|Year : 2015 | Volume
| Issue : 2 | Page : 87-94
Helminthiases: a neglected cause for reproductive ill-health and social stigma
Mulambalah Chrispinus Siteti1, Siteti Darwin Injete2, Wekesa Antony Wanyonyi3
1 Department of Medical Microbiology, College of Health Sciences, Moi University, Eldoret 30100, Kenya
2 Department of Clinical Medicine, College of Health Sciences, Jomo Kenyatta University of Agriculture and Technology, Nairobi 00100, Kenya
3 Department of Biological Sciences, Masinde Muliro University of Science and Technology, Kakamega 50100, Kenya
|Date of Submission||21-Jul-2015|
|Date of Acceptance||01-Sep-2015|
|Date of Web Publication||27-Jan-2016|
Mulambalah Chrispinus Siteti
PhD, Department of Medical Microbiology, College of Health Sciences, Moi University, Eldoret 30100
Source of Support: None, Conflict of Interest: None
Helminthic infections cause severe diseases (helminthiases) associated with significant morbidity and mortality worldwide. Many individuals are not aware of the risks and complications of helminthiases in reproductive health; hence, the infections are often neglected, leading to severe outcomes. These infections are often misdiagnosed and result in miscarriages, infertility, ectopic pregnancy, and increased risk of other conditions. Infected women of reproductive age often pass infections to their fetus during pregnancy and childbirth, which consequently affects their growth and development. In addition, the resultant morbidity affects the economic productivity and quality of life of individuals and communities. For the present review, both electronic (PubMed, Medline, EBSCO host, Science Direct) and manual literature were searched for relevant articles. The review highlights emerging issues on clinical manifestations, risks, and complications. Besides impairment of reproductive health in developing countries, helminthiases increase the transmission of viral, fungal, and bacterial infections, and promote stigma and sex inequality. The clinical and social impact of these neglected, forgotten infections largely considered to be of low public health importance is discussed. Because of the immense and increasing impact on global health and development, health professionals are encouraged to confer high priority to helminthiases.
Keywords: ectopic infections, helminthic infections, pregnancy outcomes, reproductive health
|How to cite this article:|
Siteti MC, Injete SD, Wanyonyi WA. Helminthiases: a neglected cause for reproductive ill-health and social stigma. Parasitol United J 2015;8:87-94
|How to cite this URL:|
Siteti MC, Injete SD, Wanyonyi WA. Helminthiases: a neglected cause for reproductive ill-health and social stigma. Parasitol United J [serial online] 2015 [cited 2017 Aug 17];8:87-94. Available from: http://www.new.puj.eg.net/text.asp?2015/8/2/87/175003
| Introduction|| |
Human health is a state of stable physical, mental, and social well-being. Reproductive health is a subset of health and addresses all reproductive functions and perpetuation of progeny from one generation to another  .
According to the WHO, ailments relating to reproductive health account for ~20% of the global burden of poor health among women and to a lesser extent (14%) among men. The poor health is frequently associated with common infectious diseases that affect reproductive health either directly or indirectly, causing ~60% morbidity  .
Helminthiases are the most common infections worldwide and are known to result in significant public health problems and economic loss. The high prevalence of helminthiases can be attributed to several factors including but not limited to inadequate public health education, contaminated food, low levels of personal and environmental hygiene, and close association with pets and domestic animals that act as reservoir hosts. These diseases are not easily identified because they often manifest with nonspecific signs and symptoms that cannot be directly linked with a particular helminth infection. If these infections are not identified early and promptly treated, they cause severe complications in reproductive health. In this respect, a number of species of pathogenic helminthes that in many cases do not originally localize in the reproductive system are implicated.
Although not usually sexually transmitted, they may show symptoms that mimic classical sexually transmitted infections. For instance, female genital schistosomiasis (FGS) produces wart-like lesions in the lower and upper genital tract and is increasingly becoming a common cause of infertility in endemic regions. In male genital filariasis (MGF), the main genital symptom, hydrocele is associated with stigma and impediment of procreation. Other helminthes species of reproductive health importance include Enterobius vermicularis associated with ectopic/genital enterobiasis; Ascaris lumbricoides associated with ectopic/genital ascariasis, and hookworms belonging to the family Ancylostomatidae, the causative agents of hookworm disease (HWD) ,, .
