Open access Research Acceptability and implementation challenges of smartphone-based training of community health nurses for visual inspection with acetic acid in Ghana: mHealth and cervical cancer screening Ramin Asgary,1,2 Helen Cole,3 Philip Adongo,4 Ada Nwameme,4 Ernest Maya,4,5 Amanda Adu-Amankwah,5 Hannah Barnett,1 Richard Adanu6,7 To cite: Asgary R, Cole H, Abstract Adongo P, et al. Acceptability Strengths and limitations of this study Objective To explore acceptability and feasibility of and implementation smartphone-based training of low-level to mid-level health challenges of smartphone- ►► Using a qualitative descriptive approach, this is the professionals in cervical cancer screening using visual based training of community first paper that describes perceptions and experi- inspection with acetic acid (VIA)/cervicography. health nurses for visual ences of nurses and patients in regards to smart- inspection with acetic acid in Design In 2015, we applied a qualitative descriptive phone-based visual inspection with acetic acid (VIA) Ghana: mHealth and cervical approach and conducted semi-structured interviews and for cervical cancer screening. cancer screening. BMJ Open focus groups to assess the perceptions and experiences ►► Our findings provide important insight into the over- 2019;9:e030528. doi:10.1136/ of community health nurses (CHNs) (n=15) who performed all acceptability and feasibility of this approach from bmjopen-2019-030528 smartphone-based VIA, patients undergoing VIA/ the perspectives of all stakeholders. cryotherapy (n=21) and nurse supervisor and the expert ►► Prepublication history and ►► The smartphone-based training of VIA has important additional material for this reviewer (n=2). promises for VIA implementation and sustainability paper are available online. To Setting Community health centres (CHCs) in Accra, of national programmes. view these files, please visit the Ghana. ►► This qualitative study by its nature only generates journal online (http://​dx.​doi.​org/​ Results The 3-month smartphone-based training and hypotheses, which need to be further tested quanti- bmjopen-​2019-​030528). mentorship was perceived as an important and essential tatively for validity and generalisability. complementary process to further develop diagnostic Received 18 March 2019 ►► Larger-scale health services research would further and management competencies. Cervical imaging Revised 18 June 2019 provide important lessons for addressing this bur- provided peer-to-peer learning opportunities, and helped Accepted 20 June 2019 den in low-income and middle-income countries. better communicate the procedure to and gain trust of patients, provide targeted education, improve adherence and implement quality control. None of the patients had prior screening; they overwhelmingly accepted Introduction smartphone-based VIA, expressing no significant privacy Worldwide, cervical cancer kills around a issues. Neither group cited significant barriers to quarter of a million women annually, with the performing or receiving VIA at CHCs, the incorporation of majority in low-income and middle-income smartphone imaging and mentorship via text messaging. countries (LMICs).1–3 In sub-Saharan Africa CHNs were able to leverage their existing community (SSA), lack of access to proper screening and relationships to address a lack of knowledge and misperceptions. Patients largely expressed decision- treatment of precancerous lesions contributes making autonomy regarding screening. Negative views to high cervical cancer mortality.4–8 Visual © Author(s) (or their inspection of the cervix under acetic acid and stigma were present but not significantly limiting, employer(s)) 2019. Re-use and the majority felt that screening strategies were (VIA) is an effective screening method for permitted under CC BY-NC. No commercial re-use. See rights acceptable and effective. cervical cancer,9–20 but is not readily accessible and permissions. Published by Conclusions Our findings suggest the overall in most SSA countries.10 19 20 Periodic cervical BMJ. acceptability of this approach from the perspectives of all cancer screening using VIA conducted every For numbered affiliations see stakeholders with important promises for smartphone- 24 months by trained primary health workers end of article. based VIA implementation. Larger-scale health services has resulted in a 31% reduction in cervical research could further provide important lessons for Correspondence to cancer mortality over 12 years.21 Ghana’s addressing this burden in low-income and middle-income Dr Ramin Asgary; National Screening Programme recommends countries. ​ga263@​columbia.​edu VIA screening plus cryotherapy for women Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 1 Open access aged 25–4522 23; however, it has not been widely avail- Multiple smartphones were evaluated in a pilot assess- able due to an inability to integrate VIA into the primary ment for their quality of imaging, cost and ease of use. healthcare system.5 20 23 In Ghana, the Community-based The Samsung Duos was the best option available in Ghana Health Planning and Services (CHPS) programme has at the time of this study with reasonable image resolution, significantly improved access to primary care through ability to auto and manually focus, LED camera flash community health nurses (CHNs), who provide services at and battery life. A protocolised consistent approach to the district level in community health centres (CHCs).24 25 photography and image transfer was established and used A shortage of healthcare providers and comprehen- throughout. Training in effective photography of the sive training of low-level to mid-level healthcare workers cervix using smartphones and proper lighting and posi- in VIA contribute to the lack of VIA accessibility in tion of patient as well as the camera was provided during SSA.6 7 19 26–29 Additionally, maintaining competencies the in-person training. During the immediate feedback and accuracy of VIA are major challenges as the standard phase, for each patient, the CHN sent the best image short-term onsite VIA trainings may not guarantee skills captured to the mentor for feedback; this resulted in an retention.19 28 29 The addition of cervicography to VIA average of 11 images per CHN. has improved accuracy and diagnostic abilities,30–35 but Data collection and procedures its logistical barriers and cost have impeded large-scale Data collection included semi-structured individual availability for practitioners. The use of smartphones interviews conducted at the CHCs in either English or with digital cameras has presented the opportunity to a local Ghanaian language with a trained professional use smartphones for cervicography to enhance training interpreter. Nine CHNs participated in an additional of low- to mid-level health professionals, facilitate storage focus group. CHNs responded to 10 open-ended ques- of patient’s screening records, transfer images for expert tions with probes regarding attitudes, perceptions of opinion and re-train via text messaging.36–38 However, and experience with onsite training, cervical cancer acceptability and feasibility of smartphone-based VIA screening, smartphone imaging of the cervix, a 3-month have not been systematically evaluated and have impli- mentorship via text messaging, opinions on the feasi- cations for large-scale implementation. In a related 2016 bility of VIA/cervicography screening at