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Assisted reproduction services provision in a developing country: time to act? Alfred Murage, M.R.C.O.G., Murwa C. Muteshi, M.B., Ch.B., and Francis Githae, M.B., Ch.B. Aga Khan University Hospital, Nairobi, Kenya

Objective: To conduct a survey in a developing country to gauge the extent of subfertility and the current state of assisted reproductive technology (ART) service provision and explore factors limiting access to ART services. Design: Cross-sectional online survey. Setting: The study was co-ordinated at the Aga Khan University Hospital, Nairobi, Kenya. Subject(s): One hundred eighty-eight obstetricians and gynecologists registered with the Kenya Obstetrics and Gynecology Society were invited to complete the survey. Intervention(s): None. Main Outcome Measure(s): None. Result(s): A total of 47 responses (25%) were received after completion of the survey. The overall rate of subfertility was 26.1% among the gynecology consultations, with 50% attributed to tubal factors and 15% due to male factors. Assisted reproductive service provision (IVF/intracytoplasmic sperm injection) was severely limited to only three units, despite the reported high rate of tubal disease. The high cost of treatment, patients’ limited finances, and limited local services were almost universally cited as the main barriers to ART services in Kenya. Conclusion(s): The demand for ART in developing countries is not in doubt. Simplified, less costly, and more accessible ART approaches need to be considered in developing countries, even though the benefits and outcomes of such approaches may not be apparent immediately. (Fertil Steril 2011;96:966–8. 2011 by American Society for Reproductive Medicine.) Key Words: ART, service provision, costs, developing countries

Worldwide, more than 80 million couples suffer from infertility. The majority of this population are residents of developing countries where reproductive technologies are unavailable, scarcely available, or so costly that the large majority of the population cannot afford infertility treatment at all (1, 2). Tubal factor subfertility is the most common etiologic factor in developing countries, mainly caused by sexually transmitted diseases, postpartum or postabortal infections, pelvic tuberculosis, and schistosomiasis (2, 3). This condition renders itself treatable by assisted reproductive technology (ART), which unfortunately is not readily available in developing countries. Moreover, the negative consequences of childlessness are much stronger in developing countries when compared with Western societies. In many cultures childless women are stigmatized, which may lead to isolation, neglect, or domestic violence; or these women may end up as the second wife in a polygamous marriage. There is no doubt that in most developing countries infertile women are blamed for infertility, resulting in the social stigma of childlessness, even if they are not the cause of the infertility (1, 4). Reproductive health in developing countries concentrates more on family planning and contraception. Subfertility is relatively ignored, with an emphasis on a reduction in the number of births (1). The most cost-effective approach to tackle infertility problems in developing countries is prevention and education. However, in those Received May 6, 2011; revised July 18, 2011; accepted July 19, 2011; published online August 16, 2011. A.M. has nothing to disclose. M.C.M. has nothing to disclose. F.G. has nothing to disclose. Reprint requests: Alfred Murage, M.R.C.O.G., Aga Khan University Hospital, Nairobi, Department of Obstetrics and Gynecology, P.O. Box 30270-00100, Nairobi, Kenya (E-mail: alfred.murage@aku.edu).

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cases in which prevention has failed, simplified assisted reproduction must be thought of as a valuable option (5, 6). Increasingly, there is an increase in private ART units in developing countries, mostly modeled on western ART practice and hardly affordable to most of the needy population. In this respect, the World Health Organization has previously highlighted this issue of ART in developing countries (7). Even though ART has evolved for more than 30 years, it is only accessible to a small proportion of the world population (1). This survey was therefore conducted to gauge the extent of subfertility and the current state of ART service provision and to explore factors limiting ART access in a developing country. The time has come to urgently address the fertility provision gap in developing countries, by incorporating simplified and cost-effective ART programs to serve as valid treatment protocols when other alternatives and preventive measures have failed. Data on the outcomes of such simplified and less-expensive approaches must, however, be continually monitored and analyzed, in an attempt to measure costeffectiveness and benefits.

MATERIALS AND METHODS An online electronic survey among practicing Kenyan gynecologists registered with the Kenya Obstetrics and Gynaecological Society (KOGS) was conducted for a duration of 3 months between October and December 2010. The survey was conducted using a popular commercial online platform, SurveyMonkey (8). The survey questionnaire was developed, uploaded onto the SurveyMonkey platform, and initially pretested before commencing the survey. The KOGS approved use of the e-mail database of registered members for the purposes of this survey. The pretested questionnaire was uniquely linked to each KOGS members’ specific e-mail address and then e-mailed as a hyperlink accompanied by a brief introduction of the survey. The survey introduction was sent via the first author’s official e-mail address in an attempt to mitigate the

Fertility and Sterility Vol. 96, No. 4, October 2011 Copyright ª2011 American Society for Reproductive Medicine, Published by Elsevier Inc.

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survey link being interpreted as spam. Half way through the survey, an automated reminder was sent to those who had not responded, to increase the response rates. Data collected were automatically archived and preanalyzed via SurveyMonkey’s software before being downloaded for detailed analysis.

