Copyright B 2015 Wolters Kluwer Health, Inc. All rights reserved.
Charles P. Osingada, MPH Gloria Ninsiima, MSN Rose N. Chalo, PhD Joshua K. Muliira, DNP, MA, RN Tom Ngabirano, MSN
Determinants of Uptake of Cervical Cancer Screening Services at a No-Cost Reproductive Health Clinic Managed by Nurse-Midwives K E Y
W O R D S
Background: The incidence of cervical cancer (CC) has been rising in
Cervical cancer
sub-Saharan Africa, and health authorities in this region have responded by
Determinants
increasing the availability of cheap or no-cost CC screening services (CCSS), public
Early detection of cancer
health education, and others. However, the efforts have not yet resulted into the
Nurse-midwives
expected uptake of CCSS. Objective: The aim of this study was to examine the
Preventive care
determinants of uptake of CCSS at a no-cost reproductive health clinic managed by
Screening
nurse-midwives. Methods: A descriptive design and a structured interview
Uganda
questionnaire were used to collect data from 236 women attending the reproductive
Uptake
health clinic. Logistic regression statistics were used to examine the determinants of uptake of CCSS. Results: The mean age of participants was 28.7 years, and only 29% had received CC screening. The significant determinants of uptake of CCSS were concern about the gender of the healthcare professional (HCP) (odds ratio [OR], 5.03; P = .001), age older than 25 years (OR, 3.09; P = .005), contraceptive use (OR, 0.28; P = .02), encouragement by HCPs (OR, 0.16; P = .00), and perceived quality of CCSS (OR, 0.08; P = .00). Conclusions: Gender of the HCP and encouragement or reminders by the HCP influence uptake of CCSS. Because nurse-midwives have successfully led strategies to promote other integrated reproductive health services, they can also play a key role in enhancing uptake of CCSS in resource-poor settings. Implications for Practice: Interventions to
Author Affiliations: School of Health Sciences, College of Health Sciences, Department of Nursing, Makerere University, Kampala, Uganda (Mr Osingada and Ngabirano, Ms Ninsiima, and Dr Chalo); and College of Nursing, Department of Adult Health & Critical Care, Sultan Qaboos University, Muscat, Oman (Dr Muliira). Authors’ contributions: C.P.O., G.N., R.N.C., and T.N. were responsible for the study conception, design, and data collection. C.P.O., G.N., and J.K.M. were responsible for data analysis and drafting of the first manuscript. All authors made critical revisions to the final paper for intellectual content.
Cervical Cancer Screening in Uganda
The authors have no funding or conflicts of interest to disclose. Correspondence: Joshua K. Muliira, DNP, MA, RN, College of Nursing, Department of Adult Health & Critical Care, Sultan Qaboos University, PO Box 66 Al Khod, PC 123, Muscat, Oman ([email protected]). Accepted for publication March 4, 2014. DOI: 10.1097/NCC.0000000000000156
Cancer NursingTM, Vol. 38, No. 3, 2015
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enhance service quality and deliberate policies requiring HCP to recommend encourage and remind clients may help to enhance uptake of CCSS in resource-poor settings.
A
pproximately 500 000 women are diagnosed with cervical cancer (CC), and 274 000 die of the disease annually.1,2 A large majority (80%) of the world’s CC patients live in developing countries, where this type of cancer accounts for 15% of all female cancers compared with 3.6% in the developed world.3 Unfortunately, the CC burden in developing countries is likely to worsen because these countries have access to less than 5% of the global cancer treatment resources.1,2,4 The other factors that continue to sustain the high burden of CC in developing countries include the high prevalence of risk factors, such as human immunodeficiency virus, human papillomavirus, and multiple sexual partners among men in heterosexual relationships; poor genital hygiene; and reusing of homemade feminine napkins.5 Recent reports show that, annually, in sub-Saharan Africa, CC causes approximately 50 000 deaths (age standardized rate 22.5).1 This number is likely to be considerably higher because in sub-Saharan Africa, many times, the data are unavailable or incomplete. In Uganda, the CC incidence and mortality rate are 40 in 100 000 and 25 in 100 000, respectively.6 In Kampala, Uganda’s capital city, the age-standardized incidence rate of CC for the period 2002 to 2006 was 52.4 per 100 000.7 Like in other sub-Saharan African countries, CC is the leading cause of female cancer morbidity and death in Uganda.6 The health authorities (Ministry of Health and nongovernmental agencies) have responded to the growing burden of CC by integrating CC screening services (CCSS) into the existing reproductive health services provided at no cost in government clinics or in private and nongovernmental health facilities where clients are required to pay a fee for services. Uganda’s health authorities have also trained healthcare professionals (HCPs) such as nurses and midwives in advanced skills to be able to provide CCSS, and this has increased access to screening. The government and nongovernmental organizations continue to publicize CC and CCSS through public health education, the media, and other public forums to ensure that the public understands that CC is preventable and that screening can reduce morbidity and mortality. As mentioned above, in Uganda, CCSS are offered mostly through the family planning or reproductive health clinics (RHCs), which normally provide contraceptive services, postnatal assessment, and young child clinics. The RHCs are usually well attended by women. The most commonly used methods for CC screening are visual inspection with acetic acid (VIA), visual inspection with Lugol iodine (VILI), and VIA with cryotherapy.8 Other developing countries have also adopted VIA and VILI with cryotherapy because these are cheaper, can be easily provided by commonly available and accessible HCPs such as nurses, and are more feasible in resourcepoor settings.9,10 Cervical cancer screening programs based on cytology, which assisted developed countries to reduce the in-
cidence of CC, have not had a similar effect in developing countries because they are expensive and require highly trained and skilled HCPs.3,11 The recently unveiled cheap or no-cost CCSS have not yet resulted in the expected level of impact on CC. Various studies conducted in Uganda and other sub-Saharan countries like Nigeria still show low uptake of CCSS.12,13 A recent study conducted in Uganda to examine the acceptability of CC screening using VIA or Lugol iodine showed that 40% of the women declined to receive the procedure.14 The reluctance of women to receive CC screening is partly responsible for the late diagnosis and subsequent mortality from an otherwise preventable and treatable type of cancer. Most Ugandan women (71%) with CC present to hospitals to seek care 6 months after the onset of symptoms and usually after they have started experiencing complications such as elevated serum creatinine, hydronephrosis, hydroureter, vesicovaginal fistula, and anuria.15 In sub-Saharan Africa, late diagnosis of CC and failure to receive CC screening were, in the past, attributed to inadequate services, lack of access to deliberate information about screening by patients, and lack of facilities for Papanicolaou test services.16 The other factors that have been noted to influence uptake of CCSS and related general reproductive health services include cultural beliefs about illness, economic factors, domestic gender power relations, alternative authoritative sources of reproductive health knowledge, and unfriendly HCPs.17 Lack of knowledge is still persistent because recent reports show that many women in Sub-Saharan Africa do not know the cause or manifestations of CC, and this leads to low risk perceptions and poor preventive practices.12,18 Receipt of CC screening in sub-Saharan Africa is also influenced by factors such as level of education, fear of invasion of personal privacy, fear of pain, and worry about test results.8 Therefore, the factors that are associated with receipt of CCSS by women in resource-poor settings seem to have cultural, social, and personal dimensions. A study conducted in Canada among 3 474 352 women, of which 38.6% were immigrants of African, South Asian, Chinese, and other nonYNorth American or European origins, demonstrated that after controlling for demographic factors, access to a physician, and socioeconomic factors, being an immigrant, African, Chinese, South Asian, or other Asian origins decreased the likelihood of Papanicolaou testing.19 On the other hand, studies with samples composed of predominantly women born in developed countries show that they have good CC screening practices.20
Aim The purpose of this study was to establish the determinants of uptake of CCSS offered at a no-cost clinic managed by female nurse-midwives at a referral hospital in Uganda.
