Abstract
Introduction
Syphilis and HIV screening is highly recommended for pregnant women and those at risk for infection. We used conjoint analysis to identify factors associated with testing preferences for HIV and syphilis infection.
Methods
We recruited 298 men and women 18 years and over seeking testing or care at GHESKIO (Haitian Study Group for Kaposi’s sarcoma and Opportunistic Infections) clinics. We created 8 hypothetical dual HIV-syphilis test profiles varying across six dichotomous attributes. Participants were asked to rate each profile using Likert preference scales. An impact score was generated for each attribute by taking the difference between the preference scores for the preferred and non-preferred level of each attribute. Two-sided one-sample t-test was used to generate p-values.
Results
Of 298 study participants, 61 (20.5%) were male. Of 237 females, 49 (20.7%) were pregnant. Cost (free versus US$4; p<.0001) had the highest impact on willingness to test, followed by number of blood draws (1 versus 2; p<.0001), blood draw method (fingerprick versus venipuncture; p<.0001), test type (rapid versus laboratory; p=.0005), and time-to-result (20 minutes versus 1 week; p=.0139).
Conclusion
HIV and syphilis testing preferences for this study sample in Port-au-Prince prioritized cost, single fingerprick, laboratory-based testing and timeliness.
Keywords: Conjoint analysis, HIV, syphilis, diagnostics, testing
INTRODUCTION
Screening for syphilis and HIV is highly recommended for pregnant women and those at risk for infection.(1–4) Syphilis is caused by the spirochete Treponema pallidum, which, like HIV, can be transmitted through sex, blood and from mother-to-child during pregnancy or at birth. The similarities in screening recommendations for HIV and syphilis offer an important opportunity to strengthen prevention programs for the elimination of congenital syphilis along with preventing mother-to-child transmission of HIV infection by means of integrated screening.(5) Peeling and colleagues commented on the tragedy of babies avoiding HIV through effective prevention of mother-to-child transmission of HIV programs but dying of syphilis because of the lack of screening for syphilis available to the women.(6) Integrated screening could profoundly change medical and public health practice.(5, 7) With a shortened time to diagnosis, patients may be treated and rendered less infectious or non-infectious much quicker resulting in reduced complications from untreated infection as well as the decreased spread of infection to others.
In Haiti, a demographic health survey conducted in 2005–2006 showed an HIV prevalence of 2.3% among women aged 15 to 49 and a 2.0% prevalence among men.(8) Additionally, in parts of Haiti a significant proportion (7.6%) of pregnant women have serologic evidence of syphilis.(9) Screening is the main strategy for identifying HIV and syphilis infections. Enhanced control and prevention can be accomplished through increased uptake of testing and subsequent treatment for those infected.
It is imperative to understand the variable determinants of test uptake in order to reduce barriers. Screening and treatment programs that utilize laboratory-based testing have been hampered by limited laboratory access, long turn-around time for results, and loss to follow-up of syphilis infected individuals.(10–13) When diagnostic testing involves multiple tests performed off-site, only a proportion of infected individuals receive treatment and continued transmission occurs.(14, 15) There have been several advances in point-of-care diagnostic tests; however, it is unknown what factors are associated with increased preference for testing in Haiti.
Conjoint analysis is a technique that has been used successfully in healthcare and is gaining widespread use.(16) Conjoint analysis is a method for systematically estimating consumer preferences across discrete attributes. It allows for estimation of the relative importance of different aspects of a product or healthcare, the trade-offs between these attributes, and the total satisfaction or preference that participants associate with the product or care. This analytic method is perfect for use in determining preferences of respondents in a low-resource setting like Haiti where informed decisions must be made about how to prioritize limited resources.
In order to understand preferences for the integration of HIV and syphilis testing, we used conjoint analysis to identify factors associated with willingness to test for HIV and syphilis infection.
