abstract: # Background
  .
  The National Health Policy 2000 - 2009 and Health sector strategic plans I & II emphasized that Primary Health Care (PHC) would be the main strategy for national development and would be operationalized through provision of the minimum health care package. Commitment was to spend an increasing proportion of the health budget for the provision of the basic minimum package of health services which was interpreted to mean increasing spending at health centre level. This analysis was undertaken to gain a better understanding of changes in the way recurrent funding is allocated in the health sector in Uganda and to what extent it has been in line with agreed policy priorities.
  .
  # Methods
  .
  Government recurrent wage and non-wage expenditures - based on annual releases by the Uganda Ministry of Finance, Planning and Economic Development were compiled for the period 1997/1998 to financial year 2007/2008. Additional data was obtained from a series of Ministry of Health annual health sector reports as well as other reports. Data was verified by key government officials in Ministry of Finance, Planning and Economic Development and Ministry of Health. Analysis of expenditures was done at sector level, by the different levels in the health care system and the different levels of care.
  .
  # Results
  .
  There was a pronounced increase in the amount of funds released for recurrent expenditure over the review period fueled mainly by increases in the wage component. PHC services showed the greatest increase, increasing more than 70 times in ten years. At hospital level, expenditures remained fairly constant for the last 10 years with a slight reduction in the wage component.
  .
  # Conclusion
  .
  The policy aspiration of increasing spending on PHC was attained but key aspects that would facilitate its realization were not addressed. At any given level of funding for the health sector, there is need to work out an optimal balance in investment in the different inputs to ensure efficiency in health spending. Equally important is the balance in investment between hospitals and health centers. There is a need to look comprehensively at what it takes to provide PHC services and invest accordingly.
author: Frederick Mugisha; Juliet Nabyonga-Orem
date: 2010
institute: 1Economic Policy Research Centre, Makerere University Kampala; 2Health Systems Unit, World Health Organization, Uganda Country Office
references:
title: To what extent does recurrent government health expenditure in Uganda reflect its policy priorities?

# Background

The National Health policy for Uganda (NHP) 2000 - 2009 \[1\] emphasized that Primary Health Care (PHC) would be the main philosophy and strategy for national development and would be made operational through provision of the minimum health care package. A minimum health care package, with interventions addressing the biggest burden of diseases affecting majority of the population, would form the primary focus of the health care delivery system. The welfare of the poor was to be given special consideration. Even though there was a reduction in poverty levels - from 38% in 2002/03 to 31% in 2005/2006 -, the population in poverty was still considered significant and more pronounced in rural areas \[2,3\].

The NHP\[1\] committed to allocating and spending an increasing proportion of the health budget for the provision of the basic minimum package of health services. This was interpreted during implementation to mean increasing spending at health centre level, where majority of the population, especially the rural and poor, lived and sought public health services (district health services). It is noteworthy that health centers' main focus is primary health care while hospitals' main focus is tertiary care. However, the policy provides for hospitals to offer primary health services in the absence of health centers. Spending at the central level and on referral and tertiary hospitals was to be held constant in real terms. The Health sector strategic plan (HSSP) I; 2000/01 - 2004/05 similarly stated ensuring effectiveness, efficiency, and equity in allocation and utilization of resources and expenditure on most relevant and cost effective priority health interventions, with a clear bias on protecting the poor and most vulnerable \[4\]. Review of the HSSP I noted that some progress had been made. There was an increase in funding to PHC services in absolute and relative terms targeted at peripheral health units \[5\].

HSSP II 2005/06 - 2009/10 committed to allocating resources in the health sector in line with efficiency and equity principles\[6\]. Preferential allocation of resources to cost effective activities and increasing consumption of services were measures envisaged to address allocative and technical efficiency issues respectively. Targeting increasing allocations to health care inputs with a large impact on quality of services especially drugs and other health supplies, and increasing the proportion of resources allocated to the district health services where the majority of population, especially the poor, live were among the strategies to address equity concerns.

Uganda has a decentralized system of health service delivery with roles and responsibilities for the centre and districts clearly stated. The central level is responsible for setting policies, standards and guidelines, resource mobilization, capacity building, coordination of service delivery, monitoring and supervision. The decentralized levels (districts) are responsible for service delivery.

The objective of this paper is to provide a better understanding of changes in the way recurrent funding (wage and non-wage) is allocated in the health sector in Uganda and to what extent it has been in line with agreed policy priorities.

Understanding changes in the way funding is allocated provides government and development partners an opportunity to examine not only the importance attached to its priorities but also because it provides a tool for monitoring the benefits expected from increased spending. In general expenditure on health is one of the determinants of health status. For example, in Lesotho, public expenditure on health was one of the important determinants of life expectancy at birth, infant mortality and under-five mortality \[7\]. Similar results were found in Pacific Island Countries while examining the relationship between per capita public expenditure and three measures of health outcomes (infant and under-five mortality rates and crude death rates)\[8\]. The results showed strong evidence that per capita health expenditure is an important factor in determining health outcomes. More important is the fact that when this expenditure is targeted, it is expected to yield better outcomes than when it is not. For example, Vietnam introduced a Health Care Fund for the Poor to increase access to health care and reduce the financial burden of health expenditure faced by the poor and ethnic minorities. The results suggest that despite numerous administrative challenges, the fund helped increase utilization and reduced out-of-pocket expenditure for the program's target population\[9\].

# Methods

## Data

Quantitative research methods were used. The main dataset used in this paper is the government recurrent wage and non-wage expenditures - based on outturns by the Uganda Ministry of Finance, Planning and Economic Development (MoFPED). Expenditure outturns are actual releases of funds from central government to various spending centers. Possible alternative expenditure data is that based on actual accountability for expenses made at the end of each financial year. This data is unavailable. Accountability for expenditure is meant for audit purposes and therefore is not consistently captured.

The expenditure data based on central government outturns was compiled from approved estimates of revenue and expenditure reports that MoFPED publishes annually \[10\]. The data was complied for ten financial years - from the financial year 1997/1998 to financial year 2007/2008. This data does not include funds that are recurrent in nature not expended through the common government basket. Additional data was obtained from a series of annual health sector reports \[11-13\] as well as other reports.

Data was verified by key government officials in MoFPED and Ministry of Health (MoH). The key aspect required in the verification exercise was to confirm whether the data was correct and provide input in explaining the observed patterns. The Ministry of Finance, Planning and Economic Development being the source of the data provided all the necessary data reports. Officials from the planning department of the Ministry of Health responsible for finance and budget - given the subject matter - were asked to review the data and also comment on the emerging trends. The authors shared with them the data and the paper. They made few collections on the figures and shared with the authors their own compilation - which were reconciled.

## Analysis

In order to understand the pattern of and further examine the recurrent government expenditure for PHC, the recurrent budget was categorized into two service care levels - the hospital services and the health center services. The Uganda health service structure is organized broadly in this manner. The primary health care services include services offered at Health Center I or Village Health team, Health Center II, Health Center III, and Health Center IV. Hospital services are provided at a General Hospital, Regional Referral Hospital and the National Referral Hospital.

The structure of the health sector outturns as presented in the estimates of revenue and expenditure is shown in Table 1. Hospital expenditure includes that of Mulago Hospital Complex, Butabika Hospital, Regional Referral Hospitals, General Hospitals and NGO hospitals. NGO subvention is spent at NGO Hospital and Health Centre levels. The percent of NGO expenditure on hospitals was used in computing the actual expenses for hospital services. The part of the district NGO hospitals or primary health care that is spent on hospital care was varied across the years (see Figure 1).

Example of the Health Sector Budget structure

| FY 2007/08 Out-turn |  |  |  |  |  |
|----|----|----|----|----|----|
| **SECTOR/VOTE HEALTH** |  | **Wage** | **Non-Wage Recurrent** | **Domestic Dev** | **Donor Project** |
|  |  |  |  |  |  |
| 14 | Health | 2.86 | 42.78 | 19.62 |  |
| 107 | Uganda Aids Commission (Statutory) | 0.69 | 0.63 | 1.51 |  |
| 134 | Health Service Commission | 0.45 | 1.25 | 0.04 |  |
| 151 | Uganda Blood Transfusion Service (UBTS) | 0.84 | 0.85 |  |  |
| 161 | Mulago Hospital Complex | 12.42 | 17.16 | 1.32 |  |
| 162 | Butabika Hospital | 1.58 | 1.8 | 6.8 |  |
| 163-173 | Regional Referral Hospitals | 16.93 | 8.82 |  |  |
| 501-850 | NGO subvention |  | 15.93 |  |  |
| 501-850 | District Primary Health Care | 78.9 | 19.85 | 6.31 |  |
| 501-850 | General Hospitals |  | 9.61 |  |  |
|  |  |  |  |  |  |
|  | SUB-TOTAL HEALTH | 114.66 | 118.7 | 35.6 |  |

Source: MFPED, Estimates of revenue and expenditure (recurrent and development) FY 2007/08. 2008, Ministry of Finance, Planning and Economic Development: Kampala, Uganda.