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Osingada et al
Theoretical Framework 21,22
The study was guided by the Preventive Health Model (PHM). The PHM has been used widely to explain predictors of prostate and colorectal cancer screening behaviors.23 The PHM was used because it comprehensively considers and addresses the factors that influence patient’s cancer screening behaviors and actual action of getting the screening. The PHM is composed of constructs focusing on the patient background factors (eg, demographic characteristics), patient behaviors factors (eg, worry, self-efficacy, and social influence), healthcare provider factors (eg, clinic factors, access, HCPs’ knowledge, attitude and beliefs), system of support factors (community resources, guidelines, and self-management support), and the outcome (cancer screening, eg, intention, planning, action, and experience).21,22 The PHM posits that the patient’s action leading to receipt of cancer screening (such as receipt of CC screening) is directly influenced by background factors, behavioral factors, healthcare provider factors, and systems of support factors.21 The study explored the effect of background (demographic characteristics), healthcare provider (health service factors), and system (community resources) factors on uptake of CC screening. Some aspects of all the 3 categories of factors are currently being used in Uganda to enhance uptake of CC screening.
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Methods
Population and Setting The study used a cross-sectional design to recruit women attending an RHC at a referral hospital in Uganda. The RHC provides free contraceptive (family planning) services, CCSS, and postnatal checkups on a daily basis, except on weekends and public holidays, when it is not open. On average, the RHC serves a total of 370 women per month. The method used for CC screening at the RHC is VIA or VILI, and the screening procedures are performed by nurse-midwives who are trained in providing this service. The nurse-midwives who provide care and manage the RHC are qualified with associate degrees (diploma) or bachelor degrees majoring in both nursing and midwifery. Women who require a Papanicolaou test are referred to the adjacent University Department of Pathology. The other services provided by RHC include Young Child Care Services (child growth monitoring and immunization) and health education about infant feeding and nutrition. Therefore, the RHC provided a good integrated care environment to find women eligible for CCSS. The study targeted women who were attending the RHC. Participants had to meet the following inclusion criteria: 18 years or older, sexually active, able to speak English or Luganda (languages used during healthcare service provision at the RHC), has sought care at the RHC at least twice, willing to provide permission to access client health records to confirm receipt of CC screening, and willing to spend 40 minutes to complete the study questionnaire after signing the written informed consent form. A total of 350 women were approached, and data collection was stopped once the required sample of 236 participants was at-
Cervical Cancer Screening in Uganda
tained (consented to participate in the study and had complete legible medical records).
Study Instrument The semistructured interview questionnaire used to collect data was developed by the investigators after review of literature about determinants of uptake of CCSS and following the framework outlined by PHM. Because English and Luganda (which has no major variance such as dialects) are the languages used during healthcare service delivery at the RHC, the questionnaire had to be available in both languages. The research team (all multilingualV English, Luganda, and other Ugandan languages) translated the first version of the questionnaire from English to Luganda. The research team discussed the items in the initial Luganda questionnaire version with a professional translator and linguistic expert regarding the conceptual meanings of each item as well as formulation of the response statements. The initial Luganda questionnaire version was back-translated into English by the professional translator. After the back-translation process, some discrepancies between the forward and backward translation were observed, and these pertained to the Luganda equivalent of the words quality and program. The terms were clarified with explanatory statements. The questionnaire was then pretested among 20 women at a clinic in a rural setting, and results of the pretesting showed that the questionnaire required 40 minutes to complete and that the terms cervical cancer, cervical cancer screening, and quality of screening services were understandable. The items on the questionnaire were organized under the sections of demographic characteristics, health service factors, community factors, and receipt of CC screening. The demographic characteristics emphasized were age, marital status, level of education, parity, employment status, and use of contraceptives. The section about uptake of CCSS included questions such as ‘‘Are you currently sexually active?’’ ‘‘Have you been screened for CC since becoming sexually active?’’ ‘‘Where did you receive the screening procedure from?’’ and ‘‘Who performed the screening procedure?’’ The items about health services factor focused on the gender of the HCP, perceived quality of CCSS, waiting time at the health facility, and receiving encouragement from HCPs. The community factors included having close friends who received CC screening and access to CC community outreach services.
Procedure After ethical review and approval by the School of Medicine Institutional Review Board (protocol number 2012-046) at Makerere University and Mulago National Referral Hospital, the researchers visited the RHC to plan for data collection. Data were collected daily from Monday to Friday over a period of 30 days in May 2012. On data collection days, all women who came to the RHC were approached and informed about the study. Participants were recruited consecutively until the calculated sample size was attained. The sample size was estimated using the Kish Leslie (1965) formula. Using the most recent reported prevalence of CC screening of 19% among women,13 a 95% confidence interval, and an allowable margin of error of 5%, the required Cancer NursingTM, Vol. 38, No. 3, 2015
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sample size for the study was estimated to be 236 participants. Data collection was stopped once the required sample was attained. The women who met the inclusion criteria and were willing to learn more about the study were provided both verbal and written explanations of the purpose and procedures. After providing the explanations, the women who agreed to participate in the study were requested to sign an informed consent form. The explanations and informed consent form included statements showing that participation in the study required giving permission to review medical records to confirm receipt of CC screening. The participants who consented were taken to a private room to complete a structured interview questionnaire under the guidance of trained research assistant (nurse-midwife). The structured interview questionnaire required approximately 40 minutes to be completed, and all participants who reported receipt of CC screening at least once since becoming sexually active had their medical record checked for confirmation. Data of participants (n = 12) who reported receipt of CC screening but whose medical records were incomplete, unavailable, or illegible were not included in the final analysis. There was no other information that was obtained from the participant’s medical records. After verifying receipt of CC screening, the interview questionnaire was checked for completeness before the participant was directed to where they were going to receive care. The process of verifying receipt of CC screening took between 10 to 15 minutes.
Data Analysis Data were entered into the computer using Epi info version 3.5.1 and were analyzed using STATA version 10. Descriptive statistics were used to summarize the demographic characteristics and uptake of CC screening. A # 2 test was used to determine factors associated with uptake of CC screening. Bivariate and multivariate analyses were conducted to determine factors that influenced uptake of CCSS. All variables that were significant at bivariate level and thought to be theoretically (according to PHM) important in
influencing the outcome variable (receipt of CC screening at least once since becoming sexually active or did not receive CC screening since becoming sexually active) were included in a logistic regression model. In all statistical tests, a P value e .05 was considered to be significant.
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Results
A total of 350 participants were asked to participate in this study, and 236 (67.4%) women consented. The main reason for refusal related to not having time to complete the study questionnaire; others willing to participate were not eligible because of illegible or incomplete medical records (n = 12). The mean (SD) age of participants was 28.7 (6.7) years. Most participants were married (78%), had secondary school education (55%), were using hormonal contraceptives (78%), and had been pregnant at least 3 times (56%) (Table 1).
Uptake of CC Screening All the 236 participants recruited in the study were sexually active, but only 29% (n = 68) had received CC screening since becoming sexually active (Table 2). The procedure for CC screening was performed by a nurse-midwife working at the RHC (21%) or with the health facilities’ community outreach services (8%).