METHODS
We recruited 298 men and women 18 years of age and over seeking sexually transmitted infection or HIV testing or antenatal care at GHESKIO (Haitian Study Group for Kaposi’s sarcoma and Opportunistic Infections) Health Centers between March and July of 2014. Currently, GHESKIO receives about 100,000 patient visits annually of which most (approximately 70%) are female patients. Central to the GHESKIO model is the concept that an individual at risk or already infected with HIV should be quickly identified and provided access to a package of services including voluntary counseling and testing, management of sexually transmitted infections, tuberculosis screening and treatment, reproductive health services, HIV care including antiretroviral therapy, and services to prevent mother-to-child transmission of HIV.
We utilized conjoint analysis methods to assess likelihood of testing (willingness to test).(17) The testing attributes were identified using characteristics of existing HIV and syphilis testing strategies.(7, 10, 18) Testing attributes included cost (free versus US$4), accuracy (no potential for false positive syphilis result versus potential for false positive syphilis result), time-to-result (20 minutes versus 1 week), blood draw method (finger prick versus venipuncture), number of draws (1 versus 2), and test type (rapid versus laboratory). We created scenarios that describe all possible combinations of attributes to create a hypothetical test profile. Because each attribute has two levels and we have six attributes, there will be 64 (26) different combinations that can be made using these attributes. Using the fractional factorial design, we reduced the number of scenarios to 8 hypothetical test scenarios across the six dichotomous attributes to measure the main effect of each attribute.(19) This design method assumes no interactions between attributes.
Preferences for the hypothetical test scenarios were determined using an interview conducted by a trained counselor in Haitian Creole. We assessed willingness to test by asking participants to rate how likely they were to test using each individual test profile on 5-level Likert preference scales: (1) Very unlikely, (2) Somewhat unlikely, (3) Neutral/Do not know, (4) Somewhat likely, (5) Very likely.
Ratings were converted to 100-point preference scores; higher scores suggest increased willingness to test. The mean of each hypothetical test scenario was determined. An impact score was generated for each attribute by taking the difference between the average preference scores between the preferred scenarios and non-preferred scenarios of each attribute. Two-sided one-sample t-test was used to generate p-values for the comparisons between the preferred and non-preferred levels for each attribute. Data analysis was conducted using SAS software v9.3 (Cary, NC, USA).
RESULTS
Of 298 study participants, 61 (20.5%) were male. Of 237 females, 49 (20.7%) were pregnant.
For the overall population, cost (free vs. $4; impact score=27.2, SD=36.6, p<.0001) had the highest impact on willingness to test, followed by number of blood draws (1 vs. 2; impact score=17.5, SD=29.8, p<.0001), blood draw method (fingerprick vs. venipuncture; impact score=9.7, SD=26.5, p<.0001), test type (rapid vs. laboratory; impact score= −4.5, SD=21.9, P=.0005), and time-to-result (20 minutes vs. 1 week; impact score=3.6, SD=25.6, p=.0139) [Tables I and II].
Table I.
Acceptability (mean) of hypothetical HIV and Syphilis tests with different attributes in Port-au-Prince, Haiti. (n=298)
| Test Attributes | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Hypothetical test profile |
Test acceptability among total sample mean (SD)a |
Test acceptability among pregnant females (n=49) (SD)a |
Test acceptability among non- pregnant females (n=188) (SD)a |
Test acceptability among males (n=61) (SD)a |
Cost | Potential for Syphilis False Positive |
Time to Result |
Number of Blood Draws |
Blood Draw Method |
Test Type |
| One | 45.05 (43.41) | 33.16 (37.98) | 46.94 (44.19) | 48.77 (44.12) | Free | No | 20 Minutes |
One | Finger prick | Laboratory |
| Two | 85.91 (30.20) | 91.84 (20.66) | 84.97 (31.19) | 84.02 (33.24) | Free | No | 20 Minutes |
Two | Venipuncture | Rapid |
| Three | 66.70 (43.86) | 51.02 (47.04) | 69.41 (42.98) | 70.90 (41.88) | Free | Yes | One Week |
One | Venipuncture | Rapid |
| Four | 42.11 (45.74) | 48.98 (46.20) | 39.23 (45.83) | 45.49 (45.07) | $4 | No | One Week |
One | Finger prick | Rapid |
| Five | 35.40 (45.10) | 36.22 (45.66) | 32.98 (44.36) | 42.21 (46.89) | $4 | No | One Week |
Two | Venipuncture | Laboratory |
| Six | 57.97 (46.89) | 48.46 (47.16) | 58.64 (47.34) | 63.52 (44.85) | Free | Yes | One Week |
Two | Finger prick | Laboratory |
| Seven | 48.74 (47.99) | 44.39 (46.57) | 48.80 (48.66) | 52.05 (47.50) | $4 | Yes | 20 Minutes |
One | Venipuncture | Laboratory |
| Eight | 27.85 (42.89) | 19.90 (35.35) | 28.59 (44.15) | 31.97 (44.28) | $4 | Yes | 20 Minutes |
Two | Finger prick | Rapid |
Abbreviation: SD, standard deviation
Test acceptability score is based on a 5-point Likert scale converted to 0–100 point scale; higher results indicate higher preference
Overall test acceptability: 51.22 (SD: 25.05)
Overall test acceptability among pregnant women: 46.75 (SD: 19.68)
Overall test acceptability among non-pregnant women: 51.20 (SD: 26.39)
Overall test acceptability among men: 54.87 (SD: 24.38)
Table II.