The adverse effects of parasites on reproductive health differ depending on the sex of the individual, and clinical presentation varies with the helminthes species involved. For instance, FGS is associated with genital deformation, inflammation, infertility, spontaneous abortion, and stillbirth in women, whereas MGF causes genital deformation. Some of the helminthic infections enhance the likelihood of bacterial, viral, and fungal coinfections. Typically, many infected women show several symptoms in the genital tract where vaginal bleeding is common, with urogenital schistosomiasis lesions in the cervix and vagina, and abnormal discharge because of vulvovaginitis caused by ectopic enterobiasis. These may lead to low self-esteem, depression, and stigma.
The most important reason why we should focus more attention toward helminthiases is the health status of neonates and infants, which is mainly a function of the mother's health status and of her access to appropriate reproductive healthcare , .
Highlighting the clinical manifestations, risk of other infections, genital, and pregnancy complications, and impact on reproductive health will hopefully refocus the attention of the health professionals on the morbidity associated with these neglected helminthiases currently considered to be of low public health significance worldwide. Many of these infections have been forgotten even when increasing numbers of cases are closely linked to increasing risk of other dangerous infections and widespread complications.
Information sources and processing
A search for publications on helminthiases indexed between the second half of the 20th century and the first quarter of the 21st century produced a total of 97 accessible articles. These described cases of helminth infection were closely associated and linked with a wide range of adverse effects in human reproductive health. The search findings were compared and summarized using a narrative review approach and described qualitatively.
Since the beginning of the 21st century, several research papers have emerged in the medical literature, highlighting new clinical reports indexed during the last 14 years indicating increased prevalence, risks, and complications associated with helminthiases.
The present review highlights the association of specific helminth parasite species with reproductive ill health and risks and complications because of coinfections. Aspects identified as not adequately addressed from the study findings are considered as research gaps and are recommended for further research.
Overview of adverse effects, risks, and complications
Helminth species associated with ectopic and aberrant infections prevalent in reproductive-age of women and men include species of the genus Schistosoma, Wuchereria, Ancylostoma, Necator, Enterobius, and Ascaris. The infections may be associated with minor and nonspecific clinical signs and thus may be underdiagnosed and untreated. Such infections eventually become chronic and undetected for several years, with severe effects and risks , .They are variously associated with inflammation of the vagina, uterus, and other parts of the reproductive system in women. The infections result in generalized inflammation, infertility, preterm birth, low birth weight, and increased risk of cervical cancer, and viral infections in women , . In men, complications involve inflammation of the urethra, prostate gland, epididymis, and infertility as a result of damage to various parts of the reproductive system and or interference with the sperm development, motility, and function  .
All forms of schistosomiases are acquired by exposure of individuals to water colonized by various species of freshwater snails. The snails act as intermediate hosts in which the larval schistosomes multiply asexually before infective larval forms known as cercariae, capable of penetrating human skin, are released into water. Infection occurs during human involvement in various water-related activities. Schistosomes are believed to infect 193 million individuals in the tropics, with 85% of infections occurring in Africa  .
Genital schistosomiasis is caused by Schistosoma haematobium, the causative agent of urinary schistosomiasis. The adults localize in the veins of the urinary bladder and infection is characterized by extensive egg laying in the blood vessels. The egg is the main agent of pathology and some of the eggs may be transported to other organs including reproductive organs, resulting in inflammatory reactions. The inflammatory reactions are because of soluble egg antigens released by eggs trapped in tissues and produce a wide range of symptoms, notably hematuria, fibrosis, and genital complications. Two variants of the disease are associated with direct and indirect adverse effects on human reproductive health. These are FGS and male genital schistosomiasis (MGS). The former condition in women is mainly because of S. haematobium affection of the urinogenital system, but in rare cases, Schistosoma mansoni (associated with intestinal schistosomiasis) is also capable of migrating into the genital region to produce lesions. It is estimated that ~6-27% of women with intestinal schistosomiasis also develop genital lesions  . The extent of genital morbidity because of Schistosoma japonicum infection is rarely reported, but there is evidence that it is becoming prevalent as a cause of genital disease in humans and animals. The infection has been linked to cases of female genital tract infections in Asia  . Schistosomiasis japonica association with maternal, placental, and fetal inflammation has been reported  . Congenital infections and associated pathogenesis in animal model studies further suggest that the infection could be an important cause of genital lesions and inflammation in humans , . Summarized recent findings on disease prevalence and coinfections are reported and supported by field studies , . On the basis of field study findings, an atlas of FGS distribution in African countries indicates high disease prevalence in Southern African countries. The clinical and epidemiological evidence for the relationship between FGS and HIV and the coexistence of FGS and sexually transmitted infection in women and men in disease endemic regions has been established  .
