Anukam, Kingsley C. MSc; Osazuwa, Emmanuel O. PhD; Reid, Gregor PhD; Katsivo, Melanie N. PhD
A PAUCITY OF INFORMATION exists in sub-Saharan Africa with regard to knowledge, availability, and receptivity for probiotic products among the populace. Probiotics is defined by the Food and Agriculture Organization of the United Nations and the World Health Organization as “Live microorganisms which when administered in adequate amounts confer a health benefit on the host.”1 To date, probiotic products have mainly been delivered as freeze-dried cells or fermented foods, restricted to improving the health and well-being of the intestinal tract of humans,2 particularly in prevention and treatment of diarrhea.3 Although the development of probiotics for women’s health has been ongoing for over 20 years,4 only now are strains nearing the stage of being available for common use. Two organisms, Lactobacillus rhamnosus GR-1 and L. reuteri (formerly fermentum) RC-14 have been shown to colonize the vagina, kill viruses, and reduce the risk of infections, including bacterial vaginosis (BV).5,6 Given the strong association between BV and sexually transmitted diseases,7–9 and higher rates of BV among black women10 a good case can be made for use of these 2 strains, and others proven to have similar effects, as a natural way for women to lower their risk of disease.
In sub-Saharan Africa, approximately one fourth of females under the age of 30 have HIV and an estimated half billion are at risk of acquiring the virus through sexual contact.11 Efforts to provide condoms, develop a vaccine, and use spermicides or antiretrovirals have failed to stem the epidemic.12 In 1996, the response to the problem was summarized by Dr. Peter Piot of UNAIDS, who urged promotion of safe sex programs for women and the development of a vaccine.13 However, the recent vaccine failure14 and estimated 67% of all new cases of HIV being among are women and girls,11 further demonstrates that current approaches are not sufficiently effective.
For relatively new concepts such as probiotics to be effective, in addition to excellence in scientific and clinical studies, there has to be an educational process to inform health professionals and lay people of their benefits. To date, no surveys have been published that assess the knowledge of lay people about probiotics. In Japan and Europe where products for gut health have been available for many years, it is likely that many lay people are aware of probiotic foods. This number will be significantly lower in North America. Worldwide, the issue is further tainted by there being too many true, clinically proven probiotics as distinct from products, often extremely unreliable in formulation,15 marketed but with no proven verification of benefits.
In Nigeria, no probiotic products are available, but conventional yogurts fermented with starter cultures of Lactobacillus delbruekii var bulgaricus and Streptococcus thermophilus abound in rural and urban cities. These organisms are designed to ferment milk, and few if any pass into the gastrointestinal tract and confer health benefits beyond those of nutrition. In sub-Saharan Africa, the production of fufu (fermented cassava product), ogi (fermented maize, sorghum, or millet gruel), fura da nunu (fresh cow milk with fermented millet gruel), and pito, burukutu (cereal-based alcoholic beverages) are largely brought about by lactic acid bacteria and yeast, with Lactobacillus plantarum predominating.16–18 In a recent study, Lactobacillus plantarum and Lactobacillus brevis were the dominant lactic acid bacteria isolated in different batches of “pito” and “burukutu” cereal-based alcoholic beverages collected from local producers in Nigeria.19
Historically, the consumption of fermented food products in sub-Saharan Africa could have been lost in antiquity, although in some areas, the practice transcends from generation to generation. Black Africans could have been in contact with “protective flora” for centuries, just like the whites, and indeed a study of the healthy vaginal flora of women in Europe, North America, and Africa has shown similar dominant species (Hillier, personal communication, October 2003). The current wave of probiotic sales in developed countries could soon come to sub-Saharan Africa in various forms such as freeze-dried capsules both for oral and vaginal instillations, powders, fortified yogurts, and milk-based food products. The goal of the current study was to determine the local knowledge in Nigeria of probiotics and the willingness of young women to use them should they be introduced. University students at higher-than-average risk of HIV, as a result of being in their prime sexually active years, were surveyed.