Impact of HIV and syphilis test attributes on hypothetical test acceptability among the total sample in Port-au-Prince, Haiti. (N=298)
| Test Attributes | Attribute values | Acceptability of testing with preferred attribute (mean) |
Acceptability of testing with non- preferred attribute (mean) |
Impact on testing acceptability Mean (SD) |
P-value |
|---|---|---|---|---|---|
| Cost | Free vs. $4 | 64.83 | 37.60 | 27.22 (36.62) | <0.0001 |
| Number of Blood Draws | 1 vs. 2 | 59.94 | 42.49 | 17.45 (29.80) | <0.0001 |
| Sample Collection Method | Fingerprick vs. Venipuncture |
56.08 | 46.35 | 9.73 (26.52) | <0.0001 |
| Test Type | Rapid vs. Laboratory | 48.97 | 53.46 | −4.49 (21.85) | 0.0005 |
| Time to Result | 20 minutes vs. 1 week | 53.04 | 49.39 | 3.64 (25.46) | 0.0139 |
| Potential for Syphilis False Positive |
No vs. Yes | 51.89 | 50.55 | 1.34 (23.69) | 0.3288 |
Abbreviation: SD, standard deviation
Scores were converted from preferences described using a 5-scale Likert to scores on a 100-point scale.
Additionally, we looked at differences among 3 groups included in our sample: pregnant women, non-pregnant women and men. Each of the groups had similar prioritization of attributes. Cost was the most important driving factor for all groups, followed by number of blood draws and sample collection method. However, among the 3 groups, only pregnant women prioritized time to result (impact score=17.22, SD=30.15, p=0.0002). Additionally, males did not prioritize test type (impact score=−2.77, SD=20.4, p=0.2937), while females did.
DISCUSSION
We used conjoint analysis to determine factors associated with willingness to test simultaneously for HIV and syphilis in Port-au-Prince, Haiti. The study participants in all three groups, males, pregnant and non-pregnant females, prioritized cost and a single blood draw using a fingerprick. It was only pregnant women that prioritized timeliness from specimen collection to result for HIV and syphilis tests. In addition, females prioritized laboratory-based testing while males did not.