CHCs and at the pilot study, the authors have demonstrated the impact of national level, and overall logistical barriers and further smartphone-based imaging and mentorship on improving recommendations (for interview tool, please see online and maintaining VIA diagnostic skills among CHWs.36 In supplementary file 1). Topics for the expert reviewer this study, we aimed to evaluate the perceptions and expe- and head nurse included logistical barriers, opportuni- riences of both CHNs who performed smartphone-based ties and experiences with VIA/cervicography training VIA/cervicography and women undergoing VIA/cryo- and mentorship. Patients were posed 10 open-ended therapy in CHCs in Accra, Ghana. questions with directing probes regarding knowledge, attitudes and experience with cervical cancer screening, VIA/cervicography or cryotherapy and imaging of the cervix using smartphones, privacy concerns, stigma and Methods perceptions of community members, and suggestions to Setting and study participants improve the screening programme (for interview tool, The catchment area for this study included 15 CHPS please see online supplementary file 2). Interviewers (RA demarcated zones in the Ga East Municipal of Greater and AN) had previously worked with CHNs in the CHPS Accra Region, Ghana, with a total of 30 CHNs. In 2015, programme, and had prior knowledge of the programme, 15 CHNs were recruited from two subdistricts (Dome working conditions and health system characteristics and Taifa) in collaboration with officials from the CHPS in the CHCs. At the beginning of each interview, it was programme. These CHNs, who had prior working knowl- made clear that the information from the participants edge of community and health resources, participated in would be deidentified with no direct link between inter- a 2-week onsite introductory VIA/cervicography training view data and participants’ identifying information so modelled after the JHIPEGO course used globally,39 plus that they could discuss their experience openly. All inter- 3 months smartphone-based mentorship for improving views were audiorecorded. Notes were taken by trained VIA diagnostic and management skills using imaging of interpreters, translated into English when needed and the cervix.36 We interviewed all CHNs (n=15) who partic- checked for interpreter accuracy. Informed consent was ipated in this study. They had 2 years of nurse training obtained from all participants. We clarified that partici- and were employed by the Ghana Health Service that pation would not affect participants in any negative way participated in this study. Additionally, we used prospec- and that they could withdraw answers or from the study at tive purposive and criteria sampling techniques to recruit any time and that non-participation would not adversely patient participants (n=21, of 169 screened) including affect participants. those of different ages, those receiving cryotherapy or further treatment (n=6), and from both CHCs. To trian- Data analysis gulate data, an expert reviewer and a head nurse were Data were analysed by two researchers (RA and HC) additionally interviewed. using a qualitative descriptive approach and content 2 Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 Open access analysis to identify core perceptions, experience and atti- that negative cases were easier. CHNs also agreed that tudes. We developed preliminary coding, performed crit- almost all patients understood when they were told to wait ical deliberation about initial codes and reviewed codes for the expert to confirm a potentially positive or negative for similarities and variations to assure a high level of case during mentorship period, as feedback was provided agreement. Codes fell into distinct but overarching cate- by the mentor either immediately or within 24 hours, gories. Reviewers independently reviewed and coded all depending on availability of the mentor. Another helpful transcripts, then met to review codes, discuss and iden- aspect of the 3-month training period was peer-to-peer tify concepts grouped into the specific categories and support from colleagues for diagnostic input. described and agreed on major important emergent Overall, the CHNs found smartphones easy to use for themes. The study was approved by the Noguchi Institute cervicography and sending photos to the mentor, and Institutional Review Board in Ghana as well as the IRB of experienced few logistical issues (such as issues with SIM New York University School of Medicine. cards, texting or network). Electricity outage was an occa- sional barrier which was largely addressable. Although Patient and public involvement some nurses had some initial difficulty with taking quality At early stage of this study, formal and informal discus- photos, the expert support helped to improve quality sions with patients and non-study staff of CHCs were held of images over time. CHNs elaborated that describing to better develop the research question and understand the process to patients and showing them their cervical the potential impact of research, and factor in their pictures made them more assured and comfortable with current experience and priorities to the extent they were screening. Almost all CHNs felt that smartphone-based relevant and possible. cervicography VIA is very easy to integrate into the screening process. Overall, nurses were proud of their work. They suggested a peer support network to discuss Results pictures and cases. Nurses overwhelmingly mentioned Average age for nurses was 28.2 years (SD, 2.9); 100% that they would appreciate having a certificate of training female. Average age for the patients was 33.8 years (SD, completion to mark their achievement and competency. 7); 69% were married or had partners; average age at first CHNs believed that more and more people will come to sexual intercourse was 20.1 years (SD, 4.1); average life- get screened because it has already received attention, and time sexual partners was 3.1 (SD, 2) and average number both information and acceptability seem to be increasing of living children 2.1 (SD, 1.6). Analysis of interviews in the community. Nurses believed that they are the most and focus groups with screening providers, patients and appropriate personnel to administer this service, espe- health staff revealed distinct but overarching themes. cially considering the sensitive nature of the procedure, and because of the familiarity and trust they have garnered Perception and experiences of community health nurses within communities. CHNs acknowledged that poten- Quotes supporting findings on the perceptions and expe- tial screening cost would be a barrier, and that assuring riences of CHNs can be found in table 1. CHNs viewed the screening was free of charge was important. They the onsite training and its format as effective and comfort- reported a general lack of knowledge of cervical cancer able. The majority reported that working with a combi- and screening as challenges to attracting patients. CHNs nation of the speculum, mannequins, real patients and reported that some patients believed that screenings were flashcards helped prepare them for actual screenings. unnecessary because they were asymptomatic. Other Although all agreed that learning the pelvic anatomy was barriers to convincing patients included anticipated pain interesting, some mentioned that classroom lectures were during the procedure, potential cost and fear of knowing