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Breast compression and reported pain during mammographic screening
Radiography xxx (xxxx) xxx
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Breast compression and reported pain during mammographic screening N. Moshina a, *, S. Sagstad a, S. Sebuødegård a, G.G. Waade b, E. Gran c, J. Music c, S. Hofvind a, b a b c
Cancer Registry of Norway, P.O. 5313 Majorstuen, 0304, Oslo, Norway Oslo Metropolitan University, P.O. 4, St. Olavs Plass, 0130, Oslo, Norway Akershus University Hospital, Sykehusveien 25, 1478, Lørenskog, Norway
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 July 2019 Received in revised form 1 October 2019 Accepted 5 October 2019 Available online xxx
Introduction: We aimed to investigate the association between breast compression and experienced pain during mammographic screening. Methods: Using a questionnaire, we collected information on pain experienced during mammography from 1155 women screened in Akershus, FebruaryeMarch 2018, as a part of BreastScreen Norway. The questionnaire provided information on pain using a numeric rating scale (NRS, 0e10) and related factors. Data on compression force (Newton, N), pressure (kilopascal, kPa) and breast characteristics were extracted from the DICOM-header and a breast density software. Log-binomial regression was used to determine the relative risk (RR) of severe versus mild/moderate experienced pain associated with compression parameters, adjusting for breast characteristics and related factors. Results: Mean score of experienced pain was 2.2, whereas 6% of the women reported severe pain (7) during the examination. High body mass index (BMI) (27.3 kg/m2) was associated with a higher RR of pain scores 7 (RR 1.86, 95%CI 1.02e3.36) compared to medium BMI (23.7e27.2 kg/m2). Low compression pressure (4.0e10.2 kPa) was associated with a higher RR of severe pain (RR 2.93, 95%CI 1.39 e6.20), compared with medium compression pressure (10.3e13.5 kPa) after adjusting for contact area, age, compressed breast thickness, volumetric breast density and BMI. The risk of severe versus mild/ moderate pain (7 versus <7) decreased by 2% with increasing compression force (RR 0.98, 95%CI 0.97 e1.00). Conclusion: Women reported low levels of pain during mammography. Further knowledge about factors affecting experienced pain is needed to personalize the examination to the individual woman. Implications for practice: Pain in shoulder(s) and/or neck prior to screening should be considered by the radiographers in a practical screening setting. A compression force of 100e140 N and pressure of 10.3 e13.5 kPa are acceptable with respect to reported pain during mammography. © 2019 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Keywords: Compression force Compression pressure Mammography Pain Breast cancer screening
Introduction Breast compression immobilizes the breast between a compression paddle and the image receptor of the mammography machine,1 and is aimed to optimize image quality and reduce radiation dose. Vendors of mammographic equipment and countries
* Corresponding author. E-mail addresses: [email protected] (N. Moshina), Silje. [email protected] (S. Sagstad), Sofi[email protected] (S. Sebuødegård), [email protected] (G.G. Waade), Evy.Gran@ahus. no (E. Gran), [email protected] (J. Music), Solveig.Hofvind@kreftregisteret. no (S. Hofvind).
offering mammographic screening recommend optimal ranges of breast compression.2 However, there is limited or no evidence to support these ranges according to image quality and the women's experience of pain. Women might experience pain associated with breast compression during and/or after mammography.3e5 This experience may prevent women from undergoing mammography or attending screening.3e7 A review concluded that 25e46% of the women indicated pain associated with breast compression as the reason for not attending the next screening.6 In previous studies, breast compression during mammography has mainly been discussed as a subjective measure or using compression force (Newton, N).1,3e5,8,9 However, experience of pain
https://doi.org/10.1016/j.radi.2019.10.003 1078-8174/© 2019 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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during mammography is also influenced by the communication between the radiographer and the woman, the equipment and the situation.7,10 As far as we are aware, there is limited knowledge about these combinations, which hampers any recommendations for optimal compression.10 Data on compression force are available to the radiographers when they compress the breast. The data are stored in the DICOMheader of the image and could be extracted for research. Recent studies have reported substantial variation in applied compression force between breast centres and between radiographers.11e14 Compression pressure (kilopascal, kPa) is considered a more sensitive measure than compression force in relation to experienced pain as it takes into account the size of the breast.15e17 Pressure is typically estimated retrospectively by different types of software and not visible during the screening examination.17 However, recent developments in fixed paddle technology provides data on compression pressure during the examination.18 Studies have shown promising results on the use of pressure standardized mammography, but substantial knowledge gaps associated with the practical implementation in screening and/or clinical setting still need to be filled in order to recommend the use pressure instead of force based compression.16,17 In this study, we wanted to investigate possible relations between compression force and pressure and reported pain among women who attended mammographic screening in Akershus as a part of BreastScreen Norway. Materials and methods This study was permitted under the Cancer Registry Regulations and approved by the Data Protection Official at Oslo University Hospital (2017/6481).19 BreastScreen Norway The Cancer Registry of Norway administers the populationbased breast cancer screening program, BreastScreen Norway, that serves about 650,000 women aged 50e69 years. The women are offered biennial mammographic screening that typically includes four digital mammograms (DM) with craniocaudal (CC) and mediolateral oblique (MLO) views of each breast. The annual participation rate is about 75%. The program has been described in detail elsewhere.20 Study sample Among 2934 women, who attended one of the two screening units in the Akershus county during the study period, FebruaryeMarch 2018, 1373 (46.8%) agreed to participate in this study (Fig. 1). We excluded women who did not report their experience of pain (n ¼ 40), information about pain in shoulder(s) and/or neck prior to screening (n ¼ 56) or did not give any information about weight and height (n ¼ 92). We also excluded women without information about breast volume (n ¼ 30). The final study population consisted of 1155 women. All women were screened using Philips MicroDose SI (Amsterdam, the Netherlands) and a fixed compression paddle available in two sizes, 24 31 cm and 19 23 cm. The radiographers performing screening mammography had from one week to 20 years of working experience and worked in mixed pairs: the first radiographer examined the left breast (CC and MLO) and the second radiographer examined the right breast (CC and MLO). The compression and positioning of the breast were performed according to the national guidelines.21 During the study period, all attending women were invited to participate in this study at the standard prescreening interview
Figure 1. Study population.