We found that the most impactful attribute of HIV and syphilis tests was the cost; this is not surprising in a country where more than half of the population live under the national poverty line of US$2.42 per day.(20) GHESKIO Health Centers offer HIV and syphilis screening free of charge; however, we recommend that screening tests be offered free of charge in other settings around Haiti that are aiming to increase test uptake. The results of this study can influence the way that people are getting tested for syphilis and HIV. Additionally, groups prioritized one blood draw over two when testing for the two infections and preferred fingerprick specimen collection to venipuncture. Dual rapid tests could be used to meet these preferred methods of testing. Dual rapid tests that have multiple analytes for the detection of antibodies for both HIV and syphilis infections are now available.(21) Those tests use one drop of fingerprick whole blood and one device to test for two infections in minutes at the point-of-care. Dual tests enable testing for both HIV and syphilis at the same time. There are several advantages of rapid point-of-care tests that include rapid time to result, low cost, minimal equipment, minimal training needed (easy to perform), and suitable for use in non-clinical settings.(10, 11, 22–26)
In contrast with our hypothesis, women prioritized laboratory testing over rapid testing that can be performed at the point-of-care. We hypothesized that rapid testing would be preferred however we had a negative (but statistically significant) impact score among females, indicating that females preferred laboratory-based testing. One explanation for this is the setting in which the study was performed may have driven this preference. At GHESKIO, most testing for syphilis and HIV is performed in a laboratory/phlebotomy setting even when rapid tests are used. Therefore, the participants could be more comfortable in this setting away from the waiting room and patient rooms. In a study in a U.S. urban hospital, patients reported that they believed the rapid test was less accurate than a laboratory-based test.(27) This is perhaps also the case in Haiti, which would highlight the need for appropriate pre-screening education to explain to the patient the utility and high performance of rapid testing.
We also found attributes of HIV and syphilis tests that are less important to consumers. Participants’ willingness to test for HIV and syphilis was not as affected by a potential for false positive syphilis result. This result has implications on roll out of dual testing for HIV and syphilis, which can include screening tests that may require further confirmatory testing for positive results.
This study was subject to some limitations. Some of the attributes were not necessarily 100% mutually exclusive. Sample collection method could be related to test type, laboratory based versus rapid point-of-care. Therefore, there might be some overlap in attributes even though our analysis assumed independence. However, creating separate attributes for potentially related factors allowed us to parse out the specific impact of a characteristic related to willingness to test. An additional limitation is that participants were presenting to GHESKIO, a site where they had access to free HIV and syphilis testing, making these results less generalizable to other places where the patient population may be unaccustomed to diagnostic access. Another limitation is that we do not have any formal measure of whether participants fully understood the meaning of each choice. Specifically, it would be useful to know whether participants realized that rapid testing implies rapid treatment and would avoid another visit to obtain results. However, the data collection tool was piloted prior to use and was successfully understood among pilot participants. We also suspect that the concept of a false positive result may not have been fully understood. In order to maximize comprehension on this attribute, we used simple language explaining that there would be a chance the test will show that a patient has syphilis when they do not, and therefore may be treated for syphilis when they do not need to be.
Based on this first study using conjoint analysis in Haiti to detect preferences around attributes of tests for HIV and syphilis, we have found several attributes that affect people’s decision about how to test. Future research could look at interactions across the most impactful attributes as well as additional levels of each attribute. For example we used only 2 levels of cost, free and $4. Additional levels of cost could be explored to identify a threshold of cost that would be prohibitory.
CONCLUSIONS
Our study provides important information on preferences for HIV and syphilis testing which in combination with studies on test efficacy, cost, and feasibility can help identify best practices for prevention, screening, and treatment to reduce the continued burden of sexual and reproductive health-related diseases, like HIV and syphilis, in low-resource settings. Other studies have also found that the implementation of an accurate and low cost integrated rapid testing strategy for HIV and syphilis has been deemed acceptable, often preferred by patients and providers, and has the capacity to improve the rates of screening.(28–30) Implementation of a low-cost dual rapid test in the laboratory for HIV and syphilis could improve screening uptake and accessibility to accelerate time to treatment in Haiti.
Acknowledgments
Funding statement
The study was supported in part by Standard Diagnostics. Funding for this study was also provided by the UCLA Center for AIDS Research (CFAR) NIH/NIAID AI028697 and NIH/NICHD R21HD076685.
