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Original Article

BREAST CANCER SCREENING IN A RESOURCE POOR COUNTRY:


ULTRASOUND VERSUS MAMMOGRAPHY

Olubukola A.T Omidiji1, Princess C. Campbell2, Nicholas K. Irurhe1, Omolola M. Atalabi3 and Ol-
uyemisi O.Toyobo4
Ghana Med J 2017; 51(1): 6-12 DOI: http://dx.doi.org/10.4314/gmj.v51i1.2
1
Department of Radiation Biology, Radiotherapy, Radiodiagnosis and Radiography, College of Medicine,
University of Lagos, Lagos, Nigeria, 2Department of Community Medicine and Primary Care, College of
Medicine University of Lagos, Nigeria, 3Department of Radiodiagnosis, College of Medicine University of
Ibadan/University College Hospital, Ibadan. Oyo State Nigeria 4Department of Radiology, Olabisi Onabanjo
University Teaching Hospital, Ogun State, Nigeria

Corresponding author: Dr. Olubukola A. T. Omidiji E-mail: [email protected]


Conflict of interest: None declared

SUMMARY
Background: Breast cancer is the commonest female cancer in Nigeria. Despite its increased awareness, affordabil-
ity of available screening tools is a bane. Mammography, the goal standard for screening is costly and not widely
available in terms of infrastructure, technical/personnel capabilities. Ultrasound is accessible and affordable.
Objectives: This study compared the use of ultrasound and mammography as breast cancer screening tools in wom-
en in South West Nigeria by characterizing and comparing the prevalent breast parenchyma, breast cancer features
and the independent sensitivity of ultrasound and mammography.
Methods: This cross sectional comparative descriptive study used both ultrasound and mammography as screening
tools in 300 consenting women aged 30 to 60 years who attended a free breast cancer screening campaign in a ter-
tiary hospital in Lagos. Categorical variables were presented in tables and Chi squares for associations P- value set
at ± 0.1.
Results: Mean age was 41.01 + 6.5years with majority in the 30 – 39 year age group 139 (55%). Fatty (BIRADS A
and B) parenchyma predominated {ultrasound 237 (79%); mammography 233 (77.7%)} in all age groups. 7 (2.3%)
were confirmed malignant by histology with (6) in the 30-39 age group and (1) in the 40-49 age group. Ultrasound
detected all the confirmed cases 7(100%), whereas mammography detected 6 (85%). Sensitivity was higher using
ultrasound (100%) than mammography (85.7%).
Conclusion: Ultrasound can be utilized as a first line of screening especially in remote/rural areas in developing
world.

Funding: Part funding from Run for Cure governmental organization


Keywords: Breast Cancer, Women, Ultrasound, Mammography, Sensitivity

INTRODUCTION
Breast cancer is the leading female malignancy globally, with late presentation of the disease, inadequate diag-
and the most common female cancer in Nigeria.1 It ac- nostic and treatment facilities in the developing coun-
counts for three-fourths of total deaths from the disease tries.3 Early detection improves the outcomes or surviv-
worldwide.2 Late presentation of patients at advanced al rates of breast cancer, hence screening of asympto-
stages when little or no benefit can be derived from any matic, apparently healthy women is very essential, es-
form of therapy has been the hallmark of breast cancer pecially when there are risk factors such as the history
in Nigerian women, with survival rates less than 10%.2 of breast cancer in immediate relatives.4

Survival rates are much higher in the developed coun- A number of screening tests are being employed; these
tries than in the developing countries with lower inci- include breast examinations, mammography, molecular
dence rates, due to lack of early detection programmes imaging and genetic screening; ultrasound and magnetic

