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Association for Academic Surgery

Characterizing lobular carcinoma of the male breast usingthe SEER database

Ambria Moten, BA,a Augustine Obirieze, MBBS, MPH,a and Lori L. Wilson, MD, FACSa,b,*aHoward University College of Medicine, Washington, District of ColumbiabDivision of Surgical Oncology, Department of Surgery, Howard University Hospital, Washington, District of Columbia

a r t i c l e i n f o

Article history:

Received 5 January 2013

Received in revised form

3 May 2013

Accepted 9 May 2013

Available online 3 June 2013

Keywords:

Lobular carcinoma

Male breast cancer

Outcomes

Health disparity

Breast surgery

* Corresponding author. Division of SurgicalAvenue, Northwest, Towers Building Suite 2

E-mail address: lori.wilson@howard.edu0022-4804/$ e see front matter ª 2013 Elsevhttp://dx.doi.org/10.1016/j.jss.2013.05.043

a b s t r a c t

Background: Lobular carcinoma of the male breast is rare. We sought to investigate the

clinical characteristics, treatment, and outcomes of men and women with lobular breast

cancer, using a population-based database.

Methods: We reviewed the Surveillance, Epidemiology, and End Results database 1988e2008

and identified patients with a lobular breast cancer diagnosis (invasive lobular carcinoma

[ILC] and lobular carcinoma in situ [LCIS]) using the “International Classification of Diseases

for Oncology, Third Edition” codes. Bivariate analyses compared the male and female

patients on demographics, clinical characteristics, and treatment modalities. Multivariate

logistic regression analysis determined the risk-adjusted likelihood of receiving treatment.

Survival analysis was done and hazard ratios were obtained using Cox proportional

models.

Results: Overall, 133,339 patients were identified, including 133,168 women (99.9%) and 171

men (0.1%). Most had ILC (82.08%). The median age was 66 � 20 y for the men and 61 � 21 y

for the women. The men with ILC were more likely to have poorly differentiated tumors

(26.45% versus 15.61%; P < 0.001) and stage IV disease (9.03% versus 4.18%; P ¼ 0.005) than

were the women. The cancer-specific 5-year survival rates for ILC were 82.9% for the men

and 91.9% for the women. Adjusted survival was better for patients with ILC receiving

surgery plus radiotherapy than patients receiving neither (hazard ratio 0.52, 95% confi-

dence interval 0.49e0.56). Women with ILC had a 55% increased odds of receiving surgery

plus radiotherapy compared with men (odds ratio 1.55, 95% confidence interval 1.08e2.22).

Conclusions: ILC presents at a higher grade and stage in men. The difference in disease

characteristics and survival rates suggests that the treatment of men with lobular breast

cancer should be adjusted to improve their outcomes.

ª 2013 Elsevier Inc. All rights reserved.

1. Introduction

BRCA mutation, Klinefelter syndrome), radiation exposure,

Male breast cancer is rare, constituting about 1% of all breast

cancer cases [1]. The risk factors for male breast cancer include

age, family history of breast cancer, genetic conditions (e.g.,

Oncology, Department o322, Washington, DC 200(L.L. Wilson).ier Inc. All rights reserved

estrogen exposure, obesity, liver disease, and other factors [1].

An especially rare type of male breast cancer is invasive lobular

carcinoma (ILC). It constitutes about 1% of allmale breast cancer

cases [2]. This type of cancer is unusual in men, because male

f Surgery, Howard University College of Medicine, 2041 Georgia60. Tel.: þ1 202 865 6409; fax: þ1 202 865 6433.

.

j o u rn a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) e 7 1ee 7 6e72

breasts lack lobules. A few case reports have attempted to

describe thisrare typeof cancer ingreaterdetail, and thenumber

of case reports seems tobe increasing [3e9]. The casespresented

in these reports have differed with respect to tumor size,

hormone receptor status, stage, treatment, and other variables.

Also, little to no information is available on the long-term

outcomes of the patients described in the reports. To the best

of our knowledge, no comprehensive analysis has been done of

multiple casesof ILCof themalebreast. Theaimofour studywas

to use a large population-based database to investigate the

tumor characteristics, treatment, and outcomes of men with

lobular type breast cancer and to compare these variables to

those of women with lobular type breast cancer.