RESULTS A total of 188 e-mail links were generated after excluding duplicate and nonactive e-mail accounts. A total of 47 completed responses were received after one automated reminder, giving a total response rate of 25%. The response rate was relatively comparable to reported average online survey response rates, which are approximately 30% (8, 9). The majority of respondents, 88.4%, were engaged in both hospital and office-based practice (this is a common gynecologic practice pattern in Kenya). Seven respondents (17.5%) were practicing mainly reproductive medicine, either as subspecialists or as an area of special interest. The rest of the respondents were mostly general gynecologists (72.5%), with 10% having other obstetrics and gynecology subspecialties. Just over half (54.8%) reported maintaining a database of their practice, thus enhancing survey data reliability. The overall rate of subfertile patients seeking gynecologic consultations was 26.14%, or one out of every four patients (Fig. 1). Although this figure may be an overestimate, adjusting this to only those who had a practice database still resulted in a high rate of fertility consultations of approximately one in eight. Access to fertility investigations was almost universal. In terms of disease category, just over half of all fertility-related consultations (50.3%) were due to tubal factors, whereas 14.8% were due to male factors. This finding implied that more than 50% of new fertility-related consultations were likely to require ART (other disease patterns that may eventually require ART, e.g. ovulatory disorders, were not surveyed). Assisted reproductive service provision (IVF/intracytoplasmic sperm injection [ICSI]) was severely limited to only three units in the survey, despite the reported high rate of tubal disease. This was in stark contrast to almost universal access to fertility investigations, with the obvious implications of practitioners being able to make a diagnosis but having limited choice in terms of offering treatment. Referrals for ART were mainly to the local units but also as far away as South Africa and India. However, simple ovulation induction with

FIGURE 1 Categories of new gynecologic consultations per month (n ¼ 1,977).

Murage. Assisted reproduction services in Kenya. Fertil Steril 2011.

Fertility and Sterility

antiestrogens was universally practiced by all respondents. Just over half (55.6%) used gonadotropins in combination with IUI for ovulation induction. The high cost of treatment, patients’ limited finances, and limited local services were almost universally cited as the main barriers to ART services in Kenya. Verbatim quotes on ART services provision barriers included ‘‘exorbitant cost,’’ ‘‘high cost and few facilities,’’ ‘‘unavailability of services and costs,’’ ‘‘cost and lack of competition.’’ The costs of treatment were almost universally borne through self-funding, severely limiting access to ART.

DISCUSSION This survey has shed some light on the scope of subfertility in a developing country, where such data are either scanty or completely lacking. The data, even though not generalizable to other developing countries, is in keeping with similar rates and needs related to subfertility reported elsewhere in developing countries (1). The 25% response rate is close to the reported average response rates of online surveys (9). Although it would have been desirable to achieve a higher response rate, the data collected likely represent the current state of subfertility in Kenya. Previous local data are dated and mainly hospital-based (10, 11). There is a local paucity of gynecologists compared with the population (and even fewer fertility subspecialists), but subfertile patients are more likely to consult or be referred to the targeted population of gynecologists. The overall estimated rate of subfertility (26%) compares to reported rates in other developing countries, with a predominance of tubal disease (12, 13). In Nigeria, for example, it was previously reported that subfertility is the most common reason for gynecologic consultations, again with tubal disease being the most prevalent (12). This immediately brings into prominence prevention strategies for tubal disease and their effectiveness. The most common causes are already known to include sexually transmitted infections and postabortal sepsis, which easily render themselves amenable to public health–focused initiatives. A public health strategy focusing on primary prevention would reduce the prevalence of infertility, improve health and quality of life, and avert the costs of infertility treatment, including the unaffordable downstream costs produced by adverse outcomes of such treatment on mothers and children (14). The data show an obvious disparity between availability of investigations to make a diagnosis and consequent service provision in terms of ART. There is almost 100% availability of biochemical, hormonal, and imaging tests to arrive at a diagnosis. The predominance of tubal disease, 50.3% in this survey, implies a high demand for IVF services. At least half the patients consulting for fertility problems are likely to require IVF/ICSI, judging by the reported rates of tubal disease and oligospermia. The reported rates of oligospermia may be an underestimate, however, because culturally most African men shy away from semen analysis. The contrast between diagnosed primary disease and service availability is clear, to say the least, with only three fully fledged IVF/ICSI units (at the time of the survey); there are, however, more readily available options for ovulation induction/IUI. Some patients were referred to as far away as India and South Africa. But the majority of patients needing ART came to an abrupt stop in pursuing treatment after diagnosis, mostly because of the high cost of treatment. For such patients, this is a tragic end to their desire for childbearing. Reproductive health care in developing countries focuses on other priorities, and with limited budgets this means that fertility treatment is often ignored. This should not be the case, however. Cost-effective prevention and education

