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Background Sickle cell disease (SCD) is one of the most frequent and traumatizing genetic disease in Uganda, with the prevalence of the sickle cell trait (SCT) estimated at 13.3% leading to serious psycho-social and economic impact on the patients and their families.
Aim This study aimed to determine the burden of SCT and factors influencing the uptake of screening services among secondary school students in Uganda.
Methods We used an analytical cross-sectional design with a multi-stage sampling approach. A total of 399 students from four secondary schools in Kampala City were enrolled in this study. Data were gathered using semi-structured questionnaires and blood screening. We used the sickling test to determine the presence of sickle cell alleles among the participants and hemoglobin electrophoresis as a confirmatory test. Data gathered using the questionnaire were analyzed using descriptive and inferential statistics.
Results In total, 5.8% of participants who were tested during this study had SCT. Most (80.2%) participants were not in an intimate relationship at the time of data collection. The majority (60.4%) had moderate knowledge about SCT screening and obtained information about screening from the school. Only 29 (7.3%) participants knew of a family member with sickle cell. Overall, participants had a negative attitude toward SCT screening (67%), although 41.6% believed that most people who were sickle cell carriers did not live long and were often sick. Statistically significant associations were found between testing for SCT and knowing a partner’s sickle cell status (odds ratio [OR] 2.112, p = 0.043) and Anglican religion (OR 2.075, p = 0.047).
Conclusion Despite the moderate level of knowledge and negative attitudes, a relatively large number of participants had SCT. This highlights the need for a comprehensive health education package targeting adolescents to promote SCD/SCT screening

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eCommons@AKU School of Nursing & Midwifery, East Africa Faculty of Health Sciences, East Africa 1-19-2024 Prevalence of sickle cell trait and needs assessment for uptake of sickle cell screening among secondary school students in Kampala City, Uganda Shamim Namukasa Sarah Nakaziba Grace Among Lydia A sasira Posiano Mayambala See next page for additional authors Follow this and additional works at: https://ecommons.aku.edu/eastafrica_fhs_sonam  Part of the Communication Sciences and Disorders Commons, Maternal, Child Health and Neonatal Nursing Commons, Public Health and Community Nursing Commons, and the Public Health Education and Promotion Commons Authors Shamim Namukasa, Sarah Nakaziba, Grace Among, Lydia A sasira, Posiano Mayambala, Joseph Atukwatse, Mary Namuguzi, Ahmed Sarki, and Rose Maina RESEARCH ARTICLEPrevalence of sickle cell trait and needsassessment for uptake of sickle cell screeningamong secondary school students in KampalaCity, UgandaShamim NamukasaID1*, Rose MainaID2, Sarah NakazibaID1, Grace Among1,Lydia Asasira1, Posiano Mayambala3, Joseph Atukwatse1, Mary Namuguzi1, AhmedM. SarkiID1,41 School of Nursing and Midwifery, Aga Khan University, Kampala, Uganda, 2 School of Nursing andMidwifery, Aga Khan University, Nairobi, Kenya, 3 Mengo Hospital Blood Bank, Kampala, Uganda, 4 Familyand Youth Health Initiative (FAYOHI), Duste, Jigawa State, Nigeria* shamim.namukasa@aku.eduAbstractBackgroundSickle cell disease (SCD) is one of the most frequent and traumatizing genetic disease inUganda, with the prevalence of the sickle cell trait (SCT) estimated at 13.3% leading to seri-ous psycho-social and economic impact on the patients and their families.AimThis study aimed to determine the burden of SCT and factors influencing the uptake ofscreening services among secondary school students in Uganda.MethodsWe used an analytical cross-sectional design with a multi-stage sampling approach. A totalof 399 students from four secondary schools in Kampala City were enrolled in this study.Data were gathered using semi-structured questionnaires and blood screening. We usedthe sickling test to determine the presence of sickle cell alleles among the participants andhemoglobin electrophoresis as a confirmatory test. Data gathered using the questionnairewere analyzed using descriptive and inferential statistics.ResultsIn total, 5.8% of participants who were tested during this study had SCT. Most (80.2%) par-ticipants were not in an intimate relationship at the time of data collection. The majority(60.4%) had moderate knowledge about SCT screening and obtained information aboutscreening from the school. Only 29 (7.3%) participants knew of a family member with sicklecell. Overall, participants had a negative attitude toward SCT screening (67%), although41.6% believed that most people who were sickle cell carriers did not live long and werePLOS ONEPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 1 / 16a1111111111a1111111111a1111111111a1111111111a1111111111OPEN ACCESSCitation: Namukasa S, Maina R, Nakaziba S,Among G, Asasira L, Mayambala P, et al. (2024)Prevalence of sickle cell trait and needsassessment for uptake of sickle cell screeningamong secondary school students in Kampala City,Uganda. PLoS ONE 19(1): e0296119. https://doi.org/10.1371/journal.pone.0296119Editor: Gorica Maric, Faculty of Medicine,University of Belgrade, SERBIAReceived: January 7, 2023Accepted: December 6, 2023Published: January 19, 2024Copyright: © 2024 Namukasa et al. This is an openaccess article distributed under the terms of theCreative Commons Attribution License, whichpermits unrestricted use, distribution, andreproduction in any medium, provided