2. Methods

The data analyzed in the present study were obtained from

the Surveillance, Epidemiology, and End Results (SEER)

Program of the National Cancer Institute. SEER contains data

regarding cancer incidence and outcomes fromapproximately

28% of the US population. The SEER population is similar to

the US population regarding education and poverty levels but

has a slightly greater proportion of urban and foreign-born

individuals [10].

Using SEER code 26000, which corresponds to “Interna-

tional Classification of Diseases for Oncology, Third Edition”

codes C500eC509 for breast cancer, we identified men and

women aged �20 y with a primary breast cancer diagnosis

from 1988e2008. The cohort was then limited to those with

lobular histologic type breast cancer using “International

Classification of Diseases for Oncology, Third Edition”

histology codes 8520/2, 8520/3, 8522/2, 8522/3, and 8524/3. This

population was further classified into two groups: those with

invasive lobular carcinoma (ILC) and those with lobular

carcinoma in situ (LCIS). Although we were interested in

studying men, women were included in the study to have

a comparison group. The information retrieved included age,

race or ethnicity, marital status, stage and grade at diagnosis,

tumor size, hormonal assay, treatment type (surgery, radio-

therapy, or surgery and radiotherapy), and the SEER registry

data. Because of the nonavailability of socioeconomic status

information in the SEER public use data, US Census Bureau

data were used to obtain socioeconomic status proxy vari-

ables, including county-level information on median house-

hold income and percentages of individuals living below the

poverty level, living in urban areas, who were unemployed,

who were “white collar” employees, and with less than a high

school education by age 25 y, just as in a previous study [11].

Bivariate analyses compared the men and women on demo-

graphics, clinical characteristics, and treatment modalities

within the ILC and LCIS subgroups. Multivariate logistic

regression analysis was used to assess the likelihood of

receiving surgery plus radiotherapy between the men and

women, adjusting for demographics, clinical characteristics,

SEER registry, year of diagnosis, and socioeconomic status. A

cancer-specific survival analysis was done, and hazard ratios

(HRs) were derived from the Cox proportional model, adjust-

ing for year of diagnosis, stage, grade, race, and treatment

type.

3. Results

The study population included 133,339 individuals, of whom

171 (0.13%) were men and 133,168 (99.9%) were women. Most

werewhite (81%) andmarried (56.9%), and themedian agewas

61 � 21 y. Of the 133,339 subjects, 109,447 (82.1%) had been

diagnosed with ILC and 23,892 with LCIS.

The distribution of demographics, clinical characteristics,

and treatment, overall and within the LCIS and ILC subgroups

are listed in Tables 1e3. Among the subgroup of patients with

LCIS, the men had a median age of 50 � 25.5 y and the women

amedian age of 53 � 16 y. The rate of receipt of surgery within

this subgroup was lower for the men than for their female

counterparts (68.8% versus 86.4%, P ¼ 0.039). However, no

significant difference was found in grade, stage, tumor size,

estrogen or progesterone receptor status, number of regional

lymph nodes involved, or type of surgery received between

the men and women with LCIS. Within the ILC subgroup, the

men had amedian age of 68� 20 y andwere significantlymore

likely to be aged �70 y (47.1% versus 35.0%, P ¼ 0.002) and

married (69.7% versus 55.6%, P < 0.001) compared with the

women with ILC. Also, in this subgroup, the men were more

likely to have higher grade (grade 3) tumors (26.5% versus

15.6%, P < 0.001), higher stage (stage III or IV) disease (24.5%

versus 14.4%, P ¼ 0.005), and distant metastasis (9.0% versus

4.1%, P ¼ 0.002) compared with their female counterparts. No

significant difference was found in the estrogen receptor

status, progesterone receptor status, or number of regional

lymph nodes involved between the men and women.

All the men were less likely to receive surgery than the

women (Table 3). Men with ILC were less likely to receive

surgery plus radiotherapy (P ¼ 0.007) than the women. Of

those men with ILC who did receive surgery, 57.6%, who had

undergone partial mastectomy, 15.6%, who had undergone

total mastectomy, and 29.5%, who had undergone modified

radical mastectomy, had also received radiotherapy. The

difference between these values and those for women with

ILC were not statistically significant. Of those with ILC who

received surgery, the men were significantly more likely to

undergo modified radical mastectomy, and the women were

most likely to undergo partial mastectomy (P < 0.001). No

significant differencewas found between themen andwomen

with LCIS in the type of surgery received.