The total expenditure on PHC is shown as "District Primary Health Care" plus the amount expended on NGO Health Centers. Expenditure by the MoH headquarters and district health offices is included as a separate category. The MoH headquarters and district health offices do conduct management functions on behalf of the Health Centers and Hospitals.

Expenditure on Uganda Aids Commission, Health Service Commission and Uganda Blood Transfusion Service is considered to be other expenditure. Other expenditure items that have been phased out over the years include the Health Training Schools and the lunch allowances. The training schools were transferred to be under the Ministry of Education while the lunch allowance was consolidated in the wage component.

# Results

## Overall Recurrent Expenditure

Figure 2 shows recurrent (wage and non-wage) expenditure for the health sector over a period of ten financial years.

Three messages are noticeable from the results. First, during the year 2000-01, there was a pronounced increase in the amount of funds released for recurrent expenditure. It increased by about UGX 60 Billion or 76 percent between 2000/01 - 2001/02. This coincided with Government of Uganda policy to focus on PHC as a strategy.

Second, prior to 2005-06 the non-wage component of recurrent expenditure was higher than the wage. However after this financial year, the wage component caught-up with the non-wage component.

Third, we notice that the wage component of the recurrent expenditure increased consistently each year during the period under review while the non-wage did not show significant increase. This suggests that increases in the wage component contributed most to the increase in recurrent expenditure.

## Recurrent Expenditure Across Levels

Figure 3 shows the recurrent expenditure across different levels in the health system.

PHC services showed the greatest increase over the ten year period. Between 1997 and 2000, primary health care services attracted less recurrent expenditure than hospital services or the ministerial and district headquarters. In the financial year 2000-01, a policy directive was made to focus spending on PHC as a strategy to bring services closer to the population. Indeed, following this pronouncement, in the financial year 2001-02, expenditure on PHC shot up beyond that of hospital services. The rate of increase after this time continued to be higher than that of hospital services. Recurrent expenditure at district and ministry headquarters, and other health institutions remained rather constant over this period. In the rest of the paper, no further analysis of ministerial and district headquarters is done. Further analysis was done for hospital services and primary health care services.

## Recurrent Expenditure On Phc Services

In line with the policy decision, recurrent expenditure on PHC services has gone up from 1.5 billion in 1997-98 to 106 billion in 2007-08 in nominal terms, increasing more than 70 times in ten years (see Figure 4). We notice that the increase was mainly driven by wage component of the recurrent expenditure. In fact the non-wage component actually started to decline in 2003/2004 and continued to decline.

Considering the wage and non-wage components as percentages of the total, Figure 5 shows that the percentage of non-wage has continued to decline. This is in contrast to the wage, which moved from a negligible percentage to about 80 percent in 2007-08. This result creates an impression that expansion of health services was pushed by the wage component with increasingly less resources to deliver the services.

## Recurrent Expenditure On Hospital Services

Recurrent expenditure for hospital services went up from 27 billion in 1997/1997 to 76 billion in 2007/2008 in nominal terms, increasing almost 3 times in ten years (Figure 6). Unlike with PHC services, non-wage expenditure was consistently higher than the wage component. The expenditure pattern at hospital level differs from that seen at PHC level.

Figure 7 shows the two components of recurrent expenditure - wage and non-wage - in terms of percentage. The results show that, unlike the expenditure on PHC services that on hospital services is consistent. The percent expenditure on wage is consistently lower than that of non-wage for all the years.

# Discussion

We begin the discussion with a comment on the scope of the paper. The paper does examine recurrent government recurrent expenditure. It therefore leaves out government development expenditure. It also leaves out expenditure that is not done through the government medium expenditure framework (MTEF), that is, the off budget expenditure. This off budget expenditure is done mainly by development partners and non-government organizations. The proportion of the government recurrent expenditure to the total expenditure of the sector is difficult to estimate. No data is collected either for the non-government organizations or for the development partners. However, analysis of recurrent expenditure in itself is a an important aspect of understanding government priorities.

Simultaneous changes as part of the implementation of the policy are noteworthy. A one off capital investment for Primary Health Care was made four years into the implementation of the policy. Capital expenditure increased from Ushs 10.6 billion in the 2001-2002 financial year to Ushs 75.8 billion shillings in the next financial year (2002-2003) - Based on analysis of the mid-term expenditure framework. This investment enabled further expansion of health centers with an additional 400 HCIIs. In addition, the recruitment of health workers was re-instituted in 2001. By mid 2002, more than 85% (2,538) of health workers under the Poverty action funds targeting PHC services had been recruited\[5\].

The sector wide analysis has shown an increase in recurrent expenditure largely accounted for by increase in the wage component while the non wage recurrent remained fairly constant. The noted increase in the wage bill may be explained by several reasons, increase in salaries, adjustment for inflation and recruitment of more health workers. We note that increase in public servants wages have been very modest, for example, between 1999 and 2002 wages grew by 4.8% per annum\[14\] while between 2002 - 2007, average monthly earnings only increased by 13%\[15\]. Inflation was maintained below 8% between 2000 and 2008\[16\]. Percentage of approved posts filled by trained staff in the health sector improved from 33% in 1999/00 to 69% in 2004/05\[11\] and given this, increase in number of health workers accounts for the increasing wage bill.

The availability of human resource without adequate inputs affects quality of care and leads to further loses, having to pay salaries for health workers who are not providing services. Underfunding other key inputs has affected service delivery, for example, medicines stock outs is a long standing problem. The percentage of health facilities registering stock outs in essential medicines has consistently been over 60% for the last 10 years \[11-13\]. Per capita expenditure on essential medicines and health supplies has remained below US\$2 per capita for the last six years \[11-13,17-19\]. Functionality of available equipment ranges from as low as 33% at the general hospital level to 52% at the Health Centre four (HC IV) level\[19\]. Available investments cannot be put to optimal use.

Looking at recurrent expenditure by level, the policy decision of capping of expenditures at tertiary level hospitals, which were viewed to serve a small urban population was achieved. Similarly, the high and increasing recurrent expenditure at the district level shows that the policy decision to target peripheral units serving mainly the poor \[17\]was also met. Eighty percent (80%) of the population live in rural areas and poverty is more prevalent in rural areas compared to urban areas However, expenditure at the national level health institutions remained the lowest and constant over the review period. These institutions offer support services and their proper functioning is crucial for realization of PHC provision. As a result of underinvestment in these institutions, key aspects of PHC have not been effectively provided. Inadequate blood transfusion services for example have affected delivery of emergency obstetric care services. The mid-term review report noted the markedly inadequate and poorly furnished blood transfusion structure and lack of enough blood supply\[18\]. Out of the seven recommended regional blood banks, only five are in place with no expansion made for the last three years\[20\]. Operations of the Health service commission, charged with the responsibility of establishing an efficient health workforce continue to be constrained\[18\]. Occasionally, funding for the wage bill has been returned to the treasury because of failure to recruit health workers.

The patterns of expenditure within hospitals and health centers have been analyzed. We have noted that between 2000/01 and 2001/02, at the hospital level, there was a reduction in the wage and an increase in the non wage recurrent while at the health centre level, there was a reduction in the non wage recurrent and an increase in the wage. This has affected availability of essential supplies, for example, percentage of health centre IIs experiencing stock outs of essential medicines has been close to 80% for the last 3 years compared to the national average of close 70%. Only 52% of HC II were able to provide antenatal care compared to hospitals at 95% \[21\]. Percentage of HCIIs, offering child immunization with all equipment available, was only 55% compared to hospitals at 90%. Preferential investment in wage at the expense of the non wage recurrent at HC level has affected service delivery at this level with resultant congestion at hospitals of cases that could be treated at lower levels. Similarly, evidence suggests that human resource utilization is suboptimal when investment in other areas like of the capital (i.e. medical equipment, etc.) is inadequate. They recommended that reorientation of the resource allocation towards the capital investments would save more lives \[22\].

# Conclusion

In this analysis we have shown that the policy aspiration of increasing spending on PHC was attained but key aspects that would facilitate its realization were not addressed. Support services like blood transfusion and the human resource commission which facilitates recruitment of health workers were not supported. At any given level of funding for the health sector, there is need to work out an optimal balance in investment in the different inputs to ensure efficiency in health spending. Much as improving availability of health workers is important, they must have necessary inputs to provide services. Equally important is the balance in investment between hospitals and health centres. There is need to look comprehensively at what it takes to provide PHC services and invest accordingly.

# Competing interests

The authors declare that they have no competing interests.

# Authors' contributions

Both authors contributed substantially in the conception and design of the paper, acquisition of data, analysis and interpretation of data. Both authors drafted the manuscript, revised it critically for important intellectual content and gave final approval of the version to be published.