the originalauthor and source are credited.Data Availability Statement: Data set can beaccessed at DOI 10.5281/zenodo.7825680.Funding: The authors received no funding for thiswork.Competing interests: The authors declare that theyhave no competing interests.Abbreviations: Hb, hemoglobin; SCD, sickle celldisease; SCT, sickle cell trait.often sick. Statistically significant associations were found between testing for SCT andknowing a partner’s sickle cell status (odds ratio [OR] 2.112, p = 0.043) and Anglican religion(OR 2.075, p = 0.047).ConclusionDespite the moderate level of knowledge and negative attitudes, a relatively large number ofparticipants had SCT. This highlights the need for a comprehensive health education pack-age targeting adolescents to promote SCD/SCT screening.BackgroundSickle cell trait (SCT) is a carrier state arising from the inheritance of one sickle cell “S” allelefrom one parent and one normal hemoglobin (Hb) “A” allele from the other parent. A personwith SCT or heterozygote (HbAS) typically does not show symptoms of sickle cell disease(SCD) or mutated homozygote (HbSS), although they may pass the trait on to their offspring[1]. Globally, SCD is the most prevalent genetic blood disorder and is characterized by pro-gressive organ damage coupled with episodes of acute illness [2, 3]. An estimated 312,000infants are born with SCD each year, meaning the disease is associated with a significant bur-den on communities globally [4]. However, only 10% of all patients with SCD are in the devel-oped world [5]. Sub-Saharan Africa contributes more than 75% of all SCD cases, which isexpected to increase by 2050 [6]. This projected increase in SCD necessitates more aggressiveinterventions to help reduce the number of children born with SCD [6, 7].Although newborn sickle cell screening programs have been implemented in wealthynations, sub-Saharan Africa lags, with many countries lacking the necessary infrastructure forscreening [8]. In addition, in many African communities, SCD causes significant stigmatiza-tion of mothers of affected children, and screening can sometimes create discord in homesthat may result in marital violence or broken marriages [9]. Low knowledge of SCD, such aspeople assuming that their spouses were not carriers or that their children could not haveSCD, is another factor for the low uptake of SCD screening programs [10, 11]. In addition,some people believed SCT screening was a difficult and painful process, and others thought itwould be challenging to persuade their spouses to undergo screening [10]. Other problemsincluded the worry that they would miss out on a "good" spouse if their results were favorableand the worry that their relationship would end if their partner discovered their unusual geno-type [12], and the lack of awareness of the occurrence of SCD in their family [10]. Althoughmany teenagers are in relationships that could end in teenage pregnancies, marriage, and chil-dren, poor sickle cell screening uptake among young people may mean that adolescents areunaware of their SCT status.Uganda has the fifth highest sickle cell burden in Africa, with 13.3% of children having SCTand 5,000–20,000 babies born with SCD each year, of which 80% die before reaching 5 years ofage [13]. The prevalence of SCT ranges across Uganda, with reported rates of 12.8%–19.8% inCentral Uganda and 13.6% in Kampala District [14]. Despite efforts to implement a freescreening program for SCD or SCT for newborns and infants under age 2 years in high HIV-burden districts in Uganda [15], social barriers exist for improving SCD care and outcomes,including an overall lack of awareness about SCD, understanding of SCD as a medical condi-tion, and its inheritance. It has been also reported that there is poor parental knowledge of thegenetic cause of SCD, awareness of the potential for transmission of SCD to one’s children,and knowledge of one’s own sickle cell status. In addition, families may have to meet the costsPLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 2 / 16associated with screening if they wish to determine their sickle cell status. Moreover, the con-firmatory test (Hb electrophoresis) is relatively expensive and limited to a few health facilities.Therefore, most Ugandans only discover they have the sickle cell allele when they have givenbirth to a child with SCD [16].A few young people in Uganda know their sickle cell status and knowledge of the diseaseand preventive measures is limited, many secondary school students may be likely to start rela-tionships with no awareness of their sickle cell status. This increases the likelihood of morechildren born with SCD, even though a simple blood test can easily detect carriers of the dis-ease. Following screening, couples can receive the proper counseling and information regard-ing their odds of having affected children. As a result, it’s important to ascertain the prevalenceof SCT and assess the variables affecting secondary school students in Kampala City’s uptakeof SCT screening. The goal of managing SCD as a priority disease will advance as a result ofthis information.Methods and materialsStudy designAn analytical cross-sectional design was used to determine the prevalence of SCT and factorsinfluencing screening among secondary school students. Quantitative data were collectedusing semi-structured questionnaires that covered knowledge about and attitudes toward SCTand factors influencing the uptake of SCT screening among secondary school students inKampala City, Uganda. The prevalence of SCT was determined by testing blood samples thatwere taken from the students.Inclusion & exclusion criteriaThe target population included all secondary school