The unadjusted cancer-specific 5- and 10-year survival

rates formenwith LCISwere both 100%. The cancer-specific 5-

and 10-year survival rate for women with LCIS was 99.7% and

98.9%, respectively. For ILC, the cancer-specific 5- and 10-year

survival rates for men were both 82.9%. The cancer-specific 5-

and 10-year survival rate for women with ILC was 91.9% and

84.5%, respectively.

The adjusted cancer-specific mortality HRs revealed that

blacks and Hispanics with ILC had worse survival than their

white counterparts (HR 1.57, 95% confidence interval [CI]

1.47e1.67, and HR 1.10, 95% CI 1.02e1.18, respectively). The

patients with ILC who had received surgery plus radiotherapy

hadbetter survival comparedwith thepatientswhohadreceived

surgeryalone (HR0.91,95%CI0.87e0.95), andalsocomparedwith

patients with ILC who had received neither (HR 0.55, 95% CI

0.48e0.55). On multivariate analysis, the women with ILC had

Table 1 e Demographics of patients with LCIS or ILC.

LCIS ILC

Male (n) Female (n) P value Male (n) Female (n) P value

Total 16 (0.07) 23,876 (99.93) 155 (0.14) 109,292 (99.86)

Age group (y) 0.625 0.002*

20e34 0 (0) 175 (0.73) 1 (0.65) 857 (0.78)

35e49 6 (37.50) 8207 (34.37) 22 (14.19) 19,181 (17.55)

50e69 6 (37.50) 12,330 (51.64) 59 (38.06) 51,023 (46.69)

70e80 3 (18.75) 2558 (10.71) 59 (38.06) 26,150 (23.93)

> 80 1 (6.25) 606 (2.54) 14 (9.03) 12,081 (11.05)

Race <0.001 0.052

White 10 (62.50) 19,102 (80.01) 120 (77.42) 89,100 (81.52)

Black 0 (0.0) 1691 (7.08) 18 (11.61) 6669 (6.10)

Hispanic 2 (12.50) 1632 (6.84) 9 (5.81) 7950 (7.27)

Other 1 (6.25) 1010 (4.23) 8 (5.16) 5007 (4.58)

Unknown 3 (18.75) 441 (1.85) 0 (0.0) 566 (0.52)

Marital status 0.101 <0.001*

Single 2 (12.50) 3067 (12.85) 10 (6.45) 11,646 (10.66)

Married 8 (50.00) 14,910 (62.45) 108 (69.68) 60,811 (55.64)

Separated 0 (0) 153 (0.64) 1 (0.65) 834 (0.76)

Divorced 1 (6.25) 2222 (9.31) 11 (7.10) 10,707 (9.80)

Widowed 1 (6.25) 1980 (8.29) 14 (9.03) 21,427 (19.61)

Unknown 4 (25.00) 1544 (6.47) 11 (7.10) 3867 (3.54)

Data in parentheses are percentages.

* Statistically significant at P < 0.05.

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) e 7 1ee 7 6 e73

55%higheroddsof receivingsurgeryplusradiotherapycompared

with their male counterparts (odds ratio 1.55, 95% CI 1.08e2.22).

4. Discussion

This population-based study has described several clinical

characteristics of a relatively large sample of men with breast

cancer of lobular histologic type, a disease that has not been

thoroughly studied in men. Furthermore, our study showed

that men tended to undergo different treatments and have

poorer outcomes than their female counterparts.

Men with breast cancer of lobular histologic type were

usually white and married, and those with ILC had a median

age of 68 � 20 y. This is consistent with published case reports

of ILC of the male breast, which have typically described

a white man aged >50 y [7e9]. Information on marital status

was not reported in any previous case reports. Women with

ILCwere usually white andmarried, with amedian age of 63�22 y. This is also consistent with the published data. Arpino

et al. [12] noted that most women with ILC have been > 50 y

old. Vo et al. [13] observed that women with ILC had a median

age of 60 y, and about 93% of these women were white.