Chronic inflammation, a common feature of S. haematobium infection, is known to generate conditions and microenvironment conducive to the initiation of cervical cancer. The inflammatory response around the eggs and the inflammatory cells involved generate free radicals implicated in the damage of DNA, leading to genetic instability in cells, and subsequently result in malignant transformation of cervical cells. It is for this reason that S. haematobium infection in humans is classified as carcinogenic and is therefore an important risk factor for the increasing cases of cervical cancer in disease-endemic areas  . Furthermore, extensive tissue inflammation because of FGS results in mucosal erosion and ulcerations, leading to a friable epithelium of the cervix, which persists even after successful treatment with praziquantel, enhancing viral entry and acting as a facilitating factor for acquisition of HIV. Both sexes develop genital complications, but the genital morbidity is much greater and more severe in women. This is because unlike in men, the infection is not restricted to a specific site in women. The adverse effects spread widely to all parts of the female reproductive system, leaving very few or no areas intact.
As the eggs penetrate through the veins surrounding the urinary bladder, they find their way into the female reproductive tract and induce the formation of granulomas in all parts of the reproductive system including the uterus, fallopian tube, and ovaries. Such infected women develop an enlarged uterus, experience menstrual disorders, inflamed cervix, and consequently infertility. Externally, lesions are reported to develop in the vulva and perianal areas in 30% of women. Lesions in these areas appear as ulcerations, hypertrophy, or in some cases fistulas  .
FGS is also reported to affect the uterine environment in pregnant women and an estimated 10 million women in Africa develop this disease in pregnancy  . Several studies have shown that pregnant women infected with FGS develop moderate to severe anemia, give birth to low weight infants, and have an increased infant and maternal mortality rate ,,,, . Some cases of schistosomiasis detected in the placenta and newborns confirm that cases of congenital transmission of infection do occur in endemic areas  . In addition, FGS is reported to lead to a higher rate of spontaneous abortions and presents a higher risk for ectopic pregnancies  . Infected women in disease-endemic regions who do not seek early and appropriate treatment suffer more severe and chronic disease, often leading to gross organ damage and death. Furthermore, the increased pelvic blood flow associated with pregnancy is believed to accelerate the wider spread of eggs, thus increasing the infection  . This confirms the association of FGS with the most common gynecological conditions in sub-Saharan Africa for instance ectopic pregnancy, subfertility, and tissue changes , . It is therefore evident that FGS affects fertility and may reduce a woman's reproductive health capacity by up to 75%  . Infected pregnant women are advised to seek treatment as WHO-supported studies have confirmed the safety and efficacy of praziquantel in pregnancy ,, .
Clinical manifestations in FGS can be at times confusing. Confusion of cervical lesions with carcinoma and of vulvar lesions with genital warts is common, and if not correctly diagnosed and treated, can lead to severe morbidity. However, the so-called 'sandy patches' of the vagina and cervix that result from subepithelial calcification of schistosome ova are especially distinctive lesions  .
It has been postulated that FGS exacerbates the effects of human papillomavirus infection. In this respect, FGS is likely to lead to swifter development and spread of cervical cancer in women  . In many endemic regions in Africa and other developing countries, reported study findings indicate that many women who develop cervical cancer are also reported to be positive for FGS, human papillomavirus, and HIV infections , . The links between urogenital schistosomiasis in women and HIV possibly explain why HIV and other sexually transmitted infections increase three-fold in women with FGS in Africa, where recent estimates indicate that between 20 million and 150 million girls are affected  .