not contextual, and that they learnt more working with about a positive screening result. CHNs reported that real patients. Majority stated that it was beneficial that the educating patients on cervical cancer and screening, and trainer taught them how to use the speculum, take photos its importance in preventing cancer helped overcome and do the gynaecology exam. Largely, nurses did not these barriers. CHNs also relied on their existing trusting feel that financial incentives were needed to encourage relationships with patients to encourage screening. They learning. felt that most patients accepted undressing for the exam, Overwhelmingly, they agreed with adequacy of 3 months with some patients comparing the nudity to the experi- mentorship and emphasised the importance of having ence of childbirth. CHNs reported that their patients had a back-up expert to further interpret the images and minimal privacy concerns with having their cervix photo- mentor them after the initial onsite training. Although graphed, since the picture was anonymous and viewed some CHNs expressed anxiety about performing the only by the patient, nurse and the expert reviewer. screenings, almost all agreed that having expert support Overwhelmingly, nurses did not face any major made them and the patients feel more confident during technical challenges in performing VIA. A minority the process and that the expert reviewer’s responsiveness mentioned that it was difficult at times, but manageable, and individualised support improved their competency. to find the actual cervix. Logistical challenges included Most CHNs elaborated that seeing positive VIA cases was the cost of transportation, both for patients and CHNs; very important and was integral in learning, but all agreed at times, securing a steady supply of equipment and Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 3 4 Table 1 Experiences and perceptions of CHNs, smartphone-based VIA cervical cancer screening, Accra, Ghana, 2015 Theme Quote Perceptions and experiences regarding onsite training and smartphone-based mentorship  In-person training perceptions “During the training because of the way our teacher taught us, the whole thing, I became very much confident that when it comes to screening a client it wouldn’t be difficult for me because from the beginning we learnt about the theory and as the Open access time went on we learnt about the practical. At least I had the chance during a day to screen about three to four clients by the end of the program (so) I was very much confident to screen clients for cervical cancer” [CHN3]. “…the theory was a bit in a haste, I didn’t understand what (the lecturer) was saying and that was my first time of hearing those big big words but when I got to the practical stage I understood” [CHN6]  Importance of 3-month support period “That one it has been very much helpful to us because there’re some cases that you will see them to be positive or sometimes you will see them to be negative but when you communicate with them (mentors) you will see that sometimes the feedback or the answer they give you is quite different from what you see… after we communicate with them (mentors) sometimes they freshen our memories on what we learnt so far so that you will be able to know (why) that that this is also a positive or a negative so communicating with them has been very good.” [CHN7]  Importance of exposure to positive “…when we went for the training and we came back, it wasn’t easy to locate the SC junction and those things so for the first cases in learning one month it was very perfect that we had to send the pictures to them, there were sometimes that we misjudged, for instance I had a client within that month from the first month I thought she was negative but then when I sent the picture to (mentor) she said she is not negative but positive…I didn’t see the pre-cancerous there like the way I was expecting to see but then she was able to let me see it that the person was positive so it was good that they were there to correct us before we got used to the whole thing.” [CHN7]  Adequacy of 3-month training time “More benefits because at least I had the opportunity to train on cervical cancer and even though I may not know many things about it at least I have gotten the opportunity to know certain things about cervical cancer, I can conduct screening without any support from any facilitator, it’s a big plus for me.” [CHN4]  Peer-to-peer support and feedback “I call some of my colleagues to help me…I will tell them I got negative so come and check, the person too will come and check, we do collaborative work we don’t do it alone, with the help of our colleagues its ok.” [CHN6] Perceptions and experiences with using smartphone for VIA screening  Comfort with smartphone imaging “It was very much comfortable and it was good for the clients because we made the clients aware that…we will take a picture and send it to our (expert) for them to confirm on the results that would come… (and) we made it clear to them that we would take a picture and allow them to see how their cervix is looking like so working with the smart phone has been very very good.” [CHN3]  Dealing with technical challenges for “…at first when we were taking the pictures it was somehow challenging so we just told our facilitator and she told us to zoom smartphone use and take the picture so when we started doing that it was ok.” [CHN4] Views on the feasibility of implementation within national programme (CHPS)  Feasibility of continuing programme “It is possible because even now people are still asking, we give talks on it, and even after this three months we give talks, before then when we started we were finding it difficult to get the clients in doing it but after we’ve got some of them they also sent the information to others” [CHN2] Nurses’ views and experiences regarding acceptance and comfort of screening by patients  Lack of perceived susceptibility as a “…you are not feeling sick and nothing is wrong with you and somebody just comes and says that it is harmful it can cause this challenge to recruitment for screening and that while she knows that she is not sick so it wasn’t easy that way so you have to convince and convince before they will accept it that way” [CHN2] Continued Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 Table 1 Continued Theme Quote  Education to overcome lack of “…it was very difficult and some too were afraid that eeeiii what if I go and they tell me that I have cancer what am I going to knowledge and fear of screening results do? So that fear was there but the education that we gave them we managed to bring them (in)” [CHN1]  Importance of existing relationships “It depends on the relationship we have with them, for the churches that we went to, my church per se I have been with them with patients all the time so after I gave them the talk they were like ok and they received the (cervical) screening…” [CHN7]  Minimal privacy concerns “(patients think) even if someone sees the picture of the cervix they wouldn’t know that it is you” [CHN7] Technical, logistical and financial challenges during VIA screening  Challenges conducting the procedure “For me (it) would be finding the cervix, some of them immediately you enter you find the cervix some too you suffer, some you screening have to try, push side and side before you get the cervix” [CHN2]  Logistic challenges conducting the “…you know the speculum we have