Factors Influencing Uptake of CC Screening Bivariate analysis was performed using the # 2 test to determine the participants’ background factors associated with uptake of CC screening. The participant factors that were associated with uptake of CC screening were age (P = .001) and use of contraceptives (P = .006). There was no significant relationship found between uptake of CC screening and factors such as marital status, level of education, number of pregnancies, or having a
Table 1 & Participants’ Demographic Characteristics (N = 236) Variable
Response Category
Age in years (mean [SD], 28.7 [6.7])
Marital status Highest level of education attained
Number of pregnancies (mean [SD], 3.0 [1.7])
Employment status Using contraceptives (hormonal based or intrauterine device)
18Y25 26Y35 36Y45 Q46 Currently married Not married No formal education Primary school Completed secondary school Completed tertiary 0 1Y2 3Y4 Q5 Not employed Employed Yes No
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n (%) 93 106 33 4 184 52 15 70 129 22 4 100 89 43 117 119 184 52
(39.4) (44.9) (14.0) (1.7) (78.0) (22.0) (6.4) (29.7) (54.7) (9.3) (1.7) (42.4) (37.7) (18.2) (49.6) (50.4) (78.0) (22.0)
Osingada et al
Table 2 & Uptake of Cervical Screening by Participants (N = 236) Variable
Response Category
Client is still sexually active
Yes No Yes No Reproductive health clinic Community outreach service Has never received screening Nurse-midwife Others Had never received screening
Client has received cervical screening since becoming sexually active (confirmed by medical record) Facility where cervical cancer screening was performed
Healthcare professional providing cervical cancer screening service
friend who has received the screening (Table 3). The health service delivery factors that were associated with uptake of CC screening include attendance at community outreach services for CC screening (P = .002), being concerned about the gender of HCPs performing the screening procedure (P = .001), receiving encouragement from HCPs to do the screening (P G .001), having a health facility that provides screening in the community (P = .04), and perceived quality of CCSS (P G .001) (Table 4). Logistic regression analyses were performed to identify the determinants of uptake of CC screening; the odds ratios indicate that participants older than 25 years were 3 times more likely to be screened for CC compared with those who were younger than 25 years. Participants who were not concerned about the gender of the HCPs performing the screening procedure were 5 times more likely to have been screened for CC compared with those who were concerned about the gender of the person performing the screening. The participants who were not using hormonal contraceptives, never received encouragement from HCPs, and perceived screening services as poor were 72%, 84%, and 92% less likely, respectively, to have been screened for CC compared with their counterparts in the respective category. The Wald statistics show that age (P = .005), contraceptive use (P = .016), concern about gender of HCPs (P = .001), encouragement from HCPs (P = .000), and perceived quality of screening services (P = .000)
n (%) 236 0 68 168 49 19 168 68 0 168
(100) (0) (28.8) (71.2) (20.7) (8.0) (71.2) (28.8) (0) (71.2)
contributed significantly to the prediction of uptake of CCSS (Table 5).
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Discussion
The aim of this study was to examine the determinants of uptake of CCSS by women attending a no-cost RHC managed by nurse-midwives in Uganda. The findings show that 29% of the participants had received CC screening. Although the level of uptake found in the current study is higher than the prevalence of CC screening (19%) reported in earlier studies conducted in Uganda,13 it is still lower than expected considering the increasing prevalence of the disease. The significant determinants of uptake of CC screening found in this study, such as participant’s age, concerns about the gender of HCPs performing the screening procedure, using hormonal contraceptives, encouragement from HCPs, and perceived quality of screening services, show areas in which interventions can be developed to enhance uptake of CCSS. A systematic review of studies focusing on uptake of CC screening (and other types of cancer screening) conducted in other parts of the world revealed that interventions that address aspects in line with the above determinants can have a positive
Table 3 & Client Factors Associated With Uptake of Cervical Cancer Screening Response Category
Factor Age Marital status Level of education Number of pregnancies Employment status Using of contraceptives Has friends who received cervical cancer screening
Cervical Cancer Screening in Uganda
G25 Q25 Not married Married QSecondary school ePrimary school 93 e3 Employed Not employed No Yes No Yes
Received Screening (n = 68), n (%) 16 52 14 54 38 30 24 44 39 29 7 61 49 19
Did Not Receive Screening (n = 168), n (%)
(23.5) (76.5) (26.9) (29.3) (25.2) (35.3) (30.4) (28.0) (32.8) (24.8) (13.5) (33.2) (26.6) (36.5)
77 91 38 130 113 55 55 113 80 88 45 123 135 33
(45.8) (54.2) (73.1) (70.7) (74.8) (64.7) (69.6) (72.0) (67.2) (75.2) (86.5) (66.8) (73.4) (63.5)
#2
P
10.09
.001
0.12 2.72
.733 .099
0.142 1.84
.706 .176
7.66
.006
1.94
.164
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Table 4 & Health Service Factors Associated With Uptake of Cervical Cancer Screening Factor
Response
Have heard of cervical cancer screening during community outreach programs in their community Health facilities providing cervical cancer screening in the community Concerned with gender of healthcare professional performing the screening procedure Encouraged by a healthcare professional to go for screening Concerned with waiting time at the facility where screening is provided Rating of quality of cervical cancer screening services attended
Received Screening (n = 68), n (%)
No Yes No Yes No Yes No Yes No Yes Poor Good
effect on uptake of CCSS.24,25 In this study, women who were not concerned about the gender of the HCPs performing the screening procedure were more likely to have received CC screening compared with those who were concerned. This finding suggests that women who are concerned about the gender of HCPs remain reluctant to get CC screening even when they seek care in an RHC managed by female nurse-midwives. This observation underscores the need to educate and inform the public that nursemidwives provide and lead the CCSS provision at integrated RHCs. This can help to allay women’s anxiety and misconceptions that, eventually, it will be a male HCP to perform the procedure. The current study therefore reinforces earlier findings that show high acceptability of CCSS offered by nurses and female HCPs.26Y33 A potential intervention to address this determinant would be increasing the number of female nurse-midwifeYmanaged women’s health clinics that provide expanded services. The expanded services could be implemented together with the intro-
48 20 50 18 60 8 10 58 50 18 63 5
Did Not Receive Screening (n = 168), n (%)
(24.6) (48.8) (25.9) (41.9) (34.9) (12.5) (10.4) (41.4) (26.9) (36.0) (40.9) (6.1)
21 147 143 25 112 56 89 82 136 32 91 77
(51.2) (75.4) (74.1) (58.1) (65.1) (87.5) (89.6) (58.6) (73.1) (64.0) (59.1) (93.9)
#2
P
9.65
.002
4.36
.037
11.39
.001
26.702 G.001 1.597 .206 31.61 G.001
duction of a new cadre of nurse-midwives such as nurse practitioners to maintain and enhance the quality of services. Nurse practitioners generally have been found to provide quality and cost effective services in diverse patient populations.34 Strategies to enhance the quality of CCSS are essential because in the current study, participants who perceived the quality of screening services as poor were 92% less likely to have been screened for CC compared with their counterparts in the same category. The other intervention that can be implemented to enhance quality is a policy that requires the HCP to get in contact with eligible women to teach and deliberately encourage them to go for CC screening regardless of the purpose of their visit to the RHC. The findings of this study show that participants who never received encouragement from HCPs to get CCSS were 84% less likely to have been screened. This is consistent with the findings from other studies that have already shown that physician’s recommendations or invitations are positively associated
Table 5 & Multivariable Analysis of Determinants of Uptake of Cervical Cancer Screening "
Variable and Response Category Age in years G25 Q25 Use of contraceptives No Yes Have heard of cervical cancer screening community outreach programs No Yes Health facilities providing cervical cancer screening in the community No Yes Concerned with gender of healthcare professional performing the screening No Yes Encouraged by a healthcare professional to go for screening No Yes Rating of quality of cervical cancer screening services attended Poor Good
SE
Wald
P
Exp (") (Odds Ratio)
1.129
0.405
7.785
.005
3.092
j1.266
0.525
5.805
.016
0.282
j0.836
0.460
3.309
.069
0.433
j0.453