References
- 1.WHO. PMTCT Strategic Vision 2010–2015: Preventing mother-to-child transmission of HIV to reach the UNGASS and Millennium Development Goals 2010
- 2.Wolff T, Shelton E, Sessions C, Miller T. Screening for syphilis infection in pregnant women: evidence for the U.S. Preventive Services Task Force reaffirmation recommendation statement. Annals of internal medicine. 2009;150(10):710–716. doi: 10.7326/0003-4819-150-10-200905190-00009. [DOI] [PubMed] [Google Scholar]
- 3.WHO. Prevention of mother-to-child transmission of syphilis. 2006 http://www.who.int/reproductivehealth/publications/maternal_perinatal_health/prevention_mtct_syphilis.pdf:
- 4.PAHO. Clinical Guideline for the Elimination of Mother-to-Child Transmission of HIV and Congenital Syphilis in Latin America and the Caribbean. 2011 http://www.paho.org/hq/index.php?option=com_docman&task=doc_download&Itemid=270&gid=20104&lang=en: [Google Scholar]
- 5.Klausner JD. The sound of silence: missing the opportunity to save lives at birth. Bulletin of the World Health Organization. 2013;91(3):158-A. doi: 10.2471/BLT.13.118604. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Peeling RW, Mabey D, Fitzgerald DW, Watson-Jones D. Avoiding HIV and dying of syphilis. Lancet. 2004;364(9445):1561–1563. doi: 10.1016/S0140-6736(04)17327-3. [DOI] [PubMed] [Google Scholar]
- 7.Dinh TH, Kamb ML, Msimang V, Likibi M, Molebatsi T, Goldman T, et al. Integration of preventing mother-to-child transmission of HIV and syphilis testing and treatment in antenatal care services in the Northern Cape and Gauteng provinces, South Africa. Sexually transmitted diseases. 2013;40(11):846–851. doi: 10.1097/OLQ.0000000000000042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.M C, MF P, S M, et al. Enquete mortalité, morbidité et utilisation des services EMMUS–e Haïti 2005–2006. Pétionville and Calverton: Institut Haïtien de l’Enfance, ORC Macro; 2006. [Google Scholar]
- 9.Lomotey CJ, Lewis J, Gebrian B, Bourdeau R, Dieckhaus K, Salazar JC. Maternal and congenital syphilis in rural Haiti. Rev Panam Salud Publica. 2009;26(3):197–202. doi: 10.1590/s1020-49892009000900002. [DOI] [PubMed] [Google Scholar]
- 10.Tucker JD, Bien CH, Peeling RW. Point-of-care testing for sexually transmitted infections: recent advances and implications for disease control. Curr Opin Infect Dis. 2013;26(1):73–79. doi: 10.1097/QCO.0b013e32835c21b0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Tucker JD, Bu J, Brown LB, Yin YP, Chen XS, Cohen MS. Accelerating worldwide syphilis screening through rapid testing: a systematic review. The Lancet infectious diseases. 2010;10(6):381–386. doi: 10.1016/S1473-3099(10)70092-X. [DOI] [PubMed] [Google Scholar]
- 12.Tucker JD, Hawkes SJ, Yin YP, Peeling RW, Cohen MS, Chen XS. Scaling up syphilis testing in China: implementation beyond the clinic. Bulletin of the World Health Organization. 2010;88(6):452–457. doi: 10.2471/BLT.09.070326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Yang LG, Tucker JD, Liu FY, Ren XQ, Hong X, Wang C, et al. Syphilis screening among 27,150 pregnant women in South Chinese rural areas using point-of-care tests. PloS one. 2013;8(8):e72149. doi: 10.1371/journal.pone.0072149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Fitzgerald DW, Behets FM, Lucet C, Roberfroid D. Prevalence, burden, and control of syphilis in Haiti's rural Artibonite region. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases. 1998;2(3):127–131. doi: 10.1016/s1201-9712(98)90113-8. [DOI] [PubMed] [Google Scholar]
- 15.Fonn S. A blood-result turn-around time survey to improve congenital syphilis prevention in a rural area. South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde. 1996;86(1):67–71. [PubMed] [Google Scholar]