## Acknowledgements

We acknowledge the contribution of government of Uganda for compiling the data on an annual basis. The Global Development Network is also acknowledged for facilitating the exercise. Economic Policy Research Centre and World Health Organization Uganda Office provided technical guidance.


abstract: Science and religion; never the twain shall meet.
author: Gregory A Petsko
date: 2009
institute: 1Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, MA 02454-9110, USA
title: Render unto Darwin

You probably haven't encountered a website for something called BioLogos. If you have, you will undoubtedly already have formed a strong opinion about it - it's that kind of site. If you haven't, you really ought to check it out <http://www.biologos.org>. It's the website for something called the BioLogos Foundation. According to its mission statement, "The BioLogos Foundation promotes the search for truth in both the natural and spiritual realms seeking harmony between these different perspectives." The foundation was established by Francis Collins with a grant from the John Templeton Foundation, a much older organization with a similar mission. And that, apart from its intrinsic interest, is why you should check it out, and why I'm wagering you will have strong opinions when you do. Francis Collins is the scientist who headed the publicly funded Human Genome Sequencing Project in the 1990s. Until last August he was the head of the National Human Genome Institute at the National Institutes of Health (NIH), which continues that work and funds much of the genome biology in the United States. And he just might be the next director of the NIH, the largest scientific research funding organization in the world.

In a public statement, Collins said that he established the BioLogos Foundation "to address the escalating culture war between science and faith in the United States. On one end of the spectrum, 'new atheists' argue that science removes the need for God. On the other end, religious fundamentalists argue that the Bible requires us to reject much of modern science. Many people - including scientists and believers in God - do not find these extreme options attractive. BioLogos represents the harmony of science and faith. It addresses the central themes of science and religion and emphasizes the compatibility of Christian faith with scientific discoveries about the origins of the universe and life. To communicate this message to the general public and add to the ongoing dialog, The BioLogos Foundation created BioLogos.org."

Let's dissect this statement, because if ever there was a statement that needed dissecting, this is one. I completely agree with Collins that there is a culture war between science and faith in the United States. But I do not agree that the war is due primarily to the clash between the extremists on both sides. Take the "new atheists", for example. There are many atheists in the United States, and some of them are scientists. But only a handful would take the extreme - and, to my mind, incorrect - position that science disproves the existence of God. The British scientist Richard Dawkins might, but he doesn't speak for the majority of scientists I know, and his eloquent but strident voice has only served to inflame the opposition by preaching to the converted. There are many more agnostics, who simply believe that there is no compelling evidence to believe in any deity.

Now let's look at that opposition, the "religious fundamentalists" who argue that "the Bible requires us to reject much of modern science". There are a lot more of those, especially in the United States, but - and this is a crucial distinction, as we shall see - they are almost entirely evangelical Christians, not "religious fundamentalists" in general. Evangelical Christians often take the Bible literally, and a literal reading of the Bible is certainly incompatible with many of the findings of science.

One of the missions of the BioLogos website is to advance the idea of theistic evolution, a concept discussed in depth in Collins' book *The Language of God*, which is also promoted on biologos.org. Essentially, theistic evolution means that evolution is the way God created life. I was first clued into this website by Jonathan Eisen, an evolutionary biologist and open access publishing maven at the University of California, Davis. Eisen, whose blog *The Tree of Life* <http://phylogenomics.blogspot.com/> is a delightful and thoughtful commentary on the worlds of both genomics and scientific publishing, wrote about BioLogos on 5 May. So that you will know where he's coming from, here's his opening statement: "I am all for trying to have discussions about science and religion. But I do not think the two topics are really compatible in the sense of merging them together. Science (and medicine) should be about, well, science. And religion can be about whatever it wants to be. And when we can get religious and scientific leaders together to talk about the implications of each area on the other and on the world, fine too. But merging the two together into one hybrid such as Christian Science and Creation Science? Not for me."

He goes on to make a pointed criticism of the underlying logic - or lack thereof, in his view - behind BioLogos. "The details of Collins' attempt to merge science and religion into a version of theistic evolution are really unclean. Basically, he is trying to argue that on the one hand science and religion are completely separate activities (I support this) but at the same time argues that God can intervene in the setting up of natural laws and in providing some guidance here and there in order to, for example, produce human beings in his image. The website repeats some things from Collins' book that are equally illogical - such as saying that altruism can be explained by science (and even specifically saying that science is the way to explain the natural world) but then turning around and saying that science cannot explain extreme forms of altruism (and therefore implying that actually, the natural world cannot be explained by science). Which is it? Is science for the natural world or not?" Eisen is right that this, and some of BioLogos' other talking points, smack of setting up a straw man.

But in the end, BioLogos aims to show that the findings of science are not inconsistent with the existence of God. And not just any God. BioLogos is all about the Christian God. It even says so: "The creation story of BioLogos is compatible with many faith traditions, and there is no way to give a scientific proof for one monotheistic faith over another. Therefore, this response will simply show the compatibility of Christianity with BioLogos." And again, more forcefully, in their mission statement: "the website is a reliable source of scholarly thought on contemporary issues in science and faith that highlights the compatibility of modern science with traditional Christian beliefs."

Here's another example: "For believers, these \[scientific\] discoveries must ultimately be compatible with the truth that is revealed in the Bible, and it is the conviction of BioLogos that this compatibility is not only desirable but also possible. The limitation is that our access to all forms of truth, including scientific and religious, is at best partial." The statement that it is Biblical truth that science must be compatible with (and there are other comments that make it clear BioLogos means the Christian Bible, especially the New Testament) marks a clear attempt to link science with one brand of religion.

The creators of BioLogos have every right to make the foundation and website about whatever they want. And I suppose you could argue that, as I see it, because it is evangelical Christians that are the chief opponents of modern science, especially evolution, it is sensible for scientists to promote the compatibility of science with Christian beliefs. But I don't agree. I think it's a huge mistake.

GK Chesterton, a devout Roman Catholic, has his priest-detective Father Brown say, in the superb short story *The Sign of the Broken Sword*, "When will people understand that it is useless for a man to read his Bible unless he also reads everybody else's Bible? A printer reads the Bible for misprints. A Mormon reads his Bible and finds polygamy; a Christian Scientist reads his and finds we have no arms and legs." I've always liked this quotation, and not just because I agree that one huge problem with putting your faith in the literal reading of a book is that you can find justification in that book for almost any form of behavior, from altruism to genocide to slavery. I like it for a reason that Chesterton probably never intended: it reminds me that there are many more religions than Christianity, and many more people of faith than monotheists. I think if you are going to understand people of faith and try to see how we as scientists can find common ground with them, it is discriminatory - and possibly something worse - to focus on Christians or even monotheists (which, in the modern world, pretty much consists of Muslims, Christians and Jews - Zoroastrians being in short supply nowadays - and I'm pretty sure that the BioLogos folks would not include Islam in their mission, given that faith's denial of the divinity of Christ). If you are going to read the Christian Bible you should also read the Jewish Bible. And the Book of Mormon. And the Koran. And the Bhagavad Gita. If you really care about making contact with people of faith you should not exclude most of them just because they worship different gods from yours.

In some temples in India, during services the priest will read from the Hebrew or Christian Bible and the Muslim Koran as well as the Hindu Gita, moving from one to the other as though it did not matter what precise words were being spoken as long as there was something greater than the individual self that was being worshipped. How can we as scientists find common ground with people of faith unless we recognize the commonalities they share with each other? At its best, all religion is about a love for the natural world, a desire to help other people, and a sense that life is well lived only when it is not lived selfishly and pettily - values that typically underlie most scientific research. At its worst, religion is about unquestionable certainty, authoritarianism, exclusion and discrimination - things that have no place in science either. Scientists can make common cause with people of faith through the values we share, but must reject the extremist, intolerant views that poison both spheres.

And in the end, that's my big problem with BioLogos - at its heart, it strikes me as implicitly exclusionary (plus I agree with Eisen that its logic is shaky). I would have much preferred a clearcut effort to emphasize the non-connectedness of science and faith: that science is about evidence and testable hypotheses, whereas religion is about believing in things for which there is no evidence whatsoever, and cannot be. That would place them in separate realms, but with common ground as I defined it above. The moment you start trying to say that data from science is compatible with the Christian religion in particular, you imply that, for example, polytheistic religions are wrong, and maybe not just as a matter of faith, but as a matter of science.

Nothing is more dangerous than such absolutism. It sets one type of religion as being true and therefore can be used to support the branding of all the others as false. However well-intentioned, BioLogos isn't likely to bring peace to the war between science and religion if it is oriented so strongly towards one religion.

I would have loved to see the resources that the Templeton and BioLogos Foundations spent on biologos.com - both financial and in terms of human effort - devoted to clarifying and promoting the distinctions between science and religion and to a search for a common ground that does not exclude anyone of faith. That's something I could support (and, I bet, something that Jonathan Eisen and possibly Charles Darwin could support, too). But the idea that science provides information that cannot be explained by science alone - and therefore that science 'needs' the Christian God for a complete description of the universe - strikes me as the wrong thing to do. Render unto Darwin the things that are Darwin's, and unto God the things that are God's. But for God's sake (or should that be Darwin's?), don't mix them together.


abstract: The momentum towards open-access publishing has continued to build in the months since *Journal of Biology* was launched.
author: Theodora Bloom
date: 2003
institute: 1Editor, *Journal of Biology*
title: Editorial

One of the unusual features of *Journal of Biology* is its commitment to publish each research article online as it is ready, and to assemble a print issue around as few or as many research articles as are available at one time. This print issue includes two research articles along with associated commentary, and this reflects a change in the pace at which suitable articles are being submitted to the journal - although we continue to decline tens of articles for every one that is accepted for publication, as befits a journal that aims to join the top rank.