Materials and Methods
Two forms of questionnaires were used: closed-ended structured questionnaires and open-ended questionnaires. Because the idea of probiotics is novel in this environment, introductory facts on the subject were provided to the participants:
* Women are biologically more susceptible to HIV transmission than men. This is no longer a news report. The physiology of a woman’s reproductive tract means that she faces at least twice the risk of contracting the fatal virus from an infected man, compared with the risk a man faces from an infected woman.
* The use of condom, both male and female, microbicides such as Nonoxynol-9 does not adequately address intervention approaches.
* Partner reduction, monogamy, and abstinence are too idealistic to be real.
* Absence or depletion of normal vaginal bacteria such as lactic acid bacteria (LAB) is associated with pathogens that cause bacterial vaginosis (BV), which is a major risk factor for HIV, gonorrhea, chlamydia, and other sexually transmitted disease infections.
* Yeast infections, diarrhea, constipation, and a number of other intestinal discomforts can be associated with a disruption of intestinal microorganisms.
* Numerous studies have shown that humans exist together with an estimated 100 trillion resident microorganisms that play an important role in maintaining health.
* Lactobacillus and Bifidobacterium species and a few other probiotic strains have been found to be safe for human use and are termed “probiotics”—“live microorganisms which when administered in adequate amounts confer a health benefit to the host.”
* Probiotic organisms appear to work by inhibiting the growth and adhesion of pathogens by producing chemical substances such as hydrogen peroxide, bacteriocins, and biosurfactants, and by modulating the host’s immune response. New studies indicate that some strains can downregulate the virulence of pathogens.
* Yogurts and milk-based food products have been fortified with microorganisms with probiotic qualities for maintaining normal intestinal health.
* Probiotic organisms have been propagated and developed in capsules for vaginal instillation and for oral intake. The purpose is to recolonize the vagina with organisms that appear to help protect it against pathogens that could cause BV, and thereby to reduce the risk of HIV infection, which is so strongly associated with BV.
Participants and Data Collection
The study was approved by the Ethics Review Board of the University of Benin and all participants provided consent. A random sampling technique was used throughout the survey period. The respondents were all females, mainly premenopausal, from the University of Benin, Nigeria. The closed-ended questionnaires were administered to each participant and these addressed age, marital status, perceived risk of HIV infection for the next 3 years, and history of urogenital infections such as yeast vaginitis, gonorrhea, chlamydia, Trichomonas vaginalis, and others. Also using the “Likert scale,” participants were asked to “strongly agree or approve,” “agree/approve,” “disagree/disapprove,” “strongly disagree/disapprove,” or to answer “don’t know” to questions on taking antibiotics without laboratory test and prescription and on the importance of vaginal pH. The participants were also asked whether they would welcome a probiotic product in oral/vaginal form and in milk-based food products, willingness to purchase and use, how often they would use these products, preference of form, price, and where they would like to buy the products.
The second questionnaire was open-ended. It asked the participants to freely list any concerns or worries they had in relation to probiotic products.
A total of 280 participants were enrolled in this study. The age group and marital characteristics of the sample are shown in Table 1. The highest number of participants was in the age group 26 to 30 years, representing 47% of the sampled population, whereas only 10 (3%) participants belonged to the age group 36 years and above. None of the participants in the age group 16 to 20 years were married. The sample largely involved single premenopausal women accounting for 83.3% (233) of the total participants.
Of the respondents, 55.3% (155) reported varied perceived risk of HIV in the next 3 years. Only 24.6% (69) reported a history of urogenital infection, mostly as a result of Candida. A total of 57.5% (161) of the participants indicated strongly agreed (Table 2) that taking antibiotics without laboratory tests or prescription could kill some beneficial bacteria in the vagina and/or intestine, whereas 10.7% (30) indicated they did not know.
Also, 29.2% (82) of the respondents reported “agree” that any activity that elevates the vaginal pH increased the risk of infection, including HIV, whereas 32.1% (30) did not know.
