Lime Use and Reproductive Health in Northern Nigeria: A Feasibility Study
Executive Summary - 02/03/2004

Draft: Not to be Quoted Or Cited without Permission Of the Authors

This study was conducted in the northern Nigerian cities of Maiduguri, Kano and Abuja to explore the use of limes with sex.

Contacts

Purpose of the Study

In vitro studies suggest that lemon/lime juice could prove to be both an effective contraceptive (Clarke 2003) and microbicide with anti-HIV potential (McCoombe 2003). It appears that 0.5 ml of pure lemon/lime juice can cause irreversible sperm immobilization within seconds to a mean volume of 2.5 ml of human ejaculate (UMEC 2003). Natural vaginal acidity (pH 4.5) constitutes one defense against infections. An acidity level lower than 4.0 can cause most pathogens (including HIV) to die within a few hours. It is not known if any component of lemon/lime juice has any microbial or spermicidal effect over and above the pH value.

In July 2003, we received anecdotal information from health care providers in northern Nigeria that a significant number of female commercial sex workers (CSWs) in the region douche with lime juice before or after sexual intercourse with clients. Three months later, we carried out a pilot study to explore the specifics of the use of limes by the CSWs and to assess the feasibility of designing a more detailed study, including a statistical analysis of the possible associations between the use of lemon or lime juice, HIV status, sexually transmitted infections and pregnancies.

We also hoped to learn more about the effects of lime use on the health of the reproductive tract. Although repeated intra-vaginal use of lemon juice in Cymologous monkeys has been shown not to damage the vaginal epithelium (Short 2003), there is still a possibility that, even if it kills HIV, in certain cases it could damage the human vagina and thus increase risk of HIV transmission.

The pilot study was sponsored by Venture Strategies for Health and Development, the Bixby Program, and the Center for Entrepreneurship in Health and Development of the School of Public Health, University of California, Berkeley.

Study Participants

Subjects in the study were female CSWs from the Nigerian cities of Abuja, Kano, and Maiduguri. The majority of the women were from the Hausa ethnic group. The Hausa people of Nigeria are mainly concentrated in the provinces of Kano, Katsina, Sokoto, and Zaria. Hausa is the native language of the majority of the population in northern Nigeria and is used as a lingua franca among Muslim populations in much of West Africa. There has been an Islamic presence in Hausaland since the11th century, but its predominance was not fully established until the nineteenth century (Callaway 1987).

The majority of the inhabitants of northern Nigeria live in family compounds. The compounds are often surrounded by high walls made of mud block in rural areas and cement block in the cities. To enter, one usually proceeds through one or more entrance rooms to a courtyard. Much of northern Nigeria is a conservative Islamic culture. A man is allowed to have up to four wives. Each wife has her own room, which faces inward toward the courtyard. The most culturally approved life path for a woman is to get married, have children, and to enter old age surrounded by kin. A woman leaves her father’s compound to live in her new husband’s compound (Pittin 2002).

However, from our interviews and from published ethnographic work it appears that divorce and remarriage is not uncommon (Albert1996; Callaway1987; Coles 1991; Pittin). Seclusion for women is still commonly practiced, though the custom appears to be declining. Men typically label as a prostitute any unmarried woman who is independent and does not live under the shelter of a father or husband.. According to this logic, a woman is either a daughter living at home, is married and living with her husband, or is a prostitute. Women tend to consider such categories with more subtlety. Pittin (2002) describes alternative life paths, such as a woman who achieves independence without being labeled a prostitute by becoming “prematurely old.” That is, she might take on the dress, work, and lifestyle of an elderly woman.

Women are often under pressure to marry young, especially in the rural areas. Escape from a coerced marriage was one of the primary reasons that the women we interviewed gave for becoming a commercial sex worker. “For a woman like me, with little education, what other work is there?” said one. Other women said they became commercial sex workers because of marriages that ended because they were unable to have children, or due to incontinence caused by an obstetric fistula. (Obstetric fistulas are more prevalent among young mothers and among poor women without access to obstetric services.) Domestic violence was another reason given by the commercial sex workers for entering the trade.