Like all peer-reviewed research journals, this one can only select for publication from among the articles submitted to it. Given our aspiration to cover the full spectrum of biology, it is gratifying to note that the research articles published so far span a broad range of biological subjects. The first articles described genome-wide characteristics of gene expression (<http://jbiol.com/content/1/1/5>) and a chemical approach to studying cell signaling during development and disease (<http://jbiol.com/content/1/2/10>). Now, the articles in this issue describe the application of a new combination of biophysicial technologies to single-molecule measurements (<http://jbiol.com/content/2/1/6>) and new insights into the coordination of cell growth with cell division in mammalian cells (<http://jbiol.com/content/2/1/7>). In the forthcoming issues, which are now being prepared, readers can look forward to further diversity, and we hope that potential authors will continue to be reassured that we do intend to cover their favorite subject area.

A notable attribute of the second research article in this print issue is that the senior author is the journal's Editor-in-Chief, Martin Raff. There will be some readers who question the propriety of the Editor-in-Chief publishing in 'his own journal' - but in a classic double bind, if he chose instead to publish in another high-profile journal there would be those who doubted his commitment to *Journal of Biology*. We can only reassure the sceptics that the peer-review process was, as usual, stringent and anonymous, and that the journal's usual standards and practices were applied especially scrupulously to this article. We hope that others, whether formally associated with this journal or not, will follow the Editor-in-Chief's lead and submit their best work to this journal and so help promote open access as the preferred method of publishing in biology.

The momentum towards open-access publishing has continued to build in the months since *Journal of Biology* was launched. The high-profile group of scientists behind the Public Library of Science (<http://www.plos.org/>) plan to launch their own open-access journals later this year. In addition, announcements of support for the open-access publishing model have continued to pile up from around the world, from both funding agencies (see, for example, those listed at <http://www.biomedcentral.com/info/about/apcfaq>) and individual institutions (see <http://www.biomedcentral.com/inst/>). Ever since the first circulation in 1999 of an idea from Harold Varmus for an NIH-funded public repository of open-access research articles, it has been clear that every author who chooses to publish their research in an open-access journal rather than one that charges a subscription fee is benefiting the community of interested researchers both immediately and in perpetuity. We urge you to bear these issues in mind when considering where to publish your next important piece of research.

**Editor's note:** The authors of the second research article in this print issue (<http://jbiol.com/content/2/1/7>) have both had close associations with *Journal of Biology*, and Martin Raff continues to do so. Neither author was involved in the refereeing of this article, in the decision to publish it, or in the choice of accompanying commentary.


abstract: # Background
  .
  Homosexual patients are affected by social factors in their environment, and as a result may not have easy access to existing health care services. Prejudice against homosexuality and homosexual patients remains a barrier to them seeking appropriate health care. The concern is that lesbians and gays might delay or avoid seeking health care when they need it because of past discrimination or perceived homophobia within the health care thereby putting their health at risk.
  .
  # Aim of the study
  .
  The aim of the study was to explore and describe the experiences of homosexual patients utilising primary health care (PHC) services in Umlazi in the province of KwaZulu-Natal (KZN).
  .
  # Method
  .
  A qualitative, exploratory, descriptive study was conducted which was contextual in nature. Semi-structured interviews were conducted with 12 participants. The findings of this study were analysed using content analysis.
  .
  # Results
  .
  Two major themes emerged from the data analysis, namely, prejudice against homosexual patients by health care providers and other patients at the primary health care facilities, and, homophobic behaviour from primary health care personnel.
  .
  # Conclusion
  .
  Participants experienced prejudice and homophobic behaviour in the course of utilising PHC clinics in Umlazi, which created a barrier to their utilisation of health services located there. Nursing education institutions, in collaboration with the National Department of Health, should introduce homosexuality and anti-homophobia education programmes during the pre-service and in-service education period. Such programmes will help to familiarise health care providers with the health care needs of homosexual patients and may decrease homophobic attitudes.
author: Nokulunga H. Cele; Maureen N. Sibiya; Dudu G. Sokhela**Correspondence to:** Maureen Sibiya, **Email:**<email@example.com>**Postal address:** PO Box 1334, Durban 4000, South Africa[^1]
date: 2015-09-28
references:
title: Experiences of homosexual patients' access to primary health care services in Umlazi, KwaZulu-Natal

# Introduction

Access to health care is a fundamental principle of health care systems around the world and is a fundamental human right of all citizens irrespective of race, class, religion, gender or sexual orientation. Access to health care can be defined as the ability of an individual to identify their health needs and to seek health care services and obtain the relevant care for their health needs (Levesque, Harris & Russell 2013:1). The Constitution of the Republic of South Africa, Section 27(1)(a), states that all citizens have the right to access health care services (Republic of South Africa 1996:6–8). The priority for public health is to eliminate health disparities in all spheres together with adverse health outcomes by improving access and utilisation of health care services (Graves 2009:46). Despite the recognition and increased awareness of homosexuality and the health needs of homosexual patients, negative attitudes persist and affect the way in which they can access health care services (Hayman *et al.* 2013:121).

A 2009 survey conducted amongst South African students in the Western Cape regarding their attitudes and beliefs towards homosexuality, found that 44% of them disapproved of the idea of homosexuality being acceptable in South Africa, and 41% believed that granting equal rights to homosexual individuals by the constitution was correct and acceptable (Mwaba 2009:803). The results of this survey indicate the general attitude some members of the community have towards homosexual patients and homosexuality. Homophobia, which is 'the irrational fear and hatred of people who are attracted to the same sex' (Müller 2013:2), is most threatening for lesbians. Many South African lesbians are living in fear of being 'found out' and becoming victims of discrimination and possible physical harm, including 'corrective rape' (Ochse 2011:3–4). Such sexual violence, driven by homophobia, places lesbians at high risk of HIV infection (Müller 2013:2).

Men who have sex with men (MSM) reported having a fear of being judged by health care providers and getting treated badly as a result of disclosure (Rispel *et al.* 2011:47). Other studies (Kennedy *et al.* 2013:3; Rosenstreich, Comfort & Martin 2011:2) assert that homosexual patients experience stigmatisation when accessing health services. O' Byrne and Watts (2014:21) point out that many homosexual patients avoid doing an HIV test because of hesitance and fear of stigmatisation. Some people in society believe that homosexual patients have violated cultural gender norms, and that stigma also adds barriers to access health care settings (Rounds, McGrath & Walsh 2013:99).

Many studies (for example Banwari *et al.* 2015; O' Byrne & Watts 2014; Ochse 2011; Rispel *et al.* 2011) reveal that lesbians (females) and gays (males), commonly known as homosexuals, experience challenges regarding access to health care services, and this has become a serious concern. The concern is that lesbians and gays might delay or avoid seeking health care when they need it because of past discrimination or perceived homophobia within the health care, thereby putting their health at risk (Müller 2013:2). For example, Bjorkman and Malterud (2009:239) found that lesbians were not following the sequence of screening programmes for females, such as pap smears. They emphasised that lesbians might suffer from health problems to a greater extent than heterosexuals or the general female population as a result of marginalisation.

Rispel *et al.* (2011:138) conducted a survey in South Africa regarding perceptions, preferences and utilisation of health care services by homosexual patients. They found that negative attitudes from health care providers discouraged them from disclosing their sexual orientation, often resulting in inadequate treatment and unmet health care needs.

Homosexual patients are affected by a range of social and structural factors around their environment, and as a result have unique health needs that might not be met by existing health care services because of ignorance by health care providers but also fear of disclosure by homosexual patients (Mitra & Globerman 2014).

In their study, Rounds *et al.* (2013:99) found that homosexual patients experience verbal abuse as well as many other forms of discrimination and a general lack of satisfactory care, including from health care professionals refusing to provide them with treatment. Eaton *et al.* (2015) report on a study in which homosexual men state that the health services offered to them were substandard. Rispel *et al.* (2011:147–149), in their study of South African homosexual men, found that some participants perceived the private health care sector to be more understanding than the public health sector.

# Profile of the researcher

The principal investigator was employed as a Clinical Nurse Specialist in one of the PHC (primary health care) facilities at Umlazi township in KZN at the time of conducting this study. She noticed that very few homosexual patients visited the clinic and that the majority of them only reported to the clinic during late stages of their illnesses or when they had complications.

# Problem statement

The rights of all South African citizens are enshrined in the Constitution of the Republic of South Africa which ensures non-discrimination by sexual orientation (Republic of South Africa 1996:13), yet it seems that homosexual patients are still discriminated against when seeking health care. They are not yet free in South African society as a result of the challenges that they daily encounter such as social stigma and homophobic attacks (Ochse 2011:4), and are often fearful and hesitant to access health care services owing to the possibility of discrimination by health care providers.