conducted by the radiographers. The women who agreed to participate received a questionnaire, which included a study identifier (running number) and questions about experienced pain related to their mammographic examination. The questionnaire was completed immediately after the examination and submitted in a closed letter case at the screening unit. Responding to the questionnaire was considered an informed consent to use the data in this study. The questionnaire A continuous numeric rating scale (NRS) was used for measuring experienced pain. The women marked their response on a line, ranging from 0 to 10, indicated by 11 marks. A score of 0 indicated no pain while 10 indicated very strong pain. The choice of NRS was associated with the use of NRS in previous studies measuring the experience of pain during mammography.15,17,23,24 The women further reported information about presence of pain in shoulder(s) and/or neck prior to screening as well as weight (kg) and height (m), which were used to calculate body mass index (BMI, kg/m2) as weight divided by squared height. Variables of interest Response to the questionnaire was manually coded at the Cancer Registry. Using the running number, the responses were linked to data about characteristics of the women and compression parameters. Information on compression force and compressed breast thickness (mm) was obtained from the DICOM header while data about compression pressure and breast characteristics, including contact area (mm2), breast volume (cm3) and volumetric breast density (%) were extracted using a software for density assessment.18 Information about the women's age and screening history (prevalently screened or (i.e. screened for the first time), and subsequently screened (i.e. screened previously) was obtained from the Cancer Registry of Norway. In the questionnaire, the women evaluated the screening examination consisted of on average four images in relation to their experience of pain. Therefore, we present
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
N. Moshina et al. / Radiography xxx (xxxx) xxx
average values for each screening examination (four images), which was considered the unit of analysis in this study. Statistical analyses Descriptive statistics included means with 95% confidence intervals (95%CI) or standard deviation (SD) to describe the women's characteristics and study parameters of interest. First, we stratified experienced pain into four groups, according to the NRS; no pain (0e2), mild,3e5 strong6e8 and intense pain.9,10 Further, we used a cut point of 7 (<7 versus 7) to categorize the experience: a score of <7 corresponded to mild or moderate pain, while a score of 7 included severe pain.15,17,22 This cut point was chosen to identify women who reported severe pain, as the values 7 was considered a strong negative experience of mammography, perceived as a procedure causing significant and/or unbearable pain. We used t-tests to compare mean values and chi-square tests to compare distributions within the groups. Means of pain were also calculated for the variables of interest categorized in tertiles: compression force [low (46e109 N), medium (110e122 N) and high (123e179 N)], compression pressure [low (4.0e10.2 kPa), medium (10.3e13.5 kPa) and high (13.6e35.2 kPa)], breast volume [tertiles: low (116e701 cm3), medium (702e1091 cm3) and high (1092e3230 cm3)], contact area [tertiles: low (3438e8800 mm2), medium (8814e12051 mm2) and high (12,054e26541 mm2)], compressed breast thickness [tertiles: low (19e55 mm), medium (56e67 mm) and high (68e96 mm)], volumetric breast density [tertiles: low (2.4e4.9%), medium (5.0e7.9%) and high (7.8e30.1%)], age (50e54; 55e60; 61e71 years). BMI was grouped into tertiles as low (<23.7 kg/m2), medium (23.7e27.2 kg/m2) and high (27.2 kg/m2). We used binomial regression with log link to determine the relative risk (RR) of severe pain (7) associated with the variables of interest categorized in tertiles. Further, we performed adjusted analyses for compression force and compression pressure, adjusting for contact area, breast volume, age, compressed breast thickness, volumetric breast density and BMI. In
3
addition, log-binomial regression models were used to estimate the RR of severe pain (7) associated with compression force or pressure (continuous), adjusted for shoulder(s) and/or neck pain prior to screening (present versus absent), breast volume (continuous), compressed breast thickness (continuous), volumetric breast density (continuous) and BMI (continuous).25 Breast volume was not included in the models with compression pressure due to colinearity of the variables.26 Two-way fractional-polynomial prediction plots with 95%CI for reported pain by applied compression force and pressure were shown. All analyses were conducted using STATA® 15.0 (StataCorp, Texas, USA). Results Mean age of the study population was 57.8 years (SD: 5.7) (Table 1). A total of 19% of the women were prevalently screened. Means of compression force and pressure were 117 N (SD: 18.0) and 12 kPa (SD: 3.9), respectively. Means of compressed breast thickness were statistically significantly lower for women who reported no pain compared to those who reported mild or strong pain (p ¼ 0.003 and p ¼ 0.01, respectively). Percentage of women with pain in shoulder(s) and/or neck prior to screening was significantly higher for women who reported strong or intense pain compared with those who reported no or mild pain. Mean pain score for the women comprising the study population was 2.2 (Table 2). High BMI (27.3 kg/m2) was associated with a higher RR of severe pain (RR 1.86; 95%CI 1.02e3.36), compared with medium BMI (23.7e27.2 kg/m2) (p ¼ 0.04) (Table 2). Low compression pressure (4.0e10.2 kPa) was associated with a higher RR of severe pain (RR 2.93; 95%CI 1.39e6.20), compared with medium compression pressure (10.3e13.5 kPa) when adjusting for contact area, age, compressed breast thickness, volumetric breast density and BMI. Increasing compression force was associated with a 2% lower RR of severe pain (RR 0.98, 95%CI 0.97e1.00) in the adjusted model, including age, breast volume, compressed breast thickness, breast
Table 1 Descriptive information for the variables of interest by four groups of experienced pain on the numeric rating scale (NRS) among 1155 women screened in Akershus as a part of BreastScreen Norway FebruaryeMarch 2018. Group 1
Group 2
Group 3
All
No pain (NRS 0e2) Mild pain (NRS 3e5)
Strong pain (NRS 6e8)
Intense pain (NRS 9e10)
n ¼ 1155
n ¼ 753
n ¼ 158
n ¼ 35
n ¼ 209 p-valuea
Age Mean (SD), years BMI Mean (SD), kg/cm2 Compression force Mean (SD), N Compression pressure Mean (SD), kPa Contact area Mean (SD), mm2 Breast volume Mean (SD), mm3 Compressed breast thickness Mean (SD), mm Volumetric breast density Mean (SD), %
a
c
p-valuea
p-valuea
57.8 (5.7)
57.6 (5.7)
58.1 (5.8)
0.340
58.1 (5.6)
0.415
57.0 (6.0)
0.516
26.2 (5.0)
26.0 (5.0)
26.7 (5.0)
0.083
26.3 (4.7)
0.495
26.9 (5.1)
0.309
117 (18.0)
117 (17.3)
117 (18.5)
0.671
116 (20.1)
0.877
111 (19.3)
0.074
12 (3.9)
12 (3.9)
12 (3.9)
0.703
13 (3.8)
0.425
12 (4.9)
0.998
10,963 (3856) 11,020 (3809)
10,987 (3920) 0.914
10,658 (3907) 0.279
10,964 (4345)
0.933
957 (476)
940 (484)
998 (457)
0.126
982 (470)
0.322
962 (462)
0.794
60 (13)
59 (13)
62 (12)
0.003
62 (12)
0.011
61 (12)
0.503
7.5 (4.3)
7.6 (4.2)
7.2 (4.2)
0.165
7.3 (4.6)
0.418
7.1 (4.1)
0.466
21% 25%
17% 27
Prevalently screenedc 19% Pain in shoulder/neck prior to screening 27% b
p-valueb
Group 4
15% 35%
17% 34%
0.268 0.037