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Original Article

resonance imaging, however the three main screening rienced radiologists were also trained; two (2) on how to
tests are breast examinations, mammography and ultra- document findings of ultrasound and two (2) on docu-
sound.4 The awareness of breast cancer and the im- mentation of findings of mammography. This was to
portance of screening have increased over the years5 reduce observer/examiner bias and variability.
however the bane of unaffordability still persists. Poor
participation in screening programs has persisted despite Study Instruments
the increase in awareness.6 The questionnaire self-designed, pre-tested and validat-
ed by two renowned experienced radiologists, consisted
Mammography, though presently the method of choice of 3 sections on socio-demography, reproductive health,
for screening and diagnosis is costly in Nigeria and not and documented findings of parenchymal types and
widely available in terms of infrastructure and tech- breast cancer features.
nical/personnel capability.5 It also has limited sensitivity
in dense breasts.7 Ultrasound is widely accessible and Imaging Technique
affordable and is presently utilized as an adjunct to Mammography: With strict adherence to standard pro-
mammography. It does not utilize ionising radiation, tocols, the standard medio-lateral oblique and cranio-
which in itself induces more cancers.7 caudal views bilaterally were used to conduct this pro-
cedure by the trained radiographers. Findings were re-
This study compared the use of ultrasound and mam- viewed and documented, and additional views taken
mography as breast cancer screening tools in women when required by the trained radiologists.
who attended free breast cancer screening exercise in a
centre in Lagos, by characterizing and comparing the Ultrasonography: Adhering to the standard protocols
prevalent breast parenchyma, features of breast cancer ultrasonography was done by the trained radiologists,
and the independent sensitivity of ultrasound and both breasts and axillae were scanned. The images were
mammography. reviewed real time on screen; findings were document-
ed. All suspicious (BIRADS 3 and above) lesions for
METHODS both modalities were sent for histology with findings
This cross sectional comparative study recruited 300 also documented.
consenting women based on calculated minimum sam-
ple size using Buderer’s formula8 for sensitivity and Data Analysis
specificity, The data was analysed using the SPSS for Windows
Sample size based on sensitivity8 version 18.0 software program. . For ease of compari-
n = Z21- α/2 x SN x (1 – SN) son, the breast parenchymal density was divided into
L2 x Prevalence two broad groups (fatty (BIRADS A and B) and fibro-
glandular (BIRADS C and D). The breast density (BI-
Where n = required sample size; SN = anticipated sensi- RADS A – D) and total number of detected participants’
tivity- 80% (0.08); SP = anticipated specificity –78% lesions were assessed for the total patient population, as
(0.78); α = size of the critical region (1 - α is the confi- well as for subpopulations grouped by age (30 -
dence level); Z21- α/2 = standard normal deviate corre- 39years, 40 - 49 years, >50 years) and hormonal status
sponding to the specified size of the critical region – (premenopausal or postmenopausal).
1.68 and L= absolute precision desired on either side
(half-width of the confidence interval) of sensitivity or The lesion detection rates were reported for each modal-
specificity – 0.10. ity, both for lesions detected solely with that modality
and for lesions detected with a combination of those
A systematic random sampling technique was used to modalities. Performance characteristics of each screen-
select participants between 30 and 60 years of age, who ing modality, including sensitivity, specificity, positive
attended the free breast cancer screening campaign in a and negative predictive values were calculated. Categor-
tertiary hospital in Lagos State. Clients with symptoms ical variables were presented in tables. For significant
(mastalgia, nipple discharge or lump), previous breast difference, chi square and a p value of 0.10 were used to
lump excisions or biopsies, history of trauma, who had reduce the dense sample of 768 to 300 in line with
never breastfed, and pregnant and lactating mothers available resource.
were excluded from the study.
Ethical approval
Two (2) experienced radiographers at the centre were Ethical approval was obtained from the Health Research
trained on the objectives, technique and rationale of the and Ethics Committee of the Lagos University Teaching
study for two days for one hour per day. Four (4) expe- Hospital, and all other research protocols were strictly

7 www.ghanamedj.org Volume 51 Number 1 March 2017


Original Article

adhered to. Assigned ethical clearance number


ADM/DCST/HREC/1486.

RESULTS
Socio-demographic and Reproductive Health
This predominantly married 261(87.0%), tertiary edu-
cated 285(95.0%), professional 227(75.7%), Yoruba
195(65.0%) respondents, had an age range of 30 to 60
years and a mean age of 41.01+ 6.5years. Over half
(55.0%) were between 30 – 39 years.