0.472
0.921
.337
0.636
1.615
0.471
11.736
.001
5.026
j1.811
0.442
16.781
.000
0.163
j2.494
0.550
20.576
.000
0.083
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Osingada et al
with uptake of CCSS.35Y37 Encouraging patients to take part in CCSS is a critical step and requires HCPs who are trusted by patients and familiar with patient education procedures. Nurses in general have both of these attributes and therefore can lead strategies to promote uptake of CCSS. Nurse-midwives as a category are even better suited for promoting uptake of CCSS because of their training, experience in implementing integrated reproductive health services, and their ability to curtail the negative effect of anxiety associated going for CCSS provided by male HCPs. Nurse-midwives can provide appropriate health education and encouragement, and this can also help to address the other factors that have been reported to affect women’s regular screening attendance such as CC-related knowledge, perceived risk, fear, and anxiety.38 In the current study, the participants who were not using hormonal contraceptives were 72% less likely to have been screened for CC. This finding shows that integration of CCSS with other reproductive health and women’s healthcare services is an important approach in promoting uptake. Therefore, the facilities used to provide contraceptive services such RHC are key resources that can be tapped to enhance uptake of CCSS.39 Studies conducted in countries such as Peru and New Zealand indicate that receipt of family planning services is 1 of the most important predictors of uptake of CCSS.40,41 In resource-poor settings, such as Uganda, with low contraceptive use42 and uptake of CCSS service, integration of services is likely to have a multifaceted positive effect because it can help to overcome opportunistic CC screening, through assured availability, access to regular HCP encouragement, reminders, and health education. The current study and others have found age to be a significant determinant of uptake of CC screening.27,35,43Y45 A study conducted in the Netherlands showed that as women age, they are more likely to be faced with increasing personal moral obligation to receive CC screening if they are invited or reminded to have CC screening (Papanicolaou test) by their HCPs.35 Increasing age is also associated with increased personal confidence and, therefore, less anxiety about invasive procedures, both of which influence uptake of CC screening.25,39 In this study, systems of support and social influences, such as community outreach programs, CC screening in the community, and having friends who received CC screening, were not significantly associated with uptake of CCSS, although these are articulated by the PHM as potential determinants. Other studies using community interventions, such as informal community health volunteers, to enhance uptake of CCSS have also found such interventions to be less effective in African women.46 On the other hand, less personal system supports, such as community media interventions and radio-drama accessed by the whole community, have been found to enhance CC screening uptake in South Africa.25 There is a need to continue to explore effective community system support interventions that can be used to enhance CC awareness and screening in resource-poor settings because they are cheaper and likely to reach a large number of eligible women. Therefore, in resource-poor settings with limited numbers of static clinical facilities, a combination of quality RHCbased services and cluster targeted system supports hold a significant potential of increasing uptake of CCSS because of their ability to reach and address the CC screening needs of at-risk women.
Cervical Cancer Screening in Uganda
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Limitations
The findings of this study are likely to have been affected by the limited sample size and using a clinic that is located in a referral hospital. The RHC used by the study receives a large number of patients, some of whom are referrals and therefore likely to have received encouragement and health education from other HCPs. The large caseload of the RHC could also have been viewed by women as overcrowding in the clinic, and this may have altered their perceptions about the quality of services provided. The RHC has male employees (technicians, medical clerks and porters), but they do not get directly involved in CCSS or in contact with clients. Seeing male employees in the RHC could affect the women’s perception about the gender of HCPs providing the CC screening procedure. The questionnaire used for data collection was not standardized, but the data for the outcome variable were verified by checking each participant’s medical records.
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Conclusions
When CCSS are perceived to be of high quality, provided in a facility where the procedure is administered by female HCPs, and where regular encouragement is given to clients to get CC screening, there is the likelihood of high uptake, especially among women older than 25 years and using hormonal contraceptives. Therefore, despite the limitations of this study, it seems that in resource-poor settings such as Uganda, some of the efforts to enhance uptake of CCSS should focus on policies or clinical practice protocols that require all HCPs to provide deliberate health education, reminders, and encouragement to eligible women about CC screening. In addition, resource-poor settings could adopt the concept of women’s health clinics where integrated health services are provided by nurse-midwives or nurse practitioners to enhance access to diverse quality CCSS, reproductive health services, and other women’s health services.
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10. Quentin W, Adu-Sarkodie Y, Terris-Prestholt F, et al. Costs of cervical cancer screening and treatment using visual inspection with acetic acid (VIA) and cryotherapy in Ghana: the importance of scale. Trop Med Int Health. 2011;16(3):379Y389. 11. Sankaranarayanan R, Nene BM, Shastri SS, et al. HPV screening for cervical cancer in rural India. N Engl J Med. 2009;360(14):1385Y1394. 12. Eze JN, Umeora OU, Obuna JA, et al. Cervical cancer awareness and cervical screening uptake at the Mater Misericordiae Hospital, Afikpo, Southeast Nigeria. Ann Afr Med. 2012;11(4):238Y243. 13. Mutyaba T, Mmiro FA, Weiderpass E. Knowledge, attitudes and practices on cervical cancer screening among the medical workers of Mulago Hospital, Uganda. BMC Med Educ. 2006;6:13. 14. Busingye P, Nakimuli A, Nabunya E, Mutyaba T. Acceptability of cervical cancer screening via visual inspection with acetic acid or Lugol’s iodine at Mulago Hospital, Uganda. Int J Gynecol Obstet. 2012;119(3):262Y265. 15. Atuhairwe S, Busingye RB, Sekikubo M, et al. Urologic complications among women with advanced cervical cancer at a tertiary referral hospital in Uganda. Int J Gynecol Obstet. 2011;115:282Y284. 16. Anorlu RI, Ribiu KA, Abudu OO, Ola ER. Cervical cancer screening practices among general practitioners in Lagos Nigeria. J Obstet Gynecol. 2007; 27(2):181Y184. 17. Mutyaba T, Faxelid E, Mirembe F, Weiderpass E. Influences on uptake of reproductive health services in Nsangi community of Uganda and their implications for cervical cancer screening. Reprod Health. 2007;4:4. 18. Muliira JK, Kisaakye E, Kizza IB, Suubi RR. Perceived cervical cancer risk, knowledge and preventive practices. Afr J Midwifery Womens Health. 2011; 5(2):87Y93. 19. Woltman KJ, Newbold KB. Immigrant women and cervical cancer screening uptakeVa multilevel analysis. Can J Public Health. 2003;98(6): 470Y475. 20. Duffett-Leger LA, Letourneau NL, Croll JC. Cervical cancer screening practices among university women. J Obstet Gynecol Neonatal Nurs. 2008;37(5): 572Y581. 21. Myers RE. Decision counseling in cancer prevention and control. Health Psychol. 2005;24:S71YS77. 22. Myers RE, Ross E, Jepson C, et al. Modeling adherence to colorectal cancer screening. Prev Med. 1994;23:142Y151. 23. Bradley EH, Curry LA, Devers KJ. Qualitative data analysis for health services research: developing taxonomy, themes and theory. Health Serv Res. 2007;42(14):1758Y1772. 24. Sabatino SA, Lawrence B, Elder R, et al. Effectiveness of interventions to increase screening for breast, cervical, and colorectal cancers: nine updated systematic reviews for the guide to community preventive services. Am J Prev Med. 2012;43(1):97Y118. 25. Risi L, Bindman JP, Campbell OMR, et al. Media interventions to increase cervical screening uptake in South Africa: an evaluation study of effectiveness. Health Educ Res. 2004;19(4):457Y468. 26. Sankaranarayanan R, Gaffikin I, Jacob M, et al. Determinants of participation of women in a cervical cancer visual screening trial in rural south India. Cancer Detect Prev. 2003;27(6):457Y465. 27. Lofters AK, Moineddin R, Hwang SW, Glazier RH. Predictors of low cervical cancer screening among immigrant women in Ontario, Canada. BMC Womens Health. 2011;11:20. 28. Ansink AC, Tolhurst R, Haque R, et al. Cervical cancer in Bangladesh:
29.