Some of the men and women we interviewed divided commercial sex workers into two categories, the “karuwai” and the “good evening girls.” They described the karuwai as being traditional Hausa courtesans. Karuwai do not solicit openly. Instead, they go to popular dances, clubs, restaurants, and festivals where they meet potential clients who must court the woman with gifts, and sometimes outings, before she will agree to physical intimacy. Karuwai are given cash and gifts by their clients, but a price is never negotiated. Karuwai tend to live in compounds with four or five other karuwai. An older karuwai often leads the group and is called the magajiya. The word magajiya comes from the title given to women who led the pre-Islamic spirit worship in the region.

“Good evening girls” differ from karuwai, according to our respondents, in that they solicit customers on the street or in bars or nightclubs, and they negotiate a price. “They lean over to your car window and say ‘good evening’ in English, which is where they get their name,” said one respondent. Their approach to their work is similar to that of many commercial sex workers found in the US or Europe.

Both the karuwai and the “good evening girls” pay a severe social price for being commercial sex workers. They are insulted on the street and have been historically blamed for causing draught and other natural disasters by their “immoral” behavior. Still, their lifestyle does seem to provide some benefits. Hajiya Bilkisu, the president of the Federation of Muslim Women’s Associations in Nigeria (with whom we collaborated on this research), rejects the labels CSW, karuwai, and “good evening girl” for these women. She calls them “independent women.” “They are virtually the only women in northern Nigeria not under the control of a father or husband,” she explains. “They can walk where they want to walk, go out when they want to go out, and pay no heed to the practice of seclusion. And if she is intelligent, has social grace, and invests her money well, she has a chance of buying her own compound and providing for her old age.”

We interviewed 104 “independent women.” Forty-four use limes with sex, while 60 do not. The women ranged in age from 18 to 55, averaging at 25 years of age. In addition to working as commercial sex workers, a number work as traders in the market (28% of the sample) and weave hair (16%). They had an average of 2 induced abortions, with 92% percent of the women having terminated at least one pregnancy. All of the women practice vaginal sex. Twenty-five percent of those using limes also practice oral sex, as compared with 33% of the non-lime users. Less than one percent of each group said they practiced anal sex.

Recruitment

The study protocol was approved by the UC Berkeley Protection of Human Subjects Committee.

The primary partner of the UC Berkeley investigators was the Nigerian non-profit organization Girl Child Concerns (G-C-C), which works with CSWs. All identified CSWs willing to give informed consent were eligible to participate in the study. We sought to recruit a minimum of 100 women in the three cities.

We employed purposive sampling. Although purposive sampling does not allow generalization with any known precision, every attempt was made to ensure adequate coverage of important subpopulations (rural/urban, younger/older, etc.).

G-C-C helped identify research assistants from NGO staff working with CSWs. One of the most important qualifications of the research assistants was their ability to develop rapport with the respondents. The investigators trained the research assistants to administer the questionnaires and conduct the face-to-face interviews and focus groups.

Methods

Dr. Daniel Perlman, a medical anthropologist, interviewed with the help of the local staff 104 women, 44 of whom used limes in conjunction with sex. Local gynecologists provided the women interviewed in the cities of Kano and Maiduguri with pelvic examinations, plus syndromic diagnoses and treatment of other STDs. Voluntary laboratory tests for HIV and gonorrhea were offered to all participants. The pelvic examinations focused on possible clinical evidence of damage to the vagina in lemon users. The women in Abuja did not participate in the clinical part of this feasibility study for reasons that will be discussed below.

Qualitative component

The qualitative component employed the Rapid Assessment Procedure (RAP) methodology, (Gittelsohn 1998; Manderson 1997; Scrimshaw 1987), and included focus groups, semi-structured interviews, and the use of a questionnaire. This approach is a way of bringing together what people say (the content of interviews) and what they do. It is especially effective when gathering sensitive information (such as condom use, prevalence of STDs, and sexual practices) and when working with stigmatized groups. Confidentiality was ensured via use of numbers in lieu of names in these diaries and all other documents generated by this research.

Four focus groups were held to provide a working vocabulary of indigenous terms and beliefs that women use to label and interpret their own and other women's sexual practices, STDs, and the use of lemons, douches, ointments and lotions. These themes were then explored in greater depth in semi-structured interviews with 15 respondents.