Up to (112, 37.0%, 75, and 25%) had 2 and 3 children


respectively, 165 (55%) were premenopausal, 8 out of
10 participants did not use any form of contraceptive
251 (83.7%). History of alcohol ingestion was by 33
(11%), and smoking 5 (1.7%). Only 17(6.7%) had a
family history of breast cancer in a close relative. Partic- Figure 1 Prevalent breast parenchyma
ipants were predominantly married, tertiary educated,
professional with over 55% between 30 -39years (see Features of breast cancer
Table 1). Majority, 181(60.3%) and 174(58.0%) of the partici-
pants had a normal study (BIRADS I) using both ultra-
Table 1 Socio-demographic distribution sound and mammography respectively. Probable benign
Frequency(N=300) Percentage lesions (BIRADS III) were seen in 7(2.3%) and 8(2.7%)
Age (Years)
30-39 139 46.3
participants using ultrasound and mammography re-
40-49 127 42.3 spectively.
>50 34 11.4
Mean age 41.01+6.5 Table 2 BIRADS category and features of suspicious
Marital Status
Single 26 8.7
lesions seen using ultrasound and mammography
Married 261 87.0 Ultra- Mammog- p-value
Others* 13 4.3 sound raphy
Level of education BIRADS CATEGO- N (%) N (%)
Completed secondary 15 5.0 RY
Tertiary 285 95.0 0 - 11 (8.0) X2 =
Others** 23 7.7 223.735
Occupation I 181 (60.3) 174 (58.0) df =12
Professional 227 75.7
Skilled 45 15.0 II 99 (33.0) 86 (28.7) P= 0.000
Unskilled 28 9.3 III 7 (2.3) 8 (2.7)
Others*=divorced, separated; Others**=Efik, Ijaw, Urobo; IV 13 (4.3) 8 (2.7)
Others***=Traditional Features of suspicious
lesions
Prevalent Breast Parenchyma Mass 20 (100) 11(73.3) 0.185
Spiculations 10 (50) 8 (53.3) 21.212
Similar findings of breast parenchyma were noted using Thick Incomplete 3 (15) 6 (40.0) Fisher
ultrasound {fatty 237(79%), fibroglandular 63(21%)} Halo
and mammography {fatty (BIRADS A and B) 233 Microlobulation 8 (40) 6 (40.0) 25.000
(77.7%), fibroglandular (BIRADS C and D) 67 Architectural Distor- 10 (50) 10 (66.7) 9.642
tion
(22.3%)} with fatty tissue predominant in all age Microcalcification 2 (10) 4 (26.7) Fisher
groups. Axillary lymphade- 4 (20) 5 (33.3) 19.792
nopathy
Mammography however detected less fatty than fibro- *0 = Inconclusive, I = normal/negative, II = benign, III = probably
glandular tissues in all the age groups. The distribution benign (2%suspicion of malignancy), IV – 34% suspicious of malig-
nancy. Only a few had category III and IV lesions; more were detected
of parenchyma in the age groups was not statistically using ultrasound. Commonest features seen were mass, spiculations
significant. Fatty parenchyma (BIRADS A and B). Fi- and architectural distortion.
bro glandular parenchyma (BIRADS C and D). Fatty
parenchyma predominated across all age groups. A total of 25(8.3%) participants had suspicious lesions,
out of which 20(6.6%) were seen by ultrasound and
15(5.0%) were seen using mammography.

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Original Article

The difference in distribution of the lesions in ultra-


sound and mammography were statistically significant
(p 0.00) (see Table 2)

Twenty five (8.3%) participants were suspected of hav-


ing breast cancer using ultrasound and mammography.
The features of breast cancer seen on ultrasound and
mammography were mass, spiculation, halo, microlobu-
lation, architectural distortion, calcification and axillary
lymphadenopathy. Ultrasound detected a mass in all its
detected cases 20(100%) of cases, more than mammog-
raphy which detected in 11(73.3%) of 15 detected cases. Figure 3 Corresponding ultrasound of the deep seated
mass shows a lobulated mass with spiculations.
Mammography however detected the other features
(spiculations 8(53.3%), architectural distortion The diagnostic yield for this study was 23 per 1000
10(66.7%), microcalcifications 4(26.7%), axillary lym- women screened (7/300). Most of the cases with differ-
phadenopathy 5(33.3%) in a higher proportion than Ul- ent categories on ultrasound and mammography were
trasonography (spiculations 10(50.0%), architectural benign. Of the mitotic lesions seen, 6 were ductal carci-
distortion 10(50.0), microcalcifications 2 (10.0%), axil- noma in situ.
lary lymphadenopathy 4(20.0%); the difference was
statistically significant (p 0.001) in all except for halo Table 3 Histologic findings in suspicious lesions; sensi-
6(40.0%). Microlobulations (ultrasound 8(40%), mam- tivity and specificity of the modalities
mography 6(40%) were seen in equal proportions using
Number of Ultrasound Mammography Histology Diagnosis
the two modalities, this was statistically significant p participants
0.001, Table 2. 2 IV III Benign Fibroadenoma
2 IV IV Benign Fibroadenoma
4 II III Benign Fibroadenoma
3 IV 0 Benign Fibroadenoma
5 III II Benign Fibroadenoma
2 III I Benign Fibroadenoma
6 IV IV Malignant DCIS*
1 IV 0 Malignant IDA*
Sensitivity 100.0 85.7
Specificity 22.2 55.5
Positive 33.3 42.8
predictive 100.0
value
Negative 100.0 90.9
predictive
Figure 2 Mediolateral mammogram of the right breast value
Accuracy 84.0 56.0
showing a deep seated highly dense breast mass