30.
31.
32.
33. 34. 35.
36.
37.
38.
39. 40.
41.
42.
43.
44.
45. 46.
community perceptions of cervical cancer and cervical cancer screening. Trans R Soc Trop Med Hyg. 2008;102(5):499Y505. McAlearney AS, Oliveri JM, Post DM, et al. Trust and distrust among Appalachian women regarding cervical cancer screening: a qualitative study. Patient Educ Couns. 2012;86(1):120Y126. Nguyen TT, McPhee SJ, Nguyen T, et al. Predictors of cervical Pap smear screening awareness, intention, and receipt among Vietnamese-American women. Am J Prev Med. 2002;23(3):207Y214. Roydhouse JK. Chinese-Australian women’s knowledge, facilitators and barriers related to cervical cancer screening: a qualitative study. J Immigr Minor Health. 2011;13(6):1076Y1083. Lyimo FS, Beran TN. Demographic, knowledge, attitudinal, and accessibility factors associated with uptake of cervical cancer screening among women in a rural district of Tanzania: three public policy implications. BMC Public Health. 2012;12:22. Holroyd E, Twinn S, Adab P. Socio-cultural influences on Chinese women’s attendance for cervical screening. J Adv Nurs. 2004;46(1):42Y52. Newhouse RP, Stanik-Hutt J, White KM, et al. Advanced practice nurse outcomes 1990Y2008: a systematic review. Nurs Econ. 2011;29(5):1Y21. Tacken MA, Braspenning JC, Hermens RP, et al. Uptake of cervical cancer screening in the Netherlands is mainly influenced by women’s beliefs about the screening and by the inviting organization. Eur J Public Health. 2007; 17(2):178Y185. Bazargan M, Bazargan SH, Farooq M, Baker RS. Correlates of cervical cancer screening among underserved Hispanic and African-American women. Prev Med. 2004;39(3):465Y473. Brown DR, Wilson RM, Boothe MAS, Harris CE. Cervical cancer screening among ethnically diverse black women: knowledge, attitudes, beliefs, and practices. J Natl Med Assoc. 2011;103(8):719Y728. Kuitto K, Pickel S, Neumann H, et al. Attitudinal and socio-cultural determinants of cervical cancer screening and HPV vaccination uptake: a quantitative multivariate analysis. J Public Health. 2010;18:179Y188. Claeys P, De Vuyst H, Mzenge G, et al. Integration of cervical screening in family planning clinics. Int J Gynecol Obstet. 2003;81(1):103Y108. Robles SC, Ferreccio C, Tsu V, et al. Assessing participation of women in a cervical cancer screening program in Peru. Rev Panam Salud Publica. 2009; 25(3):189Y195. Gao W, DeSouza R, Paterson J, Lu T. Factors affecting uptake of cervical cancer screening among Chinese women in New Zealand. Int J Gynecol Obstet. 2008;103(1):76Y82. UBOS, Uganda Bureau of Statistics (UBOS) and ICF International Inc. Uganda Demographic and Health Survey 2011. Kampala, Uganda: UBOS and Calverton, Maryland: ICF International Inc; 2012. Kahesa C, Kjaer S, Mwaiselage J, et al. Determinants of acceptance of cervical cancer screening in Dar es Salaam, Tanzania. BMC Public Health. 2012; 12(1):1093. El Mhamdi S, Bouanene I, Mhirsi A, et al. Cervical cancer screening: women’s knowledge, attitudes, and practices in the region of Monastir (Tunisia). Rev Epidemiol Sante Publique. 2012;60(6):431Y436. Lin SJ. Factors influencing the uptake of screening services for breast and cervical cancer in Taiwan. J R Soc Prom Health. 2008;128(6):327Y334. Tum SJ, Maree JE, Clarke M. Creating awareness and facilitating cervical and breast cancer screening uptake through the use of a community health worker: a pilot intervention study. Eur J Cancer Care. 2013;22:107Y116.
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Osingada et al
Charles P. Osingada, MPH Gloria Ninsiima, MSN Rose N. Chalo, PhD Joshua K. Muliira, DNP, MA, RN Tom Ngabirano, MSN
Determinants of Uptake of Cervical Cancer Screening Services at a No-Cost Reproductive Health Clinic Managed by Nurse-Midwives K E Y
W O R D S
Background: The incidence of cervical cancer (CC) has been rising in
Cervical cancer
sub-Saharan Africa, and health authorities in this region have responded by
Determinants
increasing the availability of cheap or no-cost CC screening services (CCSS), public
Early detection of cancer
health education, and others. However, the efforts have not yet resulted into the
Nurse-midwives
expected uptake of CCSS. Objective: The aim of this study was to examine the
Preventive care
determinants of uptake of CCSS at a no-cost reproductive health clinic managed by
Screening
nurse-midwives. Methods: A descriptive design and a structured interview
Uganda
questionnaire were used to collect data from 236 women attending the reproductive
Uptake
health clinic. Logistic regression statistics were used to examine the determinants of uptake of CCSS. Results: The mean age of participants was 28.7 years, and only 29% had received CC screening. The significant determinants of uptake of CCSS were concern about the gender of the healthcare professional (HCP) (odds ratio [OR], 5.03; P = .001), age older than 25 years (OR, 3.09; P = .005), contraceptive use (OR, 0.28; P = .02), encouragement by HCPs (OR, 0.16; P = .00), and perceived quality of CCSS (OR, 0.08; P = .00). Conclusions: Gender of the HCP and encouragement or reminders by the HCP influence uptake of CCSS. Because nurse-midwives have successfully led strategies to promote other integrated reproductive health services, they can also play a key role in enhancing uptake of CCSS in resource-poor settings. Implications for Practice: Interventions to
Author Affiliations: School of Health Sciences, College of Health Sciences, Department of Nursing, Makerere University, Kampala, Uganda (Mr Osingada and Ngabirano, Ms Ninsiima, and Dr Chalo); and College of Nursing, Department of Adult Health & Critical Care, Sultan Qaboos University, Muscat, Oman (Dr Muliira). Authors’ contributions: C.P.O., G.N., R.N.C., and T.N. were responsible for the study conception, design, and data collection. C.P.O., G.N., and J.K.M. were responsible for data analysis and drafting of the first manuscript. All authors made critical revisions to the final paper for intellectual content.
Cervical Cancer Screening in Uganda
The authors have no funding or conflicts of interest to disclose. Correspondence: Joshua K. Muliira, DNP, MA, RN, College of Nursing, Department of Adult Health & Critical Care, Sultan Qaboos University, PO Box 66 Al Khod, PC 123, Muscat, Oman ([email protected]). Accepted for publication March 4, 2014. DOI: 10.1097/NCC.0000000000000156
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enhance service quality and deliberate policies requiring HCP to recommend encourage and remind clients may help to enhance uptake of CCSS in resource-poor settings.