The interviews focused on the following topics related to use of lemons:

• Prevalence of use among the target population
• Frequency of use
• Reasons for use
• Methods of application
• Duration of use
• Sexual behavior
• History of sexually transmitted diseases, including HIV
• Pregnancy
• History of contraceptive use (modern or traditional)
  

A questionnaire was then developed and administered to 104 respondents.

The major analytical approach employed in this component was thematic and qualitative. The participant’s responses were examined for major recurring themes, from which a list of preliminary categories was prepared. These categories were then examined for and grouped under a smaller number of integrating concepts. The outcome of this process was a taxonomy that systematically described the qualitative data.

Clinical Component

All women who volunteered to participate in the study and who gave informed consent were offered basic reproductive health care, including: 1) a pelvic exam; 2) laboratory tests for HIV and gonorrhea; and 3) treatment of all STDs. A Pap smear was also performed. In addition to the diagnosis of STDs, the purpose of the pelvic exams was to detect any lasting damage to the vaginal epithelium or cervix that might be caused by the use of limes. A culposcope was not available, but all the physicians were certified OB/GYNs.

The physicians were blind to the results from the qualitative section of the study. The clinical form contained information related to macroscopic characteristics of the reproductive organs and the presence or absence of diseases/conditions. The results from the examination and laboratory tests were later matched with the questionnaire using participants’ ID numbers.

Subjects diagnosed with STDs were counseled and treated free of charge. Subjects who were HIV-positive were counseled by a trained professional, offered condoms, and referred to a support service agency. Treatment for HIV/AIDS or related opportunistic infections was not provided by this study.

Data from the questionnaire and clinical sections were entered in a database specific for the study. Data analysis was done using the statistical software package STATA. Descriptive statistics were produced for all variables in the sample. We divided the sample according to use and frequency of use. Bivariate analysis was performed for all independent variables using these two main outcomes. For comparison of two proportions we used a binomial test for proportions, and to compare means a t-test was performed. Significance was established at p-value <0.05.

Results

How, when, and why the women use limes with sex

Most of the women interviewed who use limes (84%) do so in the belief that it prevents sexually transmitted diseases. A minority (16%) believes that lime douches make their vaginas tighter, thus making sex more pleasurable for their clients. The most common method of using limes is to mix the juice from one to four limes with one to four teaspoons of water, and douche with the solution. A minority of the women (30%) dilutes the lime juice with more water, using from 1/2 to one cup of water with the juice of one to four limes. Some women then clean the vagina with the leftover lime halves.

A great majority (77%) of the women learned about this practice from colleagues. When asked how many times a day they used limes, 33% of the women responded that they used lime juice once per client, 12% said they used the solution three times a day, and 45% said they douched with limes once or twice a day. Sixty percent of the women use limes after sex, twenty-eight percent use the douche before sex, and the remaining twelve percent use limes in the morning or before going to bed. On average, the women interviewed have used lime juice douches with sex for 18 months, with some having used limes for as long as eight years.

Half of the women using limes say that they have never experienced pain or discomfort from the practice. The other fifty percent responded that they have at least once experienced a burning sensation or minor discomfort upon douching with lime juice. However, all said that the burning sensation disappeared after a few minutes and all continued to use limes after this experience. One of the interviewers spoke to several married women who were not commercial sex workers, but who use limes with sex. The women said they use the lime douche to make themselves “tighter, and more like a younger woman.”

The use of lime juice and the prevalence of STDs

Because of the very small sample size in this feasibility study, virtually none of the clinical results were statistically significant. However, we did encounter a number of interesting patterns. The women using lime juice had a lower prevalence of every STD they were tested for (See table 1).

Microbiology: Culture Results (Table 1)

Does lime juice cause such problems as micro tears in the vaginal epithelium and thus hasten HIV transmission?