# Aim of the study

The aim of the study was to explore and describe the experiences of homosexual patients utilising PHC services in Umlazi in KZN.

# Research method design

## Design

A qualitative research study that was exploratory, descriptive and contextual in nature was conducted. A qualitative study has a subjective approach and is used to define life experiences and give them meaning (Grove, Burns & Gray 2013:23). The study provides an overview of the real life situation of homosexual patients, particularly lesbians, regarding access to health care services at the PHC level in Umlazi.

The exploratory design explores the dimensions of a phenomenon in order to better understand the context in which an intervention unfolds. The exploratory design sheds light on the various ways in which a phenomenon is manifested and on underlying processes (Polit & Beck 2012:640). The researcher used an exploratory design to better understand the accessibility of PHC services for homosexual patients.

A descriptive research design provides an accurate account of the characteristics of a particular group in real-life situations for the purposes of describing what exists, determining the frequency with which something occurs, and categorising information (Grove *et al.* 2013:26). The study was contextual in nature as the validity of the findings is only claimed in a specific context. This design was used to obtain more information about characteristics of homosexual patients regarding their experiences of utilising primary health care services in Umlazi. The purpose of a descriptive study is to provide a picture of what is happening in real life situations (Grove *et al.* 2013:215).

## Sampling and sampling technique

Purposive sampling was used to select the study participants. In qualitative research, purposive sampling is used to recruit participants for whom the research topic is relevant and the goal is to gather information about their experiences (Knudsen *et al.* 2012:85). Purposive sampling was used because it enabled the researcher to select informative cases that could provide rich and substantial information based on the personal experiences of homosexual patients regarding accessing and using PHC services in the Umlazi area. Inclusion criteria were 18 years of age or older, self-identified as either lesbian or gay, experience of PHC services in Umlazi within the past year, and able to conduct a conversation in either English or isiZulu.

Purposive sampling was modified by time-space probability based sampling. This technique is used when there is a relatively small number of people who usually gather at a specific place and time and who experience stigma and discrimination. These samples are often called hard-to-reach populations and include homosexual patients (Berry *et al.* 2013:39; Semaan 2010:61). Potential participants were approached at a gay club with the permission of the club owners. The recruitment flyers were posted at the clubhouse one week before the researcher began data collection.

According to Polit and Beck (2012:521), qualitative research has no direct fixed sample size; it is driven by the information needs of the study. The sample size was guided by the principle of data saturation. This point is reached when no new information is obtained from participants during the later stages of data collection, when subsequent interviews produce repetitions of information, indicating the completeness of the data gathered. In this study, data saturation was reached after interviewing 10 participants, but 2 more were interviewed to confirm that no new information could be elicited.

## Data collection

Data collection took place from September to November 2014. The researcher approached the club-goers whom she did not know personally and introduced herself and screened them based on the inclusion criteria. If the participant met the study's inclusion criteria, the researcher explained the purpose and the importance of the study. Participants were interviewed in a quiet locked room in the club to allow for privacy and minimise disruptions during interviews. Potential participants were given an information letter to read and were encouraged to ask questions to clarify matters. Consent forms were signed by those who agreed to participate. Semi-structured interviews were conducted using an interview guide. The following four questions were asked:

-   Describe what made you visit the PHC clinic during the past year.

-   Describe your experience at the PHC clinic starting from the time you entered the clinic, enquiries, waiting for help (in the queue), the service point (the health provider's room), waiting for medicine and receiving the medicine, leaving the clinic.

-   How were you treated? Was that the way you would like to be treated? If yes, why? If not, why?

-   Describe how accessible PHC services are to you.

All interviews were conducted by the researcher in English or isiZulu according to the language preference of the participant and lasted 30 to 45 minutes. All interviews were recorded using a digital recorder supplemented by field notes.

## Pre-testing of the interview guide

The interview guide was pre-tested to assess whether the research questions were realistic and understood by the pre-test participants. Pre-test participants are patients who meet the inclusion criteria but their data are not included in the actual study (Brink, Van der Walt & Van Rensburg 2012:174). The interview questions were pre-tested on two consenting participants at the clinic where the researcher worked. The data collected were not included in the final data analysis. No amendments were made to the interview questions.

## Data analysis

According to Polit and Beck (2012:556), data analysis involves organising the data that the researcher has collected, providing structure and eliciting meaning from it. Data were analysed using content analysis. Content analysis is used to analyse and interpret data by classifying the words in the text into categories in order to give it meaning. Repeated ideas or patterns of thought are grouped by organising data into categories and concepts that the researcher has developed (Grove *et al.* 2013:281).

## Ethical considerations

All consenting participants were given written and verbal information about the process of the study. They signed consent forms after reading and understanding the information letter. Privacy was maintained by not disclosing participants' information to any third party. Justice was maintained because the participants were informed that they could decline participation at any stage of the research, or withdraw during the interview, and could do so without incurring any negative consequences. The right to confidentiality was ensured throughout the research process; names would be known only to the researcher and codes were used to identify data associated with them. The master list of participants and their codes was kept under lock and key. No family member, health worker or any other person had – or will have – access to the raw data to prevent breach of confidentiality. The Durban University of Technology Institutional Research Ethics Committee provided ethical clearance for the research proposal (IREC number 61/14).

## Trustworthiness

Guba's model of trustworthiness was applied to ensure the trustworthiness of this study in regard to credibility, dependability, confirmability and transferability (Brink *et al.* 2012:172). Credibility was maintained through using the same interview guide for all participants. The researcher visited the club over a period of three months, meeting with different participants. Member checks were conducted whereby the researcher returned to give feedback to participants and checked their reactions to themes emerging from the data. In order to ensure dependability the researcher developed an audio trail by keeping all the original audio records of interviews and discussions on a disc. To ensure confirmability, the researcher interpreted and analysed the data through identifying themes and subthemes which were supported by direct quotations from the participants in order to eliminate subjectivity and bias. A thorough description of the research report was provided to ensure transferability so that other researchers could evaluate and test the applicability of the data in other contexts.

# Results

Two major themes emerged from the data analysis:

**Theme 1:** Prejudice against homosexual patients by health care providers and other patients at PHC facilities.

**Theme 2:** Homophobic behaviour from PHC personnel.

Several sub-themes emerged from the interview in line with the two major themes. The themes and sub-themes are presented in Table 1.

Themes and sub-themes.

Themes
Sub-themes

Prejudice against homosexual patients by health care providers and other patients at primary health care facilities.

Stigma from health care providers.

Rejection by other patients.

Homosexual patients' satisfaction and dissatisfaction with primary health care services.

Homophobic behaviour from primary health care personnel.

Lack of understanding of homosexuality.

Attitudes of homosexual patients towards health care providers.

Influence of religious and cultural beliefs of health care providers on their perceptions of homosexual patients.

Heteronormativity amongst health care providers.

Attitudes of health care providers towards homosexual patients.

Inappropriate curiosity of health care providers regarding homosexuality.

Personal involvement of health care providers with homosexual patients.

## Prejudice against homosexual patients by health care providers and other patients at primary health care facilities

Participants cited experiences of prejudice and stigmatisation as the major reasons for not receiving fair treatment from the health care providers after gaining entry to such services. Discrimination was noted by participants when they received treatment which was different from that of heterosexuals. Their perception of being stigmatised was when they were labelled on the basis of their appearance or dress code. This prejudice was experienced as coming from other patients as well as from health care providers. The sub-themes that emerged were stigma from health care providers, rejection by other patients, lack of equality for homosexual patients in PHC services, and their satisfaction and dissatisfaction with PHC services.