different sizes, there was a time I was about to do a screening and I couldn’t get a screenings speculum, all those around were small so I had to go to the other facility and get it from there and explain things to my client and ask her to go home and call her back the next day” [CHN6]  Patients lost to follow-up “I will say some are very difficult bringing them here, when we even call them they will say I will come but at long last they don’t come.” [CHN1] Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528  Importance of screening as a free “…it was free to them but now when we start doing it as part of our duty then it means the speculum and other things they service would have to pay for it so it will be a bit of a challenge” [CHN3]. Overall feedback and suggestions to improvement  Pride in ability to provide screenings “It was rewarding, being able to do it alone and then knowing that I was able to do (it), I was able to identify whether the person was negative or positive before showing it to my supervisor and the supervisor too will check and say its negative, you did a great job, its rewarding.” [CHN6]  Certificate of completion “…we need to get certificate to prove to people because there are some educated people when they come to do the screening they expect to see something that shows that you are really trained to do the screening on them.” [CHN3]  Suggestion to use mass media for “Making the community know about the cervical cancer screen so creating awareness with the information … I think it will help, education telling them what it is.” [CHN4] “the education must be mass as in nationwide in the media and all this.” [CHN1]  Suggestion to expand screenings to “…provide us with logistics …like the beds for the cervical cancer screening…all the bed were normal beds so it wouldn’t be community-based locations easy for our clients to lie down for the procedure…at our weighing centers, where we do our weighing so that we will just clean the place small for privacy and then do the cervical cancer for our nursing mothers because all of them really love to do it…” [CHN3]  Suggestion to add additional chronic “…anytime we go into the community it is health education, health education so the community members are expecting us to disease screenings do something practical to help them like checking their BP and other things and they are expecting all of these things to be free so actually we also would love to provide them with all these services (blood pressure and checking sugar).” [CHN3] Numbers indicate the specific nurses. CHN, community health nurse; CHPS, Community-based Health Planning and Services; VIA, visual inspection with acetic acid. Open access 5 Open access resources; the quality of equipment including exam beds Perception and experiences of patients and the relatively small size of the screening area which Largely, both patients who were screened negative and posed minor challenges to maintaining patient privacy. those who were screened positive and received cryotherapy Commonly used medical exam beds were available in shared similar perceptions and experiences. Quotes all facilities or mobile units. Lighting was supported from patients exemplifying each theme are presented in by stationery medical exam lamps. Bedsheets, gloves, table 2. None of the patients, including the cryotherapy and other supplies and materials for screening were all patients, had ever been screened before, and most had part of usual supplies in the clinics/health facilities and no prior knowledge of cancer or screening. For the few used based on Ghana’s Ministry of Health recommen- with some prior knowledge, past exposure included TV or dations for infection control and OBGYN exam. Smart- radio, or informal information from nurses when visiting phones had flashlights and were used for photography health facilities on unrelated occasions. Only a small in a protocolised fashion developed for this study. None number of patients understood the concept of screening, of the CHNs perceived transport time as a barrier for prevention and the importance of knowing ones’ disease patients; however, the transportation cost was among the status. Many expressed misconceptions, either their own most common reasons women missed screening appoint- or beliefs they had heard from others. One patient elabo- ments. Almost all CHNs agreed that paying for trans- rated on misconceptions, sharing her belief that cervical portation would improve the screening process. CHNs cancer is caused by inserting things into the vagina. Other suggested ways to improve awareness and education by misconceptions about screening included worrying making announcements through radio, TV, newspapers about being ‘clean’ or ‘neat’ enough to be screened or and social media. To improve patient screening partici- that nurses would put their hands inside patients. Most pation, they suggested going door-to-door, and reaching patients did not discuss the screening with anyone, and out to local churches. They also indicated the need for decided to participate in the screening on their own. both nationwide education and community mobilisation. Only a few asked partners for approval and the majority Other improvements of the experience included access reported that their husbands or partners supported their to equipment for screening such as better quality, sturdier decision. They elaborated that some men did not think exam beds; offering screenings at opportune times like the screening was relevant to them; however, most, but when women are at health centres for other reasons, or not all, men in the community support screening. A few screening in the community. They suggested expanding said that some men had issues with it but generally if screening services to include breast cancer, diabetes and women decided to get screened, then they could find a blood sugar levels, hepatitis B and hypertension. Several way without their partner’s approval. mentioned a recent reduction in previous services due to Most patients appreciated cervical photography and a lack of funding, emphasising the importance of keeping wanted to see the picture of their own cervix. For many, the photos helped answer their questions and, for some, these services free to the public. it reassured them about the procedure. Some women wanted to take their cervical images to show to their part- Perceptions and experiences of the nurse supervisor and ners or keep as a record. Therefore, if and when patients expert reviewer requested to have their cervical digital images and had Both the supervisor and expert reviewer generally a smartphone, providers allow them to take the picture agreed with CHNs regarding the appropriateness of the or transferred images securely to the patient’s smart- training and its incorporation and adequacy of both phone. These images were all deidentified and anony- theoretical and practical trainings. They added the mised. Printing images was not possible or provided. Due need to reduce the size of the training groups in order to the anonymity, the majority were comfortable with to provide more personalised attention to each training having pictures taken. Only one patient had questions during the initial onsite sessions (groups of 6–7 rather and requested reassurance about potential sharing of her than 15–20). This would also allow the trainer to iden- images on the internet. Most others trusted the CHNs tify and provide targeted attention to