Cross-border reproductive care: a review of the literature

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1 Reproductive BioMedicine Online (2011) 22, REVIEW Cross-border reproductive care: a review of the literature Nicky Hudson a, *, Lorraine Culley b, Eric Blyth c, Wendy Norton d, Frances Rapport e, Allan Pacey f a School of Applied Social Sciences, De Montfort University, 0.15b Hawthorn Building, The Gateway, Leicester LE1 9BH, UK; b School of Applied Social Sciences, De Montfort University, 0.15a Hawthorn Building, The Gateway, Leicester, LE1 9BH, UK; c Human and Health Sciences, University of Huddersfield, Queensgate, Huddersfield, HD1 3DH, UK; d School of Nursing and Midwifery, De Montfort University, London Road, Leicester, LE2 1RQ, UK; e School of Medicine, Swansea University, Singleton Park, Swansea, SA2 8PP, UK; f Academic Unit of Reproductive and Developmental Medicine, Level 4 The Jessop Wing, Tree Root Walk, University of Sheffield, Sheffield, S10 2SF, UK * Corresponding author. address: nhudson@dmu.ac.uk (N Hudson). Nicky Hudson is a sociologist and researcher at De Montfort University with interests in medicine, reproduction, gender and ethnicity. Lorraine Culley is Professor of Social Science and Health at De Montfort University and has lead several projects exploring social aspects of assisted reproduction treatment. Eric Blyth is Professor of Social Work at Huddersfield University and co-chairs the British Association of Social Workers Project Group on Assisted Reproduction. Wendy Norton is Senior Lecturer in Nursing at De Montfort University, specializing in the management of sexual health, gynaecology and infertility. Frances Rapport is Professor of Qualitative Health Research and leads the Qualitative Research Unit (QUARU) at Swansea University. Allan Pacey is Senior Lecturer in Andrology at the University of Sheffield and Head of Andrology for Sheffield Teaching Hospitals. Abstract Cross-border reproductive care (CBRC) has attracted considerable attention in media and professional publications. The aim of this review is to present a critical narrative overview of the published evidence on CBRC. A systematic search of key academic databases was undertaken with no time restrictions set for publication. This was supplemented by additional searches of key websites, reference chaining and enquiries to people working in the field. A total of 54 items are included in the review, including both empirical research studies (18) and debate papers (36). The key themes discussed are: terminology and definitions; incidence; experiences; explanations; implications; and policy responses. Significant methodological limitations and gaps in the literature are identified. Evidence on incidence is scant, though it suggests that CBRC is increasing. The literature suggests legal, social and political drivers, which vary in importance geographically and between individuals. Limited findings on patient perceptions suggest a broadly positive patient experience. Suggested policy responses include prohibition, regulatory harmonization and harm minimization. There is a need for better international data collection tools and both quantitative and qualitative work which encompasses views of patients, donors, surrogates and professionals and which explores the implications for healthcare services in sending countries. RBMOnline ª 2011, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. KEYWORDS: cross-border reproductive care, fertility tourism, reproductive tourism Introduction Seeking assisted reproduction technologies across borders appears to be a growing phenomenon, part of a wider trend of what is often termed medical tourism (Gray and Poland, 2008). The globalization of assisted reproduction technology has paralleled the growth of a consumer culture in health care more generally (Slater, 1997). Technical /$ - see front matter ª 2011, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. doi: /j.rbmo

2 674 N Hudson et al. advances in treatment have accompanied a growth in the commodification of reproduction, producing a highly lucrative fertility industrial complex (Spar, 2006) operating in a global market that transcends national boundaries. This phenomenon has attracted a steady increase in public, professional and academic discourse. A review of the evidence base and emergent academic debates in the context of these developments was therefore considered timely. This review of the current state of knowledge on cross-border reproductive care (CBRC) in the English-language literature was conducted as part of a research project exploring the experiences of UK residents who are seeking travel abroad for fertility treatment, the results of which will be published separately. 36 records retrieved via reference chaining and contacts Stage One Database search 875 potentially relevant titles Stage two 46 potentially relevant database abstracts reviewed 829 excluded titles 28 excluded records Materials and methods Database search Given the new and contested nature of the topic and the fragmented nature of the literature on CBRC, a conventional systematic review was not considered appropriate. Instead, this study undertook a systematic search of academic databases, combined with additional searches to Table 1 Search terms. Cross-border egg/sperm donation Cross-border in/fertility treatment Cross-border IVF Cross-border reproduction Cross-border reproductive care Cross-border reproductive treatment Cross-border surrogacy Egg donor/donation abroad/overseas Fertility tourism Fertility travel Health tourism Health travel Infertility treatment abroad/overseas International egg/sperm donor/donation International in/fertility treatment International IVF International reproduction International surrogacy IVF abroad/overseas Medical tourism Medical travel Overseas in/fertility treatment Overseas reproductive care PGD abroad/overseas Procreative tourism Reproductive exile Reproductive tourism Reproductive travel Single-embryo transfer Sperm donor/donation abroad/overseas Surrogacy abroad/overseas Transnational reproduction produce a critical narrative overview of the current state of knowledge, rather than attempting to rank individual research papers (Dixon-Woods et al., 2006). Given the fact that the phenomenon of travelling across borders for fertility treatment has been variously described (see later), a large number of search terms were employed in the database search (Table 1). The databases searched were Academic Search Premier, ASSIA, BHI, British Nursing