Different from Group 1. Chi-square test. Screened for the first time in the program.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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density and BMI (Table 3). No association between compression pressure and severe pain was observed when compression pressure was presented as a continuous variable (Table 4). The lowest predicted reported pain scores (2.1e2.2 on NRS) were observed for the compression force between 100 N and 140 N (Fig. 2). The highest predicted pain scores (4.0e7.0 on NRS) were shown for the compression force of 60 N. The lowest predicted reported pain scores (2.1e2.2 on NRS) were observed for the compression pressure between 8 kPa and 13 kPa (Fig. 3). The highest predicted reported pain scores (3.0e3.8 on NRS) were shown for the compression pressure of 7 kPa. Discussion The whole scale of reported pain scores from 0 to 10 on a NRS were used, with a mean of 2.2 for 1155 women who underwent mammographic screening in Akershus, as a part of BreastScreen Norway. Only six percent of the women reported severe pain. Low versus medium compression pressure was associated with a higher relative risk of severe pain, however there was no association between increasing compression pressure and risk of severe pain. Increasing compression force was associated with a lower relative risk of severe versus mild/moderate pain. Our findings are in line with results from other studies,3,27,28 but contradict the findings from de Groot et al. and Branderhorst et al., indicating that standardization of compression pressure could lead
to reduction of pain during mammography.15,16 It should be noted that our results are not directly comparable with the studies by de Groot et al. and Branderhorst et al. and we assume that our findings are associated with women's expectations and reaction to breast compression, while the results of the aforementioned studies are related to the use of different protocols of compression force and pressure standardisation. Women who experience or anticipate severe pain usually ask the radiographer to stop compressing, and receive generally lower compression force and pressure than those who tolerate higher forces and pressures. Our interpretation of the findings on compression pressure and force are supported by the correlations between these parameters and experienced pain depicted by the polynomial prediction plots, indicating higher pain scores for lower pressures and forces. Compressed breast thickness was higher for women who reported mild to strong pain (NRS 3e8) compared to those who reported no pain (NRS 0e2). Compressed breast thickness might depend on the volume of the breast, compression force and compressibility of the breast. As fatty tissue is easier to compress than the fibroglandular tissue, it is assumed that fatty breasts have lower compressed breast thickness and larger contact breast area.16,26 This suggests that women with less compressible breasts experience more pain compared to women with easy compressible breasts. However, our study did not show any association between breast density and experienced pain. On the other hand, the compressibility of the breast might be related to different factors
Table 2 Mean pain scores and relative risk (RR) of severe pain (7) associated with compression force and pressure, contact area, breast volume, compressed breast thickness, volumetric breast density, shoulder(s)/neck pain prior screening, body mass index, and age groups, among 1155 women screened in Akershus as a part of BreastScreen Norway, FebruaryeMarch 2018. Mean pain score Total 2.2 Compression force (N) 1. Low (46e109 N) 2.3 2. Medium (110e122 N) 2.1 3. High (123e179 N) 2.3 Compression pressure (kPa) 1. Low (4.0e10.2 kPa) 2.1 2. Medium (10.3e13.5 kPa) 2.1 3. High (13.6e35.2 kPa) 2.4 2 Contact area (mm ) 1. Low (3438e8800 mm2) 2.4 2. Medium (8814e12051 mm2) 2.2 3. High (12,054e26541 mm2) 2.1 Breast volume (cm3) 1. Low (116e702 cm3) 2.1 2. Medium (703e1091 cm3) 2.2 3 3. High (1092e3230 cm ) 2.4 Compressed breast thickness (mm) 1. Low (18e55 mm) 2.1 2. Medium (56e67 mm) 2.1 3. High (68e96 mm) 2.5 Volumetric breast density (%) 1. Low (2.4e4.9%) 2.4 2. Medium (5.0e7.9%) 2.1 3. High (7.8e30.1%) 2.1 Pain shoulder(s)/neck prior screening 1. Yes 2.5 2. No 2.1 Body Mass Index (kg/m2) 1. Low (<23.7 kg/m2) 2.1 2. Medium (23.7e27.2 kg/m2) 2.1 2 3. High (27.3 kg/m ) 2.4 Age (years) 1. <55 2.3 2.55-60 2.1 3. >60 2.3 a b
Crude RR
95% Confidence interval
P-value
Adjusted RRa,b
95% Confidence interval
P-value
1.62 1.00 1.13
(0.91e2.87)
0.10
(0.83e2.68)
0.19
(0.61e2.11)
0.70
1.49 1.00 1.14
(0.60e2.18)
0.68
1.55 1.00 1.67
(0.84e2.85)
0.16
(1.39e6.20)
0.01
(0.91e3.06)
0.10
2.93 1.00 1.06
(0.50e2.24)
0.87
1.42 1.00 0.83
(0.82e2.44)
0.21
(0.45e1.55)
0.57
0.98 1.00 0.86
(0.56e1.71)
0.95
(0.48e1.53)
0.60
1.30 1.00 1.34
(0.72e2.33)
0.39
(0.75e2.41)
0.33
(0.98e2.67)
0.17
(0.65e2.20)
0.58
1.42 1.00
(0.87e2.31)
0.16
1.40 1.00 1.86
(0.74e2.62)
0.30
(1.02e3.36)
0.04
(0.98e3.22)
0.06
(0.60e2.26)
0.64
1.50 1.00 1.19
1.78 1.00 1.17
Adjusted for contact area, breast volume, age, compressed breast thickness, volumetric breast density and body mass index for compression force. Adjusted for contact area, age, compressed breast thickness, volumetric breast density and body mass index for compression pressure.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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Table 3 Log-binomial regression for the association between severe pain (7) using <7 as reference, and continuous variables: compression force, age, breast volume, compressed breast thickness, volumetric breast density, and body mass index (BMI) among 1155 women screened in Akershus as a part of BreastScreen Norway, FebruaryeMarch 2018.
Compression force (N) Age (years) Breast volume (cm3) Compressed breast thickness (mm) Volumetric breast density (%) BMI (kg/m2) a
Pain <7.0 vs pain 7.0
Pain <7.0 vs pain 7.0
Relative risk
Relative risk
Crude
95% Confidence interval
p-value
Adjusteda
95% Confidence interval
p-value
0.98 1.00 1.00 1.01 1.02 1.03
(0.97e1.00) (0.95e1.04) (0.95e1.00) (1.00e1.04) (0.98e1.09) (0.96e1.09)
0.03 0.87 0.93 0.63 0.49 0.29
0.98
(0.97e1.00)
0.01
Adjusted for age, breast volume, compressed breast thickness, breast density and body mass index.
Table 4 Log-binomial regression for severe pain as an outcome (7) using <7 as reference with continuous variables: compression pressure, age, breast volume, compressed breast thickness, volumetric breast density and body mass index among 1155 women screened in BreastScreen Norway, FebruaryeMarch 2018.
Compression pressure (kPa) Age (years) Compressed breast thickness (mm) Volumetric breast density (%) BMI (kg/m2) a
Pain <7.0 vs pain 7.0
Pain <7.0 vs pain 7.0
Relative risk
Relative risk
Crude
95% Confidence interval
p-value
Adjusteda
95% Confidence interval
p-value
1.01 1.00 1.01 1.03 1.03
(0.95e1.07) (0.95e1.04) (1.00e1.05) (0.98e1.10) (0.96e1.09)
0.71 0.85 0.51 0.37 0.33
1.01
(0.92e1.10)
0.83
Adjusted for age, compressed breast thickness, volumetric breast density and body mass index.
Figure 2. Two-way fractional-polynomial prediction plot with 95% confidence interval for compression force (N) by reported pain on the numeric rating scale for 1155 women screened in BreastScreen Norway, FebruaryeMarch 2018.
Figure 3. Two-way fractional-polynomial prediction plot with 95% confidence interval for compression pressure (kPa) by reported pain on the numeric rating scale for 1155 women screened in BreastScreen Norway FebruaryeMarch 2018.
not indicated in a volumetric measure of mammographic density, such as tissue composition and breast tenderness.29e31 The women with high BMI reported higher levels of pain scores compared to women with medium BMI in our study. This might indicate that women with high BMI are among those with low compressibility of the breasts, which might be more sensitive to pain. We observed a higher percentage of women with pain in shoulder(s) and/or neck prior to screening among those who reported strong to intense pain (NRS 6e10). A similar finding has been observed in another study from Norway comparing compression paddles for screening mammography, and might suggest that pain in shoulder(s) and/or neck prior screening is an important confounder in the relationships between compression force, compression pressure and experienced pain, which should be considered by the radiographers in a practical screening setting.