students at an advanced level of educationstudying in day schools in Kampala District, which is in the central region of Uganda. Thisregion has one of the highest burdens of SCT in Uganda at 12.8%–19.8% [14]. The district con-tains 149 registered secondary schools, of which 133 schools cater to advanced-level students.All students who were present during the study period (2022 academic year). We excluded stu-dents who had acute illnesses, had received blood transfusions within the previous 3 months(because the Hb in transfused blood is dominant and may obscure the true picture), had bleed-ing tendencies, were too weak to participate in this study, or were too busy to devote the neces-sary time to complete the questionnaire.Sample sizeThe sample size was estimated based on a design effect of 2 and multi-stage sampling. Theminimum sample size required was 356 students. To cater for non-response, this minimumsample size was adjusted by 10% (356 × 10% = 35.6), meaning we recruited an additional 36participants. Therefore, a total sample of 392 participants was considered the minimum sam-ple required for this study.EthicsEthical approval for this study was sought from the School of Medicine Research and EthicsCommittee, Makerere University (Mak-SOMREC-2021-55), and the Uganda National Coun-cil for Science and Technology (SS818ES). Permission to conduct the study was sought fromthe Kampala District Health Office, the District Education Officer, and the administration ofeach school. An information letter that explained the purpose of this study was sent to thePLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 3 / 16parents of the students offering them the opportunity for them to opt out of having their chil-dren participate in testing. In cases when a student was identified with a problem during thisstudy, a referral was made for appropriate clinical management. Written informed consentwas obtained from the participants aged 18 years and above, where a participant was<18years old, we obtained written informed consent from their legal guardians/parents and writ-ten assent from the participants. Only participants who provided informed consent wereincluded in the study. Because this study was carried out after COVID and schools had beenshut down for two years, some of the participants were older than what was typical for second-ary school students.Data collectionThe participants were given information about the study for them to consent/assent beforeparticipation. After providing consent, participants completed a self-administered semi-struc-tured questionnaire covering socio-demographic characteristics, knowledge, attitudes, and fac-tors influencing the uptake of sickle cell screening services. Thereafter, students whoseparents/guardians had consented to sickle cell testing were counseled about the procedure.Four milliliters of blood were taken from each student by venipuncture under an aseptic tech-nique following strict blood sample withdrawal and samples were stored at room temperature(22˚C–27˚C) [17].Laboratory proceduresTwo sickle cell tests were performed to determine the prevalence of SCT. The sickling test wasperformed using sodium metabisulphite to determine those that were positive for the sicklecell allele [17] Those who had a positive sickling test underwent a confirmatory test using Hbelectrophoresis [18] for positive results via solubility testing. The Hb electrophoresis test wasrun in duplicate to check for consistency in the results. Furthermore, to ensure the quality ofthe test results, all experimental procedures were conducted according to the manufacturer’sinstructions (Minicap hemoglobin [E] using the minicap flex-piercing) and results were avail-able in 3–7 days. Known HbAS and HbSS blood samples were used as positive controls, andthe remaining blood samples were appropriately disposed of. After counseling, the resultswere shared with the participant and their parents/guardians. Those with positive SCT resultswere referred for further clinical management.Data analysisData were entered and analyzed using SPSS version 20. Univariate analysis was conducted toobtain a general description of the study participants. Categorical variables and factors influ-encing the uptake of SCT screening services were summarized using frequencies and percent-ages and then displayed in tables. Continuous demographic variables and the proportion ofSCT were summarized as means, medians, standard deviations, inter-quartile ranges, andranges and presented in percentage frequency distribution tables for description purposes. Wescored completed surveys using a previously established method [19]. Participants’ knowledgeabout SCT was categorized as poor (scores below 50%), moderate (scores of 50%–80%), orexcellent (scores above 80%). Attitude responses were scored using a 5-point Likert scale(1 = Strongly Disagree to 5 = Strongly Agree). This scale was converted to a 0–100 scale, whereStrongly Disagree = 0, Disagree = 25, Neutral = 50, Agree = 75, and Strongly Agree = 100. Neg-atively worded items were reverse-scored. A positive attitude was defined as a score of�75 outof 100 [19]. Knowledge levels and attitudes were summarized using frequencies andpercentages.PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 4 / 16All predictor variables with a p-value <0.2 in the bivariate analysis were entered into abinary logistic regression model to identify the predictors of screening for SCT versus noscreening for SCT. A probability value less than 0.05 was considered statistically significant.ResultsIn total, 399 students from four secondary schools in Kampala City were enrolled in this study.Most (90.2%) participants were aged 17–20 