MGS was identified with the emergence of reports from male sexual clinics worldwide , . The ability of MGS to cause bleeding and egg deposition within semen has been reported  . Men complaining of yellow discoloration and reduction in semen volume, or inconsistencies, have been associated with S. haematobium infection  . Related reports have also described the development of hemospermia and lumpy semen in men with MGS ,, . Parasite ova deposited in the vesicles initiate inflammatory reactions that result in calcifications of the seminal vesicles and the prostate glands  . There are reports of lesions associated with MGS that develop within the testes and simulate carcinoma; other lesions result in infarction, and inflammation of epididymis and the penis ,,, . Male infertility resulting from such lesions has been reported ,, .
Hemospermia is caused by a variety of conditions involving the accessory sexual glands or their ducts, the urethra, or the bladder. In MGS, causes of hemospermia include prostatitis, seminal vesiculitis, and prostatic hyperplasia, induced by schistosome-related inflammatory reactions. From morbidity studies, the condition is rarely reported in S. haematobium-endemic areas. It is possible that the condition usually occurs unnoticed. It may also be mistaken as a case of blood on the penis after a sexual encounter and attributed to vaginal and or cervical bleeding of the female partner.
Pathologically, hemospermia, is the early stage of MGS and its severity depends on the intensity of infection. In disease-endemic areas, male genital lesions associated with hemospermia develop early in life, becoming chronic when infected individuals reach sexual maturity. However, inflammatory changes in other parts of the male genital tract, for instance the seminal vesicles and prostate, reduce the probability of hemospermia in some individuals. In areas with perennial transmission, where there is repeated exposure to infection and high parasite burden, it is possible that hemospermia persists in the population unnoticed. These inconsistencies suggest that the epidemiology and pathogenesis of hemospermia are either not adequately known or neglected. Hence, the prevalence of this early symptom in MGS in S. haematobium-endemic areas is largely unknown. There is a need for awareness of the condition as a symptom of urogenital schistosomiasis and medical personnel should specifically consider hemospermia in the context of medical examination in populations in disease-endemic areas.
E. vermicularis (pinworm or threadworm) is a common large intestinal parasite in humans that causes pinworm infection also known as enterobiasis. The nematode predominantly occurs in young children who present with perianal and perineal pruritus because of migration of gravid females and deposition of ova on the skin of this area. The chief symptom of itching in the perianal region is an allergic reaction because of deposition of eggs, and the infection often manifests as irritability and disturbed sleep. Adults may also be affected. Spread of infection is by autoinfection from contaminated hands and fully developed hatched larvae in the intestine and on the perineum, as well as direct from one individual to another by handling of contaminated food. Individuals of every socioeconomic group may acquire pinworm infection and it remains quite prevalent worldwide  .
Enterobiasis is not considered a serious disease, although ectopic infections, reported most commonly in women, cause significant morbidity , . Ectopic infections resulting from spread of larvae or ova from the anal region to a wide variety of ectopic sites is associated with a local inflammatory response accompanied by secondary viral, fungal, and bacterial infections  . Migration of parasite larvae from the perineum into the female genital tract is most common in severe infections. Such navigational errors by the larval and adult parasite are widely reported to result in fallopian tube infiltration, salpingo-oophoritis, tube-ovarian abscess, or granulomata of the vulva, vagina, uterus, fallopian tubes or ovaries, and destruction of the human embryo ,,,,,,,,,,,, . Escape of worms through the fallopian tubes into the peritoneal cavity is associated with pelvic inflammatory disease (PID), abdominal peritonitis, and granulomata of the pelvic peritoneum ,,, .
Another possible means of ectopic spread into the peritoneum is perforation of the intestine or appendix, allowing for the penetration of the pinworms through the damaged intestinal wall into the peritoneal cavity. This alternative route of parasite migration accounts for the upsurge in previously reported cases of ectopic infection in women  .