Based on the information provided, 82% women they would welcome a product called “probiotics” in capsular form for vaginal instillation or to be taken orally to improve vaginal health, whereas only 3.9% (11) strongly disagreed.
Most respondents stated they would buy a probiotic product as part of their daily self-care (Table 3) and only 7.1% stated that they “don’t know.”
In terms of form of probiotics, 40% indicated a preference for yogurt, whereas 16% and 20.7% indicated preference for oral or vaginal capsule form, respectively (Table 4).
In another closed-ended response, 64% (180) preferred purchase of probiotics in pharmacy/chemist stores, whereas 18.5% (58) indicated supermarkets and 14.6% (41) in clinics/hospitals. Only 2.5% (7) of the respondents indicated preference for a food market.
In answer to the price that would be reasonable per dose for a probiotic product that could enhance their inner health, the majority of respondents (39.6%) indicated #10.00 Naira, which is equivalent to US $0.08 per dose, whereas less than 20% indicated amount above #100.00 (US $0.75) (Table 5).
The results from the open-ended questionnaire that asked the participants to freely write down any concern or fears concerning probiotics proved revealing. One fourth of the respondents raised various concerns on the safety of probiotics and these are listed in Table 6.
This is the first survey study performed on probiotics and the first to assess the interest of women at high risk of infection by sexually transmitted pathogens to consider food and dietary supplement concepts for health retention. With the alarming prevalence of HIV acquisition in women, especially in sub-Saharan Africa, the findings provide insight into a woman’s perceived risk of infection and interest in exploring self-directed approaches to reducing their risk of disease. Of the 280 participants, 55.3% indicated that they believed they were at risk of acquiring HIV within the next 3 years, a rate much higher than a Zimbabwe study where only 30% of women with the highest rates of HIV/sexually transmitted diseases were aware of their vulnerability to infection.20 This illustrates the enormity of the problem in Africa and the feelings among women that they cannot easily control sexual relationships and have partners use condoms.
The fact that 24.6% women indicated having had a urogenital infection previously emphasizes the extent of these infectious problems, but also suggests that women in this part of the world are becoming more open about their urogenital health status. Also, 57.5% (161) of the participants indicated that taking antibiotics without laboratory tests or prescription could kill some beneficial bacteria in the vagina and/or intestine, whereas 10.7% (30) indicated they did not know. We were trying to perceive their level of knowledge on antibiotics, notably, about possible adverse effects. We tested their perception that taking antibiotics without indication could deplete LAB and thereby expose them to overgrowth of BV-associated pathogens. It also shows their knowledge of anatomy, drugs, and risk of infection.
At no time in this study were probiotics presented as an alternative method to prevent HIV. Rather, the participants were presented with the proven scientific and clinical evidence that certain strains of lactobacilli have been shown to prevent and treat diarrhea (a highly prevalent illness among AIDS patients), and others have been shown to colonize the vagina, displace and kill urinary and BV pathogens, and kill viruses in vitro. Given the significantly increased risk of HIV when lactobacilli are replaced by BV pathogens, the suggestion was made that use of lactobacilli could help reduce the risk of HIV, although this has not yet been tested. Indeed, it is not envisaged that probiotics would replace condom use or antiretrovirals to prevent HIV spread to women. Nevertheless, they provide a means for women to gain back some control of the risk factors, especially when men rape them or refuse to use condoms.
Clearly, the ability to take probiotics had great appeal, with 82% women stating they would welcome probiotic products in capsular form for vaginal instillation or to be taken orally to improve vaginal health against infections, including HIV. An interesting point is that this population only has a 5.2% HIV prevalence according to a 2001 National HIV/AIDS sentinel seroprevalence survey.21
Over one third of the respondents indicated a willingness to purchase a product containing lactobacilli for vaginal insertion to enhance protection against infection and promote health. The insertion of a probiotic product vaginally could have been viewed by the participants as a form of vaginal practice. Traditional vaginal practices, including tampon use, douching, and hygiene, are usually taught to young women by their older female relatives, female peers, or other women in the community and represent, to some extent, a culture’s norms and ideologies about the body.22 The ability of specific strains such as Lactobacillus GR-1 and RC-14 to colonize the vagina and confer health benefits23 appealed to the respondents.