Index, CINAHL, HMIC, IBSS, Ingenta Connect, Medline, NRR, PsycINFO, Science Direct, Science Citation Index, Scopus and COPAC using the terms in Table 1. This generated 875 papers (see Figure 1), of which 829 papers were excluded because they did not contain a discussion of CBRC, were duplicate titles, were not available in English or were press reports. Of the remaining 46, a further 28 were excluded because they were about a related issue (e.g. medical tourism more generally) (n = 22), were commentaries with only a secondary focus on CBRC (n = 5) or were further duplicates (n = 1). This left 18 full text papers from the database search for inclusion in the review. Additional searches To access other potentially important literature in this emerging field of enquiry, the database search was complemented with reference chaining, searches of key websites and contacts in the field to identify additional papers (Dixon-Woods et al., 2006). This yielded an additional 36 items which were included in the review following assessment. It is noteworthy that these searches produced a number of papers that were recently published, partially published or in press and this was regarded as a particular strength of the study s approach. Results Stage three Abstraction 54 full papers (18 database papers 36 additional papers) Figure 1 Study selection process. The strategy described above yielded 54 papers to be included in the review. To assist the presentation of the review the papers are grouped according to their focus, publication status and whether or not they are based on

3 Cross-border reproductive care: A review of the literature 675 Table 2 Publication Papers included in the review. Sample and location Method Focus of paper Published research studies based on empirical data with a central focus on CBRC (n = 9) Blyth (2010) 28 Patients, Canada and Australia Online questionnaire Patient views of actual or intended CBRC Hughes and Dejean (2010) 28 Canadian and 125 American clinics, Canada and US Questionnaire Clinician experiences of receiving or sending CBRC patients Inhorn and Shrivastav (2010) 125 Patient couples, United Arab Emirates Interviews Explores patient experiences of CBRC in the Middle East using the work of Appardurai Nygren et al. (2010) 23 Countries, Worldwide Survey National estimated data on numbers of patients engaged in CBRC Pennings et al. (2009) 16 Infertility clinics, Belgium Questionnaire Clinician experiences of receiving CBRC patients Pennings (2010) 270 Patients, drawn from larger sample of 1230, Europe Questionnaire Discussion of ESHRE data on European patient travel for sperm donation Shenfield et al. (2010) 1230 Patients, Europe Questionnaire Patient experience of CBRC in Europe Smith et al. (2009) Whittaker and Speier (2010) 21 Accredited and 2 nonaccredited fertility clinics, Argentina 6 Couples in Thailand, 3 former USbased clients and 2 owners of an IVF holiday company, Czech Republic Comparative website analysis Interviews Comparison of services offered and marketing strategies of private fertility clinics Uses cases drawn from two independent studies to discuss broader theoretical and ethical debates on CRBC Unpublished or partially published research studies based on empirical data with a central focus on CRBC (n = 6) Bartolucci (2008) 500 Infertility patients, Italy Questionnaire Ongoing study looking at numbers and experiences of patients travelling outside of Italy for treatment Bergmann (2007) Sample not stated, Spain Observation Practices of gamete donation in Spanish clinics and implications for transnational kinship Bergmann (2010) 4 Case studies: Spain, Denmark, Czech Republic Interviews Uses empirical patient case studies to highlight broader theoretical and ethical debates on CBRC Patient views of actual or intended CBRC Discussion of reproductive tourists and the women who assist them: egg donors, maids and nannies Infertility Network UK (2008) 75 Members, UK Online questionnaire Inhorn (2009) 3 Case studies from larger sample Interviews of 125 couples, United Arab Emirates Inhorn and Patrizio (2009) 125 Couples, United Arab Emirates Interviews Discusses problematic nature of the term reproductive tourism and the complexity of the reasons for travel Published research studies based on empirical data with a secondary focus on CBRC (n = 3) McKelvey et al. (2009) 24 Patients, UK NHS data audit Numbers of patients with multiple pregnancies having conceived abroad (continued on next page)

4 676 N Hudson et al. Table 2 (continued) Publication Sample and location Method Focus of paper Pande (2009) 42 Interviews Experiences of surrogates in India Surrogates, India Whittaker (2009) 3 Couples, Interviews Study of local users of fertility clinics in Thailand Thailand Published commentary/debate with a central focus on CBRC (n = 36) Blyth (2006) NA Commentary Outlines concerns and risks associated with CBRC Blyth and Farrand (2005) NA Commentary Considers patient motivations and implications of CBRC Chung (2006) NA Commentary Discusses the market in human gametes and suggests that CBRC is an expression of this Ciocci et al. (2006) NA Commentary Expresses concerns about the rights of children born via CBRC Cohen (2006) NA Commentary Considers patient motivations and suggests that CBRC is an expression of moral autonomy Collins and Cook (2010) NA Commentary Discussion of issues raised at first forum on CBRC held in Ottawa Culley and Hudson (2009) NA Commentary Presents a sociological agenda for the study of CBRC Davies (2010) NA Commentary Describes the role and remit of the Human Fertilization and Embryology Authority in relation to CBRC Deech (2003) NA Commentary Draws on legal cases involving import and export of gametes to discuss harmonisation of leglisation Ferraretti et al. (2010) NA Commentary Discusses causes and implications of, and solutions to, CBRC Heng (2006a) NA Commentary Expresses concerns about referral practices and financial benefits involved in CBRC Heng (2006b) NA Commentary As above. Also suggests that doctors who refer patients abroad should be penalised Heng (2007a) NA Commentary As above Heng (2007b) NA Commentary Discusses CBRC in South East Asia focusing on payment of donors in Tawain Ikemoto (2009) NA Commentary Raises concerns about inequalities caused and perpetuated by CBRC Mainland and Wilson (2010) NA Commentary Reports on reasons for the establishment of the first forum on CBRC Martin (2009) NA Commentary Discusses the role of globalisation in the emergence of CBRC Matorras (2005) NA Commentary Discussion