The tumors in men with ILC averaged 2.34 cm and were of

higher grade than those discovered in women. The men also

presented with higher stage disease. In the current data, the

tumor cells in men with ILC were occasionally described, but

a grade was rarely assigned. However, the tumor size was

nearly always reported, and case reports have revealed that

the tumor sizes ranged from 2e4 cm [3e9]. One of the smallest

tumors was reported by Briest et al. [8], who described

a patient with a 2.4-cm subareolarmass categorized as Elston-

Ellis grade 2 or 3. One of the larger tumors was reported by

Mariolis-Sapsakos et al. [7], who described a 74-y-oldmanwith

a 3 � 4-cm subareolar mass. The tumor size in women with

ILC tends to be >2 cm [12]. The tumor size averaged 2.35 cm in

a study by Winchester et al. [14], and the median tumor size

was 3.0 cm in a study by Vandorpe et al. [15].

Men with ILC presented with higher stage disease

compared with women, but no significant difference was

found in regional lymph node involvement between men and

women. A few case reports of men with ILC described lymph

node invasion [7,8]. In a case reported by Scheidbach et al. [9],

an 85-y-old man had disease that infiltrated the thoracic wall

and involved 26 of 29 lymph nodes. The musculature, skin,

and lymphaticswere infiltrated. However, several case reports

described no lymph node involvement [3e6]. Likewise, the

published data on women with ILC have revealed that most

cases did not have lymph node involvement [12,13,15,16].

Furthermore, we observed that distantmetastasis was rare

and more likely to occur in men than in women. Most pub-

lished case reports did not describe distant metastasis in men

with ILC [4e9]. However, an instance of metastasis was re-

ported by Koc et al. [3], who described a patient who died of

progression of lung metastases. Although that patient had

presented with stage IIA (T2N0M0) and was treated with

radical mastectomy and radiotherapy, he developed bone and

lung metastases 3 y after treatment. Our finding that distant

metastasis is rare in women is also supported by several

studies that showed that women with stage IV disease

constituted <5% of women with ILC [14,17].

Moreover, when the hormone receptor status was known,

most men with ILC had tumor cells that were positive for

estrogen and progesterone receptors. However, no significant

difference was found between the men and women. This is

consistent with published case reports, which usually re-

ported positive estrogen receptor status inmenwith ILC, if the

information was known [3,4,6e8]. The progesterone receptors

Table 2 e Clinical tumor characteristics among patients with LCIS or ILC.

LCIS ILC

Male (n) Female (n) P value Male (n) Female (n) P value

Grade* 0.511 <0.001y

1 1 (6.25) 1195 (5.01) 9 (5.81) 18,906 (17.30)

2 0 (0) 2309 (9.67) 69 (44.52) 43,939 (40.20)

3 1 (6.25) 1071 (4.49) 41 (26.45) 17,059 (15.61)

Unknown 13 (81.25) 18,844 (78.92) 34 (21.94) 28,134 (25.74)

Stage 0.005y

I 56 (36.13) 44,377 (40.60)

II 50 (32.26) 40,880 (37.40)

III 24 (15.48) 11,212 (10.26)

IV 14 (9.03) 4566 (4.18)

Unknown 11 (7.10) 8257 (7.55)

Estrogen receptor 0.210 0.086

Negative 1 (6.25) 197 (0.83) 3 (1.94) 2141 (1.96)

Positive 1 (6.25) 2174 (9.11) 68 (43.87) 36,291 (33.21)

Borderline 0 (0) 7 (0.03) 0 (0) 57 (0.05)

Not tested 3 (18.75) 4963 (20.79) 1 (0.65) 1195 (1.09)

Unknown 11 (68.75) 16,532 (69.25) 83 (53.55) 69,605 (63.69)

Progesterone receptor 0.783 0.070

Negative 1 (6.25) 446 (1.87) 13 (8.39) 7950 (7.27)

Positive 1 (6.25) 1887 (7.90) 57 (36.77) 30,112 (27.55)

Borderline 0 (0) 17 (0.07) 1 (0.65) 298 (0.27)

Not tested 3 (18.75) 4968 (20.81) 1 (0.65) 1195 (1.09)

Unknown 11 (68.75) 16,558 (69.35) 83 (53.55) 69,737 (63.81)

Data in parentheses are percentages.