Our results are in line with the findings reported by Myklebust et al. regarding experience of pain and discomfort during mammography among women undergoing breast cancer screening in Norway.5 High compression forces might thus be justifiable for acquiring mammograms of good quality. However, an important skill of the radiographers is to individualize the compression. Our study indicated a compression force between 100 N and 140 N and a compression pressure between 10.3 kPa and 13.5 kPa to be acceptable with respect to reported pain during the examination, without taking the image quality into consideration. Further studies on image quality associated with various compression will add valuable knowledge on this topic. The preferred value of compression force and pressure were 130 N and <10 kPa according to results of early outcome measures in a previous study from Norway.32 Another study performed on
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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N. Moshina et al. / Radiography xxx (xxxx) xxx
Norwegian data supported the range of 100e130 N for force and 9.0e17.9 kPa for pressure with regard to subsequent attendance among prevalently screened women.33 A study from the UK also concluded that the force of 90e130 N should be could be an appropriate compression termination point.34 Our results indicate that further knowledge is needed before evidence based recommendations of compression during mammography can be given. The results also indicate that recommendations of ranges should serve the individualization of the compression force and pressure and thus make the screening examination a better experience for the women. This study included data from 1155 women screened in the organized breast cancer screening program in Norway. Several factors as breast tenderness, menstrual status, breast pain prior to screening, education level, presence or absence of benign or malignant lesions, and anxiety level, were not considered in the study, which represents a limitation.35 One of the four mammographic views could be more painful for the screened women in the study. We were unable to determine this, because we used averaged measures of compression force and pressure as the questionnaire specified the experience of pain during the entire mammographic examination. The information given before the examination takes place, the general atmosphere at the screening unit, the communication, behavioural and technical skills might have affected the women's experience of pain during mammography. These factors were not investigated in our quantitative study, but may be well fitted for investigation in a qualitative study design. It should also be mentioned that the positioning of the breast could play an important role in the distribution of compression and pain experience.36,37 In this study, we assumed that the radiographers complied with the current national recommendations on breast positioning during screening mammography.21 Conclusions Mean pain score during mammographic screening was reported to be 2.2 on a 0e10 numeric rating scale, and 6% of the screened women reported severe pain during mammography. Low versus medium compression pressure was associated with a higher risk of severe pain. Increasing compression force was associated with a lower risk of severe versus mild/moderate pain. The results support a range for compression force of 100e140 N and a range of compression pressure of 10.3e13.5 kPa, but further knowledge about other factors affecting experienced pain is needed to personalize the examinations and by that reduce the risk of experiencing severe pain. Conflict of interests Nataliia Moshina declares that she has no conflict of interest. Silje Sagstad declares that she has no conflict of interest. Sofie Sebuødegård declares that she has no conflict of interest. Gunvor G. Waade declares that she has no conflict of interest. Evy Gran declares that she has no conflict of interest. Jasmina Music declares that she has no conflict of interest. Solveig Hofvind has permanent employment as a researcher at the Cancer Registry of Norway, independent of her job as administrative leader of BreastScreen Norway. Acknowledgement The study was funded by Raagholtstiftelsen (no number has been assigned). We would like to thank the radiographers
conducting screening mammography for this study and the women who agreed to participate in the study. We thank Morten Olsen and Wenche Melby at the Cancer Registry of Norway for administrative support.
References 1. Yaffe MJ. Basic physics of digital mammography. In: Bick U, Diekmann F, editors. Digital mammography. Berlin, Heidelberg: Springer Berlin Heidelberg; 2010. p. 1e11. 2. Perry NBM, de Wolf C, Tornberg S, Holland R, von Karsa L. European guidelines for quality assurance in breast cancer screening and diagnosis. 4 ed. Luxemburg: European Communities; 2006. 3. Poulos A, Rickard M. Compression in mammography and the perception of discomfort. Australas Radiol 1997;41(3):247e52. 4. Miller D, Martin I, Herbison P. Interventions for relieving the pain and discomfort of screening mammography. Cochrane Database Syst Rev 2002;4: Cd002942. 5. Myklebust AM, Seierstad T, Stranden E, Lerdal A. Level of satisfaction during mammography screening in relation to discomfort, service provided, level of pain and breast compression. Eur J Radiogr 2009;1(2):66e72. 6. Whelehan P, Evans A, Wells M, Macgillivray S. The effect of mammography pain on repeat participation in breast cancer screening: a systematic review. Breast 2013;22(4):389e94. 7. Keemers-Gels ME, Groenendijk RP, van den Heuvel JH, Boetes C, Peer PG, Wobbes TH. Pain experienced by women attending breast cancer screening. Breast Canc Res Treat 2000;60(3):235e40. 8. Poulos A, McLean D, Rickard M, Heard R. Breast compression in mammography: how much is enough? Australas Radiol 2003;47(2):121e6. 9. Dibble SL, Israel J, Nussey B, Sayre JW, Brenner RJ, Sickles EA. Mammography with breast cushions. Women's Health Issues 2005;15(2):55e63. 10. Nightingale JM, Murphy FJ, Robinson L, Newton-Hughes A, Hogg P. Breast compression e an exploration of problem solving and decision-making in mammography. Radiography 2015;21(4):364e9. 11. Waade GG, Moshina N, Saebuodegard S, Hogg P, Hofvind S. Compression forces used in the Norwegian breast cancer screening program. Br J Radiol 2017: 20160770. 12. Mercer CE, Hogg P, Lawson R, Diffey J, Denton ER. Practitioner compression force variability in mammography: a preliminary study. Br J Radiol 2013;86(1022):20110596. 13. Mercer CE, Hogg P, Szczepura K, Denton ERE. Practitioner compression force variation in mammography: a 6-year study. Radiography 2013;19(3):200e6. 14. Mercer CE, Hogg P, Cassidy S, Denton ERE. Does an increase in compression force really improve visual image quality in mammography? e an initial investigation. Radiography 2013;19(4):363e5. 15. de Groot JE, Broeders MJ, Branderhorst W, den Heeten GJ, Grimbergen CA. A novel approach to mammographic breast compression: improved standardization and reduced discomfort by controlling pressure instead of force. Med Phys 2013;40(8):081901. 16. Branderhorst W, de Groot JE, Highnam R, Chan A, Bohm-Velez M, Broeders MJ, et al. Mammographic compression-a need for mechanical standardization. Eur J Radiol 2015;84(4):596e602. 