different trainees. and understood and agreed with the process of smart- The expert reviewer did not cite any logistical challenges phone-based VIA. Patients were generally appreciative with receiving and sending images and mentoring and of CHNs’ persistence in educating them and addressing providing feedback. Actually, the reviewer spent some misunderstandings and misconceptions through time helping a few CHNs improve the quality of their describing the screening process, cancer detection photos but she did not find this a significant challenge. and treatment, and relaying the importance of preven- She found the process very rewarding and elaborated on tion. Some patients mentioned that the CHNs showing the importance of providing 3-month remote mentor- pictures of cancerous lesions and describing risk factors ship to help advance and further polish CHNs’ diagnostic for cervical cancer was often effective in encouraging skills as a more practical training that complemented screening. The majority of patients reported little or no classroom exposure. This in turn improved the reviewer stigma from relatives or community members for getting confidence regarding the competence of CHNs and screened. Although most patients stated that a large screening quality. number of women in the community support screenings, 6 Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 Table 2 Patient quotes on their perceptions and experiences, smartphone-based VIA cervical cancer screening, Accra, Ghana, 2015 Theme Quote Knowledge and attitude regarding cancer and screening and health decision-making process  Lack of prior knowledge “…when I heard about the disease at that time I did not take it seriously because I did not really understand it very well but when the nurse came to explain then I knew how important it was to go for the screening.” [SP6] Even though I heard about it I was not scared of it because when I started life as a young lady I did not insert those things that people put into their private part and I did not do those rough things. So even though I heard about it I never went to check or screen.” [SP2]  Low education levels “Where I live, most of the people there have low educational background so I think they don’t (know) much about health so maybe for them if they experience any problem in their private part they can grind pepper and insert it there and (for) such people it is not easy to convince them to come for this screening.” [SP5]  Misperceptions about screening “In fact it was not easy convincing them (other women) because some of them were saying that when you go they will be inserting hands in their vagina and others were saying all sorts of things so I told them that when I went I did not experience that.” [SP2] “she (another woman in community) was saying if she comes they will say this today and that tomorrow and she does not know what they will be inserting into her” [SP5]  Support of partners for “Well, I explained to the man I live with about the screening but I had decided to do the screening already so when I explained it to him screening too he said it was good so I should come and do it so that if they give medicine I can also get some.” [SP4]  Support of men in the “…the day the nurse was telling me about the screening, there was a man there and he was even more interested in listening to what community for screenings the nurse had to say and he even said he will tell his wife and sister to go for the screening” [SP6] Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528  Appreciation for effort of CHNs “Well she educated me, first of all she explained to me what cervical (cancer) is and how it is contracted…and she explained to me how everything is going inside. I was asking a lot of questions so she kept explaining to me.” [SP3]  Photos as an educational tool “…When they came to my workplace they showed the picture to us, I mean to the nursing mothers as well telling them how the disease looks like, so it was the pictures that I saw that got me scared so I decided to come for the screening.” [SP7]  Shyness as barrier to screening :“…they (other women) support it but it is just that some of them are shy.” [SP13] Patients’ expectations and experiences of screening and logistical barriers  Importance for preventing “…you can see that it is dangerous, I saw the pictures. If you have this infection (disease) how will you know, so if they are able to cancer fatality check and see if you have the disease and they cure it for you then it is good and if they check and they see that you don’t have it then you can protect yourself. So it will be good if it is detected early rather than you will wait till the disease becomes worse when nothing can be done about it.” [SP2] “…even though the time they did the screening I had to go to work I decided to use that time to come…because I wanted to know if I had the cancer or not.” [SP12]  Trust for CHNs “I did not have any expectations and I also trust the nurse who came to inform me about the screening.” [SP1].  Screening was less complex “I thought that when I come they were going to do an operation or something of that sort before they can see it but when I came they than expected said it was not like that, they made me lie down and they put under me and took a picture of it and showed it to me” [SP15] “as for me when they say they want to look at the mouth of the womb I think (hahahahah) they will remove it and wash and then they can see if it has a disease or not so that is what I think…” [SP2].  Minor discomfort “I was ok I did not experience any discomfort, it was just a little bit painful but later it was ok.” [SP15]  No cost as a motivator “…when she said the screening is free I decided to come” [SP2]  Importance of improving “I think that the announcement and awareness should be more, because the nursing mothers they came to speak to, at my workplace, awareness are just a few women so they should speak to a lot of people so that they can also come for the screening.” [SP11] Continued Open access 7 Open access some alluded that barriers included embarrassment “it was ok, the time, she came on Saturday it was ok because if she had come within the week I would not have been able to come but “I was ok with it because she has to do it and that is her work, you are a woman when you go for consultation you need to be free and or shyness and low health literacy. While some women Because I have to see it myself, if I don’t see it I may say she is telling lies because I have been to a number of places and they say I discussed misconceptions in their community regarding “…if she does not take a picture of it how would she know if I have the disease or not and how will she be able to show it to me? the procedure itself, most clients were optimistic that more men and women would support the screening if they were educated more about the procedure. let the person do her work so that she will know what is happening to you so I wasn’t having any problem with it.” [SP3] Majority of clients had no specific expectations of the screening prior to their procedure, and they largely trusted the CHNs as health professionals. Overall, clients found it easier, shorter, and less painful than expected. Some expected a much more complicated or painful procedure such as that the uterus to be taken out and washed and inspected. Although a few experienced initial discomfort, it was often relatively minor and short-lived. None of the clients had any significant logistical barriers during the screening. A few mentioned issues with trans- port cost, the majority thought that screening time was reasonable, and appreciated the screening being free. Some clients skipped work to be screened. Majority of clients were happy with the screening, and did not offer any specific recommendations for improvement. Some clients inquired about and suggested providing breast cancer screening. Most of them acknowledged it was important to have more announcements and awareness, in one case suggesting that nurses go house to house in order to educate people. Individual women who received cryotherapy after screening positive through VIA cited positive experiences with the process and did not report any specific privacy issues, or additional pain or discom- don’t have any problem but I don’t see it.” [SP15] fort or logistical barriers. the time she came it was favorable.”