* The percentages for grade might not sum to 100% because some data in the SEER database were not listed in the three-tiered format of the

Nottingham histologic score (Elston grade) typically used for ILC and were, therefore, not included.yStatistically significant at P < 0.05.

j o u rn a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) e 7 1ee 7 6e74

were positive in some published case reports [6e9] but were

negative in others [3]. Regarding women, we found that

estrogen receptors were positive in about 33% and proges-

terone receptors were positive in about 27%. These values

were lower than those reported in published studies. Vo et al.

[13] reported that 65.5% of women with ILC had positive

estrogen receptors and 47.6% of women had positive proges-

terone receptors. Other studies found even higher proportions

of positive estrogen and progesterone receptors in women

with ILC [12,17]. The lower proportion of positive hormone

receptors found in the present studymight have been because

a large portion of our sample had an unknown hormone

Table 3 e Type and combination of treatment received by pati

LCIS

Male (n) Female (n)

Surgery

No 5 (31.25) 3242 (13.58)

Yes 11 (68.75) 20,634 (86.42)

Combination

Surgery only 9 (56.25) 18,500 (77.48)

Radiotherapy only 0 (0) 29 (0.12)

Neither 5 (31.25) 3213 (13.46)

Surgery plus radiotherapy 2 (12.50) 2134 (8.94)

Data in parentheses are percentages.

* Statistically significant at P < 0.05.

receptor status (53%e70%). With this amount of data

unknown, the true proportion of patientswith tumors positive

for hormone receptors could not be accurately determined in

the present study.

Our analysis of treatmentmodalities demonstrated that all

men were significantly less likely to receive surgery compared

with thewomen. Themenwith ILCwho received surgerywere

significantly more likely to undergo modified radical mastec-

tomy compared with the women. This was consistent with

the published data, which demonstrated that modified radical

mastectomy was the treatment of choice for men with ILC

[4,7e9]. We found that women with ILC were most likely to

ents with LCIS or ILC.

ILC

P value Male (n) Female (n) P value

0.039* 0.016*

21 (13.55) 8990 (8.23)

134 (86.45) 100,302 (91.77)

0.177 0.007*

89 (57.42) 56,948 (52.11)

5 (3.23) 1423 (1.30)

16 (10.32) 7567 (6.92)

45 (29.03) 43,354 (39.67)

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) e 7 1ee 7 6 e75

undergo partial mastectomy. The use of partial mastectomy

for the treatment of ILC has been increasing during the

past few decades and has become the predominant surgical

treatment of the disease [18].

Regarding LCIS, most men (68.75%) and women (86.42%)

received surgery, but the men were significantly less likely to,

although no difference was found in the type of surgery

received. The treatment of LCIS has typically been close

observation [19e21]. The large proportion of individuals in our

study who underwent surgery might have represented an

effort to diagnose the breast lesion rather than to treat it.

Regarding treatment combinations, surgery only was the

predominant treatment for both men and women with ILC,

but women were more likely to receive the combination of

surgery plus radiotherapy than were men. When assessing

receipt of radiotherapy by the type of surgery received, the

men with ILC were equally likely to receive radiotherapy in

addition to surgery as their female counterparts. Although the

treatment regimens variedwidely, published studies generally

reported that men with ILC were treated with a combination of

surgery, radiotherapy, chemotherapy, and/or hormonal ther-

apy. Erhan et al. [4] reported the case of a patient treated with

modified radical mastectomy, six cycles of cyclophosphamide,

epirubicin, 5-fluorouracil, and tamoxifen, and the patient des-

cribed by Koc et al. [3] received radical mastectomy, radio-

therapy, and tamoxifen. However, somepatientswere reported

to have received surgery only [5,9]. Women with ILC generally

receive breast conservation therapy (partial mastectomy plus

radiotherapy) or total mastectomy [14,18].

The present study also demonstrated that the number of

men and women with ILC was increasing greatly during the

periods studied. This information coincides with the increase

in the number of published case reports describing men

with ILC over the years. Mariolis-Sapsakos et al. [7] included

a review of the published data in their case report and deter-

mined that the first case of male ILC was reported in 1982.