years (mean age 18±1.191 years), and 51.1% werefemale. The most common religion was Pentecostal (32.1%), and most (80.2%) participantswere not in an intimate relationship at the time of data collection. Moreover, most (78.2%)participants thought it was important to know their boy/girlfriend’s sickle cell status. None ofthe female participants who had boyfriends knew their partners’ sickle cell status. Of all partici-pants, only six (1.5%) reported having been tested for sickle cell before this study. All six par-ticipants who had previously been tested reported that they were negative. About 66.7% ofthose who claimed to have been tested before were tested in a hospital setting. Among thosethat were tested, 93.3% did not have the sickle cell allele (HbAA). However, about 5.8% of par-ticipants had SCT (HbAS) [Table 1].Most (89.7%) participants who agreed to be tested for sickle cells in this study wanted toknow their sickle cell status. Of those who did not want to be tested for sickle cell, about 2.3%indicated this was because of what they perceived sickle cell to be [Table 2].Generally, majority (67%) of the participants had a negative attitude toward testing for SCT[Table 3]. Most (83.2%) participants agreed that it was important for both partners (boyfriendsand girlfriends) to be tested to confirm their sickle cell status before sexual intercourse/mar-riage. About one-third (32%) of participants disagreed that two people who have the sickle cellallele (sicklers)/trait should be discouraged from having a child together or marrying eachother. Majority (85.7%) of the participants agreed that it was necessary to provide geneticcounseling about sickle cell to all people intending to have a serious intimate relationship. Inaddition, 75.9% of participants agreed that testing all newborn babies for the sickle cell allelewas necessary [Table 3].Fig 1 showed that 268 (67%) participants had a negative attitude toward testing for SCT.A large number (93.9%) of the participants agreed that it would be useful to know if theirboy/girlfriend were sickle cell carriers. Majority (87.4%) of the participants agreed they wouldencourage their boy/girlfriend to be tested for sickle cell if they were found to have SCT. Sur-prisingly one in five (20.1%) participants disagreed that knowing the risk of having a childwith SCD would change their plan to have a child or marry [Table 3].More than a third (39.6%) of participants reported experiencing discomfort during theirsickle cell test, and more than half (53.1%) of the participants expressed fear of positive sicklecell results. It would be difficult to persuade their boyfriend/girlfriend to take the test, accord-ing to 50% of participants (50.4%). Additionally, 108 participants (51.7%) felt that having sicklecell anemia would make them less confident in dating, and almost six out of ten (53.4%) partic-ipants were concerned about being stigmatized after the results were made public. In addition,despite not having sickle cell disease, 53.7% of participants said they would discontinue theirrelationship with their boyfriend or girlfriend if they learned they had the disease. Most partic-ipants (67.9%) believed that SCT screening was necessary at their current age. Most partici-pants supported SCT testing (88.5%) and indicated that they would like to know their sicklecell status (85%), respectively. Most participants, 72.2%, agreed that SCT/carrier testing oughtto be done on everyone [Table 3].Majority (n = 241, 60.4%) of participants had moderate knowledge about SCD and testing.Only 29 (7.3%) participants knew of a family member with sickle cell. Most (n = 330, 82.7%)PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 5 / 16participants knew that a carrier/sickler could pass on sickle cell to their children, and themajority (n = 301, 75.4%) stated that the sickle cell allele can be confirmed by a blood test.Around half of the participants (n = 199, 49.9%) obtained information about sickle cell fromschools [Table 4].Table 1. Participants’ sociodemographic characteristics (n = 399).Variable Frequency Percentage (%)Age, yearsMean 18±1.19117–20 360 90.221–24 39 9.8GenderMale 195 48.9Female 204 51.1ReligionCatholic 97 24.3Muslim 46 11.5Pentecostal 128 32.1Anglican 108 27.1Others* 20 5.0Currently in an intimate relationshipNo 320 80.2Yes 79 19.8Important to know your boy/girlfriend’s sickle cell statusI don’t know 50 12.5No 37 9.3Yes 312 78.2Want to be tested for sickle cell alleleYes 328 82.2No 71 17.8Ever tested for sickle cellNo 393 98.5Yes 6 1.5Sickle cell results (n = 6)Negative (normal) 6 100Place of testingHospital 4 66.7Clinic 1 16.7Others 1 16.7SCT prevalenceNegative 306 93.3Positive 22 6.7Hemoglobin genotypesAA 306 93.3AS 19 5.8SS 3 0.9*Others = Hindu, Jehovah’s Witness, Pagan, Seventh Day Adventists. SCT, sickle cell trait.https://doi.org/10.1371/journal.pone.0296119.t001PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 6 / 16A large number (n = 326, 81.7%) of participants stated that people who were sickle cell car-riers had inherited it from at least one of their parents but only 150 (37.6%) participants knewthat people who were sicklers had inherited it from both parents. In addition, 166 (41.6%) par-ticipants stated that most people who were sickle cell carriers did not live long and were oftensick, and 180 (45.1%) participants stated that sickle cell carriers had many medical problems.More than half (n = 217, 54.4%) of the participants disagreed that all children of a sickle cellcarrier would also be carriers. In addition, 176 (44.1%) participants stated that SCD was notcurable. The majority (n = 240, 60.2%) stated that when one parent was a carrier, there was achance that they