17. de Groot JE, Branderhorst W, Grimbergen CA, den Heeten GJ, Broeders MJ. Towards personalized compression in mammography: a comparison study between pressure- and force-standardization. Eur J Radiol 2015;84(3):384e91. 18. VolparaSolutions. VolparaResearch. Available from: http://volparasolutions.com/ solutions/volpararesearch/; 2017. 19. Forskrift om innsamling og behandling av helseopplysninger i Kreftregisteret (Kreftregisterforskriften). 2001. 20. Hofvind S. Cancer in Norway 2016. In: Special issue: the Norwegian breast cancer screening program, 1996-2016: celebrating 20 years of organised mammographic screening. Oslo: Cancer Registry of Norway; 2017. 21. cancer Registry of Norway Quality assurance manual. Norwegian breast cancer screening program. Directions for radiographers. 2011. Available from: https:// www.kreftregisteret.no/globalassets/mammografiprogrammet/arkiv/ publikasjoner-og-brosjyrer/kval-man-radiograf_v1.0_innholdsfortegnelse.pdf. 22. Williamson A, Hoggart B. Pain: a review of three commonly used pain rating scales. J Clin Nurs 2005;14(7):798e804. 23. Branderhorst W, de Groot JE, Neeter LM, van Lier MG, Neeleman C, den Heeten GJ, et al. Force balancing in mammographic compression. Med Phys 2016;43(1):518. 24. Broeders MJM, ten Voorde M, Veldkamp WJH, van Engen RE, van LandsveldeVerhoeven C, t JongeGunneman MNL, et al. Comparison of a flexible versus a rigid breast compression paddle: pain experience, projected breast area, radiation dose and technical image quality. Eur Radiol 2015;25(3): 821e9. 25. Zhang J, Yu KF. What's the relative risk? A method of correcting the odds ratio in cohort studies of common outcomes. Jama 1998;280(19):1690e1. 26. Moshina N, Roman M, Waade GG, Sebuodegard S, Ursin G, Hofvind S. Breast compression parameters and mammographic density in the Norwegian breast cancer screening programme. Eur Radiol 2018;28(4):1662e72.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
N. Moshina et al. / Radiography xxx (xxxx) xxx 27. Feder K, Grunert JH. Is Individualizing Breast Compression during Mammography useful? - Investigations of pain indications during mammography €fo relating to compression force and surface area of the compressed breast. Ro 2017;189(1):39e48. 28. Moshina N, Sebuødegård S, Evensen KT, Hantho C, Iden KA, Hofvind S. Breast compression and experienced pain during mammography by use of three different compression paddles. Eur J Radiol 2019;115:59e65. 29. Boyd NF, Li Q, Melnichouk O, Huszti E, Martin LJ, Gunasekara A, et al. Evidence that breast tissue stiffness is associated with risk of breast cancer. PLoS One 2014;9(7):e100937. 30. Carp SA, Selb J, Fang Q, Moore R, Kopans DB, Rafferty E, et al. Dynamic functional and mechanical response of breast tissue to compression. Opt Express 2008;16(20):16064e78. 31. Saunders Jr RS, Samei E. The effect of breast compression on mass conspicuity in digital mammography. Med Phys 2008;35(10):4464e73. 32. Moshina N, Sebuodegard S, Hofvind S. Is breast compression associated with breast cancer detection and other early performance measures in a population-
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based breast cancer screening program? Breast Canc Res Treat 2017;163(3): 605e13. Moshina N, Sebuodegard S, Holen AS, Waade GG, Tsuruda K, Hofvind S. The impact of compression force and pressure at prevalent screening on subsequent re-attendance in a national screening program. Prev Med 2018;108: 129e36. Hogg P, Taylor M, Szczepura K, Mercer C, Denton E. Pressure and breast thickness in mammographydan exploratory calibration study. Br J Radiol 2013;86(1021):20120222. Davey B. Pain during mammography: possible risk factors and ways to alleviate pain. Radiography 2007;13(3):229e34. Dustler M. Pressure distribution in mammography. Mechanical imaging and implications for breast compression. Lund University; 2016. Lund University, Faculty of Medicine. Dustler M, Andersson I, Brorson H, Frojd P, Mattsson S, Tingberg A, et al. Breast compression in mammography: pressure distribution patterns. Acta Radiol 2012;53(9):973e80.
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Radiography journal homepage: www.elsevier.com/locate/radi
Breast compression and reported pain during mammographic screening N. Moshina a, *, S. Sagstad a, S. Sebuødegård a, G.G. Waade b, E. Gran c, J. Music c, S. Hofvind a, b a b c
Cancer Registry of Norway, P.O. 5313 Majorstuen, 0304, Oslo, Norway Oslo Metropolitan University, P.O. 4, St. Olavs Plass, 0130, Oslo, Norway Akershus University Hospital, Sykehusveien 25, 1478, Lørenskog, Norway
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 July 2019 Received in revised form 1 October 2019 Accepted 5 October 2019 Available online xxx
Introduction: We aimed to investigate the association between breast compression and experienced pain during mammographic screening. Methods: Using a questionnaire, we collected information on pain experienced during mammography from 1155 women screened in Akershus, FebruaryeMarch 2018, as a part of BreastScreen Norway. The questionnaire provided information on pain using a numeric rating scale (NRS, 0e10) and related factors. Data on compression force (Newton, N), pressure (kilopascal, kPa) and breast characteristics were extracted from the DICOM-header and a breast density software. Log-binomial regression was used to determine the relative risk (RR) of severe versus mild/moderate experienced pain associated with compression parameters, adjusting for breast characteristics and related factors. Results: Mean score of experienced pain was 2.2, whereas 6% of the women reported severe pain (7) during the examination. High body mass index (BMI) (27.3 kg/m2) was associated with a higher RR of pain scores 7 (RR 1.86, 95%CI 1.02e3.36) compared to medium BMI (23.7e27.2 kg/m2). Low compression pressure (4.0e10.2 kPa) was associated with a higher RR of severe pain (RR 2.93, 95%CI 1.39 e6.20), compared with medium compression pressure (10.3e13.5 kPa) after adjusting for contact area, age, compressed breast thickness, volumetric breast density and BMI. The risk of severe versus mild/ moderate pain (7 versus <7) decreased by 2% with increasing compression force (RR 0.98, 95%CI 0.97 e1.00). Conclusion: Women reported low levels of pain during mammography. Further knowledge about factors affecting experienced pain is needed to personalize the examination to the individual woman. Implications for practice: Pain in shoulder(s) and/or neck prior to screening should be considered by the radiographers in a practical screening setting. A compression force of 100e140 N and pressure of 10.3 e13.5 kPa are acceptable with respect to reported pain during mammography. © 2019 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Keywords: Compression force Compression pressure Mammography Pain Breast cancer screening
Introduction Breast compression immobilizes the breast between a compression paddle and the image receptor of the mammography machine,1 and is aimed to optimize image quality and reduce radiation dose. Vendors of mammographic equipment and countries
* Corresponding author. E-mail addresses: [email protected] (N. Moshina), Silje. [email protected] (S. Sagstad), Sofi[email protected] (S. Sebuødegård), [email protected] (G.G. Waade), Evy.Gran@ahus. no (E. Gran), [email protected] (J. Music), Solveig.Hofvind@kreftregisteret. no (S. Hofvind).