Sensitivity of Mammography and Ultrasound Seven (7) participants had malignant features and com-
Of the 25 suspected cases of breast cancer, 7 were con- monest was ductal carcinoma in situ (DCIS). Ultrasound
firmed malignant histologically. 6 were suspicious on had higher sensitivity than mammography.
both ultrasound and mammography (BIRADS IV), and
1 on ultrasound alone. The one missed on mammogra- Ultrasound had high sensitivity in detecting breast can-
phy was seen in an extremely dense (fibroglandu- cer (100%) but very low specificity (22%). Mammogra-
lar/BIRADS D) breast. phy had reduced sensitivity (85.7%) compared with
ultrasound but was more specific (55.4%). Positive pre-
dictive value was also low in ultrasound (33.3%) com-
pared with mammography (42.8%).

Negative predictive value (100%) was however higher


in ultrasound compared with mammography (90.9%).
Ultrasound also had a higher accuracy of detecting
breast cancer (84%) compared with mammography
(56%). Table 3

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Of the cases confirmed histologically, 6 (85.7%) were More benign 106 (35.3%) than malignant lesions
within the 30-39 age group with 4 (57.1%) having fatty 7(2.3%) were seen in the study, as was noted in other
parenchyma. The masses seen on ultrasound measured 5 studies conducted.10,11 Akinola et al also had multiple
- 28mm in width in size for both ductal carcinoma in benign lesions in the study of spectrum of mammo-
situ and invasive ductal carcinoma. Table 4, Figures 2 graphic findings; however the frequency was not men-
and 3. tioned.12