Young women of reproductive age with ectopic enterobiasis have an increased incidence of urinary tract infections, probably because of migration of worms into the urethra and bladder, causing inflammatory reactions. Transfer of enteric or cutaneous organisms to these normally sterile sites along with the pinworms has been documented as an explanation for the isolation of bacteria from the peritoneum of some patients with ectopic enterobiasis  . In these patients, bacterial species in the genera Staphylococcus and Streptococcus have been isolated from pelvic fluid and linked to pelvic inflammation and abdominal pain. Such ascending genital tract infection in the presence of lower abdominal pain and cervical changes such as cervicitis and cervical intraepithelial neoplasia fits the definition of PID. Pathogens commonly associated with PID in women are various species of bacteria (Neisseria gonorrhoeae, Gardnerella vaginalis, Haemophilus influenza) and Mycoplasma spp. associated with specific infections. The presence of eosinophilia in their clinical presentation is in many cases suggestive of coinfection with ectopic enterobiasis. Previously reported findings indicated that ectopic enterobiasis related-PID, long-term pelvic pain, impaired pregnancy, and associated infertility are common in young and adult women  . This highlights the potential importance of ectopic enterobiasis in female reproductive ill-health ,,, . For instance, infection of the fallopian tubes results in inflammatory reactions that subsequently lead to tubal obstruction and infertility. There is a need for long-term wider prospective studies to establish the prevalence of ectopic enterobiasis in relation to women reproductive health.
Filariasis refers to a group of related diseases caused by tissue helminth parasites collectively referred to as filarial worms of various genera in the family Filariidae. Two species of filarial worms cause genital disease in humans. The most important is Wuchereria bancrofti, which accounts for 90% of filarial infections, and is estimated to infect 100 million individuals in the tropics. About 40% of them develop disfiguring manifestations and ~27 million men are reported to suffer from genital deformity  . Genital morbidity in women is much rarer  . Bancroftian (lymphatic) filariasis is the leading cause of male genital deformity worldwide, whereas onchocerciasis caused by Onchocerca volvulus is associated with minor deformities of scrotal skin and pendulous scrotum , .
Bancroftian filariasis is prevalent in the tropics and subtropical regions. Transmission is through the bite of infected female mosquito that transmits larvae that develop into adult worms in the lymphatics of the human host. In men, lymphatics of the spermatic cord are the preferred location. The presence of infection leads initially to asymptomatic pathogenic dilation of lymph vessels  . Subsequent death of adult worms elicits acute inflammatory reactions and lymphatic dysfunction, and the late effects of the disease increase the risk of superimposed bacterial and fungal infections in the affected areas of the lymphatic system.
The clinical manifestations that result from these processes in the male genital area include enlarged lymphatics around the spermatic cords; acute/chronic hydrocele; inflammation of scrotum and penis; and elephantiasis of the scrotum and inguinal adenitis. Their combination results in deformation of male genitalia. This is associated with social stigma including loss of physical intimacy and unfulfilling procreation; problems in finding appropriate marriage partners; poor social relationships; reduced mobility; and inadequate participation in viable economic activities. Increasing cases of suicidal ideation as a result of isolation and stigma are being reported. Penile deformity leads to rejection by female partners. The wider social impact of genital filariasis was documented in the medical literature , .
Ascariasis is a disease caused by a helminth parasite, A. lumbricoides, an intestinal roundworm of humans  . It is one of the most common parasites found in humans and infects ~1-1.5 billion individuals worldwide, with the most heavily affected populations being in sub-Saharan Africa, Latin America, and Asia , . As of 2010, ascariasis is reported to have caused about 2700 deaths, compared with 3400 in 1990 , .
Most people harboring A. lumbricoides show no signs of infection, except for early pulmonary symptoms and eosinophilia during the larval migration of the parasite. Later on, and depending on the intensity of infection, some patients also show abdominal symptoms associated with adult worms  .