of the terminology used to describe CBRC Merrick (2007) NA Commentary Discusses the potential causes and implications of CBRC Mladovsky (2006) NA Commentary Discusses the potential causes and regulation of CBRC Pennings (2002) NA Commentary Discusses the potential causes and regulation of CBRC Pennings (2004) NA Commentary Discusses causes and implications of, and solutions to, CBRC Pennings (2005) NA Commentary Response to Mattoras. Discussion of terminology Pennings (2006a) NA Commentary Discusses causes and implications of, and solutions to, CBRC Pennings (2006b) NA Commentary Discusses causes and implications of, and solutions to, CBRC Pennings (2009) NA Commentary Discusses causes and implications of, and solutions to, CBRC Pennings et al. (2008) NA Commentary ESHRE task force discuss reasons for and solutions to CBRC Pennings and Mertes (2010) NA Commentary Discussion of possible state responses to CRBC Sauer (1997) NA Commentary Argues that restriction of payment to donors in the UK will lead to CBRC Smith-Cavros (2010) NA Commentary Discusses causes and implications of CBRC Spar (2005) NA Commentary Discusses legal, political and financial aspects of CBRC in the US context Storrow (2005a) NA Commentary Compares CBRC with sex tourism and overseas adoption. Expresses concerns about the exploitation of women Storrow (2005b) NA Commentary Compares Atwood s The Handmaid s Tale to CBRC. Expresses concern about the exploitation of women (continued on next page)

5 Cross-border reproductive care: A review of the literature 677 Table 2 Publication (continued) Sample and location Method Focus of paper Storrow (2010) NA Commentary Discusses legislative implications of CRBC Thorn and Dill (2010) NA Commentary Suggests that patient organisations have a central role to play in supporting those who engage in CBRC Turone (2006) NA Commentary Discusses CBRC in the Italian context CBRC = cross-border reproductive care; ESHRE = European Society of Human Reproduction and Embryology; NA = not applicable. empirical research or are commentary or opinion papers (Table 2). In summary, they are organized as follows: (i) published studies based on empirical data with a central focus on CBRC (n = 9); (ii) unpublished or partially published studies based on empirical data with a central focus on CRBC (n = 6); (iii) published studies based on empirical data with a secondary focus on CBRC (n = 3); and (iv) published commentary/debate with a central focus on CBRC (n = 36). It was not appropriate to undertake a conventional systematic assessment of the research quality of such a heterogeneous collection of work (Centre for Reviews and Dissemination, 2009). Consequently, this review presents a narrative, thematic summary and appraisal of the field, together with the identification of significant gaps in the research literature. The themes for the review were generated through thematic coding of the content and were discussed and agreed by all team members. They are presented here under the following headings: terminology and definitions of CBRC; incidence of CBRC; experiences of CBRC; explanations for CBRC; implications of CBRC; and policy responses to CBRC. Terminology and definitions of CBRC This theme describes the terminology and definitions of CBRC used in the papers reviewed here. As discussion about the nature and extent of travelling abroad to access assisted reproduction technology has grown, so too has debate about appropriate terminology to describe it (Culley and Hudson, 2009; Inhorn and Patrizio, 2009; Matorras, 2005; Pennings, 2005, 2006a). The term procreative tourism was first used by Knoppers and LeBris (1991). Subsequently, the term reproductive tourism (also fertility tourism ) has been frequently employed (Bergmann, 2010; Blyth, 2006; Blyth and Farrand, 2005; Chung, 2006; Ciocci et al., 2006; Cohen, 2006; Culley and Hudson, 2009; Deech, 2003; Heng, 2006b, 2007b; Ikemoto, 2009; Inhorn, 2009; Inhorn and Shrivastav, 2010; Martin, 2009; McKelvey et al., 2009; Mladovsky, 2006; Pennings, 2002, 2004, 2006a,b; Spar, 2005; Smith et al., 2009; Storrow, 2005a,b) since the phenomenon is conceived as a variant of the wider trend of medical tourism. However, an emerging consensus has begun to question the appropriateness of the word tourism, as this implies choice, pleasure and relaxation; a representation not in keeping with the physical and emotional challenges of fertility treatment (Inhorn and Patrizio, 2009). The term reproductive exile has featured in some publications, suggesting that patients are compelled into leaving their home countries in order to access the services they need (Inhorn and Patrizio, 2009; Mattorras, 2005). Others object to the term s negative connotations, arguing that compulsion is not always evident (Pennings, 2005). The terms reproductive travel or assisted reproduction technology travel (see Inhorn and Patrizio, 2009) suggest a more neutral stance, though they have not achieved wide usage so far. Transnational reproduction has been proposed since it links the process of procreation with the more general processes of globalization (Culley and Hudson, 2009; Whittaker, 2009), although this does not adequately account for travel within countries such as Australia or the USA where there are inter-state regulatory differences. More recently, cross-border reproductive care (CBRC) has been proposed by several commentators, including European Society of Human Reproduction and Embryology (ESHRE) (Pennings et al., 2008), and will be adopted in this review. It is used here with the acknowledgement that for some, care may not necessarily be an appropriate term. Incidence of CBRC Fifteen items in the review were based on empirical research and had a primary focus on CBRC (Bartolucci, 2008; Bergmann, 2007; Bergmann, 2010; Blyth, 2010; Hughes and Dejean, 2010; Infertility Network UK, 2008; Inhorn, 2009; Inhorn and Patrizio, 2009; Inhorn and Shrivastav, 2010; Nygren et al., 2010; Pennings, 2010; Pennings et al., 2009; Shenfield et al., 2010; Smith et al., 2009; Whittaker and Speier, 2010). These papers vary in coverage and methodology, but give some indications of the incidence of CBRC. They include quantitative, questionnaire-based surveys conducted with patients (Bartolucci, 2008; Blyth, 2010; Infertility Network UK, 2008; Pennings, 2010; Shenfield et al., 2010) clinics (Hughes and Dejean, 2010; Pennings et al., 2009) or at the global level (Nygren et al., 2010). A smaller number of qualitative studies also give some suggestions of patterns of patient travel (Bergmann, 2010; Inhorn, 2009; Inhorn and Shrivastav, 2010; Whittaker and Speier, 2010). European studies Shenfield et al. (2010) provide the most comprehensive survey of CBRC to date, surveying 46 clinics in Belgium, the Czech Republic, Denmark, Switzerland, Slovenia and Spain for 1 month between October 2008 and March A total of 1230 completed patient questionnaires were analysed. Receiving countries reported patients travelling from 49 countries: Italy (31.8%), Germany (14.8%), the Netherlands (12.1%) and France (8.7%) emerging as the four major sending countries, followed by Norway (5.5%), the UK (4.3%) and