would have a child with SCD, and almost three quarter 288 (72.2%) partici-pants said that when both parents were carriers, there was a chance that they would have achild with SCD [Table 5].Statistically significant associations were found between SCT testing and knowing a part-ner’s sickle cell status (odds ratio [OR] 2.112, p = 0.043) and being of Anglican religion (OR2.075, p = 0.047) [Table 6]. Participants who thought that it was important to know their part-ner’s status were two times more likely to screen for SCT than those who did not know that itwas important. In addition, participants who were Anglican were two times more likely toscreen for SCT compared with participants who were of the Catholic religion. There were nostatistically significant association between testing for SCT and whether the participant hadbeen tested before and gender. However, prior testing status (tested before) confounded therelationship between testing and the importance of knowing a partner’s sickle cell status[Table 6].DiscussionSCD is a debilitating chronic genetic blood disorder that places psychosocial, financial, andfrequently painful burdens on affected individuals and their families. Those who had previ-ously been tested said they had received a negative result. Among those examined for thisstudy, 93.3% were normal, 0.9% had HbSS genotype (sicklers), and 5.8% had the HbAS geno-type (carriers). This calls for public health interventions that encourage people to undergoscreening to confirm their sickle cell status to make informed decisions [20]. A prior study dis-covered a high prevalence of sickle cell trait, which contrasts with our findings of HbASTable 2. Reasons for screening/not screening for sickle cell.Variable Frequency Percentage (%)Reasons for accepting to be tested for sickle cell*Know my sickle cell status 358 89.7Family history SCD 5 1.3Free of charge 1 0.3Assist in reproductive health decision-making 32 8.0Reasons for declining to be tested for sickle cell*Fear of results 7 1.8Perceived knowledge about sickle cell 9 2.3Tested before 4 1.0No family member has signs 2 0.5Think it is painful 4 1.0*Multiple responses permitted. SCD, sickle cell disease.Perceived knowledge about sickle cell testing: not ready to test, don’t want to give blood, God heals SCD.https://doi.org/10.1371/journal.pone.0296119.t002PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 7 / 16(18.7%, 42/225) among secondary school students in Kenya [20]. Another cross-sectionalstudy conducted among secondary school students aged 9–25 years showed that 59% knewtheir genotype and 11.1% claimed they were AS genotype [21].Only 19.8% of participants in the present study were currently in an intimate relationship.None of these participants knew their partner’s sickle cell status, although 78.2% of all partici-pants knew that it was important for an individual to know their partner’s status. Becausemany participants were under 20, there’s a chance they didn’t feel the need to be aware of suchinformation because they don’t often take intimate relationships seriously. This calls for healtheducation programs about SCD targeted at young people. The price of SCD testing could alsobe a deterrent, as a study from Uganda revealed that testing for SCD was made more difficultby the availability and affordability of testing services [22]. That study also highlighted theTable 3. Attitudes toward sickle cell screening.Variable StronglyDisagreeDisagree Uncertain Agree StronglyAgreen (%) n (%) n (%) n (%) n (%)Sickle cell disease can be prevented byTesting of both boyfriend and girlfriend before sexual intercourse/marriage 18 (4.5) 19 (4.8) 30 (7.5) 113(28.3)219 (54.9)Discouraging two people who have the sickle cell allele from having a child together ormarrying each other64 (16.0) 64 (16.0) 56 (14.0) 85 (21.3) 130 (32.6)Providing genetic counseling about sickle cell to all people intending to have a serious intimaterelationship20 (5.0) 14 (3.5) 23 (5.8) 141(35.3)201 (50.4)Testing all newborn babies for the sickle cell allele 14 (3.5) 33 (8.3) 49 (12.3) 121(30.3)182 (45.6)Benefit of testing for sickle cell traitIt is useful to know if I am a sickle cell carrier 7 (1.8) 5 (1.3) 10 (2.5) 123(30.8)254 (63.7)It is useful to know if my boy/girlfriend is a sickle cell carrier 4 (1.0) 6 (1.5) 13 (3.3) 161(40.4)215 (53.9)I would encourage my boy/girlfriend to be tested for sickle cell if I was found to be a sickle cellcarrier6 (1.5) 14 (3.5) 30 (7.5) 151(37.8)198 (49.6)Knowing the risk of having a child with sickle cell disease would change my pregnancy/marriage plans39 (9.8) 41 (10.3) 58 (14.5) 108(27.1)153 (38.3)Testing for sickle cell is painful 56 (14.0) 100(25.1)85 (21.3) 111(27.8)47 (11.8)I fear getting positive results 59 (14.8) 77 (19.3) 51 (12.8) 131(32.8)81 (20.3)It will be hard to convince my boy/girlfriend to have the test 50 (12.5) 84 (21.1) 64 (16.0) 109(27.3)92 (23.1)Being a sickle cell carrier would make me less confident about forming relationships 54 (13.5) 82 (20.6) 57 (14.3) 108(27.1)98 (24.6)I fear being stigmatized after the results are out 76 (19.0) 70 (17.5) 41 (10.3) 120(30.1)92 (23.1)I would break up with my boy/girlfriend if I found out that she/he is a sickle cell carrier even ifI am not81 (20.3) 78 (19.5) 66 (16.5) 92 (23.1) 82 (20.6)Should screening for sickle cell be made widespreadI support sickle cell disease testing 19 (4.8) 16 (4.0) 11 (2.8) 79 (19.8) 274 (68.7)I would want to know my sickle cell status 27 (6.8) 15 (3.8) 18 (4.5) 102(25.6)237 (59.4)Sickle cell testing is important at my present age 61 (15.3) 28 (7.0) 39 (9.8) 81 (20.3) 190 (47.6)I support sickle cell disease/carrier testing for all people 10 (2.5) 13 (3.3) 10 (2.5) 78 (19.5) 