offering mammographic screening recommend optimal ranges of breast compression.2 However, there is limited or no evidence to support these ranges according to image quality and the women's experience of pain. Women might experience pain associated with breast compression during and/or after mammography.3e5 This experience may prevent women from undergoing mammography or attending screening.3e7 A review concluded that 25e46% of the women indicated pain associated with breast compression as the reason for not attending the next screening.6 In previous studies, breast compression during mammography has mainly been discussed as a subjective measure or using compression force (Newton, N).1,3e5,8,9 However, experience of pain
https://doi.org/10.1016/j.radi.2019.10.003 1078-8174/© 2019 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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N. Moshina et al. / Radiography xxx (xxxx) xxx
during mammography is also influenced by the communication between the radiographer and the woman, the equipment and the situation.7,10 As far as we are aware, there is limited knowledge about these combinations, which hampers any recommendations for optimal compression.10 Data on compression force are available to the radiographers when they compress the breast. The data are stored in the DICOMheader of the image and could be extracted for research. Recent studies have reported substantial variation in applied compression force between breast centres and between radiographers.11e14 Compression pressure (kilopascal, kPa) is considered a more sensitive measure than compression force in relation to experienced pain as it takes into account the size of the breast.15e17 Pressure is typically estimated retrospectively by different types of software and not visible during the screening examination.17 However, recent developments in fixed paddle technology provides data on compression pressure during the examination.18 Studies have shown promising results on the use of pressure standardized mammography, but substantial knowledge gaps associated with the practical implementation in screening and/or clinical setting still need to be filled in order to recommend the use pressure instead of force based compression.16,17 In this study, we wanted to investigate possible relations between compression force and pressure and reported pain among women who attended mammographic screening in Akershus as a part of BreastScreen Norway. Materials and methods This study was permitted under the Cancer Registry Regulations and approved by the Data Protection Official at Oslo University Hospital (2017/6481).19 BreastScreen Norway The Cancer Registry of Norway administers the populationbased breast cancer screening program, BreastScreen Norway, that serves about 650,000 women aged 50e69 years. The women are offered biennial mammographic screening that typically includes four digital mammograms (DM) with craniocaudal (CC) and mediolateral oblique (MLO) views of each breast. The annual participation rate is about 75%. The program has been described in detail elsewhere.20 Study sample Among 2934 women, who attended one of the two screening units in the Akershus county during the study period, FebruaryeMarch 2018, 1373 (46.8%) agreed to participate in this study (Fig. 1). We excluded women who did not report their experience of pain (n ¼ 40), information about pain in shoulder(s) and/or neck prior to screening (n ¼ 56) or did not give any information about weight and height (n ¼ 92). We also excluded women without information about breast volume (n ¼ 30). The final study population consisted of 1155 women. All women were screened using Philips MicroDose SI (Amsterdam, the Netherlands) and a fixed compression paddle available in two sizes, 24 31 cm and 19 23 cm. The radiographers performing screening mammography had from one week to 20 years of working experience and worked in mixed pairs: the first radiographer examined the left breast (CC and MLO) and the second radiographer examined the right breast (CC and MLO). The compression and positioning of the breast were performed according to the national guidelines.21 During the study period, all attending women were invited to participate in this study at the standard prescreening interview
Figure 1. Study population.
conducted by the radiographers. The women who agreed to participate received a questionnaire, which included a study identifier (running number) and questions about experienced pain related to their mammographic examination. The questionnaire was completed immediately after the examination and submitted in a closed letter case at the screening unit. Responding to the questionnaire was considered an informed consent to use the data in this study. The questionnaire A continuous numeric rating scale (NRS) was used for measuring experienced pain. The women marked their response on a line, ranging from 0 to 10, indicated by 11 marks. A score of 0 indicated no pain while 10 indicated very strong pain. The choice of NRS was associated with the use of NRS in previous studies measuring the experience of pain during mammography.15,17,23,24 The women further reported information about presence of pain in shoulder(s) and/or neck prior to screening as well as weight (kg) and height (m), which were used to calculate body mass index (BMI, kg/m2) as weight divided by squared height. Variables of interest Response to the questionnaire was manually coded at the Cancer Registry. Using the running number, the responses were linked to data about characteristics of the women and compression parameters. Information on compression force and compressed breast thickness (mm) was obtained from the DICOM header while data about compression pressure and breast characteristics, including contact area (mm2), breast volume (cm3) and volumetric breast density (%) were extracted using a software for density assessment.18 Information about the women's age and screening history (prevalently screened or (i.e. screened for the first time), and subsequently screened (i.e. screened previously) was obtained from the Cancer Registry of Norway. In the questionnaire, the women evaluated the screening examination consisted of on average four images in relation to their experience of pain. Therefore, we present
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
N. Moshina et al. / Radiography xxx (xxxx) xxx
average values for each screening examination (four images), which was considered the unit of analysis in this study. Statistical analyses Descriptive statistics included means with 95% confidence intervals (95%CI) or standard deviation (SD) to describe the women's characteristics and study parameters of interest. First, we stratified experienced pain into four groups, according to the NRS; no pain (0e2), mild,3e5 strong6e8 and intense pain.9,10 Further, we used a cut point of 7 (<7 versus 7) to categorize the experience: a score of <7 corresponded to mild or moderate pain, while a score of 7 included severe pain.15,17,22 This cut point was chosen to identify women who reported severe pain, as the values 7 was considered a strong negative experience of mammography, perceived as a procedure causing significant and/or unbearable pain. We used t-tests to compare mean values and chi-square tests to compare distributions within the groups. Means of pain were also calculated for the variables of interest categorized in tertiles: compression force [low (46e109 N), medium (110e122 N) and high (123e179 N)], compression pressure [low (4.0e10.2 kPa), medium (10.3e13.5 kPa) and high (13.6e35.2 kPa)], breast volume [tertiles: low (116e701 cm3), medium (702e1091 cm3) and high (1092e3230 cm3)], contact area [tertiles: low (3438e8800 mm2), medium (8814e12051 mm2) and high (12,054e26541 mm2)], compressed breast thickness [tertiles: low (19e55 mm), medium (56e67 mm) and high (68e96 mm)], volumetric breast density [tertiles: low (2.4e4.9%), medium (5.0e7.9%) and high (7.8e30.1%)], age (50e54; 55e60; 61e71 years). BMI was grouped into tertiles as low (<23.7 kg/m2), medium (23.7e27.2 kg/m2) and high (27.2 kg/m2). We used binomial regression with log link to determine the relative risk (RR) of severe pain (7) associated with the variables of interest categorized in tertiles. Further, we performed adjusted analyses for compression force and compression pressure, adjusting for contact area, breast volume, age, compressed breast thickness, volumetric breast density and BMI. In
3