6 678 N Hudson et al. Sweden (4.3%). Italians were most likely to seek treatment in Spain or Switzerland, Germans in the Czech Republic, Dutch and French patients in Belgium, British patients in the Czech Republic and Spain, and Swedish and Norwegian patients in Denmark. Intrauterine insemination was sought by 22.2% of patients, assisted reproduction technology by 73% and both by 4.9%; 22.8% were using donor eggs, 18.3% donor sperm and 3.4% donor embryos. Although the authors caution against extrapolation to the rest of Europe, they do offer some generalizations based on their findings, suggesting that 24,000 30,000 cycles of cross-border treatment could be taking place within Europe annually, involving 11,000 14,000 patients. These data were also analysed according to patients use of gamete and embryo donation (Pennings, 2010). This second article shows that patients from France, Norway and Sweden were the most likely to travel for donor insemination and that German and British patients the most likely to travel for egg donation. Denmark, Belgium and Switzerland were the most commonly visited countries amongst patients seeking sperm donation, with Spain and the Czech Republic popular amongst those seeking egg and embryo donation. A second separate European survey (Pennings, 2010; Pennings et al., 2009) draws on questionnaire data gathered from staff in 16 Belgian infertility clinics (88.8% of invited clinics responded). Data for a 3-year period from 2005 to 2007 demonstrated that the principal home countries for foreign patients were France (38%), the Netherlands (29%), Italy (12%) and Germany (10%). Partial clinic figures for also show a steady increase of international patients seeking treatment in Belgium, rising from 1456 patients in 2003, to 2117 patients in During this period, international patients were most likely to seek donor insemination (n = 3071, 34%), intracytoplasmic sperm injection (ICSI) (n = 2646, 29%), IVF with own gametes (n = 977, 11%) or treatment with donor eggs (n = 746, 8%). Treatment type was also analysed by country (for the period ); the most common combination was French patients seeking donor insemination (80% of donor insemination patients) and Dutch patients using ICSI (66% of ICSI patients). Focusing specifically on Britain, the patient organization Infertility Network UK carried out an online survey in 2008 (n = 339 responses), in which 76% of respondents indicated they would consider travelling abroad for treatment, with just 22% (n = 75) reported having done so. The three main treatments sought were egg donation (41.3%), ICSI (25.3%) and IVF (13.3%), and the most commonly mentioned destination was Spain. Spain was also found to be a destination of choice amongst a small number of participants in Bergmann s ethnographic study of European clinics (Bergmann, 2010). Early findings from this research show patient movement between France and Spain, the UK and Spain, and Germany and the Czech Republic. However, this paper is based on only four cases. US, Canadian and Australian studies Hughes and Dejean (2010) undertook a questionnaire survey of Canadian and US clinics and clinicians in Although partially based on estimates, their survey begins to show some patterns of movement of Canadian patients to the USA and a smaller number of US patients seeking IVF in India, Asia, Europe and Canada. Twenty-eight responses were received from Canadian clinics/clinicians (82% response rate) and 125 from US clinics/clinicians (32% response rate). Canadian clinics reported that 452 patients sought treatment outside Canada each year. The majority of these were seeking treatment with anonymous donor eggs in the USA. A small movement from the USA to Canada was also described (representing approximately 1.5% of treatment in Canada), with these patients primarily seeking IVF. US clinics reported 1399 women entering the USA for treatment per year (4% of their treatments). The largest groups of incoming patients were from Latin America (39%) and Europe (25%). Fifty-one percent of patients entering the USA sought IVF. The majority of women seeking anonymous egg donation in the USA were from Europe (45%) and Latin America (22%). US clinics estimated that 217 of their patients left the USA each year for treatment in another country, with 72% seeking standard IVF. Thirty-nine percent of these patients went to India/Asia and 22% to (unspecified) European countries. Just over half of those seeking anonymous egg donations (13/25) sought treatment in India/Asia. Whittaker and Speier (2010) also highlight patient movement from the USA to the Czech Republic, though this paper is based on data collection with only a small sample (n = 3) of US patients. In a second survey, using an amended version of Infertility Network UK s online patient questionnaire (Infertility Network UK, 2008), Blyth (2010) collected data via three patient organization websites: ACCESS Australia, Infertility Awareness Association of Canada and Infertility Network Canada. Between July and September 2008, 95 useable responses were posted by users or intended users of CBRC, including 28 from people who had used a clinic in a foreign country. Data on country of origin, destination country and treatment sought was only available for 21 of the latter, demonstrating that the USA was the most popular destination for Canadian patients (n = 10), the majority of whom (n = 7) used donor eggs. Three patients from Australia reported travelling to the USA for treatment. The survey also included one patient from Greece, two from the UK and two from the USA. Egg donation was the most commonly stated treatment for those who had been abroad (15/28, 54%), whilst IVF was the most frequently mentioned treatment by those who were considering travelling (39/59, 66%). The majority of respondents who gave their age (n = 91) were over 30. Of those answering, 86% (of 88 responses) had received treatment in their own country prior to considering travel and 56% (of 64 responses) had been in treatment for at least 3 years before seeking or considering CBRC. Worldwide studies Nygren et al. (2010) report a retrospective study involving 49 countries currently participating in international data collection for the publication of IVF World Reports. However, just 23 countries provided data in 2008, and 20 responses were only able to provide estimated data at country level (rather than clinic or patient level). Based on information regarding outgoing treatment cycles provided by 11 countries, the paper estimates that over 5000 cross-border treat-