288 (72.2)https://doi.org/10.1371/journal.pone.0296119.t003PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 8 / 16need for targeted SCD education to groups such as adolescents who may not think of the possi-bility of having the sickle cell allele. In the same study, 27.3% of participants reported it wouldbe hard to convince their partner to have the test, although those who knew their partner’ssickle cell status were more likely to undergo testing themselves than those who did not. Thiscould be a reminder of the likelihood of having a child with SCD. Similarly, a study conductedin a division of Kampala, Uganda, showed that most (90.2%) respondents did not know theirpartner’s genotype [13].Only 1.5% of participants in our study reported having been previously tested for sicklecells. This might be due to the absence of SCT testing from secondary school or the fact thatscreening for diseases is not something that people often consider doing, especially if they arenot feeling ill. It could also be explained by the fact that SCD testing is only offered in a fewspecific medical facilities and is not a free service. In this study, most secondary school stu-dents did not know their Hb genotype. Participants who had already undergone screeningwere most frequently tested to determine whether they had sickle cell disease. Among partici-pants who did not want to be tested, six participants (23.1%) feared positive results, feared thepain associated with testing, and indicated that no family member had signs of SCD. Similarly,a cross-sectional study among adults (mean age 29 years) in Muscat, Oman, showed that 36%thought SCT screening was a difficult and painful process, which explained the small percent-age who had been screened (24.4%), and 37.8% felt it would be hard to convince their partnersto go for screening [23]. In another study, most (94.6%) youths (aged 22–29 years) in SouthNigeria knew their Hb genotype (SCD carrier status), with the most common reason forchecking their sickle cell status being a school entry requirement [24].Fig 1. Attitude of secondary school students about SCT screening.https://doi.org/10.1371/journal.pone.0296119.g001PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 9 / 16To prevent SCD, one must first be aware of their genotype. In this study, many participants(60.4%) had a basic understanding of SCD and testing. Similarly, a study conducted amongyouths aged 22–29 years in Nigeria showed that most respondents (63.5%) had a fair knowl-edge of SCD [24]. This implies that those who have SCD but do not know their genotype maynot be able to access care for the disease, thereby increasing SCD-related morbidity and mor-tality. Most participants in this study had heard about SCD at school. This is presumablybecause students had easy access to tools like the Internet while they were in school and werealso taught about hereditary illnesses. This finding was consistent with previous studies [25,26] that reported that most participants learned about SCD from media and school. This sug-gests that schools and the media can be effective institutions and platforms for educating peo-ple about SCD. Carriers of the disease who do not know their genotype may not seek thenecessary genetic counseling to make informed marital choices. Therefore, school authoritiesshould encourage parents to find out their children’s Hb genotype as well as students olderthan 18 years [27].Table 4. Knowledge about sickle cell screening.Variable n (%)Overall knowledgePoor 58 (14.5)Moderate 241 (60.4)Excellent 100 (25.1)How to confirm that someone has the sickle cell alleleThey look sick 23 (5.8)Urine test 4 (1.0)By a blood test 301 (75.4)Don’t know 67 (16.8)Others 4 (1.0)Anyone in your family have sickle cellDon’t know 204 (51.1)No 166 (41.6)Yes 29 (7.3)A carrier/sickler can pass on sickle cell to their childrenDon’t know 58 (14.5)No 11 (2.8)Yes 330 (82.7)Positive response (yes) about the source of information about sickle cell and testing **Radio 39 (9.8)Television 73 (18.3)Health camps 34 (8.5)Posters/fliers 1 (0.3)Magazines/newspapers 18 (4.5)School 199 (49.9)Family 29 (7.3)Hospital 11 (2.8).Others* 8 (3.5)* Others: friends, Internet, online, parents.**Multiple responses allowed.https://doi.org/10.1371/journal.pone.0296119.t004PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 10 / 16Table 6. Factors associated with sickle cell screening uptake.Variable Screening status Unadjusted OR p-value Adjusted OR 95%CI p-valueScreened Not Screenedn (%) n (%)GenderMale 40 (56.3) 155 (47.3) Ref 1.000 RefFemale 31 (43.7) 173 (52.7) 1.44 0.166 1.594 0.929, 2.733 0.090ReligionCatholic 25 (35.2) 72 (22.0) Ref 1.000 RefMuslim 6 (8.5) 40 (12.2) 2.563 0.090 2.500 0.920, 6.798 0.073Pentecostal 22 (31.0) 106 (32.3) 1.792 0.119 1.703 0.879, 3.299 0.114Anglican 16 (22.5) 92 (28.0) 2.168 0.053 2.075 1.010, 4.260 0.047*Others 2 (2.8) 18 (5.5) 3.841 0.144 3.629 0.759, 17.350 0.106Important to know partner’s sickle cell statusI don’t know 0 (0.0) 1 (1.4) Ref 1.000 RefNo 20 (100.0) 59 (85.5) 0.776 0.860 0.786 0.296, 2.088 0.629Yes 0 (0.0) 9 (13.0) 2.191 0.022 2.112 1.023, 4.357 0.043*Tested beforeNo 323 (98.5) 70 (98.6) 1.000 1.000 RefYes 5 (1.5) 1 (1.4) 1.084 0.942 0.964 0.106, 8.729 0.974AttitudeNegative 7 (9.9) 18 (5.5) 1.000 1.000 RefPositive 64 (90.1) 310 (94.5) 1.884 0.174 1.418 0.535, 3.755 0.483*Statistically significant; OR- odds ratio; CI, confidence interval.https://doi.org/10.1371/journal.pone.0296119.t006Table 5. Knowledge about sickle cell disease.Variable Don’tknowFalse Truen (%) n (%) n (%)Sickle cell disease is curable 152 (38.1) 176(44.1)71(17.8)People who are sickle cell carriers inherited it from at least one of their parents 51 (12.8) 22 (5.5) 326(81.7)People who are sicklers inherited it from both parents 122 (30.6) 127(31.8)150(37.6)Most people who are sickle cell carriers live long and healthy lives 110 (27.6) 166(41.6)123(30.8)Sickle cell carriers have many medical problems 123 (30.8) 96(24.1)180(45.1)If a person is a sickle cell carrier, all their children will be sickle cell carriers 121 (30.3) 217(54.4)61(15.3)When one of the parents is a carrier, there is a chance that they will give birth to achild who has sickle cell disease60 (15.0) 99(24.8)240(60.2)When both parents are carriers, there is a chance that they will give birth to achild who has sickle cell disease82 (20.6) 29 (7.3) 288(72.2)https://doi.org/10.1371/journal.pone.0296119.t005PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 11 / 16More than eight in ten respondents (82.7%) were aware that carriers can pass sickle cell totheir offspring, but more than half (51.1%) were unaware of whether anyone in their familyhad the condition. This may be because some parents may not reveal certain medical informa-tion to their children, especially if there is no one suffering major complications. In addition, aprevious study by Okwi, Byarugaba [16] reported that most Ugandans only discovered theyhad the sickle cell allele when they had a child with SCD yet sickle cell is known to play a causalrole in several morbidities, which makes the disclosure process critical [28]. Similar findingswere reported in another study Tusuubira, Nakayinga [13] in which more than half (54.0%) ofthe participants knew SCD was inherited from both parents, and the majority (62.9%) had afamily member with SCD. Most participants in the present study knew that there was a chanceof having a child with SCD if one parent was a carrier (81.7%) or if both parents were carriers(37.6%). This suggested that many participants had incomplete knowledge regarding thespread of SCD, which could result in unwise health choices. These results concurred withthose of an earlier study that found the majority of participants accurately thought that SCDwas inherited from parents [21].Three-quarters of the participants in this study stated that the sickle cell allele can be con-firmed by a blood test, and more than half believed SCD was curable. Similarly, in anotherstudy, Ghimire [29] found that 63.1% of respondents knew that blood tests could detect thedisease and 71.7% mentioned that SCD had treatment. Surprisingly, 30.8% of participants inour survey believed sickle cell carriers did not live long and healthy lives, and more than half(45.1%) believed sickle cell carriers had several medical issues. This demands ongoing teachingabout SCD in schools and the public [13], so that those with SCT become knowledgeable oftheir carrier status, are educated on how they can potentially pass the trait or disease on totheir offspring, and better understand the outcomes of SCD.We discovered that compared to Catholics, Anglicans were twice as likely to have a sicklecell test. This is likely because Anglicanism is one of Uganda’s most prevalent religions, and itspriests urge people to have children and use reproductive health care facilities, which go handin hand with screening for certain diseases like sickle cell disease. Scholars have shown thatreligious leaders play a vital role in the implementation and development of health interven-tions that promote the health of people [30, 31]. Some religious organizations educate the pub-lic through counseling sessions or seminars, and the majority require genetic counselingbefore marriage. In other studies, religious bodies were mentioned among the sources ofhealth information [27]. This calls for strengthening the integration of health and religiousinstitutions in the dissemination of health information. Religious organizations have been suc-cessfully used in disseminating health information in other disease situations such as HIV/AIDS [27]. As a result, religious groups and healthcare professionals must collaborate on SCDpreventive initiatives. If few youths know their sickle cell status and most only have moderateknowledge of the disease, many young people may enter relationships without learning theirsickle cell status, which will increase the chances of having children with SCD.Most (66%) of the participants in this study had a negative attitude toward SCD/SCT andtesting. This can be due to Uganda’s general awareness of SCD and continuous public aware-ness programs. This may lead to stigmatization, have an impact on how sickle cell patientsrespond to cues, and how they seek care, and ultimately have an impact on patient outcomes.Similar findings have been reported in a Nigerian study that explored the stigmatising attitudeof secondary school students towards peers with SCD. It was indicated that a significant pro-portion of students still had negative attitudes towards peers with SCD despite having had con-tact with people who have SCD [32]. A sixth (16%) of participants disagreed that two peoplewho have the sickle cell allele (sicklers)/trait should be discouraged from having a childPLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 12 / 16together or marrying each other. In addition, 10.3% disagreed that knowing the risk of havinga child with SCD would change their pregnancy/marriage plans.This might be the case because participants don’t understand the pain and psychosocialtrauma that affected children go through and think they are immune to the illness. The beliefsof people about several factors, such as perceived susceptibility to the disease, the severity ofthe disease, the advantages of screening, and the barriers to screening, have an impact on theuptake of screening services for