addition, log-binomial regression models were used to estimate the RR of severe pain (7) associated with compression force or pressure (continuous), adjusted for shoulder(s) and/or neck pain prior to screening (present versus absent), breast volume (continuous), compressed breast thickness (continuous), volumetric breast density (continuous) and BMI (continuous).25 Breast volume was not included in the models with compression pressure due to colinearity of the variables.26 Two-way fractional-polynomial prediction plots with 95%CI for reported pain by applied compression force and pressure were shown. All analyses were conducted using STATA® 15.0 (StataCorp, Texas, USA). Results Mean age of the study population was 57.8 years (SD: 5.7) (Table 1). A total of 19% of the women were prevalently screened. Means of compression force and pressure were 117 N (SD: 18.0) and 12 kPa (SD: 3.9), respectively. Means of compressed breast thickness were statistically significantly lower for women who reported no pain compared to those who reported mild or strong pain (p ¼ 0.003 and p ¼ 0.01, respectively). Percentage of women with pain in shoulder(s) and/or neck prior to screening was significantly higher for women who reported strong or intense pain compared with those who reported no or mild pain. Mean pain score for the women comprising the study population was 2.2 (Table 2). High BMI (27.3 kg/m2) was associated with a higher RR of severe pain (RR 1.86; 95%CI 1.02e3.36), compared with medium BMI (23.7e27.2 kg/m2) (p ¼ 0.04) (Table 2). Low compression pressure (4.0e10.2 kPa) was associated with a higher RR of severe pain (RR 2.93; 95%CI 1.39e6.20), compared with medium compression pressure (10.3e13.5 kPa) when adjusting for contact area, age, compressed breast thickness, volumetric breast density and BMI. Increasing compression force was associated with a 2% lower RR of severe pain (RR 0.98, 95%CI 0.97e1.00) in the adjusted model, including age, breast volume, compressed breast thickness, breast
Table 1 Descriptive information for the variables of interest by four groups of experienced pain on the numeric rating scale (NRS) among 1155 women screened in Akershus as a part of BreastScreen Norway FebruaryeMarch 2018. Group 1
Group 2
Group 3
All
No pain (NRS 0e2) Mild pain (NRS 3e5)
Strong pain (NRS 6e8)
Intense pain (NRS 9e10)
n ¼ 1155
n ¼ 753
n ¼ 158
n ¼ 35
n ¼ 209 p-valuea
Age Mean (SD), years BMI Mean (SD), kg/cm2 Compression force Mean (SD), N Compression pressure Mean (SD), kPa Contact area Mean (SD), mm2 Breast volume Mean (SD), mm3 Compressed breast thickness Mean (SD), mm Volumetric breast density Mean (SD), %
a
c
p-valuea
p-valuea
57.8 (5.7)
57.6 (5.7)
58.1 (5.8)
0.340
58.1 (5.6)
0.415
57.0 (6.0)
0.516
26.2 (5.0)
26.0 (5.0)
26.7 (5.0)
0.083
26.3 (4.7)
0.495
26.9 (5.1)
0.309
117 (18.0)
117 (17.3)
117 (18.5)
0.671
116 (20.1)
0.877
111 (19.3)
0.074
12 (3.9)
12 (3.9)
12 (3.9)
0.703
13 (3.8)
0.425
12 (4.9)
0.998
10,963 (3856) 11,020 (3809)
10,987 (3920) 0.914
10,658 (3907) 0.279
10,964 (4345)
0.933
957 (476)
940 (484)
998 (457)
0.126
982 (470)
0.322
962 (462)
0.794
60 (13)
59 (13)
62 (12)
0.003
62 (12)
0.011
61 (12)
0.503
7.5 (4.3)
7.6 (4.2)
7.2 (4.2)
0.165
7.3 (4.6)
0.418
7.1 (4.1)
0.466
21% 25%
17% 27
Prevalently screenedc 19% Pain in shoulder/neck prior to screening 27% b
p-valueb
Group 4
15% 35%
17% 34%
0.268 0.037
Different from Group 1. Chi-square test. Screened for the first time in the program.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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density and BMI (Table 3). No association between compression pressure and severe pain was observed when compression pressure was presented as a continuous variable (Table 4). The lowest predicted reported pain scores (2.1e2.2 on NRS) were observed for the compression force between 100 N and 140 N (Fig. 2). The highest predicted pain scores (4.0e7.0 on NRS) were shown for the compression force of 60 N. The lowest predicted reported pain scores (2.1e2.2 on NRS) were observed for the compression pressure between 8 kPa and 13 kPa (Fig. 3). The highest predicted reported pain scores (3.0e3.8 on NRS) were shown for the compression pressure of 7 kPa. Discussion The whole scale of reported pain scores from 0 to 10 on a NRS were used, with a mean of 2.2 for 1155 women who underwent mammographic screening in Akershus, as a part of BreastScreen Norway. Only six percent of the women reported severe pain. Low versus medium compression pressure was associated with a higher relative risk of severe pain, however there was no association between increasing compression pressure and risk of severe pain. Increasing compression force was associated with a lower relative risk of severe versus mild/moderate pain. Our findings are in line with results from other studies,3,27,28 but contradict the findings from de Groot et al. and Branderhorst et al., indicating that standardization of compression pressure could lead
to reduction of pain during mammography.15,16 It should be noted that our results are not directly comparable with the studies by de Groot et al. and Branderhorst et al. and we assume that our findings are associated with women's expectations and reaction to breast compression, while the results of the aforementioned studies are related to the use of different protocols of compression force and pressure standardisation. Women who experience or anticipate severe pain usually ask the radiographer to stop compressing, and receive generally lower compression force and pressure than those who tolerate higher forces and pressures. Our interpretation of the findings on compression pressure and force are supported by the correlations between these parameters and experienced pain depicted by the polynomial prediction plots, indicating higher pain scores for lower pressures and forces. Compressed breast thickness was higher for women who reported mild to strong pain (NRS 3e8) compared to those who reported no pain (NRS 0e2). Compressed breast thickness might depend on the volume of the breast, compression force and compressibility of the breast. As fatty tissue is easier to compress than the fibroglandular tissue, it is assumed that fatty breasts have lower compressed breast thickness and larger contact breast area.16,26 This suggests that women with less compressible breasts experience more pain compared to women with easy compressible breasts. However, our study did not show any association between breast density and experienced pain. On the other hand, the compressibility of the breast might be related to different factors
Table 2 Mean pain scores and relative risk (RR) of severe pain (7) associated with compression force and pressure, contact area, breast volume, compressed breast thickness, volumetric breast density, shoulder(s)/neck pain prior screening, body mass index, and age groups, among 1155 women screened in Akershus as a part of BreastScreen Norway, FebruaryeMarch 2018. Mean pain score Total 2.2 Compression force (N) 1. Low (46e109 N) 2.3 2. Medium (110e122 N) 2.1 3. High (123e179 N) 2.3 Compression pressure (kPa) 1. Low (4.0e10.2 kPa) 2.1 2. Medium (10.3e13.5 kPa) 2.1 3. High (13.6e35.2 kPa) 2.4 2 Contact area (mm ) 1. Low (3438e8800 mm2) 2.4 2. Medium (8814e12051 mm2) 2.2 3. High (12,054e26541 mm2) 2.1 Breast volume (cm3) 1. Low (116e702 cm3) 2.1 2. Medium (703e1091 cm3) 2.2 3 3. High (1092e3230 cm ) 2.4 Compressed breast thickness (mm) 1. Low (18e55 mm) 2.1 2. Medium (56e67 mm) 2.1 3. High (68e96 mm) 2.5 Volumetric breast density (%) 1. Low (2.4e4.9%) 2.4 2. Medium (5.0e7.9%) 2.1 3. High (7.8e30.1%) 2.1 Pain shoulder(s)/neck prior screening 1. Yes 2.5 2. No 2.1 Body Mass Index (kg/m2) 1. Low (<23.7 kg/m2) 2.1 2. Medium (23.7e27.2 kg/m2) 2.1 2 3. High (27.3 kg/m ) 2.4 Age (years) 1. <55 2.3 2.55-60 2.1 3. >60 2.3 a b
Crude RR
95% Confidence interval
P-value
Adjusted RRa,b
95% Confidence interval
P-value
1.62 1.00 1.13
(0.91e2.87)
0.10
(0.83e2.68)
0.19
(0.61e2.11)
0.70
1.49 1.00 1.14
(0.60e2.18)
0.68
1.55 1.00 1.67
(0.84e2.85)
0.16
(1.39e6.20)
0.01
(0.91e3.06)
0.10
2.93 1.00 1.06
(0.50e2.24)
0.87
1.42 1.00 0.83
(0.82e2.44)
0.21
(0.45e1.55)
0.57
0.98 1.00 0.86
(0.56e1.71)
0.95
(0.48e1.53)
0.60
1.30 1.00 1.34
(0.72e2.33)
0.39
(0.75e2.41)
0.33
(0.98e2.67)
0.17
(0.65e2.20)
0.58
1.42 1.00
(0.87e2.31)
0.16
1.40 1.00 1.86
(0.74e2.62)
0.30
(1.02e3.36)
0.04
(0.98e3.22)
0.06
(0.60e2.26)
0.64
1.50 1.00 1.19
1.78 1.00 1.17
Adjusted for contact area, breast volume, age, compressed breast thickness, volumetric breast density and body mass index for compression force. Adjusted for contact area, age, compressed breast thickness, volumetric breast density and body mass index for compression pressure.