# Stigma from health care providers

Participants reported that they felt stigmatised by health care providers. They reported that they were being judged because of their personality and because of the way they dressed, talked or walked. Their perceptions of being stigmatised are evident in the following quotations:

> 'Are you here for family planning? The nurse asked me while she was holding and reading my card. As I was getting ready for the injection she continued to say 'you are also wearing men's underwear?' I was there for a different injection but a nurse kept on asking about family planning, saying lesbians do not do prevention …' (P8)
>
> '… \[*F*\]rom the nurses, umm, you get lots of questions? In the consultation room, the first question that the nurse asked me was what type of a person I was. I ignored the question and told her that I was sick …' (P1)
>
> '… \[*A*\]t the PHC facility people have their own prejudices and there is a lot of stigmatisation. If you are a homosexual you go there looking for help for your sickness but they always include things that are unnecessary. Despite telling the nurse that you are a male and gay, they always make you to explain yourself and emphasise that you are different. They repeatedly ask if you are male or female.' (P11)

# Rejection by other patients

Participants reported that they felt rejected by other patients in the PHC facility's waiting area. Some patients in the waiting area made comments which scared participants, causing some of them to leave the PHC facility before they were attended to by the health care practitioner. Rejection by other patients is revealed in the following quotations:

> '… \[*W*\]hen I went to the PHC facility, at the gate, I enquired from the security guard, an old man, who looked at me, clicked his tongue and swore at me. But I could not care less because I am used to things like that. When I got inside the PHC facility patients laughed at me because I was wearing tight pants and they were looking at my private parts, but still I did not care. I put my earphones on, ignored them and sat in the queue …' (P7)
>
> 'When I was still sitting in the queue there were women behind me who were laughing, but I did not know what they were laughing at, but I noticed when the woman next to me also started laughing. When I listened carefully they were debating about homosexuals. Someone said it was a fashion. The other woman added; if I can see a homosexual here I can put a tyre around her neck and burn her. I could not stay long, I decided to go back home because these people made me uncomfortable and I felt that they could harm me. I decided that when I have money I will go to the private doctor.' (P2)
>
> '… I felt very disturbed and unhappy because people were sitting away from me because I am gay.' (P5)

# Homosexual patients' satisfaction and dissatisfaction with primary health care services

Only one participant reported satisfaction with the treatment received from the health care provider who had good communication skills and treating all patients the same. This was expressed in the following excerpt:

> '… I don't want to lie; I was so satisfied with the treatment that I got from the health care provider who was helping me. That nurse did not treat me differently from heterosexuals. She did not have that in her mind that I am a homosexual client.' (P6)

The majority of participants reported dissatisfaction with the treatment received from health care providers. This was mainly because of the experience of participants regarding health care providers' attitudes toward homosexual patients and of being treated differently to the way heterosexuals were being treated. This is expressed in the following quotations:

> … \[*I*\]t is so difficult to use PHC facility. I was so dissatisfied with the treatment that I received and please do not ask how it ended. I just left the clinic without receiving any help.' (P4)
>
> '… I was uncomfortable, as a result I could not disclose my real problem because I had an anal problem, I decided to go to a private doctor.' (P7)
>
> 'Our clinics are not in a good standard they don't accommodate all of us as we having different sexual orientations …' (P8)
>
> 'It was almost over in 15 minutes, a nurse busy asking me questions about being gay, and not helping me and I was no longer there I wanted help and go home but I felt very disappointed about everything.' (P5)

# Homophobic behaviour from primary health care personnel

Participants reported that they experienced a range of homophobic behaviours from health care providers and in the waiting area from other patients. The following seven sub-themes emerged from this: lack of understanding of homosexual patients; attitudes of homosexual patients towards health care providers; influence of religious and cultural beliefs of health care providers on their perceptions of homosexual patients; heteronormativity amongst health care providers; attitudes of health care providers towards homosexual patients; inappropriate curiosity of health care providers regarding homosexuality; personal involvement of health care providers with homosexual patients.

# Lack of understanding of homosexuality

The findings of the study revealed that health care providers and members of the public who were patients in the PHC lacked an understanding of homosexuality. This was evident from the questions they asked and the disbelief that often accompanied the answers. Participants were not believed nor taken seriously when they reported that they had been infected with sexually transmitted infections, as noted in the following excerpts:

> '… \[*W*\]hen I got into the consultation room a nurse asked what I was suffering from and I told her that I had a problem in my private part and I think it is a sexually transmitted infection. She asked me how come I have a sexually transmitted infection while I am in a relationship with a female. The nurse asked me to explain how I have sexual intercourse. I told her that I could not explain something like that, and I asked her to help me with treatment as I wanted to leave the room.' (P9)
>
> '… \[*T*\]he nurse asked me about my HIV status as I was having some sort of sexually transmitted infection and I told her that I was HIV negative. She asked if I was using condoms and I told her that I was not, and I told her I did not even know homosexuals' condoms, I had never seen them before.' (P5).

# Attitudes of homosexuals towards health care providers

Some participants who went to the PHC facility had a positive attitude towards health care providers or health facilities because of previous positive experience. One participant expressed her experience of a positive attitude regarding the PHC provider by saying:

> 'The nurse who attended to me did not treat me differently. I did not feel discriminated.' (P6)

Other participants reported that their own attitudes were negative towards the PHC providers prior to them reaching the PHC facility, because of preconceived ideas about health care providers which might or might not have been factual. This caused problems for the participants as they became agitated without provocation from the health care providers. The participants who had experienced negative attitudes from health care providers had this to say:

> '… \[*W*\]hat I don't like most with the clinic is the attitude of nurses towards homosexuals. I always see it …' (P6)
>
> 'However, I was lazy to go there because of what my friend told me, the questions he went through. Before I got helped I was asked many questions too and criticised too much.' (P11)
>
> '… Umm … It is not easy to use the clinic; you end up getting hurt.' (P7)

# Influence of religious and cultural beliefs of health care providers on their perceptions of homosexuals

The religious beliefs of health care providers were perceived as problematic by participants. The participants reported that health care providers tended to want to convert or impose their religious beliefs on them and expected them to behave and lead their lives according to those beliefs. An example of such a view is expressed in the following excerpt:

> '… \[*I*\]t wasn't good news to a nurse to discover that I am a lesbian. The nurse started preaching saying she feels sorry for my mother, I need to go to church and pray because what I am doing is against God's will …' (P12)

Some patients believed that homosexuality could be 'corrected or healed' using cultural methods they were familiar with:

> 'The conversation continued until a person next to me said, being homosexual is not right, because it is Satanism and it is kind of a fashion and someone said homosexuals need slaughtering of goats because this is against culture.' (P6)

# Heteronormativity amongst health care providers

When health care providers managed patients, they never seemed to give a thought to the fact that there could be homosexual patients seeking medical assistance. They tended to treat everyone as if they were heterosexual. Participants witnessed heteronormativity in the following instances:

> '… I told the nurse that I wanted to do an HIV test. The first question was; why do you want to do HIV test? I told her that I want to know my status; she then asked if I use condoms. Hey! I was taken aback for a moment, seriously I was confused by the question … I answered no, now a nurse gave me health education on using condoms and asked if am not aware of the importance of using condoms, I told her I knew. She did not ask me about the type of partner I have or the reason for not using condoms. Later on, she asked me if my partner has tested, and I told her that she's outside. She then asked me to call him so that she will give us both health education about the use of condoms. When my partner got inside the nurse just changed her facial expression \[*frowning*\] she was surprised and looked very shocked to see that it was a female. And she said: 'this is the reason you are not using condoms', I said 'yes'.' (P3)
>
> '… \[*T*\]he nurse asked the usual questions as to a female, she asked about pregnancy, my last menstrual periods, and use of condoms? When I said no to using condoms, she immediately educated me on the importance of using them. I explained my sexuality to her and she was taken aback and was speechless for some time. It wasn't good news to a nurse to discover that I'm a lesbian. Nurse started preaching me saying she feel ashamed for my mother …' (P12)

# Attitudes of health care providers towards homosexuals

Participants reported negative attitudes from health care providers. They verbalised moments where their sexual orientation seemed to upset the health care providers. The negative attitudes of health care providers towards homosexual patients are portrayed in the following excerpts:

> '… \[*W*\]hen I entered to a consultation room the first thing a nurse said to me was 'what's going on here?', and I looked back because I thought maybe there was something happening behind me, and a nurse said no I am asking you 'what type of a person are you really?' (P8)
>
> '… \[*W*\]hen I got into the consultation room I explained to a nurse that I needed contraceptives, a doctor had referred me because of my abnormal menstrual periods, a nurse refused to give me contraceptives, no matter how hard I tried to explain that I am not sleeping with males I need it for abnormal periods. A nurse said I am a lesbian and I don't need contraceptives and she did not give them to me.' (P10)

# Inappropriate curiosity of health care providers regarding homosexuality

The majority of participants reported that they had been asked about how they engaged in sexual intercourse by health care providers. The participants perceived this to be inappropriate curiosity on the part of the health care providers, and they felt that this question was irrelevant to the history taking or the diagnosis and treatment as noted in the following excerpts:

> '… \[*I*\]f things were done my way, I wish lesbians and gays had a dedicated clinic in order not to get tortured by nurses with lots of questions, that are private like asking how do we engage in sexual intercourse with the person of the same sex?' (P12)
>
> '… \[*T*\]he question that followed was; how do you engage in sexual intercourse as you're both females?' (P8)
>
> '… \[*T*\]he nurse asked me to explain how I have sexual intercourse. I told her that I could not explain something like that, and I asked her to please help me with treatment as I wanted to leave the room.' (P9)

# Personal involvement of health care providers with homosexuals

Sometimes health care providers were somewhat personally affected by homosexuality either having a homosexual child or the health care provider admitting to having feelings for homosexual patients. Some participants felt offended whilst others felt that this helped the health care provider understand homosexuality better. An example of a participant who felt offended is provided below:

> '… \[*W*\]hen I got inside the consulting room the male nurse asked if he should write female or male, I told him that I am a gay male, I am not a female. After that he told me that he was married but wished to have relations with a gay person like me. I became so angry because I thought that he was provoking me. He then told me that we will book a place where we can sleep. I was so annoyed and uncomfortable as he was continuing with the conversation …' (P7)

# Discussion

## Prejudice against homosexual patients by health care providers and other patients at primary health care facilities

Participants identified prejudice against them as an obstacle to their utilisation of health care services. This is consistent with findings of other studies (for example Kennedy *et al.* 2013; Müller 2013; Rounds *et al.* 2013). Rosenstreich *et al.* (2011:302) state that throughout the world health care providers and communities still discriminate against and marginalise homosexual patients. Some health care providers lack the tolerance required to work with them because of their personal affiliations which interfere with their professionalism (Röndahl 2009:146). Many health care providers found it difficult to render care to them as they cannot tolerate their sexuality and end up failing to give quality nursing care equal to that given to heterosexuals (Röndahl 2009:147). Participants in this study reported that they were not treated in the same way as heterosexuals. Only one participant reported the experience of being treated fairly. Two studies report that patients verbalised satisfaction with health care services when their health needs were met (McNair, Szelacha & Hughes 2011; Tjepkema 2008). These authors further assert that satisfaction is reported to be higher when health care providers show acceptance and respect towards patients' homosexuality and display positive attitudes towards them. Rounds *et al.* (2013:99) reported that homosexual patients received substandard care from health care providers.