numerous diseases [33]. Moreover, participants in this studyagreed that being a sickle cell carrier would make them less confident about forming relation-ships (27.1%) and many feared being stigmatized based on their results (30.1%). Communitiesstill have misconceptions about SCD, its cause, management, and outcomes that affect howthey view people with SCD. This was supported by similar findings in a study that highlightedstigmatization as a barrier to screening for SCD [34]. In contrast to the above findings, anotherstudy reported that more than half (56%) of students agreed they should not marry someonewith SCT/SCD irrespective of their genotype [12].Half (50.4%) of the participants in this study strongly agreed that genetic counseling aboutsickle cell should be provided to all people intending to have a seriously intimate relationshipand if they were found to have SCT, almost half (49.6%) of people would highly advise theirboyfriend/girlfriend to get tested for sickle cell. This may be because SCD is a fatal disease andthe union between two SCT carriers gives a 25% risk of having a sick child in each pregnancyMaboulou, Ngoutane [35].Most individuals (72.2%) supported testing for SCD carriers in all people, and the majority(45.6%) strongly agreed that newborns should all be tested for the SCD allele. A free screeningprogram for SCD/SCT for newborns and infants under 2 years in Uganda was established inhigh HIV-burden districts [15], although mechanisms for informing families were locallydetermined and may not be systematic. In addition, students/families may have to meet associ-ated screening costs if they are interested in finding out their SCD status. A previous studyshowed that 55% of youths agreed with legislation prohibiting marriage between trait carriersto prevent the births of babies with SCD [24]. The World Health Organization also advocatesfor carrier detection and genetic counseling [36], which were reported to be effective in thecontrol of thalassemia in countries such as Cyprus and Iran [37]. Primary preventive measuressuch as avoidance of carrier marriages/pregnancies through health education, populationscreening, carrier detection, genetic counseling, and pre-conceptual diagnosis should thereforereceive greater emphasis in efforts to control SCD in Uganda.ConclusionMost individuals in this study had negative attitudes toward testing, moderate understandingof SCD/SCT, and moderate knowledge of their genotype. The knowledge of the partner’s sta-tus and religion was substantially linked to SCT testing. The participants’ understanding ofSCD’s causes and prevention was lacking. Therefore, cooperation between the health and edu-cation sectors is necessary for SCD prevention, diagnosis, and management. Regular healtheducation campaigns on SCD are also necessary, as are free Hb electrophoresis tests for teenag-ers who are enrolled in school. To inform parents about the benefits of early SCD diagnosis fortheir children through Hb genotype testing, policymakers in the education sector should alsofocus on Parents Teachers Associations in schools. The nurses at the schools should also peri-odically teach the students about inherited illnesses like SCD/SCT. The cross-sectional natureof the study design, which prevents the researchers from deducing causality, is one of thestudy’s shortcomings. The sample was taken from the Central region of Uganda, one of thecountry’s five geographical regions, which is a conceivably plausible limitation. However, thePLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 13 / 16data from this study will serve as a starting point for additional research. There is a need formore research projects using nationally representative samples from all five geographicalregions.Supporting informationS1 File. Questionnaire.(PDF)S2 File. Summary statistics.(ZIP)S3 File. Laboratory protocol. https://www.protocols.io/file-manager/1219B065DBA911EDBE2A0A58A9FEAC02.(RAR)AcknowledgmentsWe acknowledge the help of all teachers in the selected secondary schools in Kampala whohelped in organizing study participants. We also offer special thanks to the participants foragreeing to participate in this study.Author ContributionsConceptualization: Shamim Namukasa, Rose Maina, Sarah Nakaziba, Grace Among, JosephAtukwatse, Mary Namuguzi, Ahmed M. Sarki.Data curation: Shamim Namukasa, Sarah Nakaziba, Grace Among, Lydia Asasira, MaryNamuguzi.Formal analysis: Shamim Namukasa, Lydia Asasira, Posiano Mayambala, Mary Namuguzi.Investigation: Grace Among, Posiano Mayambala, Joseph Atukwatse.Methodology: Shamim Namukasa, Rose Maina, Sarah Nakaziba, Grace Among, Mary Namu-guzi, Ahmed M. Sarki.Project administration: Shamim Namukasa, Grace Among, Mary Namuguzi.Resources: Shamim Namukasa, Rose Maina, Sarah Nakaziba, Grace Among, Mary Namuguzi,Ahmed M. Sarki.Supervision: Shamim Namukasa, Sarah Nakaziba, Mary Namuguzi.Validation: Shamim Namukasa.Visualization: Shamim Namukasa.Writing – original draft: Shamim Namukasa, Rose Maina, Sarah Nakaziba, Grace Among,Lydia Asasira, Posiano Mayambala, Joseph Atukwatse, Mary Namuguzi, Ahmed M. Sarki.Writing – review & editing: Shamim Namukasa, Rose Maina, Mary Namuguzi, Ahmed M.Sarki.References1. Roseff SD. Sickle cell disease: A review. Immunohematology. 2009; 25(2):67–74. 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Thalassemia in Iran in last twenty years: the carrier rates and the births trend. یهلجم7–11:)1(6;2013.ناریاناطرسونوخ .PLOS ONE Factors affecting of sickle cell trait screening among secondary school students in Kampala City, UgandaPLOS ONE | https://doi.org/10.1371/journal.pone.0296119 January 19, 2024 16 / 16

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