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
N. Moshina et al. / Radiography xxx (xxxx) xxx
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Table 3 Log-binomial regression for the association between severe pain (7) using <7 as reference, and continuous variables: compression force, age, breast volume, compressed breast thickness, volumetric breast density, and body mass index (BMI) among 1155 women screened in Akershus as a part of BreastScreen Norway, FebruaryeMarch 2018.
Compression force (N) Age (years) Breast volume (cm3) Compressed breast thickness (mm) Volumetric breast density (%) BMI (kg/m2) a
Pain <7.0 vs pain 7.0
Pain <7.0 vs pain 7.0
Relative risk
Relative risk
Crude
95% Confidence interval
p-value
Adjusteda
95% Confidence interval
p-value
0.98 1.00 1.00 1.01 1.02 1.03
(0.97e1.00) (0.95e1.04) (0.95e1.00) (1.00e1.04) (0.98e1.09) (0.96e1.09)
0.03 0.87 0.93 0.63 0.49 0.29
0.98
(0.97e1.00)
0.01
Adjusted for age, breast volume, compressed breast thickness, breast density and body mass index.
Table 4 Log-binomial regression for severe pain as an outcome (7) using <7 as reference with continuous variables: compression pressure, age, breast volume, compressed breast thickness, volumetric breast density and body mass index among 1155 women screened in BreastScreen Norway, FebruaryeMarch 2018.
Compression pressure (kPa) Age (years) Compressed breast thickness (mm) Volumetric breast density (%) BMI (kg/m2) a
Pain <7.0 vs pain 7.0
Pain <7.0 vs pain 7.0
Relative risk
Relative risk
Crude
95% Confidence interval
p-value
Adjusteda
95% Confidence interval
p-value
1.01 1.00 1.01 1.03 1.03
(0.95e1.07) (0.95e1.04) (1.00e1.05) (0.98e1.10) (0.96e1.09)
0.71 0.85 0.51 0.37 0.33
1.01
(0.92e1.10)
0.83
Adjusted for age, compressed breast thickness, volumetric breast density and body mass index.
Figure 2. Two-way fractional-polynomial prediction plot with 95% confidence interval for compression force (N) by reported pain on the numeric rating scale for 1155 women screened in BreastScreen Norway, FebruaryeMarch 2018.
Figure 3. Two-way fractional-polynomial prediction plot with 95% confidence interval for compression pressure (kPa) by reported pain on the numeric rating scale for 1155 women screened in BreastScreen Norway FebruaryeMarch 2018.
not indicated in a volumetric measure of mammographic density, such as tissue composition and breast tenderness.29e31 The women with high BMI reported higher levels of pain scores compared to women with medium BMI in our study. This might indicate that women with high BMI are among those with low compressibility of the breasts, which might be more sensitive to pain. We observed a higher percentage of women with pain in shoulder(s) and/or neck prior to screening among those who reported strong to intense pain (NRS 6e10). A similar finding has been observed in another study from Norway comparing compression paddles for screening mammography, and might suggest that pain in shoulder(s) and/or neck prior screening is an important confounder in the relationships between compression force, compression pressure and experienced pain, which should be considered by the radiographers in a practical screening setting.
Our results are in line with the findings reported by Myklebust et al. regarding experience of pain and discomfort during mammography among women undergoing breast cancer screening in Norway.5 High compression forces might thus be justifiable for acquiring mammograms of good quality. However, an important skill of the radiographers is to individualize the compression. Our study indicated a compression force between 100 N and 140 N and a compression pressure between 10.3 kPa and 13.5 kPa to be acceptable with respect to reported pain during the examination, without taking the image quality into consideration. Further studies on image quality associated with various compression will add valuable knowledge on this topic. The preferred value of compression force and pressure were 130 N and <10 kPa according to results of early outcome measures in a previous study from Norway.32 Another study performed on
Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003
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N. Moshina et al. / Radiography xxx (xxxx) xxx
Norwegian data supported the range of 100e130 N for force and 9.0e17.9 kPa for pressure with regard to subsequent attendance among prevalently screened women.33 A study from the UK also concluded that the force of 90e130 N should be could be an appropriate compression termination point.34 Our results indicate that further knowledge is needed before evidence based recommendations of compression during mammography can be given. The results also indicate that recommendations of ranges should serve the individualization of the compression force and pressure and thus make the screening examination a better experience for the women. This study included data from 1155 women screened in the organized breast cancer screening program in Norway. Several factors as breast tenderness, menstrual status, breast pain prior to screening, education level, presence or absence of benign or malignant lesions, and anxiety level, were not considered in the study, which represents a limitation.35 One of the four mammographic views could be more painful for the screened women in the study. We were unable to determine this, because we used averaged measures of compression force and pressure as the questionnaire specified the experience of pain during the entire mammographic examination. The information given before the examination takes place, the general atmosphere at the screening unit, the communication, behavioural and technical skills might have affected the women's experience of pain during mammography. These factors were not investigated in our quantitative study, but may be well fitted for investigation in a qualitative study design. It should also be mentioned that the positioning of the breast could play an important role in the distribution of compression and pain experience.36,37 In this study, we assumed that the radiographers complied with the current national recommendations on breast positioning during screening mammography.21 Conclusions Mean pain score during mammographic screening was reported to be 2.2 on a 0e10 numeric rating scale, and 6% of the screened women reported severe pain during mammography. Low versus medium compression pressure was associated with a higher risk of severe pain. Increasing compression force was associated with a lower risk of severe versus mild/moderate pain. The results support a range for compression force of 100e140 N and a range of compression pressure of 10.3e13.5 kPa, but further knowledge about other factors affecting experienced pain is needed to personalize the examinations and by that reduce the risk of experiencing severe pain. Conflict of interests Nataliia Moshina declares that she has no conflict of interest. Silje Sagstad declares that she has no conflict of interest. Sofie Sebuødegård declares that she has no conflict of interest. Gunvor G. Waade declares that she has no conflict of interest. Evy Gran declares that she has no conflict of interest. Jasmina Music declares that she has no conflict of interest. Solveig Hofvind has permanent employment as a researcher at the Cancer Registry of Norway, independent of her job as administrative leader of BreastScreen Norway. Acknowledgement The study was funded by Raagholtstiftelsen (no number has been assigned). We would like to thank the radiographers
conducting screening mammography for this study and the women who agreed to participate in the study. We thank Morten Olsen and Wenche Melby at the Cancer Registry of Norway for administrative support.
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Please cite this article as: Moshina N et al., Breast compression and reported pain during mammographic screening, Radiography, https:// doi.org/10.1016/j.radi.2019.10.003