7 Cross-border reproductive care: A review of the literature 679 ment cycles were performed in more than 25 countries. Of 15 recipient countries reporting, an estimated 7000 couples received treatment, travelling from more than 38 different countries, most of them in nearby regions. It is difficult to draw firm conclusions from this study due to the underlying incomplete and largely estimated data, although the study does confirm that minimal monitoring of the incidence of CBRC at the national or international level is taking place. Early reports from Marcia Inhorn s recent research demonstrate the United Arab Emirates as a popular destination for patients, particularly those who have familial, cultural or economic affinities with this region (Inhorn, 2009; Inhorn and Patrizio, 2009; Inhorn and Shrivastav, 2010). Finally, in an ethnographic study not directly focused on CBRC, Thailand was highlighted as a destination for couples seeking fertility treatment away from home, again, particularly those with familial links to the country (Whittaker, 2009; Whittaker and Speier, 2010). Experiences of CBRC Ten papers make reference to the experiences of patients or the clinicians providing their care (Bergmann, 2010; Blyth, 2010; Hughes and Dejean, 2010; Infertility Network UK, 2008; Inhorn, 2009; Inhorn and Shrivastav, 2010; Pennings et al., 2009; Shenfield et al., 2010; Whittaker, 2009; Whittaker and Speier, 2010). These tend to be drawn from predefined survey questions and are limited in both scope and depth, or in the case of papers providing early reports from qualitative studies, draw on only a very small number of cases and provide little detail about patient experiences (Bergmann, 2010; Whittaker and Speier, 2010). One further empirically based, qualitative study discusses the experiences of Indian women who act as surrogates, some of whom carry pregnancies for international couples (Pande, 2009). Patient experiences Eight papers report on data collected directly from patients (Bergmann, 2010; Blyth, 2010; Infertility Network UK, 2008; Inhorn, 2009; Inhorn and Shrivastav, 2010; Shenfield et al., 2010; Whittaker, 2009; Whittaker and Speier, 2010), whilst two report data about patient experiences collected from clinicians (Hughes and Dejean, 2010; Pennings et al., 2009). The key issues reported were sources of information, how treatment was arranged, language/communication, waiting times, cost, availability of donors (see also Bergmann, 2007), significance of place and counselling. The internet emerges as a major source of information for patients travelling or planning CBRC. Shenfield et al. (2010) highlight some nuance in this picture, demonstrating that although the internet was the main source of information for Swedish, German and British patients, for Italian women it was their own doctor. Other sources of information include friends, relatives and patient organizations, although these appeared to be less significant (Blyth, 2010; Shenfield et al., 2010). Two studies found that patients frequently make their own arrangements when seeking treatment: 76% in Blyth (2010) and 88% in Infertility Network UK (2008). In contrast, 60% of respondents in the study by Shenfield et al. (2010) reported receiving some help from a doctor in their own country with German, French and Swiss patients receiving most and Dutch, British and Swedish patients receiving least. When organizing their own treatment, some patients reported difficulties making travel arrangements and accessing blood tests and scans in their home country (Blyth, 2010). One small-scale study found that US patients use medical travel agencies to organize treatment in the Czech Republic (Whittaker and Speier, 2010). Over 90% of participants in the study by Shenfield et al. (2010) reported receiving satisfactory information in their own language. This contrasts with the view expressed by clinicians who identified administrative and language factors as posing the biggest potential problems for patients engaged in CBRC (Pennings et al., 2009). Of the 19 participants who reported difficulties with accessing cross-border treatment by Infertility Network UK (2008), language and communication problems were the most commonly cited (n = 9). The (sometimes unexpectedly higher) cost of treatment abroad was also mentioned as a negative factor (Infertility Network UK, 2008; Shenfield et al., 2010; Whittaker and Speier, 2010). However, generally studies found a relatively high level of patient satisfaction with cross-border treatment (Blyth, 2010; Infertility Network UK, 2008; Pennings et al., 2009). Positive factors reported include the availability of donors (Bergmann, 2007, 2010; Infertility Network UK, 2008; Blyth, 2010), shorter waiting times (Blyth, 2010; Infertility Network UK, 2008) and the ability to have treatment in a culturally and linguistically familiar country (Inhorn, 2009; Inhorn and Shrivastav, 2010; Whittaker, 2009; Whittaker and Speier, 2010). Two studies (Blyth, 2010; Infertility Network UK, 2008) report that few patients received counselling in foreign clinics. In some cases this was because it was not offered (64% and 48%, respectively) or because it was not accepted when it was available (50% and 13%, respectively). Health care providers experiences Only two studies describe the experience of healthcare providers involved in CBRC. Belgian clinicians reported few problems when dealing with patients from other countries (Pennings et al., 2009). When asked if they adapted their service to foreign patients, staff reported asking for advance payment (10/16), providing all appointments on one day (13/18), providing interpreters (14/16), adapting treatment (13/16), collaborating with doctors in the home country (14/16) and providing consent forms in appropriate languages (12/16). Fewer clinics helped with travel arrangements (3/16), restricted the number of international patients they treated (3/16) or asked international patients to recruit their own egg donor (5/16). Over half of Canadian clinicians reported always recommending a destination to their patients and 21% recommended a specific provider (Hughes and Dejean, 2010). They reported taking into account factors related to effectiveness, safety, past patient experiences, regulations and language, when doing so. When asked about information they sent with patients, only a third thought that a referral letter was important, but almost 90% reported that they always provided information requested by the receiving clinic. US clinicians reported that they would like to receive