A large portion of women (82.1%) were willing to purchase a similar probiotic formula added to yogurt or in milk-based food products for general women’s health as well as to enhance resistance to infection. The participants responded similarly when asked how they would prefer to use a probiotic product. Yogurt remains a staple food in Nigeria, and various LAB are often combined to produce fermented milk, which has desirable effects such as improving the health of the host.24 Many people consume yogurts and fermented milks on a daily basis in sub-Saharan Africa, and in the current study, 36% of the participants indicated they would be willing to use the probiotic products as part of their daily self-care. Such daily intake of greater than 108 viable probiotic lactobacilli has been shown to provide a degree of stability to the fluctuating vaginal flora.6 The willingness to purchase such products at US $0.08 per dose could surprise people in developed countries because it equals the price paid there for daily antibiotic prophylaxis for urinary tract infections and contradicts the perception that women in developing countries cannot afford such costs.
Clearly, there is a market for probiotics in Africa (Nigeria has 25% of the continent’s population), yet no pharmaceutical or food company has embraced it fully. The global market for functional foods in the coming years is predicted to grow rapidly.25 It is expected that 29 years from now, marketing food products for disease prevention and treatment will be commonplace.26 A recent study conducted in Europe showed that the probiotic yogurt market in 9 European countries totaled 250 million kg in 1997, with France representing the largest market, having sales of 90 million kg, valued at US $219 million.27
In the current study, 64% of respondents preferred pharmacy and chemist stores to purchase probiotics, reflecting that pharmacists will play an important role in healthcare delivery in Nigeria.
In terms of concerns, these were only expressed by 25% respondents and were highly expected given that the probiotic products were not available during the survey. Safety of all products must be monitored, but evidence to date indicates a low risk with use of probiotics.28–31
Prevention of HIV/AIDS, the modern world’s worst pandemic, has to be linked to more than use of antiretrovirals and provision of condoms, and must include providing practical support for illness such as diarrhea and self-help products that empower people and contribute to their health.32 This current study has demonstrated that even in a developing country like Nigeria, there is a resounding willingness of young women to receive information about their vaginal health and to receive probiotic products that contribute to this well-being. Because strains such as Lactobacillus GR-1 and RC-14 can be delivered in dairy and freeze-dried forms, the opportunity exists to make these and other similarly well-tested organisms accessible in various product forms to women in sub-Saharan Africa. Such approaches are based on natural methods to retain health, rather than high-end drugs accessible to the select few, or condoms, which too often are not used. In addition, the relative low cost of probiotics compared to drugs makes them attractive, even if they only help prevent a small portion of HIV infections.33 It is time for the healthcare community to: 1) consider women’s concerns about acquiring HIV, and the practical, self-use options open to them; 2) be sensitive to women’s desire for products like probiotics, and their various food and supplement formulations that can be widely distributed and provide nutritional value as well as a degree of protection against infections and enhanced remediation from diarrheal diseases; and 3) develop appropriate educational materials to assist women in understanding, in a simple format, the mechanisms of action of probiotic agents and how they might be practically used. The fertility of women and the very survival of nations and cultures are at stake.34,35
The findings in this survey could be generalized to some extent, across the country, but the answer could depend on what one could perceive to be the level of education and knowledge of people.
Even poor women with little education will at least be aware that natural remedies are healthy, although they could likely not know about vaginal risk of HIV, antibiotics, or the link between fortified food and reproductive health. Nevertheless, if probiotic products could be introduced in the country, there could be a need for more surveys, using a situational analysis approach, which should cut across the entire population representing different socioeconomic demographic strata in Nigeria.
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