We found no evidence that this practice damages the vagina. In fact, more lime users than non-users had a normal perineum, vulva, and cervical exam, and fewer had micro tears, excoriation, venereal warts, redness, erosions, bleeding on contact, or vaginal discharge. The results of the Pap smear were similar (Table 2). Pap smear results were divided into six categories ranging from adequate (category 1) to malignant (category 6). Of the 12 women who had inflammatory smears (categories 4 and 5), only two were lime users (Table 3). However, due to the small number of subjects this comparison is not statistically significant.

Pelvic Exam Results (Table 2)

Pap Smear Results (Table 3)

The use of lime juice and HIV status

Forty-eight women agreed to take an HIV test. Of those, 16 use limes and 32 do not. Fifty percent of the lime users tested HIV-positive, while 41% of the non-users were HIV-positive. This is the only case in which the lime users had greater disease prevalence. As above, this comparison is not statistically significant due to the small numbers of subjects involved. Furthermore, the women using limes who tested HIV-positive had worked as commercial sex workers an average of 2 1/3 years before starting the practice of douching with limes. They also saw more clients per week. The lime users averaged 26 clients a week, as compared with 19 for the non-users. In addition, the lime users worked as CSWs an average of 35 months, while non-users averaged 28 months (Table 4).

HIV Prevalence (Table 4)

The women in the study varied greatly in the amount of water with which they diluted the lime juice. Some mixed the juice of four limes with one teaspoon of water. Others squeezed one lime into a cup of water. In addition, frequency of lime use varied greatly, from douching with every client to douching once a day. Now that our recruiting networks in Maiduguri and Kano are stronger and more fully developed, it would be possible to screen for lime users who started the practice shortly after becoming a CSW, and who douche with lime juice in a less diluted form after every client.

Lime juice as a contraceptive?

The women who use limes had an average of 1.7 pregnancies. The non-users had a mean of 2.9 pregnancies. The lime users had a mean of 1.7 abortions, as opposed to 2.2 abortions for the non-users. The average age of the lime users was 27.4 years. The average age of the non-users was 23.5. Modern contraceptives are used by 78% of the lime users and 70% of the non-users. One again, these comparisons are not statistically significant.

Contraceptive Use

Discussion

Another of our objectives was to ascertain if the CSWs would be willing to be interviewed and accept the offer of voluntary counseling and testing for HIV. We were pleased to find that the women recruited in the cities of Kano and Maiduguri were very open to being interviewed and to receiving a pelvic exam and having the laboratory tests done.

Only Abuja was an exception. The women in Abuja were willing to be interviewed but requested a fee for undergoing the lab tests and pelvic exam. Abuja is more cosmopolitan than the cities further north and the CSWs there come from all over Nigeria. Fewer of the women practiced the traditional life of the Karuwai. The field workers in Maiduguri and Kano had long experience working with CSWs and were trusted in the community. The field worker in Abuja did not have this advantage and was not able to build adequate rapport with the commercial sex workers. For these reasons we decided not to pursue the clinical component of the study in the city of Abuja.

However, this feasibility study allowed the field workers in Maiduguri and Kano to greatly extend their contacts among the CSWs. They are confident in their ability to recruit and screen CSWs for future studies, and feel that they could recruit a much larger cohort of CSWs who douche with limes frequently, use the juice in less diluted form, and who adopted the practice shortly after entering the trade.

A third objective of this feasibility study was to assess the level of professional skill of our partners in northern Nigeria and their ability to carry out a larger study. The talent, commitment, and experience of our Nigerian colleagues impressed us immensely. We worked with three gynecologists, Dr. Mandara, Dr. Mairiga, and Dr. Sadauki, all of whom teach at major university hospitals and who are among the most qualified physicians in Nigeria. The interviews were conducted by highly capable nurse midwives and social workers, who in the cities of Maiduguri and Kano had many years of experience working with commercial sex workers. Dr. Mairo Mandara, our in-country project director, teaches at Ahmadu Bello University, and has served as a consultant for the Packard Foundation, USAID, and International Family Health. Girl Child Concerns, the local NGO that acted as the administrative base for the field study, has been in existence for more than a decade.