8 680 N Hudson et al. laboratory reports and complete medical records for their international patients from the referring clinic (Hughes and Dejean, 2010). Surrogates experiences In a unique ethnographic study, Pande (2009) describes the experiences of surrogates in a clinic in Western India. Although not specifically about CBRC, 29 of the 42 surrogates included were carrying pregnancies for couples from outside of India. Pande s work highlights the significance of the financial rewards received by the women, but simultaneously draws attention to the meaning that surrogates attach to their role in the process. Pande suggests that kinship ties are created between surrogates, resulting offspring and intended mothers, which often transcend class, caste and religious boundaries. Explanations of CBRC There has been much discussion about the possible reasons for CBRC. This debate draws on both hypothetical reasons for its existence (Sauer, 1997; Pennings, 2002, 2004, 2006a,b; Blyth and Farrand, 2005; Storrow, 2005a; Cohen, 2006; Chung, 2006; Mladovsky, 2006; Heng, 2007b; Pennings et al., 2008; Culley and Hudson, 2009; Ikemoto, 2009; Martin, 2009; Pennings, 2009; Smith-Cavros, 2010), as well as empirical evidence (Blyth, 2010; Hughes and Dejean, 2010; Infertility Network UK, 2008; Inhorn and Patrizio, 2009; Inhorn and Shrivastav, 2010; Pennings et al., 2009; Shenfield et al., 2010; Whittaker, 2009; Whittaker and Speier, 2010). Suggestions in the commentary The first set of explanations concern regulatory, ethical or legal restriction of treatment (Pennings, 2002, 2006a,b, 2009; Blyth and Farrand, 2005; Storrow, 2005a; Chung, 2006; Cohen, 2006; Mladovsky, 2006; Turone, 2006; Pennings et al., 2008; Culley and Hudson, 2009; Inhorn and Patrizio, 2009; Martin, 2009; Ferraretti et al., 2010). Restrictions due to safety concerns are specifically highlighted (Pennings, 2004, 2006a, 2009; Blyth and Farrand, 2005; Mladovsky, 2006; Pennings et al., 2008b; Ferraretti et al., 2010). Several authors mention eligibility criteria as an important reason why some patients travel (for example, restrictions on providing treatment to single or lesbian women in some countries) (Pennings, 2004, 2006a, 2009; Blyth and Farrand, 2005; Chung, 2006; Mladovsky, 2006; Pennings et al., 2008; Culley and Hudson, 2009; Ferraretti et al., 2010). Several additional factors are identified, including a lack of expertise in a patient s home country (Pennings, 2004, 2006a, 2009; Blyth and Farrand, 2005; Cohen, 2006; Pennings et al., 2008; Ferraretti et al., 2010), cost of treatment (Pennings, 2004, 2006a,b, 2009; Blyth and Farrand, 2005; Cohen, 2006; Pennings et al., 2008; Ferraretti et al., 2010), lack of publicly funded treatment (Culley and Hudson, 2009), excessive waiting times (Pennings, 2004, 2006a, 2009; Mladovsky, 2006; Ferraretti et al., 2010) and waiting times caused specifically by a shortage of donor eggs (Pennings, 2006b, 2009). Some authors propose that inadequate financial compensation of egg donors will increase the incidence of reproductive travel because it reduces supply (Chung, 2006; Sauer, 1997). Conversely Heng (2007b) suggests that payment to donors should be restricted since it will encourage patient travel to destinations in which donors are paid, and are therefore more plentiful. Pennings et al. (2008) also advise that personal wishes, one of which might be a desire for privacy, may be important in explaining CBRC. A small number of authors examine globalization and associated social and cultural changes to analyse broader contextual factors which may be encouraging CBRC (Storrow, 2005a,b; Culley and Hudson, 2009; Martin, 2009). These include increased availability of low-cost travel (Culley and Hudson, 2009; Mladovsky, 2006) and the growth of the internet enabling clinics to market their services internationally (Chung, 2006; Smith et al., 2009). Blyth and Farrand (2005) and Chung (2006) also note the potential contribution of a market in fertility treatment. The inequality and unevenness of the process of globalization is argued as both fuelling (Storrow, 2005b) and reflecting (Martin, 2009) CBRC. Findings from empirical research Although these authors identify similar patient motivations to those described in the commentaries, it is difficult to draw conclusions as to which factors are most significant. Moreover, empirical data from clinics (Hughes and Dejean, 2010; Nygren et al., 2010; Pennings et al., 2009) provide clinicians perceptions about the most significant reasons for patient travel, rather than patients own views. A majority of Belgian clinics (69%) responding to Pennings et al. (2009) mentioned regulatory, legal or ethical restrictions on treatment as encouraging travel, as did patients themselves, with respondents reporting unavailability of treatment in Belgium (Pennings et al., 2009; Shenfield et al., 2010). In a study of infertility clinics in Thailand, one couple mentioned age limits on treatment in the home country (UK) (Whittaker, 2009; Whittaker and Speier, 2010). Belgian clinics (Pennings et al., 2009) and French, British, German, Swedish and Norwegian patients (Shenfield et al., 2010) mentioned a desire for anonymous donors. Shenfield et al. (2010) differentiate the reasons for patient travel by country. They reported legal reasons as the most important for Italian, German, French, Norwegian and Swedish patients. The increased movement of Italian patients, possibly as a result of the introduction of more restrictive legislation since 2004, has also been highlighted by others (Bartolucci, 2008; Ferraretti et al., 2010). Previous treatment failure was the most commonly mentioned factor for UK patients, as well as issues of access and quality of treatment (Shenfield et al., 2010). Previous failures and the quality of treatment offered abroad were commonly mentioned amongst all patient groups. However, despite national variations, most patients mentioned a combination of factors leading them to seek cross-border treatment (Inhorn and Shrivastav, 2010; Shenfield et al., 2010). Other studies have found that the availability of donors abroad (Blyth, 2010; Infertility Network UK, 2008), better success rates (Blyth, 2010; Infertility Network UK, 2008), shorter waiting times (Blyth, 2010; Infertility Network UK, 2008; Pennings et al., 2009), cost (Blyth, 2010; Infertility Network UK, 2008; Whittaker and Speier, 2010) and expertise (Inhorn and Shrivastav, 2010; Pennings et al., 2009) were important reasons. There is emerging evidence about