A
pproximately 500 000 women are diagnosed with cervical cancer (CC), and 274 000 die of the disease annually.1,2 A large majority (80%) of the world’s CC patients live in developing countries, where this type of cancer accounts for 15% of all female cancers compared with 3.6% in the developed world.3 Unfortunately, the CC burden in developing countries is likely to worsen because these countries have access to less than 5% of the global cancer treatment resources.1,2,4 The other factors that continue to sustain the high burden of CC in developing countries include the high prevalence of risk factors, such as human immunodeficiency virus, human papillomavirus, and multiple sexual partners among men in heterosexual relationships; poor genital hygiene; and reusing of homemade feminine napkins.5 Recent reports show that, annually, in sub-Saharan Africa, CC causes approximately 50 000 deaths (age standardized rate 22.5).1 This number is likely to be considerably higher because in sub-Saharan Africa, many times, the data are unavailable or incomplete. In Uganda, the CC incidence and mortality rate are 40 in 100 000 and 25 in 100 000, respectively.6 In Kampala, Uganda’s capital city, the age-standardized incidence rate of CC for the period 2002 to 2006 was 52.4 per 100 000.7 Like in other sub-Saharan African countries, CC is the leading cause of female cancer morbidity and death in Uganda.6 The health authorities (Ministry of Health and nongovernmental agencies) have responded to the growing burden of CC by integrating CC screening services (CCSS) into the existing reproductive health services provided at no cost in government clinics or in private and nongovernmental health facilities where clients are required to pay a fee for services. Uganda’s health authorities have also trained healthcare professionals (HCPs) such as nurses and midwives in advanced skills to be able to provide CCSS, and this has increased access to screening. The government and nongovernmental organizations continue to publicize CC and CCSS through public health education, the media, and other public forums to ensure that the public understands that CC is preventable and that screening can reduce morbidity and mortality. As mentioned above, in Uganda, CCSS are offered mostly through the family planning or reproductive health clinics (RHCs), which normally provide contraceptive services, postnatal assessment, and young child clinics. The RHCs are usually well attended by women. The most commonly used methods for CC screening are visual inspection with acetic acid (VIA), visual inspection with Lugol iodine (VILI), and VIA with cryotherapy.8 Other developing countries have also adopted VIA and VILI with cryotherapy because these are cheaper, can be easily provided by commonly available and accessible HCPs such as nurses, and are more feasible in resourcepoor settings.9,10 Cervical cancer screening programs based on cytology, which assisted developed countries to reduce the in-
cidence of CC, have not had a similar effect in developing countries because they are expensive and require highly trained and skilled HCPs.3,11 The recently unveiled cheap or no-cost CCSS have not yet resulted in the expected level of impact on CC. Various studies conducted in Uganda and other sub-Saharan countries like Nigeria still show low uptake of CCSS.12,13 A recent study conducted in Uganda to examine the acceptability of CC screening using VIA or Lugol iodine showed that 40% of the women declined to receive the procedure.14 The reluctance of women to receive CC screening is partly responsible for the late diagnosis and subsequent mortality from an otherwise preventable and treatable type of cancer. Most Ugandan women (71%) with CC present to hospitals to seek care 6 months after the onset of symptoms and usually after they have started experiencing complications such as elevated serum creatinine, hydronephrosis, hydroureter, vesicovaginal fistula, and anuria.15 In sub-Saharan Africa, late diagnosis of CC and failure to receive CC screening were, in the past, attributed to inadequate services, lack of access to deliberate information about screening by patients, and lack of facilities for Papanicolaou test services.16 The other factors that have been noted to influence uptake of CCSS and related general reproductive health services include cultural beliefs about illness, economic factors, domestic gender power relations, alternative authoritative sources of reproductive health knowledge, and unfriendly HCPs.17 Lack of knowledge is still persistent because recent reports show that many women in Sub-Saharan Africa do not know the cause or manifestations of CC, and this leads to low risk perceptions and poor preventive practices.12,18 Receipt of CC screening in sub-Saharan Africa is also influenced by factors such as level of education, fear of invasion of personal privacy, fear of pain, and worry about test results.8 Therefore, the factors that are associated with receipt of CCSS by women in resource-poor settings seem to have cultural, social, and personal dimensions. A study conducted in Canada among 3 474 352 women, of which 38.6% were immigrants of African, South Asian, Chinese, and other nonYNorth American or European origins, demonstrated that after controlling for demographic factors, access to a physician, and socioeconomic factors, being an immigrant, African, Chinese, South Asian, or other Asian origins decreased the likelihood of Papanicolaou testing.19 On the other hand, studies with samples composed of predominantly women born in developed countries show that they have good CC screening practices.20
Aim The purpose of this study was to establish the determinants of uptake of CCSS offered at a no-cost clinic managed by female nurse-midwives at a referral hospital in Uganda.
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Osingada et al
Theoretical Framework 21,22
The study was guided by the Preventive Health Model (PHM). The PHM has been used widely to explain predictors of prostate and colorectal cancer screening behaviors.23 The PHM was used because it comprehensively considers and addresses the factors that influence patient’s cancer screening behaviors and actual action of getting the screening. The PHM is composed of constructs focusing on the patient background factors (eg, demographic characteristics), patient behaviors factors (eg, worry, self-efficacy, and social influence), healthcare provider factors (eg, clinic factors, access, HCPs’ knowledge, attitude and beliefs), system of support factors (community resources, guidelines, and self-management support), and the outcome (cancer screening, eg, intention, planning, action, and experience).21,22 The PHM posits that the patient’s action leading to receipt of cancer screening (such as receipt of CC screening) is directly influenced by background factors, behavioral factors, healthcare provider factors, and systems of support factors.21 The study explored the effect of background (demographic characteristics), healthcare provider (health service factors), and system (community resources) factors on uptake of CC screening. Some aspects of all the 3 categories of factors are currently being used in Uganda to enhance uptake of CC screening.
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Methods
Population and Setting The study used a cross-sectional design to recruit women attending an RHC at a referral hospital in Uganda. The RHC provides free contraceptive (family planning) services, CCSS, and postnatal checkups on a daily basis, except on weekends and public holidays, when it is not open. On average, the RHC serves a total of 370 women per month. The method used for CC screening at the RHC is VIA or VILI, and the screening procedures are performed by nurse-midwives who are trained in providing this service. The nurse-midwives who provide care and manage the RHC are qualified with associate degrees (diploma) or bachelor degrees majoring in both nursing and midwifery. Women who require a Papanicolaou test are referred to the adjacent University Department of Pathology. The other services provided by RHC include Young Child Care Services (child growth monitoring and immunization) and health education about infant feeding and nutrition. Therefore, the RHC provided a good integrated care environment to find women eligible for CCSS. The study targeted women who were attending the RHC. Participants had to meet the following inclusion criteria: 18 years or older, sexually active, able to speak English or Luganda (languages used during healthcare service provision at the RHC), has sought care at the RHC at least twice, willing to provide permission to access client health records to confirm receipt of CC screening, and willing to spend 40 minutes to complete the study questionnaire after signing the written informed consent form. A total of 350 women were approached, and data collection was stopped once the required sample of 236 participants was at-
Cervical Cancer Screening in Uganda
tained (consented to participate in the study and had complete legible medical records).
Study Instrument The semistructured interview questionnaire used to collect data was developed by the investigators after review of literature about determinants of uptake of CCSS and following the framework outlined by PHM. Because English and Luganda (which has no major variance such as dialects) are the languages used during healthcare service delivery at the RHC, the questionnaire had to be available in both languages. The research team (all multilingualV English, Luganda, and other Ugandan languages) translated the first version of the questionnaire from English to Luganda. The research team discussed the items in the initial Luganda questionnaire version with a professional translator and linguistic expert regarding the conceptual meanings of each item as well as formulation of the response statements. The initial Luganda questionnaire version was back-translated into English by the professional translator. After the back-translation process, some discrepancies between the forward and backward translation were observed, and these pertained to the Luganda equivalent of the words quality and program. The terms were clarified with explanatory statements. The questionnaire was then pretested among 20 women at a clinic in a rural setting, and results of the pretesting showed that the questionnaire required 40 minutes to complete and that the terms cervical cancer, cervical cancer screening, and quality of screening services were understandable. The items on the questionnaire were organized under the sections of demographic characteristics, health service factors, community factors, and receipt of CC screening. The demographic characteristics emphasized were age, marital status, level of education, parity, employment status, and use of contraceptives. The section about uptake of CCSS included questions such as ‘‘Are you currently sexually active?’’ ‘‘Have you been screened for CC since becoming sexually active?’’ ‘‘Where did you receive the screening procedure from?’’ and ‘‘Who performed the screening procedure?’’ The items about health services factor focused on the gender of the HCP, perceived quality of CCSS, waiting time at the health facility, and receiving encouragement from HCPs. The community factors included having close friends who received CC screening and access to CC community outreach services.