[SP1]. Discussion Cervical cancer screening using VIA and smartphone was highly accepted by the clients, none of whom had “I was very comfortable.” [SP5] prior screening, and by CHNs who were performing this screening for the first time. Neither group cited signif- CHN, community health nurse; VIA, visual inspection with acetic acid. icant barriers to receiving or performing VIA at CHCs, Cervicography and smartphone-based VIA, and cryotherapy the incorporation of smartphone imaging, the process SP indicates patients; numbers indicate the specific patients . of mentorship via text messaging, privacy or confiden- tiality, or other issues with stigma or logistical barriers. Some barriers to screening cited by both clients and CHNs closely resembled those of patients in more devel- oped regions, such as fear, embarrassment or lack of Quote knowledge or awareness.40 The training, including initial on-site and subsequent mentorship using smartphone imaging and texting, was very well received. The 3-month  Smartphone as a reassurance mentorship was an important and effective complemen-  Experience of cryotherapy tary training to further develop and enhance the needed competencies. Both CHNs and their trainer and super-  Trust of providers and visor regarded the didactic and practical components of Continued the onsite training as interrelated and vital to its effec- professionalism tiveness. CHNs found the training to be empowering and welcomed the opportunity to learn a new skill, and the opportunity to provide additional services to women in Table 2 Theme their catchment areas. The importance, value and syner- gistic effect of having continuous diagnostic support in the first 3 months was essential. Smartphone-based 8 Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 Open access imaging provided opportunities to see and discuss cases were generally not significant barriers. Despite important that they did not see during their initial training such as misinformation regarding the causes of cancer and side identifying more positive or complicated cases,36–38 and effects of the screening, the majority felt that screening provided the opportunity to revisit images and discuss strategies were acceptable. difficult cases with colleagues, all of which facilitated CHNs were generally satisfied with conducting the learning. Discussing images with the mentor further rein- screening, felt empowered and gained more confidence forced clients’ trust, and clients overwhelmingly accepted in their capacities, and saw their efforts as a meaningful smartphone-based imaging, had no significant privacy component of their jobs. Nurses were keen to be certi- issues and felt more reassured of the procedure. fied and considered that an important factor for career The possibility to discuss and learn from their own development but also to further gain confidence and experience, and individualised support and mentorship trust from clients. All CHNs who participated in this during this 3-month period improved competency and project were women and had experience providing basic confidence in managing their clients. Adult learning maternal and child care and health education to resi- theory describes the main mechanisms by which adults dents of their respective catchment areas. Strong prior learn skills when they relate to daily activities and working relationships with clients and perhaps their gender responsibilities, learning is hands-on and takes place seemed to foster an ease of the process and better over time, there are peer-to-peer learning opportunities convince clients for screening, and helped address issues and there are possibilities to ask for and receive targeted feedback related to their cases/questions as opposed of privacy and sensitivity. Equally important compared to learning in classroom settings.41 42 The use of smart- with knowledge and attitude is trust of providers, which phones provided a likely unmatched opportunity to could ultimately encourage clients to make the deci- connect new providers to peers and senior providers, and sion regarding seeking care especially screening for improved access to case-by-case learning. This important asymptomatic conditions.5 CHNs were able to leverage mentorship component has been largely missing from their existing relationships and their own persistency widespread standard VIA trainings.43 There were addi- to address a significant lack of knowledge regarding tional important and unanticipated benefits of photog- cancer and screening. Women had other barriers and raphy including using photos to better communicate competing priorities such as cost of transport, time with clients about the procedure and gain more trust, constraints and childcare responsibilities. These were further provide targeted health education regarding often locally managed by women and CHNs working sexual and reproductive health, and implement some together, and providing some transportation support form of quality control. The ease of using smartphones to clinics for the procedure. Other logistical barriers and the lack of serious logistical barriers were important such as screening supplies were generally managed findings on feasibility from the perspective of all stake- by existing resources at the centres. Having screening holders, and highlight the potential of smartphones and free of charge was an important factor and needs to be mentorship in improving quality, accuracy and efficacy of factored in for implementation strategies. VIA.36–38 Smartphone imaging could be used to further Clients and CHNs had some suggestions to improve the create a peer-support network such as a virtual journal experience including providing more and better-quality club to reinforce peer learning and support, which could facilities and mobile clinics at churches or in the commu- be used as a measure for quality control. There is also nity to bypass transport to clinics. However, this needs the potential for better effectiveness of VIA strategies to be balanced to ensure that quality is not impacted by through improving adherence and acceptance by clients mobile units. CHNs generally felt positively regarding the due to better understanding of the procedure, addressing feasibility of incorporating VIA screening into existing misconceptions among clients and their partners and services as a long-term strategy. Clients requested addi- possibility for medical record keeping by clients. tional screening programmes such as breast cancer, which The majority of clients had no, or very