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strategies must be put in place, and where these have failed, affordable ART must be thought of as a valuable option (1). The main barrier to ART in developing countries is cost, both in terms of unit setup and direct costs of diagnosis and treatment. Data from this survey show that nearly 90% of patients had to self-fund their treatment, with costs amounting to approximately US $4,000 per one IVF cycle (calculated from one private local IVF unit). There is hardly any funding from the public or insurance companies, thus cutting off the majority of patients from ever accessing any treatment. Strategies can be put in place to incorporate fertility care into already existing health care services, even if only at the preventive and educational levels, and this may equate to potential reduction in the prevalence of subfertility. Additionally, the medical insurance industry should view subfertility as a disease meriting insurance benefits. Savings would be realized by eliminating hidden infertility costs, eliminating payments for ineffective treatments, and providing coverage for effective 21st century treatments with already proven outcomes (1, 15). Much has been written and debated about strategies to improve access to fertility treatment in developing countries, but the implementation of such strategies has not been forthcoming. Current fertility treatments in developing countries are modeled on standards and protocols in use in affluent and developed countries, where funding for treatment is usually available or incorporated into existing health care programs. Clearly this is not practical in most developing countries. Simplified diagnostic procedures, monitoring, and

treatment protocols must be put in place. Use of adaptive technology (e.g., low-tech incubators, like converted humidicribs) may also contribute to reduction in cost (1, 16, 17). Such strategies may be associated with lower pregnancy rates or longer conception intervals. This would therefore mandate well-maintained prospective data and/or pilot studies to assess the economics and costeffectiveness of such approaches. Additionally, there is hardly any fertility practice regulation in developing countries. This potentially exposes patients to substandard and costly care, with the potential for complications and unwanted outcomes (for example multiple pregnancies resulting from multiple ETs). This could easily be addressed via medical regulatory authorities, with lobbying and support from local gynecologic/fertility societies. In conclusion, the demand for ART in developing countries is not in doubt. Although preventive measures are undoubtedly the most cost-effective approach in such low socioeconomic settings, not offering assisted reproduction is not an alternative when prevention and other options have failed. The real benefits of simplified, less costly, and more accessible ART approaches may not be apparent immediately. In the longer run, this may be the only alternative for millions of couples in the developing world with infertility, who presently have no choice but to contend with undesired childlessness. Acknowledgments: The authors thank the Kenya Obstetrical and Gynaecological Society for permission to use their database of registered members.

REFERENCES 1. Ombelet W, Campo R. Affordable IVF for developing countries. Reprod Biomed Online 2007;15:257–65. 2. Nachtigall RD. International disparities in access to infertility services. Fertil Steril 2006;85:871–5. 3. World Health Organization. Infections, pregnancies and infertility: perspectives on prevention. Fertil Steril 1987;47:944–9. 4. Van Balen F, Gerrits T. Quality of infertility care in poor-resource areas and the introduction of new reproductive technologies. Hum Reprod 2001;16:215–9. 5. Leke RJ, Oduma JA, Bassol-Mayagoitia S, Bacha AM, Grigor KM. Regional and geographical variations in infertility: effects on environmental, cultural, and socioeconomic factors. Environ Health Perspect 1993;101(Suppl 2):73–80. 6. Malpani A, Malpani A. Simplifying assisted conception techniques to make them universally available— a view from India. Hum Reprod 1992;7:49–50.

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7. Daar AS, Merali Z. Infertility and social suffering: the case of ART in developing countries. In: Vayena E, Rowe PJ, Griffin PD, editors. Current practices and controversies in assisted reproduction: Report of a WHO meeting. Geneva: WHO; 2002. p. 15–21. 8. SurveyMonkey. Online survey software and questionnaire tool. Available at: www.surveymonkey. com. Accessed September 1, 2010. 9. SurveyMonkey. Best Practices for Survey Design: Available at: http://help.surveymonkey.com/euf/assets/docs/ pdf/SmartSurvey.pdf?noIntercept/1. Accessed February 12, 2011. 10. Mathews T, Mati JK, Fomulu JN. A study of infertility in Kenya: results of investigation of the infertile couple in Nairobi. East Afr Med J 1981;58:288–97. 11. Muthuuri JM. Male infertility in a private Kenyan hospital. East Afr Med J 2005;82:362–5.

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12. Okonofua FE. The case against new reproductive technologies in developing countries. Br J Obstet Gynaecol 1996;103:957–62. 13. Larsen U. Primary and secondary infertility in subSaharan Africa. Int J Epidemiol 2000;29:285–91. 14. Macaluso M, Wright-Schnapp TJ, Chandra A, Johnson R, Satterwhite CL, Pulver A, et al. A public health focus on infertility prevention, detection, and management. Fertil Steril 2010;93:1–10. 15. Jones HW Jr, Allen BD. Strategies for designing an efficient insurance fertility benefit: a 21st century approach. Fertil Steril 2009;91:2295–7. 16. Pilcher H. IVF in Africa: fertility on a shoestring. Nature 2006;442:975–7. 17. Muasher SJ, Garcia JE. Fewer medications for in vitro fertilization can be better: thinking outside the box. Fertil Steril 2009;92:1187–9.

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