Procedure After ethical review and approval by the School of Medicine Institutional Review Board (protocol number 2012-046) at Makerere University and Mulago National Referral Hospital, the researchers visited the RHC to plan for data collection. Data were collected daily from Monday to Friday over a period of 30 days in May 2012. On data collection days, all women who came to the RHC were approached and informed about the study. Participants were recruited consecutively until the calculated sample size was attained. The sample size was estimated using the Kish Leslie (1965) formula. Using the most recent reported prevalence of CC screening of 19% among women,13 a 95% confidence interval, and an allowable margin of error of 5%, the required Cancer NursingTM, Vol. 38, No. 3, 2015
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sample size for the study was estimated to be 236 participants. Data collection was stopped once the required sample was attained. The women who met the inclusion criteria and were willing to learn more about the study were provided both verbal and written explanations of the purpose and procedures. After providing the explanations, the women who agreed to participate in the study were requested to sign an informed consent form. The explanations and informed consent form included statements showing that participation in the study required giving permission to review medical records to confirm receipt of CC screening. The participants who consented were taken to a private room to complete a structured interview questionnaire under the guidance of trained research assistant (nurse-midwife). The structured interview questionnaire required approximately 40 minutes to be completed, and all participants who reported receipt of CC screening at least once since becoming sexually active had their medical record checked for confirmation. Data of participants (n = 12) who reported receipt of CC screening but whose medical records were incomplete, unavailable, or illegible were not included in the final analysis. There was no other information that was obtained from the participant’s medical records. After verifying receipt of CC screening, the interview questionnaire was checked for completeness before the participant was directed to where they were going to receive care. The process of verifying receipt of CC screening took between 10 to 15 minutes.
Data Analysis Data were entered into the computer using Epi info version 3.5.1 and were analyzed using STATA version 10. Descriptive statistics were used to summarize the demographic characteristics and uptake of CC screening. A # 2 test was used to determine factors associated with uptake of CC screening. Bivariate and multivariate analyses were conducted to determine factors that influenced uptake of CCSS. All variables that were significant at bivariate level and thought to be theoretically (according to PHM) important in
influencing the outcome variable (receipt of CC screening at least once since becoming sexually active or did not receive CC screening since becoming sexually active) were included in a logistic regression model. In all statistical tests, a P value e .05 was considered to be significant.
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Results
A total of 350 participants were asked to participate in this study, and 236 (67.4%) women consented. The main reason for refusal related to not having time to complete the study questionnaire; others willing to participate were not eligible because of illegible or incomplete medical records (n = 12). The mean (SD) age of participants was 28.7 (6.7) years. Most participants were married (78%), had secondary school education (55%), were using hormonal contraceptives (78%), and had been pregnant at least 3 times (56%) (Table 1).
Uptake of CC Screening All the 236 participants recruited in the study were sexually active, but only 29% (n = 68) had received CC screening since becoming sexually active (Table 2). The procedure for CC screening was performed by a nurse-midwife working at the RHC (21%) or with the health facilities’ community outreach services (8%).
Factors Influencing Uptake of CC Screening Bivariate analysis was performed using the # 2 test to determine the participants’ background factors associated with uptake of CC screening. The participant factors that were associated with uptake of CC screening were age (P = .001) and use of contraceptives (P = .006). There was no significant relationship found between uptake of CC screening and factors such as marital status, level of education, number of pregnancies, or having a
Table 1 & Participants’ Demographic Characteristics (N = 236) Variable
Response Category
Age in years (mean [SD], 28.7 [6.7])
Marital status Highest level of education attained
Number of pregnancies (mean [SD], 3.0 [1.7])
Employment status Using contraceptives (hormonal based or intrauterine device)
18Y25 26Y35 36Y45 Q46 Currently married Not married No formal education Primary school Completed secondary school Completed tertiary 0 1Y2 3Y4 Q5 Not employed Employed Yes No
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n (%) 93 106 33 4 184 52 15 70 129 22 4 100 89 43 117 119 184 52
(39.4) (44.9) (14.0) (1.7) (78.0) (22.0) (6.4) (29.7) (54.7) (9.3) (1.7) (42.4) (37.7) (18.2) (49.6) (50.4) (78.0) (22.0)
Osingada et al
Table 2 & Uptake of Cervical Screening by Participants (N = 236) Variable
Response Category
Client is still sexually active
Yes No Yes No Reproductive health clinic Community outreach service Has never received screening Nurse-midwife Others Had never received screening
Client has received cervical screening since becoming sexually active (confirmed by medical record) Facility where cervical cancer screening was performed
Healthcare professional providing cervical cancer screening service
friend who has received the screening (Table 3). The health service delivery factors that were associated with uptake of CC screening include attendance at community outreach services for CC screening (P = .002), being concerned about the gender of HCPs performing the screening procedure (P = .001), receiving encouragement from HCPs to do the screening (P G .001), having a health facility that provides screening in the community (P = .04), and perceived quality of CCSS (P G .001) (Table 4). Logistic regression analyses were performed to identify the determinants of uptake of CC screening; the odds ratios indicate that participants older than 25 years were 3 times more likely to be screened for CC compared with those who were younger than 25 years. Participants who were not concerned about the gender of the HCPs performing the screening procedure were 5 times more likely to have been screened for CC compared with those who were concerned about the gender of the person performing the screening. The participants who were not using hormonal contraceptives, never received encouragement from HCPs, and perceived screening services as poor were 72%, 84%, and 92% less likely, respectively, to have been screened for CC compared with their counterparts in the respective category. The Wald statistics show that age (P = .005), contraceptive use (P = .016), concern about gender of HCPs (P = .001), encouragement from HCPs (P = .000), and perceived quality of screening services (P = .000)
n (%) 236 0 68 168 49 19 168 68 0 168
(100) (0) (28.8) (71.2) (20.7) (8.0) (71.2) (28.8) (0) (71.2)
contributed significantly to the prediction of uptake of CCSS (Table 5).