Table 4 Age group and parenchymal features seen in A high percentage 280 (93.3%) ultrasound and
histologically confirmed cases of breast cancer 263(87.0%) mammogram of this study population had
S/N AGE PARENCHY- Ultrasound Mammo- Histol- normal and benign findings (BIRADS 1 and 11) (Ta-
GROUP MA size (mm) graphic ogy ble 3), and is consistent with Berg et al’s study with
(years) USS (MAMMO Size
BIRADS) (mm)
only mitotic lesions in 1.5%, leaving normal and be-
1 30 - 39 Fatty ( A) 8 x 11 x 6 8 x 10 DCIS nign lesions at 98.5%.9 Benign lesions detected by
ultrasound 99 (33%) and mammography 89 (29.0%)
2 30 - 39 Fatty ( B) 28 x 17 x 24 20 x 12 DCIS in this study is in contradistinction with Devolli-Disha
3 30 - 39 Fatty (B) 5x3x3 - DCIS et al’s with 52%, their study population were symp-
tomatic women.7
4 30 - 39 Fatty ( A) 14 x 14 x 14 10 x 12 DCIS
5 30 - 39 Fibroglandular 5x4x4 - DCIS The most common features seen in this study (using
(D)
6 30 - 39 Fibroglandular 6x4x5 8x6 DCIS
both ultrasound and mammography) that raised a sus-
(C) picion of breast cancer include mass 20 (100%) ver-
7 40 - 49 Fibroglandular 28 x 26 x30 21 x 24 IDA sus 11 (73.3%), speculation 10 (50.0%) versus 8
(C) (53.3%) and architectural distortion 10 (50.0%) ver-
sus 10 (66.7%) using ultrasound and mammography
Majority were in the 30 – 39 age group and were found respectively. These findings were statistically signifi-
in fatty breasts, masses seen were comparable in size cant (p 0.001) in line with studies done.11,12 Ultrasound
using both modalities (largest 20mm) detected a mass in 20 (100%) of the suspicious cases,
more than mammography which detected 11(73.3%).
DISCUSSION
The slightly lower mean age (41.02+ 6.5years) than that This is contrary to a study by Berg et al which found
of Devolli-Disha etal7 and Berg etal9 (56.56+ more cancers using mammography than ultrasound.9
12.60years and 55.14 + 0.19years respectively) may This may be because patients who had a prior history of
probably be due to a wider age range of 30 – 79years breast cancer were not excluded from their study.9 It is
and 25 – 91years respectively. however similar to what was found during the Avon-
acrin trial by the American College of Radiology which
A lower breast density has been noted in African Amer- conducted ultrasound screening of asymptomatic wom-
ican women compared with Caucasian and Latino en with dense breasts for three consecutive years.13 Ul-
women.10 This is in consonance with what was seen in trasound detected 4.2 per 1000, more than were detected
this study as the predominant breast parenchyma in the at mammography.
entire study population was fatty (BIRADS A and B)
using both ultrasound 237 (79%) and mammography Architectural distortion is another important feature of
233 (77.7%) in almost equal proportion. Predominantly breast cancer that must not be missed or overlooked. A
fibro glandular parenchyma was seen in 21 – 23% of the study found out that of the percentage that had architec-
study participants in consonant with a Ugandan study tural distortion using mammography, 5 -7% were ma-
with 25% (BIRADS C and D).11 lignant.14 Architectural distortion was seen in 10 (50%)
and 10 (66.7%) of cases in this study using ultrasound
Breast density decreases with increasing age due to a and mammography and all the 7(2.3%) who were con-
decrease in glandular tissue and its replacement by fat.12 firmed cases of breast cancer had this feature. The dif-
ference may be due to the small study population uti-
lized in this study.
This is similar to findings in this study, as the women in Breast cancer has been known to occur more frequently
the >50year age group had less fibro glandular paren- in those with fibro glandular tissue, especially in the
chyma 7 (20.6%) and hence less density than those in Caucasians.10 A researcher estimated a four to six fold
the 40 -49year age group 29 (22.8%). increased risk of having cancer compared with women

10 www.ghanamedj.org Volume 51 Number 1 March 2017


Original Article

with less dense tissue.15 In this study however, majority


6 (85.7%) of the 7 participants who had breast cancer The features of breast cancer were mass, architectural
were identified as having fatty parenchyma using both distortion, speculations and micro calcifications. Ultra-
ultrasound and mammography. This may be because the sound detected more masses than mammography; how-
study is done in an African population who have less ever mammography was better at detecting micro calci-
dense tissue than their Caucasian or Latino counter- fications, which was one of the first features that sug-
parts.10 gest an interval cancer.

Mammography has inherent limitations with a reported RECOMMENDATIONS


false negative rate of 10 – 15%.15 Ultrasound on the The importance of screening cannot be overemphasized.
other hand is highly sensitive with a high false positive The Federal, State and Local government should devel-
rate, which results in a high cost of benign biopsies op policies and guidelines that would ensure routine
when compared with mammography.13 These findings screening of all women for breast cancer. Adequate
are similar to what was found in this study. funds should be made available and manpower
strengthened for the implementation of integrated spe-
The sensitivity and specificity of each imaging modality cific vital public health breast cancer programmes.
were assessed with ultrasound yielding a high sensitivi-
ty (100%) and low specificity (22%) and mammography It is also recommended that annual breast screening
having a lower sensitivity than ultrasound (85%), but a should commence from the age of 30years, using ultra-
much higher specificity (55.5%). sound as a first line screening tool in nulliparous women
and parous women or both ultrasound and mammogra-
The ultrasound specificity is similar to what is obtained phy in order to increase accuracy. Ultrasound can be
in older studies in which inadequate detection of smaller used as a first line of screening especially in remote
cancer and false positive biopsy rates have been docu- /rural areas of the developing world.
mented;14 however it is unlike what is now obtained in
literature, in which high specificity is recorded.14 This REFERENCES
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