Participants verbalised that some members of the public who were patients showed signs of prejudice by rejecting homosexual patients in the waiting areas at the clinics where all patients queue whilst waiting for assistance from the health care providers. Some reported leaving the PHC facilities before consultation with the health care providers because of this. According to Araújo *et al.* (2009:667), homosexual patients usually experience situations of prejudice in the community. The burden of stigma might be more severe for patients who look like homosexual patients compared to those who are not easily identifiable. These authors further state that homosexual patients might be humiliated and mocked by some members of society even in the health care settings because of their homosexuality.

## Homophobic behaviour from primary health care personnel

The participants in the current study reported experiencing homophobic behaviour from PHC personnel during their utilisation of health care services. According to Akhan and Barlas (2013:435) homophobia lies behind the judgements, negative attitudes and unfair treatment of homosexual patients in health care facilities. Berry *et al.* (2013:40) state that members of the public are generally not educated about, and lack an understanding, of homosexual people and once they discover that someone is homosexual, they change their attitudes and start looking down upon them.

Participants reported that there were moments where the health care providers preached to them instead of providing the services that they required. Röndahl (2009:149) argues that the religious health care providers can be problematic in the nursing context, especially when nursing homosexual patients. They became more concerned about influencing homosexual patients to become heterosexuals instead of treating patients holistically. This attitude can also be present in married health care providers who associate homosexuality as being against God's will for what a family should be and therefore it needs to be changed (Akhan & Barlas 2013:435). Some participants in this study experienced criticism from members of the public who were also patients in the PHC, and who believed that homosexuality was against the cultural background of African people. According to Akhan and Barlas (2013:435), these homophobic attitudes are influenced by the social arrangements and the patriarchal structures of countries. An example of patriarchal heteronormative behaviour was experienced by participants in the current study when it was assumed that they were heterosexual because health care providers did not ask about their sexual behaviour. Lesbians are becoming more visible in society but health care providers still tend to treat all females as if they are heterosexuals (Hayman *et al.* 2013:121).

One participant in the current study verbalised that she had a positive meeting with the health care provider who showed good communication skills and acknowledgement of homosexuality. According to Röndahl (2009:146), the insecurities of homosexual patients sometimes affect their interaction with health care providers as not all health care providers display negative attitudes towards them.

In this study some health care providers indicated inappropriate curiosity when they constantly enquired about how homosexuals engage in sexual relations. Hayman *et al.* (2013:120) report cases of health care providers asking about how conception takes place, laughing and joking about pregnancies amongst homosexual women. However, health care providers sometimes ask homosexual patients about their sexuality and sexual activities in order to understand their personal issues. Akhan and Barlas (2013:435) suggest that when health care providers meet homosexual patients they should seize the opportunity to educate themselves and their families about their lifestyle.

# Limitations of the study

Researching homosexual patients in South Africa is challenging because they are hard to access as many have not 'come out' about their homosexuality, especially homosexual males; hence, only those who visited a particular gay club in Umlazi were interviewed. The research was conducted on those residing in Umlazi only. The experiences of health care providers were not studied, only that of homosexual patients. Participants were not asked about their experiences of accessing and utilising private health care services, as this aspect fell beyond the scope of the current study.

# Recommendations

The following recommendations emerged:

-   Nursing education institutions, in collaboration with the National Department of Health, should introduce homosexuality and anti-homophobia education programmes during the pre-service and in-service education period. Such programmes will help to familiarise health care providers with the health care needs of homosexual patients and may decrease homophobic attitudes.

-   Guidelines on history taking from homosexual patients should be compiled. This will improve their ability to offer relevant health information and management.

-   Health care providers should not show patients that they are surprised about their sexual orientation. They need to set a relaxed tone and be aware of their negative body language.

-   Campaigns to educate the public about homosexuality could create a more conducive environment for homosexual patients so that they can access health facilities without fear of prejudice and discrimination by members of the public who are also patients at the PHCs. Such education sessions could be provided in PHC clinic waiting areas and during HIV and/or AIDS health education sessions.

-   The possibility should be investigated of offering PHC services at gay clubs, for instance one evening per week, by health care providers who are willing to treat homosexual patients with respect and without prejudice.

-   Future studies should endeavour to identify the attitudes of health care providers working at PHC clinics towards homosexual patients, as well as their knowledge of and perceptions of them.

# Conclusion

The findings indicate that some participants encountered challenges to accessing and using PHC services in the Umlazi area. The major patient-related challenge was that some participants feared discrimination at the PHC clinics and consequently they postponed or abandoned their PHC clinic visits. The major service-related challenges involved the non-professional attitudes of some health care providers who discriminated against some participants' sexual orientations, asked inappropriate questions and failed to provide adequate services. Some of the other patients in the waiting areas also showed disrespect towards participants causing some of them to fear for their safety to the extent that they left the clinic without consulting any health care professional.

Health care providers should receive pre-service and in-service education about the necessity of treating homosexual patients professionally and respectfully. Members of the public should also be educated about homosexuality and about avoiding discriminating against homosexual patients. Such education sessions could be provided in PHC clinic waiting areas, at women's and men's gatherings and during HIV and/or AIDS health education sessions. Implementation of some of these recommendations could help to facilitate homosexual patients access to and utilisation of PHC services in the Umlazi area of the KwaZulu-Natal province.

## Acknowledgements

### Competing interests

Authors declare that they have no financial or personal relationships which may have inappropriately influenced them in writing this article.

### Authors' contributions

N.H.C. was the Master's student and principal investigator, M.N.S. the primary supervisor providing guidance to the student in writing the manuscript. D.G.S. was the co-supervisor for N.H.C.

# References

[^1]: **How to cite this article:** Cele, N.H., Sibiya, M.N. & Sokhela, D.G., 2015, 'Experiences of homosexual patients' access to primary health care services in Umlazi, KwaZulu-Natal', *Curationis* 38(2), Art. \#1522, 9 pages. <http://dx.doi.org/10.4102/curationis.v38i2.1522>


abstract: A report on the joint Cold Spring Harbor Laboratory/Wellcome Trust Conference 'Genome Informatics', 15-19 September 2010, Hinxton, Cambridge, UK.
author: Zemin Ning; Stephen B Montgomery
date: 2010
institute: 1Sequencing Informatics, The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK; 2Department of Genetic Medicine and Development, University of Geneva Medical School, Geneva 1211, Switzerland
title: Out of the sequencer and into the wiki as we face new challenges in genome informatics

# Meeting report

Next generation sequencing (NGS) analysis, open-source software, cloud computing and wiki-style genomics were among the hot topics and discussions at the recent Genome Informatics meeting at the Wellcome Trust Genome Campus, Cambridge, UK. Here we summarize some highlights of the meeting.

# Accuracy of polymorphism detection

Comparison of related genomes can generate a wealth of knowledge about genome evolution and function. Recent advances in NGS technologies have greatly increased the scale and scope with which we can interrogate novel genomes and uncover genetic variation. However, for variation detection and statistical analysis, there are false positive errors for various reasons, notably incompleteness of reference genomes, read mapping errors or limitations, and sequencing-induced features. Benjamin Dickins (Penn State University, University Park, USA) discussed an approach to estimate polymorphism accuracy from NGS data by deeply sequencing a small plasmid genome and comparing it with Sanger sequencing.

Elliott Margulies (National Human Genome Research Institute, Bethesda, USA) gave an enticing presentation on this topic entitled 'Analysis of identical twins' genomes reveals sources of false-positive variation detection'. With 55× and 50× depth of read coverage from each twin's sample, they initially identified 83,538 discordant genotype calls across 97.6% of the human reference genome. Through inspection of a random set of discordantly genotyped positions, he revealed that a majority occurred in regions with poorly aligned reads. Margulies noted that he would be highly suspicious of genotype calls in regions with high coverage but with low mapping scores. When these events were filtered out, the number dropped to 13,140, a reduction of 84%. By then further introducing other filtering mechanisms, such as incorrect alignments of short reads across indels, Q20 (99% confidence) evidence in the other twin and 10% allele frequency, Margulies' final number of discordant genotype calls was only in the range of 500 to 1,000.