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Discussion
The aim of this study was to examine the determinants of uptake of CCSS by women attending a no-cost RHC managed by nurse-midwives in Uganda. The findings show that 29% of the participants had received CC screening. Although the level of uptake found in the current study is higher than the prevalence of CC screening (19%) reported in earlier studies conducted in Uganda,13 it is still lower than expected considering the increasing prevalence of the disease. The significant determinants of uptake of CC screening found in this study, such as participant’s age, concerns about the gender of HCPs performing the screening procedure, using hormonal contraceptives, encouragement from HCPs, and perceived quality of screening services, show areas in which interventions can be developed to enhance uptake of CCSS. A systematic review of studies focusing on uptake of CC screening (and other types of cancer screening) conducted in other parts of the world revealed that interventions that address aspects in line with the above determinants can have a positive
Table 3 & Client Factors Associated With Uptake of Cervical Cancer Screening Response Category
Factor Age Marital status Level of education Number of pregnancies Employment status Using of contraceptives Has friends who received cervical cancer screening
Cervical Cancer Screening in Uganda
G25 Q25 Not married Married QSecondary school ePrimary school 93 e3 Employed Not employed No Yes No Yes
Received Screening (n = 68), n (%) 16 52 14 54 38 30 24 44 39 29 7 61 49 19
Did Not Receive Screening (n = 168), n (%)
(23.5) (76.5) (26.9) (29.3) (25.2) (35.3) (30.4) (28.0) (32.8) (24.8) (13.5) (33.2) (26.6) (36.5)
77 91 38 130 113 55 55 113 80 88 45 123 135 33
(45.8) (54.2) (73.1) (70.7) (74.8) (64.7) (69.6) (72.0) (67.2) (75.2) (86.5) (66.8) (73.4) (63.5)
#2
P
10.09
.001
0.12 2.72
.733 .099
0.142 1.84
.706 .176
7.66
.006
1.94
.164
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Table 4 & Health Service Factors Associated With Uptake of Cervical Cancer Screening Factor
Response
Have heard of cervical cancer screening during community outreach programs in their community Health facilities providing cervical cancer screening in the community Concerned with gender of healthcare professional performing the screening procedure Encouraged by a healthcare professional to go for screening Concerned with waiting time at the facility where screening is provided Rating of quality of cervical cancer screening services attended
Received Screening (n = 68), n (%)
No Yes No Yes No Yes No Yes No Yes Poor Good
effect on uptake of CCSS.24,25 In this study, women who were not concerned about the gender of the HCPs performing the screening procedure were more likely to have received CC screening compared with those who were concerned. This finding suggests that women who are concerned about the gender of HCPs remain reluctant to get CC screening even when they seek care in an RHC managed by female nurse-midwives. This observation underscores the need to educate and inform the public that nursemidwives provide and lead the CCSS provision at integrated RHCs. This can help to allay women’s anxiety and misconceptions that, eventually, it will be a male HCP to perform the procedure. The current study therefore reinforces earlier findings that show high acceptability of CCSS offered by nurses and female HCPs.26Y33 A potential intervention to address this determinant would be increasing the number of female nurse-midwifeYmanaged women’s health clinics that provide expanded services. The expanded services could be implemented together with the intro-
48 20 50 18 60 8 10 58 50 18 63 5
Did Not Receive Screening (n = 168), n (%)
(24.6) (48.8) (25.9) (41.9) (34.9) (12.5) (10.4) (41.4) (26.9) (36.0) (40.9) (6.1)
21 147 143 25 112 56 89 82 136 32 91 77
(51.2) (75.4) (74.1) (58.1) (65.1) (87.5) (89.6) (58.6) (73.1) (64.0) (59.1) (93.9)
#2
P
9.65
.002
4.36
.037
11.39
.001
26.702 G.001 1.597 .206 31.61 G.001
duction of a new cadre of nurse-midwives such as nurse practitioners to maintain and enhance the quality of services. Nurse practitioners generally have been found to provide quality and cost effective services in diverse patient populations.34 Strategies to enhance the quality of CCSS are essential because in the current study, participants who perceived the quality of screening services as poor were 92% less likely to have been screened for CC compared with their counterparts in the same category. The other intervention that can be implemented to enhance quality is a policy that requires the HCP to get in contact with eligible women to teach and deliberately encourage them to go for CC screening regardless of the purpose of their visit to the RHC. The findings of this study show that participants who never received encouragement from HCPs to get CCSS were 84% less likely to have been screened. This is consistent with the findings from other studies that have already shown that physician’s recommendations or invitations are positively associated
Table 5 & Multivariable Analysis of Determinants of Uptake of Cervical Cancer Screening "
Variable and Response Category Age in years G25 Q25 Use of contraceptives No Yes Have heard of cervical cancer screening community outreach programs No Yes Health facilities providing cervical cancer screening in the community No Yes Concerned with gender of healthcare professional performing the screening No Yes Encouraged by a healthcare professional to go for screening No Yes Rating of quality of cervical cancer screening services attended Poor Good
SE
Wald
P
Exp (") (Odds Ratio)
1.129
0.405
7.785
.005
3.092
j1.266
0.525
5.805
.016
0.282
j0.836
0.460
3.309
.069
0.433
j0.453
0.472
0.921
.337
0.636
1.615
0.471
11.736
.001
5.026
j1.811
0.442
16.781
.000
0.163
j2.494
0.550
20.576
.000
0.083
182 n Cancer NursingTM, Vol. 38, No. 3, 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Osingada et al
with uptake of CCSS.35Y37 Encouraging patients to take part in CCSS is a critical step and requires HCPs who are trusted by patients and familiar with patient education procedures. Nurses in general have both of these attributes and therefore can lead strategies to promote uptake of CCSS. Nurse-midwives as a category are even better suited for promoting uptake of CCSS because of their training, experience in implementing integrated reproductive health services, and their ability to curtail the negative effect of anxiety associated going for CCSS provided by male HCPs. Nurse-midwives can provide appropriate health education and encouragement, and this can also help to address the other factors that have been reported to affect women’s regular screening attendance such as CC-related knowledge, perceived risk, fear, and anxiety.38 In the current study, the participants who were not using hormonal contraceptives were 72% less likely to have been screened for CC. This finding shows that integration of CCSS with other reproductive health and women’s healthcare services is an important approach in promoting uptake. Therefore, the facilities used to provide contraceptive services such RHC are key resources that can be tapped to enhance uptake of CCSS.39 Studies conducted in countries such as Peru and New Zealand indicate that receipt of family planning services is 1 of the most important predictors of uptake of CCSS.40,41 In resource-poor settings, such as Uganda, with low contraceptive use42 and uptake of CCSS service, integration of services is likely to have a multifaceted positive effect because it can help to overcome opportunistic CC screening, through assured availability, access to regular HCP encouragement, reminders, and health education. The current study and others have found age to be a significant determinant of uptake of CC screening.27,35,43Y45 A study conducted in the Netherlands showed that as women age, they are more likely to be faced with increasing personal moral obligation to receive CC screening if they are invited or reminded to have CC screening (Papanicolaou test) by their HCPs.35 Increasing age is also associated with increased personal confidence and, therefore, less anxiety about invasive procedures, both of which influence uptake of CC screening.25,39 In this study, systems of support and social influences, such as community outreach programs, CC screening in the community, and having friends who received CC screening, were not significantly associated with uptake of CCSS, although these are articulated by the PHM as potential determinants. Other studies using community interventions, such as informal community health volunteers, to enhance uptake of CCSS have also found such interventions to be less effective in African women.46 On the other hand, less personal system supports, such as community media interventions and radio-drama accessed by the whole community, have been found to enhance CC screening uptake in South Africa.25 There is a need to continue to explore effective community system support interventions that can be used to enhance CC awareness and screening in resource-poor settings because they are cheaper and likely to reach a large number of eligible women. Therefore, in resource-poor settings with limited numbers of static clinical facilities, a combination of quality RHCbased services and cluster targeted system supports hold a significant potential of increasing uptake of CCSS because of their ability to reach and address the CC screening needs of at-risk women.
Cervical Cancer Screening in Uganda
n
Limitations
The findings of this study are likely to have been affected by the limited sample size and using a clinic that is located in a referral hospital. The RHC used by the study receives a large number of patients, some of whom are referrals and therefore likely to have received encouragement and health education from other HCPs. The large caseload of the RHC could also have been viewed by women as overcrowding in the clinic, and this may have altered their perceptions about the quality of services provided. The RHC has male employees (technicians, medical clerks and porters), but they do not get directly involved in CCSS or in contact with clients. Seeing male employees in the RHC could affect the women’s perception about the gender of HCPs providing the CC screening procedure. The questionnaire used for data collection was not standardized, but the data for the outcome variable were verified by checking each participant’s medical records.
n
Conclusions
When CCSS are perceived to be of high quality, provided in a facility where the procedure is administered by female HCPs, and where regular encouragement is given to clients to get CC screening, there is the likelihood of high uptake, especially among women older than 25 years and using hormonal contraceptives. Therefore, despite the limitations of this study, it seems that in resource-poor settings such as Uganda, some of the efforts to enhance uptake of CCSS should focus on policies or clinical practice protocols that require all HCPs to provide deliberate health education, reminders, and encouragement to eligible women about CC screening. In addition, resource-poor settings could adopt the concept of women’s health clinics where integrated health services are provided by nurse-midwives or nurse practitioners to enhance access to diverse quality CCSS, reproductive health services, and other women’s health services.
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