- 16.Ryan M, Farrar S. Using conjoint analysis to elicit preferences for health care. BMJ. 2000;320(7248):1530–1533. doi: 10.1136/bmj.320.7248.1530. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Lee SJ, Brooks R, Bolan RK, Flynn R. Assessing willingness to test for HIV among men who have sex with men using conjoint analysis, evidence for uptake of the FDA-approved at-home HIV test. AIDS Care. 2013;25(12):1592–1598. doi: 10.1080/09540121.2013.793272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Klausner JD, EW H. Current Diagnosis & Treatment of Sexually Transmitted Diseases. United States: The McGraw-Hill Companies, Inc; 2007. [Google Scholar]
- 19.Lee SJ, Newman PA, Comulada WS, Cunningham WE, Duan N. Use of conjoint analysis to assess HIV vaccine acceptability: feasibility of an innovation in the assessment of consumer health-care preferences. International journal of STD & AIDS. 2012;23(4):235–241. doi: 10.1258/ijsa.2011.011189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Bank TW. Haiti Overview. [Accessed October 9, 2015]; http://www.worldbank.org/en/country/haiti/overview2015. [Google Scholar]
- 21.Bristow CC, Larson E, Javanbakht M, Huang E, Causer L, Klausner JD. A review of recent advances in rapid point-of-care tests for syphilis. Sexual health. 2015 doi: 10.1071/SH14166. [DOI] [PubMed] [Google Scholar]
- 22.Garcia PJ, Carcamo CP, Chiappe M, Valderrama M, La Rosa S, Holmes KK, et al. Rapid Syphilis Tests as Catalysts for Health Systems Strengthening: A Case Study from Peru. PloS one. 2013;8(6):e66905. doi: 10.1371/journal.pone.0066905. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Gaydos C, Hardick J. Point of care diagnostics for sexually transmitted infections: perspectives and advances. Expert review of anti-infective therapy. 2014;12(6):657–672. doi: 10.1586/14787210.2014.880651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Guinard J, Prazuck T, Pere H, Poirier C, LeGoff J, Boedec E, et al. Usefulness in clinical practice of a point-of-care rapid test for simultaneous detection of nontreponemal and Treponema pallidum-specific antibodies in patients suffering from documented syphilis. International journal of STD & AIDS. 2013;24(12):944–950. doi: 10.1177/0956462413487328. [DOI] [PubMed] [Google Scholar]
- 25.Kuznik A, Lamorde M, Nyabigambo A, Manabe YC. Antenatal syphilis screening using point-of-care testing in Sub-Saharan African countries: a cost-effectiveness analysis. PLoS medicine. 2013;10(11):e1001545. doi: 10.1371/journal.pmed.1001545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Mabey D, Peeling RW, Ustianowski A, Perkins MD. Diagnostics for the developing world. Nature reviews Microbiology. 2004;2(3):231–240. doi: 10.1038/nrmicro841. [DOI] [PubMed] [Google Scholar]
- 27.Merchant RC, Clark MA, Seage GR, 3rd, Mayer KH, Degruttola VG, Becker BM. Emergency department patient perceptions and preferences on opt-in rapid HIV screening program components. AIDS Care. 2009;21(4):490–500. doi: 10.1080/09540120802270284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Bristow CC, Lee SJ, Leon SR, Ramos LB, Vargas Rivera SK, Caceres CF, et al. Assessing factors to increase uptake of testing for syphilis and HIV in men who have sex with men and transgender women in Lima, Peru. Sexually Transnmitted Diseases; STD Prevention Conference; June 9–12, 2014; Atlanta, Georgia. 2014. p. S141. http://www.cdc.gov/stdconference/2014/2014-std-prevention-conference-abstracts.pdf, editor. [Google Scholar]
- 29.Valderrama M, Garcia P. Acceptance of HIV/Syphilis Duo rapid testing: survey of attitudes of antenatal care providers. In: Diseases ST, editor. STD Prevention Conference; June 9–12, 2014; Atlanta, Georgia. 2014. p. S84. http://www.cdc.gov/stdconference/2014/2014-std-prevention-conference-abstracts.pdf; [Google Scholar]
- 30.Flores EC, Lluque ME, Chiappe M, Lino R, Bayer AM. Operations research study to implement HIV and syphilis point-of-care tests and assess client perceptions in a marginalised area of Lima, Peru. International journal of STD & AIDS. 2014 doi: 10.1177/0956462414552696. [DOI] [PMC free article] [PubMed] [Google Scholar]