Conclusions

The feasibility study has demonstrated that:

• A sufficient number of women (both sex workers and married women) use limes at the time of intercourse to make it possible to design a statistically significant study of the possible association between the use of lime juice and HIV status.
• Despite living in a conservative Islamic culture, CSWs in parts of northern Nigeria are willing to be interviewed and accept the offer of voluntary counseling and testing for HIV.
• There is an excellent level of professional skill and commitment in Nigeria to carry the field work forward and an established NGO to act as the administrative base for field studies

We recommend an expanded study that would help take an important step towards discovering the answers to the following questions:

• Do women using lime juice in Nigeria exhibit a significantly different HIV status than those not using limes?
• Can the use of lime juice cause damage to the vaginal epithelium and thus hasten HIV transmission?
• Is lime juice an effective contraceptive?
• Is lime juice effective in preventing sexually transmitted infections?

While ethically and clinically acceptable studies of new microbicides are proving to be exceedingly time-consuming[1] and expensive[2] to implement, the passive collection of data and clinical examination of women who douche with lemon or lime juice (a traditional practice probably dating hundreds or even thousands of years old) is an order of magnitude easier to achieve. Given the potential advantage in terms of cost and accessibility that a female-controlled microbicidal method such as lime juice could provide, and, conversely, the biological possibility that the use of lemons or limes might promote HIV transmission, we feel that it is imperative that we carry out an expanded study as soon as possible. An expanded study could include gathering more detailed clinical data (e.g., the use of culposcope and more sophisticated laboratory tests). We feel it possible to gather enough data in a further study to obtain statistically significant results from a specific group of users (e.g., those who use limes with every act of intercourse). In the process of conducting this study, we found that the CSWs in two of the three cities and our collaborating professionals in the region are willing and prepared to carry out an expanded study.

References Cited

Albert, Olawale
1996 Women and Urban Violence in Kano, Nigeria. Lagos: Spectrum Books Limited.

Callaway, Barbara
1987 Muslim Hausa Women in Nigeria: Tradition and Change. Syracuse, NY: Syracuse University Press.

Clarke, G.
2003 Unpublished data, Department of Andrology, Royal Women’s Hospital, Melbourne, Australia.

Coles, C and Beverly Mack
1991 Hausa Women in the Twentieth Century. Madison: The University of Wisconsin Press.

Gittelsohn, Joel
1998 Rapid Assessment Procedures (RAP): Ethnographic Methods to Investigate Women's Health. Boston, Mass.: International Nutrition Foundation.

Himes, N.E
1963 Medical History of Contraception. Gamut Press Inc, New York: 17-18, 181-5.

James, S and Charis Kepron
2001 Of Lemons, Yams, and Crocodile Dung. A Brief History of Birth Control. University of Toronto Medical Journal: 79[1]: 156-158.

Manderson, Lenore
1997 Population and Reproductive Health Programmes : Applying Rapid Anthropological Assessment Procedures. New York : United Nations Population Fund, 1997.

McCoombe, S. G.
2003 Unpublished data, Department of Zoology/Department of Microbiology and Immunology, The University of Melbourne, Australia

Onwuejeogwu, M. Angulu
1999 Foundations of Hausa Civilization of North-West and North-Central Nigeria. Lagos: UTO Publications.

Pittin, Renee Ilene
2002 Women and Work in Northern Nigeria: Transcending Boundaries. New York, N.Y. : Palgrave Macmillan.

Reprotect
2003 Retrieved from the World Wide Web: http://www.reprotect.com/physio3.shtml

Scrimshaw, Susan
1987 Rapid Assessment Procedures for Nutrition and Primary Health Care : Anthropological Approaches to Improving Programme Effectiveness. Tokyo : United Nations University.

Short, R,
2003 Unpublished data, Royal Women’s Hospital, Melbourne, Australia.

UMEC
2003 Retrieved from the World Wide Web: http://www.uhmc.sunysb.edu/urology/male_infertility/SEMEN_ANALYSIS.html

UNFPA
2003 Retrieved from the World Wide Web: http://www.unfpa.org/rh/mothers/contraceptive.htm

[1] No new Phase III clinical trial is likely to be completed in the next five years and perhaps much longer.

[2] The Population Council spent an estimated $10m on Phase II studies of Carryguard and estimates it could cost $20m to 40m to complete a phase III trials.