little, prior knowl- was also suggested (with hypertension and diabetes) and edge about cervical cancer or screening. The availability deemed feasible by CHNs. Although CHNs felt that they of and persistence of CHNs, from their own communities, in providing basic education about the disease, screening were quite capable and proud of providing the screening and addressing existing misconceptions were essential in to women in their community, they expressed some ultimately encouraging women to get screened. Although scepticism regarding funding for maintaining screening there were important misconceptions, fear of screening programmes. At the national level, priority setting should or its results, and some stigma, clients were receptive include a balance between the cost and outcomes and and communicated the overall benefits for themselves competing programmes. All these findings may have and others. Women largely seemed to express autonomy implications for VIA screening strategies and their about decisions regarding screening and they were able implementation into regular health system services at to manage any potential opposition by their partners the primary care level as opposed to vertical or targeted without assistance. Negative views and stigma on the part services at tertiary care centres or flash mass screening of others (men or women) were not uncommon but programmes. Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 9 Open access 7 Limitations Obstetrics and Gynecology, Korle-Bu Teaching Hospital, Accra, Ghana Our study was not without limitations. Although the CHPS programme in Ghana was based on previous service Acknowledgements The authors extend their appreciation with special thanks to CHCs staff, translators, CHIPS staff and Ghana University School of Public Health delivery models from rural areas, the two pilot study areas for their contribution to the implementation and success of this project. This study were part of an expansion of the programme, in which received partial funding through Global Health Challenge Fund from New York the model was adapted to peri-urban and urban areas. University Global Institute of Public Health. Thus, findings may not be generalisable to rural areas, Contributors RA and HC made substantial contributions to this study including particularly given differences by region in access to social conception and design, analysis and interpretation of data, technical and material support and supervision, drafting and critical revision of the manuscript for and healthcare resources. As this evaluation was a pilot important intellectual content, and the approval of final version of the manuscript. study to evaluate the effectiveness of using mHealth strat- PA and RAd made substantial contributions to this study including conception and egies to extend and improve training in VIA to CHNs, design, technical and material support and supervision, critical revision of the additional challenges may be associated with scaling up manuscript for important intellectual content, and the approval of final version of the manuscript. AN, EM and AAA made substantial contributions to this study such an intervention to larger areas. Additionally, there including data collection and technical and material support and supervision and is a possibility of bias towards acceptability of the inter- the approval of final version of the manuscript. HB made contribution to the analysis vention. However, we included all CHNs in two facilities and interpretation of data and the final approval of the manuscript. rather than relying on a self-selected sample, and patients Funding This study was partially funded by the New York University Institute of were recruited using criteria sampling. We also included Global Health, Global Health Challenge Fund. all clients who received cryotherapy to explore their views Competing interests None declared. towards the screening and treatment strategies. Finally, Patient consent for publication Not required. this qualitative study by its nature only generates hypoth- Ethics approval This study was approved by the Noguchi Institute Institutional eses which need to be further tested quantitatively for Review Board in Ghana as well as New York University School of Medicine (Protocol validity and generalisability. Nevertheless, we were able # s14-01466). to observe existing community perceptions through the Provenance and peer review Not commissioned; externally peer reviewed. lens of participating patients and nurses as they were also Data sharing statement All data relevant to the study are included in the article or asked and subsequently elaborated on views and percep- uploaded as supplementary information. tions from their own community different or consistent Open access This is an open access article distributed in accordance with the with that of their own. Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use Conclusions is non-commercial. See: http://​creativecommons.​org/​licenses/​by-​nc/​4.​0/. Our findings indicate overall acceptability and ease of implementing smartphone-based imaging for VIA and training and mentorship of mid-level health personnel for cervical cancer screening. Anticipated barriers, such as concerns for privacy and confidentiality, knowledge References 1. Farley J, Shin HR, Bray F, et al. Estimated Cancer Incidence, Mortality and attitude gaps, fears and misconceptions and logistical and Prevalence Worldwide in 2012, France: International Agency for challenges were largely minimal or manageable. The use Research on Cancer. Lyon, France: World Health Organization, 2012. Available: http://​globocan.​iarc.​fr/​Default.​aspx [Accessed 26 Aug of smartphone imaging provided unexpected benefit as 2017]. an educational tool to increase patients’ adherence and 2. Ginsburg O, Bray F, Coleman MP, et al. The global burden of improved VIA training for CHNs by providing mentor- women's cancers: a grand challenge in global health. Lancet 2017;389:847–60. ship and peer-to-peer education opportunities. Overall, 3. Sankaranarayanan R, Ferlay J. Worldwide burden of gynaecological and especially for more remote areas, there are important cancer: the size of the problem. Best Pract Res Clin Obstet Gynaecol 2006;20:207–25. promises for quality improvement and effectiveness of 4. Forman D, de Martel C, Lacey CJ, et al. Global burden of human smartphone-based VIA screening and its implementation. papillomavirus and related diseases. Vaccine 2012;30(Suppl Further and complementary context-based implemen- 5):F12–23. 5. Ghana Demographic and Health Survey 2008. In: Accra, Ghana: tation research is needed to appropriately test smart- Ghana Statistical Service (GSS), Ghana Health Service (GHS) and ICF phone-based imaging for scale-up efforts and addressing Macro, 2009. 6. Hoppenot C, Stampler K, Dunton C. Cervical cancer screening the cervical cancer burden in LMICs. in high- and low-resource countries: implications and new developments. Obstet Gynecol Surv 2012;67:658–67. Author affiliations 7. Ditzian LR, David-West G, Maza M, et al. Cervical cancer 1 Global Health, George Washington University Milken Institute of Public Health, screening in low- and middle-income countries. Mt Sinai J Med 2011;78:319–26. Washington, District of Columbia, USA 8. Handlogten KS, Molitor RJ, Roeker LE, et al. Cervical cancer 2 Medicine, Weill Cornell Medical College, New York, NY, USA screening in Ghana, west Africa: prevalence of abnormal cytology 3 Environmental Science and Technology, Autonomous University of Barcelona and challenges for expanding screening. Int J Gynecol Pathol Barcelona Catalunya Spain, Barcelona, Spain 2014;33:197–202. 