They also reported that �18 cases of ILC of the male breast

have been reported since then [7]. Similarly, the incidence of

women with ILC has also been increasing [16,22,23].

The final variable analyzed in the present study was

survival. Men with ILC had poorer survival rates than women.

A marked difference was found in the 5-year survival rates

betweenmen and womenwith ILC, although the difference in

the 10-year survival rates between the men and women was

much less distinct. This suggests that men are more likely to

die within the first 5 y of their caner diagnosis; however, those

who survive beyond the first 5 y are more likely to live until

10 y after diagnosis.

These data regarding survival add greatly to the breadth of

knowledge regarding the outcomes of men with ILC, because

the published data have provided very little information on the

long-term outcomes ofmen with this disease. The information

on follow-up provided in case reports tended to bewithin 3 y of

diagnosis and/or treatment. A few reports stated that the

patient was disease free at follow-up [4,7,8], and a small

number of case reports reported men who were not well at

follow-up. Scheidbach et al. [9] described a patient treated with

modified radical mastectomy and tamoxifen. Although the

tumor had invaded the thoracic wall, the surgeons decided not

to resect the thoracic wall, and the patient had developed

recurrent disease of the chest wall at 15 months of follow-up

[9]. Regarding the survival of women with ILC, the women

had a cancer-specific 5-year survival rate of 91.9% and a 10-year

survival rate of 84.5%. These rates were slightly better than

those found by Bharat et al. [17], who found that women with

ILC had a 5-year survival rate of 87% and a 10-year survival rate

of 68%. Winchester et al. [14] established that women treated

with modified radical mastectomy and breast conservation

therapy had comparable survival rates, with about 87%

surviving after 5 y. Similar 5-year survival rates were found in

other studies [12]. The cancer-specific survival rates for those

with LCIS were 100% for men and nearly 100% for women. This

is in line with previous research that has also shown 100%

survival rates for patients with LCIS [24].

The present study had a few limitations, lacking data on

tumor recurrence and the use of chemotherapy and hormonal

therapy. The SEER public use data set does not include data on

these variables; therefore, we were unable to include such

information in our analysis. All these variables could poten-

tially affect the outcome of those with ILC. We were also

unable to obtain information on the insurance status of the

subjects in our study. This could have affected the individual

outcome by limiting access to treatment. Furthermore, a fair

amount of information in the present study was listed as

unknown. This could have been because several assays, such

as estrogen and progesterone receptor testing, were not per-

formed as frequently in the 1980s and early 1990s. Finally, the

disparity in the number of women included in our study

compared with the number of men was large. The number of

men diagnosed with breast cancer constitutes only about 1%

of all breast cancer cases; thus, we expected the number of

male patients to bemuch lower. Also, wewanted to include all

the female patientswhomet our inclusion criteria tomaintain

the statistical robustness.

However, the present study had several important

strengths. One strong point was that the data were obtained

from a large, nationally representative sample. This made the

data applicable to the general population of the United States.

Also, using this large sample allowed us to analyze multiple

cases of ILC of the breast in men, instead of describing single

cases of the disease, such as has been done previously.

Additionally, the present study was able to assess the trends,

optimal treatment, and long-term outcomes. However, the

greatest strength of the present study was that it is the first

large-scale comprehensive study of this very rare disease

and thus provides a wealth of information to practitioners,

healthcare providers, and researchers.

5. Conclusions

The present study has provided a great amount of information

regarding a very rare type of breast carcinoma in men. Our

major finding was that ILC of the breast in men, with the

greater likelihood of presenting at a higher grade and stage

and resulting in poorer survival, appears to be a slightly

different disease than ILC of the breast in women. The data

provided in the present study suggest that the treatment of

men with ILC might need to be adjusted to account for this

difference. Also, because the incidence of ILC of the male

j o u rn a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) e 7 1ee 7 6e76

breast is increasing, finding the optimum treatment will be

very important for the treatment of the growing number of

men who will be diagnosed with the disease. Additional

studies should aim to investigate the use of chemotherapy,

radiotherapy, and hormonal therapy for men with ILC of the

breast and assess the effects on their outcome.

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