9 Cross-border reproductive care: A review of the literature 681 the significance of the geographical and cultural specificity of destination countries with factors such as language or familiarity with the country being important (Inhorn and Shrivastav, 2010; Pennings et al., 2009; Whittaker, 2009; Whittaker and Speier, 2010). Implications of CBRC Many papers discuss the (mostly negative) implications of CBRC (Blyth and Farrand, 2005; Storrow, 2005a,b, 2010; Blyth, 2006; Chung, 2006; Ciocci et al., 2006; Heng, 2006a, 2007a,b; Pennings, 2006a, 2006b, 2009; Ikemoto, 2009; Martin, 2009; McKelvey et al., 2009; Smith et al., 2009; Hughes and Dejean, 2010; Smith-Cavros, 2010; Whittaker and Speier, 2010). These implications are discussed below according to the focus of their impact on patients, donors and surrogates, children conceived via CBRC and service providers. Patients Infertility treatment is acknowledged as a physically, emotionally and financially difficult process (Culley et al., 2009). The literature reviewed here highlights the further implications for patients involved in CBRC. The added practicalities of the travel (Blyth, 2010; Chung, 2006) and cost (Chung, 2006; Ferraretti et al., 2010; Infertility Network UK, 2008; Inhorn and Shrivastav, 2010; Shenfield et al., 2010) are identified together with potentially differing levels of safety and quality in some clinics outside home jurisdictions (Ferraretti et al., 2010; Hughes and Dejean, 2010; Pennings, 2006a,b, 2009). Commentators also highlight concerns: that patients rights might not be respected by cross-border clinics (Pennings, 2006a); about a lack of counselling offered by cross-border clinics (Ferraretti et al., 2010; Pennings, 2006a; Smith-Cavros, 2010; Thorn and Dill, 2010); about potentially lower success rates abroad (Pennings, 2006b); and about dangers arising from an absence of recourse to malpractice law abroad (Ferraretti et al., 2010; Pennings, 2006b). Increasing levels of CBRC may present a challenge to patient organizations, since they are required to provide information about a relatively under-researched and undocumented phenomenon (Thorn and Dill, 2010). Donors and surrogates There is a suggestion that a lack of (appropriate) regulation on donor and surrogate recruitment, compensation and treatment by clinics could result in the exploitation and devaluation of women, body parts and the reproductive process (Blyth, 2006; Heng, 2007a,b; Ikemoto, 2009; Pennings, 2006b, 2009; Smith-Cavros, 2010; Storrow, 2005a,b, 2010). Some view this as generating an undesirable market in reproduction (Chung, 2006; Heng, 2006a; Ikemoto, 2009; Smith et al., 2009; Smith-Cavros, 2010; Storrow, 2005a; Whittaker and Speier, 2010) with the potential to reproduce inequality at the global level (Martin, 2009; Storrow, 2005b). Children No empirical evidence was found concerning the experiences of individuals born as a consequence of CBRC. Nevertheless, a small number of authors bring the rights and interests of offspring into the debate and argue that these need adequate consideration in any future action or response to CBRC, particularly where a third party/ies is involved (Blyth, 2006; Blyth and Farrand, 2005; Ciocci et al., 2006; Merrick, 2007). Health care systems The health risks and costs of multiple pregnancies and births is one focus of concern here. For example, a retrospective audit of NHS data on high order multiple births conducted in a London-based multiple pregnancy clinic for the period (McKelvey et al., 2009) found that 22% (n = 24) had engaged in CBRC. In addition to the personal consequences of a high iatrogenic multiple birth rate for mothers and babies, the authors also point out that such pregnancies have considerable financial implications for the NHS. Others have considered the potential impact of CBRC on host countries medical systems in terms of the possibility of fertility services being stretched and resources diverted away from home patients (Chung, 2006; Ikemoto, 2009; Pennings, 2009; Smith-Cavros, 2010; Storrow, 2010), potentially eroding confidence in the provision and regulation of health care (Heng, 2006a; Pennings, 2006a; Storrow, 2005a). Pennings (2006a) proposes that CBRC could drive up the price of assisted reproduction technology artificially in the host country. Finally, two papers discuss the possible benefits of CBRC for receiving countries, including the potential stimulation of provider countries economies (Whittaker, 2009), and advances in technological developments in assisted reproduction such as those related to storing and freezing gametes (Chung, 2006). Policy responses to CBRC As highlighted above, CBRC has emerged for a number of reasons as an area of concern, generating corresponding debate about how various stakeholders should respond to this phenomenon. Similar to Pennings (2002, 2004, 2006a,b), this review discusses three broad types of response: (i) those advocating the prohibition of CBRC; (ii) those promoting harmonization of relevant regulation across borders; and (iii) those endorsing the operation of CBRC under certain conditions or with specific safeguards (or harm minimization ). This third argument has received most discussion in the literature to date and would appear to reflect current dominant thinking on interventions in CBRC. Prohibition This approach, also described as coerced conformity (Pennings, 2002), supports the abolition of CBRC. Few authors advocate this approach, but Pennings helpfully considers the means under which such a solution could theoretically operate, such as restricting the movements of citizens for the purpose of CBRC, allowing people to have treatment in their home country only and applying penalties for offenders (Pennings, 2002, 2004, 2006a,b; 2009; Pennings and Mertes, 2010). Heng (2006b) has some sympathy with this approach, suggesting that CBRC should be illegal for