4 Social and Behavioral Sciences, University of Ghana School of Public Health, Accra, 9. Denny L, Kuhn L, Pollack A, et al. Evaluation of alternative methods of cervical cancer screening for resource-poor settings. Cancer Ghana 5 2000;89:826–33. Population, Family and Reproductive Health, University of Ghana School of Public 10. Miller AB, Sankaranarayanan R, Bosch FX, et al. Can screening for Health, Accra, Ghana cervical cancer be improved, especially in developing countries? Int 6 Dean, University of Ghana School of Public Health, Accra, Ghana J Cancer 2003;107:337–40. 10 Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 Open access 11. Fokom-Domgue J, Combescure C, Fokom-Defo V, et al. Performance 27. Odoi-Agyarko H. Profile of Reproductive Health Situation in Ghana. of alternative strategies for primary cervical cancer screening in sub- Accra: World Health Organization, Country Office Ghana, 2003. Saharan Africa: systematic review and meta-analysis of diagnostic 28. Mwanahamuntu MH, Sahasrabuddhe VV, Kapambwe S, et al. test accuracy studies. BMJ 2015;351:h3084. Advancing cervical cancer prevention initiatives in resource- 12. Nessa A, Hussain MA, Rahman JN, et al. Screening for cervical constrained settings: insights from the Cervical Cancer Prevention neoplasia in Bangladesh using visual inspection with acetic acid. Int Program in Zambia. PLoS Med 2011;8:e1001032. J Gynaecol Obstet 2010;111:115–8. 29. Sherigar B, Dalal A, Durdi G, et al. Cervical cancer screening by 13. Firnhaber C, Mayisela N, Mao L, et al. Validation of cervical cancer visual inspection with acetic acid—interobserver variability between screening methods in HIV positive women from Johannesburg South nurse and physician. Asian Pac J Cancer Prev 2010;11:619–22. Africa. PLoS One 2013;8:e53494. 30. Bomfim-Hyppólito S, Franco ES, Franco RG, et al. Cervicography 14. Huchko MJ, Sneden J, Zakaras JM, et al. A randomized trial as an adjunctive test to visual inspection with acetic acid in cervical comparing the diagnostic accuracy of visual inspection with acetic cancer detection screening. Int J Gynaecol Obstet 2006;92:58–63. acid to Visual Inspection with Lugol's Iodine for cervical cancer 31. Firnhaber C, Mao L, Levin S, et al. Evaluation of a cervicography- screening in HIV-infected women. PLoS One 2015;10:e0118568. based program to ensure quality of visual inspection of the cervix 15. Basu P, Mittal S, Banerjee D, et al. Diagnostic accuracy of VIA in HIV-infected women in Johannesburg, South Africa. J Low Genit and HPV detection as primary and sequential screening tests in a Tract Dis 2015;19:7–11. cervical cancer screening demonstration project in India. Int J Cancer 32. Cronjé HS, Cooreman BF, Beyer E, et al. Screening for cervical 2015;137:859–67. neoplasia in a developing country utilizing cytology, cervicography 16. Huchko MJ, Sneden J, Sawaya G, et al. Accuracy of visual and the acetic acid test. Int J Gynaecol Obstet 2001;72:151–7. inspection with acetic acid to detect cervical cancer precursors 33. Cremer M, Jamshidi RM, Muderspach L, et al. Digital camera among HIV-infected women in Kenya. Int J Cancer 2015;136:392–8. assessment for detection of cervical intraepithelial neoplasia in rural 17. Qiao L, Li B, Long M, et al. Accuracy of visual inspection with acetic El Salvador. Int J Gynaecol Obstet 2005;91:42–6. acid and with Lugol's iodine for cervical cancer screening: Meta- 34. Mwanahamuntu MH, Sahasrabuddhe VV, Blevins M, et al. Utilization analysis. J Obstet Gynaecol Res 2015;41:1313–25. of cervical cancer screening services and trends in screening 18. Mustafa RA, Santesso N, Khatib R, et al. Systematic reviews and positivity rates in a 'screen-and-treat' program integrated with HIV/ meta-analyses of the accuracy of HPV tests, visual inspection AIDS care in Zambia. PLoS One 2013;8:e74607. with acetic acid, cytology, and colposcopy. Int J Gynaecol Obstet 35. Parham GP, Mwanahamuntu MH, Pfaendler KS, et al. eC3--a modern 2016;132:259–65. telecommunications matrix for cervical cancer prevention in Zambia. 19. Moon TD, Silva-Matos C, Cordoso A, et al. Implementation of J Low Genit Tract Dis 2010;14:167–73. cervical cancer screening using visual inspection with acetic acid in 36. Asgary R, Adongo PB, Nwameme A, et al. mHealth to Train rural Mozambique: successes and challenges using HIV care and Community Health Nurses in Visual Inspection With Acetic Acid treatment programme investments in Zambézia Province. J Int AIDS for Cervical Cancer Screening in Ghana. J Low Genit Tract Dis Soc 2012;15:17406. 2016;20:239–42. 20. Hill AG, Darko R, Seffah J, et al. Health of urban Ghanaian women 37. Yeates KE, Sleeth J, Hopman W, et al. Evaluation of a Smartphone- as identified by the Women's Health Study of Accra. Int J Gynaecol Based Training Strategy Among Health Care Workers Screening for Obstet 2007;99:150–6. Cervical Cancer in Northern Tanzania: The Kilimanjaro Method. BMJ 21. Shastri SS, Mittra I, Mishra GA, et al. Effect of VIA screening by Open 2015;5:e005828. primary health workers: randomized controlled study in Mumbai, 38. Sharma D, Rohilla L, Bagga R, et al. Feasibility of implementing India. J Natl Cancer Inst 2014;106:dju009. cervical cancer screening program using smartphone imaging 22. Ministry of Health. National Strategy for Cancer Control in Ghana: as a training aid for nurses in rural India. Public Health Nurs 2012-2016. Available: http://www.​iccp-​portal.​org/​sites/​default/​files/​ 2018;35:526–33. plans/​Cancer%​20Plan%​20Ghana%​202012-​2016.​pdf 39. Gaffikin L, Blumenthal PD, Emerson M, et al. Safety, acceptability, 23. Blumenthal PD, Gaffikin L, Deganus S, et al. Cervical cancer and feasibility of a single-visit approach to cervical-cancer prevention prevention: safety, acceptability, and feasibility of a single-visit in rural Thailand: a demonstration project. Lancet 2003;361:814–20. approach in Accra, Ghana. Am J Obstet Gynecol 2007;196:407. 40. Gesink D, Filsinger B, Mihic A, et al. Cancer screening barriers and e1–407.e9. facilitators for under and never screened populations: A mixed 24. Ghana Health Service. Community Health Planning and Services methods study. Cancer Epidemiol 2016;45:126–34. (CHPS): The Operational Policy, 2005. Available. http://www.​ 41. Taylor DC, Hamdy H. Adult learning theories: implications for learning expandnet.​net/​PDFs/​HP25.​pdf and teaching in medical education: AMEE Guide No. 83. Med Teach 25. Nyonator FK, Awoonor-Williams JK, Phillips JF, et al. The Ghana 2013;35:e1561–72. community-based health planning and services initiative for scaling 42. Brookfield SD. Understanding and Facilitating Adult Learning; up service delivery innovation. Health Policy Plan 2005;20:25–34. A comprehensive Analysis of Principles and Effective Practices. 26. Sanghvi H, Limpaphayom KK, Plotkin M, et al. Cervical cancer Buckingham, UK: Open University Press, 1996. screening using visual inspection with acetic acid: operational 43. University of Zimbabwe/JHPIEGO Cervical Cancer Project. Visual experiences from Ghana and Thailand. Reprod Health Matters inspection with acetic acid for cervical-cancer screening: test 2008;16:67–77. qualities in a primary-care setting. Lancet 1999;353:869–73. Asgary R, et al. BMJ Open 2019;9:e030528. doi:10.1136/bmjopen-2019-030528 11