors were in women at high risk (68.8 percent) or moderate risk (75.0 percent); however, the group of women with BRCA1, BRCA2, or other mutations had a high percentage of grade 3 tumors (63.2 percent), in addition to a high percentage of tumors that were negative for steroid receptors (Table 4). 
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