10 682 N Hudson et al. doctors to refer patients to countries who have different forms of regulation of assisted reproduction technology. While some would appear to favour an end to CBRC, few advocate an outright ban given the impracticality of this response. Pennings (2002, 2004, 2006a,b) also argues that such a move has the potential for the violation of individual privacy and freedom. It is noteworthy that in 2010 the Turkish Health Ministry made it illegal for Turkish citizens to travel abroad to use donor sperm, with clinicians also liable for criminal charges if they help Turkish patients access donor insemination abroad (Head, 2010). Regulatory harmonization The second approach suggests that harmonization of the current patchwork of regulation (Martin, 2009) would reduce the need for CBRC, since this variation is clearly a significant driver. Once again, however, most authors regard this as impractical (Ciocci et al., 2006; Mladovsky, 2006) and/or undesirable (Ciocci et al., 2006) and as such there is little serious discussion of how this could operate. Pennings (2004) for example, suggests that harmonization is not feasible because it would require culturally and politically diverse nation states to accept universal ethical principles or moral truths. Harm minimization The final approach focuses on how those involved in CBRC as patients (and, for some authors, donors, surrogates and offspring) can best be protected. The development of an international code of practice for professionals and/or a system of international clinic accreditation which allows patients (and presumably donors and surrogates) to identify affiliated clinics with agreed quality standards has been proposed (Chung, 2006; Collins and Cook, 2010; Deech, 2003; Ferraretti et al., 2010; Pennings et al., 2008). Central to this is the consideration of clinical safety standards and claims or assurances about effectiveness of treatments (Hughes and Dejean, 2010). Others have called for additional international protection for children conceived via CBRC (Blyth and Farrand, 2005; Ciocci et al., 2006) and for donors and surrogates. Several discussions about ways to address CBRC at the international level appear to be underway and are reported in the literature (Blyth and Auffrey, 2008; Collins and Cook, 2010; Davies, 2010; Mainland and Wilson, 2010; Pennings et al., 2008; Thorn and Dill, 2010), possibly providing a useful way forward. A first step to providing guidance for fertility clinics in Europe has been pioneered by the ESHRE Task Force on Cross Border Reproductive Care. The ESHRE Code of Practice focuses on principles of equity, safety, efficiency, effectiveness, timeliness and patientcentredness (Shenfield, 2011). Discussion The majority of papers identified in this review are based on commentary rather than empirical research. This finding is of significance, since it implies that although it is of interest to a range of disciplines, CBRC is under-researched and under-theorized. The growing range of commentaries provides important perspectives on a range of issues and highlights the anxieties that CBRC appears to generate in a number of arenas. However, without empirical data, the hypotheses presented cannot be confirmed as correct. Evidence to date suggests that there is unlikely to be one driver to engage in CBRC and it is difficult to ascertain the impact or implications that CBRC may have without more evidence about the nature and extent of reproductive travel for the purposes of family building. A related concern is that, in the absence of valid evidence, a number of academic authors (e.g. Ikemoto, 2009; Smith-Cavros, 2010) have used press reports to support their own claims about CBRC. The media reporting of this issue tends to be highly sensational and using media reports in an uncritical way may create further misunderstanding and misrepresentation of CBRC, perpetuating stereotypes and adding to a sense of moral panic (Culley and Hudson, 2009). Although there is a considerable commentary about the extent of CBRC, much of the current knowledge of incidence is based on a very small number of surveys that are diverse in their approach. These studies highlight the fact that CBRC appears to be increasing and that there is evidence of global movement. However, caution should be exercised when drawing conclusions about incidence, since in some cases the data are based on estimates (Hughes and Dejean, 2010; Nygren et al., 2010), contain missing data or gaps which make extrapolation difficult (Infertility Network UK, 2008; Pennings et al., 2009) or contain too few data from which to draw firm conclusions (Blyth, 2010). Additionally, what reporting there has been of recent qualitative studies remains partial (Bergmann, 2010) or is based only on small numbers of participants (Whittaker and Speier, 2010), some of whom are drawn from other studies (Whittaker, 2009). The study carried out by Shenfield et al. (2010) remains the most robust data set, but this survey is not without limitations, which the authors acknowledge. For example, it was carried out in countries which were presumed to be popular destinations for those undertaking CBRC. In addition, the authors do not indicate how patients were recruited to the study or how comprehensive the response rate was. The considerable difficulties of collecting data on this topic are acknowledged in several contributions (Collins and Cook, 2010; Nygren et al., 2010). Patients are not obliged to report CBRC in their home country and this has led to suggestions that it would be more effective to collect data in the receiving clinics (Nygren et al., 2010). Collins and Cook (2010), reporting on the first International Forum on CBRC, propose that collection of global data on numbers of cross-border treatments could be facilitated through the International Committee Monitoring Assisted Reproductive Technologies (ICMART), which currently collects global data. Most commentators agree that standardized, international data collection on the incidence and nature of CBRC is needed. The level of research-based knowledge of patient (and clinician) experiences of CBRC is even more limited. Studies to date reveal that a large proportion of patients appear to be making their own arrangements with clinics via the internet (Blyth, 2010; Infertility Network UK, 2008), with some experiencing difficulties in the process (Blyth, 2010). Despite this, studies generally report a high degree of satisfaction with CBRC, especially in relation to factors such as shorter waiting