Margulies' suspicion was certainly shared by Richard Durbin (Wellcome Trust Sanger Institute, Cambridge, UK), who told the audience, "If someone tells me that his accuracy on variant detection is 99%, I should be cautious". Durbin described that in the pilot phase of the 1000 Genomes Project, the sequencing strategy with low coverage (2× to 4×) worked well, and it can efficiently find shared sequence variation with good accuracy. The consortium has now started sequencing 2,500 people in five different ethnic groups. Furthermore, Durbin highlighted the recently launched UK 10 K project, which, in collaboration with clinical investigators, will involve sequencing 4,000 cohort samples with rich phenotypes. With massive sample collections under way, further advances in informatics pipelines to reduce errors in variation detection will be indispensable.

# Genome assembly and read alignment

NGS data provide challenging but exciting prospects for *de novo* assembly. There were several presentations that focused on development and evaluation of genome assemblers using such data. David Jaffe (Broad Institute, Cambridge, USA) outlined a practical and general laboratory/computational method for generating high-quality *de novo* genome assemblies. Three types of data were produced with the Illumina platform: 180 bp short-insert reads; 3,000 bp mate-pair reads; and 40,000 bp fosmid ends. The short-insert data were mainly intended to ensure contig base accuracy, whereas the longer jumping fragments provide potential for long-range connectivity. Jaffe generated data for mouse C57BL/6 and human Yoruban NA18507 and then compared the short-read assembler, ALLPATHS, with the reference assembly that used the capillary long-read assembler, Arachne. From the comparison of the results, the quality of short-read assemblies was found to be close to that of capillary assemblies, in terms of both base accuracy and contig connectivity.

Transcriptome data also offer great value and unique challenges in helping to identify and assemble gene sets for multiple species. Daniel Zerbino (University of California, Santa Cruz, USA) presented a new methodology, Oasis, which is built in with the popular short-read assembler Velvet. This new program takes in a preliminary assembly produced by Velvet and exploits the read sequence and pairing information to produce transcript isoforms. When possible, it also detects and reports standard alternative splicing events. It is specifically designed to get around the issues of unequal expression levels and alternative splicing breakpoints.

Short-read alignment saw further new developments at the meeting. New tools include: SMALT by Hannes Ponstingl (Wellcome Trust Sanger Institute, Cambridge, UK); NextGenMap by Fritz Sedlazeck (Max F Perutz Laboratories, Vienna, Austria); and YASRAT by Masahiro Kasahara (The University of Tokyo, Kashiwa, Japan). One distinguishing feature in these new alignment tools is that they all try to address the cases in which there is a higher level (over 2%) of base-pair errors in the raw reads.

# Databases and data visualization

As sequence availability has increased, data access, representation, analysis and visualizations pose significant challenges in the community. Enis Afgan (Emory University, Atlanta, USA) has developed a solution that allows experimentalists to perform large-scale analysis using cloud-computing resources (<http://usegalaxy.org/cloud>). Because the solution is built on the open-source Galaxy framework, analyses using this service are accessible, transparent and reproducible. Furthermore, popular tools and workflows for sequence analysis from various types of experiment are already built in and ready to run. Marc Fiume (University of Toronto, Canada) presented the Sequence Annotation Visualization and ANalysis Tool (Savant), a fast and interactive genome browser that can display sequence, read alignment, single nucleotide polymorphism and other genomic datasets stored in standard file formats. Harminder Sehra (European Bioinformatics Institute, Hinxton, UK) described how the well established UniProt Knowledgebase (UniProKB) has developed from manual to automatic annotation. Marcin Piechota (Institute of Pharmacology, Krakow, Poland) described <http://genes2mind.org>, an online resource for the genomic profiling of psychoactive drugs. The database contains comparisons of the effects of various classes of psychoactive drugs on transcriptional alternations of about 20,000 genes in the mouse brain. And Maximillian Hauessler (University of Manchester, UK) presented text2genome, a method for annotating the genome using sequences that are reported in scientific publications.

Although NGS has required the development and improvement of many novel visualization tools, Martin Krzywinski (British Columbia Cancer Agency, Vancouver, Canada), the author of the Circos tool, took us back to basics by redefining network diagrams in his compelling talk in which he introduced a technique for turning network diagrams from incomprehensible 'hairballs' into information-rich schematics.

# New insights from sequencing repetitive elements

Repetitive element sequencing is revealing some interesting new biology. Karen Hayden (Duke University, Durham, USA) demonstrated unique patterns of repeats in human centromeres, which could facilitate completion and understanding of specific biology in these hard-to-assemble regions. Kateryna Makova (Penn State University) highlighted the lifecycle of microsatellites and their potential functional impact near genes. And Mark Batzer (Louisiana State University, Baton Rouge, USA) showed from 37 orangutans clear differences in retrotransposon polymorphism, which could support the separation of the Sumatran from the Bornean orangutan.

Repeats are not always a good thing. There were also some presentations of genome analysis on large plant genomes. The highly repetitive wheat genome, with a size of 17 GB, poses significant challenges using the current sequencing platforms, in physical mapping as well as *de novo* assembly. Frederic Choulet (Institut National de la Recherche Agronomique, Clermont-Ferrand, France) described the effort to sequence and analyze wheat chromosome 3B. Contiguous bacterial artificial chromosome pools were sequenced by combining Roche 454 and Illumina platform sequencing. Shiran Pasternak (Cold Spring Harbor Laboratory, Cold Spring Harbor, USA) described the current progress on assembling the wheat D-genome, and Rachel Brenchley (University of Liverpool, UK) highlighted the advantages of comparative genome analysis in distinguishing genic loci from the abundance of repetitive content in the wheat genome.

# RNA-seq and epigenomics

There was one dedicated session on RNA sequencing (RNA-Seq) and its application to genome annotation, in which various issues were discussed. Specifically, identifying the underlying biases in the RNA-Seq presents a significant analytical challenge. Projects such as the RNA-Seq Genome Annotation Assessment Project (RGASP) are examples of successful collaborations that are pushing the development of algorithms that can infer accurate transcript quantification. RGASP, led by Jen Harrow (Wellcome Trust Sanger Institute, Cambridge, UK), and Felix Scheslinger (Cold Spring Harbor Laboratory) showed the utility of spike-ins in RNA-Seq experiments to achieve adequate normalization. Many talks also highlighted how RNA-Seq was used for novel interrogating of the impact of genetic variation, such as that of Emilie Graison (University of Lausanne, Switzerland) who demonstrated how RNA-Seq can be used to uncover interesting connections between copy number variants and transcript diversity.

Chromatin immunoprecipitation sequencing (ChIP-Seq) provides an extraordinary window into the dynamics of protein-DNA binding. Xin Feng (Stony Brook University, New York, USA) presented PeakRanger, a new algorithm to call peaks from ChIP-Seq data and explore complex peak structures in regions of interest. It works by identifying broad regions of enriched binding and integrates topological clues to detect narrow peaks.

# Wikis can change the way we do science

The growth of sequencing data is far outpacing the rate of curation. Previously successful models are not meeting the demands of genome biology and, in many historical cases, the majority of annotations were from a small number of contributors. A view that was heard in the conference was that it is necessary to incorporate the community to a greater extent into the annotation process using tools such as wikis. Although lack of recognition and credit may prevent scientists from actively participating, this may be only part of the story. Reasons for not giving back to the community need to be investigated. In his keynote speech, Alex Bateman (Wellcome Trust Sanger Institute, Hinxton, UK) described new approaches to engage the community of RNA biologists to improve the annotation of the Rfam RNA database as well as more generally contribute to the annotation of RNA in Wikipedia. The journal *RNA Biology*, in collaboration with Rfam, has pioneered a new model of scientific publication where scientists are required to write a Wikipedia article to go alongside their manuscript paper describing new families of non-coding RNAs. At the same time, the Wikipedia article will also be under a full peer review process. Complementing this approach, Daniel Renfro (Texas A&M University, College Station, USA) presented community-focused annotation resources using the Mediawiki software. Currently this includes two model bacterial species: *Escherichia coli* (EcoliWiki) and *Bacillus subtilis* (SubtilisWiki).

In recent years, we have seen significant changes in the bioinformatics community: from massive data flow to complicated pipelines; from big computational farms to cloud computing; from a single genome or chromosome to many thousand genomes; from different sequencing platforms to various data types and error models. The themes reviewed here reflect the fact that the field of genome informatics is constantly under change, responding with new solutions, new algorithms and new technologies. The future presents us with a new challenge in how we transform the scale of data into collective knowledge, and it is likely that, as open-source software is accelerating bioinformatics and cloud computing is helping us to scale up, the growing online collaboration offers a chance to tackle this.

## Acknowledgements

SBM is funded by the Louis-Jeantet Foundation.