Occasionally, A. lumbricoides can cause life-threatening disease from ectopic migrations of the worms, often reported in patients with high parasite loads  . Ectopic ascariasis is commonly associated with suppuration because of deterioration of the trapped worms and secondary bacterial infection. Ascaris may migrate outside the intestinal tract and adult worms were reported as early as 1924 to invade the female genital tract and cause tube-ovarian abscess, pelvic pain, and menorrhagia  . Gynecological disorders because of ectopic ascariasis as well as a case report were linked with genital ascariasis. These include cases of relapsing colpitis and changes in endoecology of the lower genital tract that led to vaginal dysbiosis , . During pregnancy, maternal ascariasis leads to the risk of fetal intrauterine growth and retardation  .The infection in pregnant women is associated with malabsorption of fat, protein, and carbohydrates that result in both maternal and fetal nutritional deficiencies that lead to inefficient intrauterine growth and retardation. Recent studies indicate that maternal Ascaris infections lead to sensitization of the fetus and elicit immune responses  . Fetal sensitization subsequently leads to either enhanced or reduced susceptibility to infant and childhood ascariasis; it may also have a negative and or a positive effect on future susceptibility to other viral and bacterial infections such as HIV and tuberculosis. This provides evidence that sensitization initiated in utero may have future modulatory effects on newborns and infants immunity. An understanding of how the parasite mediates such regulatory effects on the fetus is not clear. This is an area that needs further investigation for better understanding of the regulation of inflammation during childhood as it may affect infant response to vaccines  .
Although clinical and epidemiological studies indicate that congenital ascariasis is rare, some cases have been reported ,, . Most of these newborn cases of infected mothers were diagnosed to be positive for ascariasis and had low birth weight and diarrhea. This confirms that maternal parasitism leads to congenital ascariasis and insufficient development of the fetus, and yet it is not widely reported. The extent of congenital ascariasis-associated morbidity and mortality is not yet known and needs to be investigated.
This disease affects tens of millions worldwide, with a prevalence of up to 50% documented in some regions in sub-Saharan Africa, the majority of them children and pregnant women  . In a study on parasitic infection in pregnancy carried out in coastal Kenya, about 32% of women were found to be infected with hookworm  . Estimates suggest that more than 25% of pregnant women worldwide are infected, resulting in HWD. Two hookworm species, Ancylostoma duodenale and Necator americanus, are associated with HWD in pregnant women. Infection is acquired by penetration of the skin by infective filariform larvae found in the soil in endemic areas. Adult male and female worms live in the small intestine attached to the wall by their teeth and cutting plates, respectively. The disease is often associated with intestinal bleeding and blood loss, and has been consistently linked with anemia  . HWD leads directly and indirectly to a spectrum of adverse maternal and fetal/placental effects , associated with poor pregnancy outcomes including increased risk of fetal death and preterm birth, maternal anemia, increased risk of maternal mortality because of obstetric hemorrhage, and severe morbidities ,, . Anemia in pregnancy contributes toward maternal morbidities and increased risk for mortality associated with conditions such as postpartum hemorrhage  . Maternal anemia may also lead to anemia of the fetus and subsequently to anemia in the infant. Long-term childhood adverse effects include impaired brain development  .
In many countries worldwide, there is lack of recognition and action to date on helminthiases as a public health problem. This has to change, and the need and importance of partnerships and new approaches to scale up intervention strategies is required. To make progress in this area, there is a need for joint action among the endemic communities, public health professionals, health policy makers, and those involved in reproductive health-related matters. Health workers and endemic communities need more information on the multiple negative impacts of helminthiases on general and reproductive health and how the infections can be treated and/or prevented.
Given the safety, efficacy, and low cost of antihelminthic drugs, programs should be put in place for large-scale diagnosis and treatment of populations in endemic areas. In such intervention programs, special attention should be focused on women to reduce the disease burden and improve pregnancy and fetal outcomes.
Prevention and control of helminthic infections should be continuous and involve all age groups, but focused more on children and young adults  . If such intervention programs can target this population segment, there is a likelihood of improving reproductive health and general well-being of those living in endemic areas.
| Conclusion|| |
Helminthiases are generally chronic infections. If not diagnosed and appropriately treated early, the infections cause devastating morbidity with severe consequences on general and reproductive health.
Millions of individuals are infected worldwide and many others are at increased risk of becoming infected in endemic areas. Many of those infected suffer from urinary and reproductive tract damage, which enhances the likelihood of coinfections, subfertility, and associated social stigma. Therefore, by preventing helminthic infections in sexually active individuals of child-bearing age, we have an innovative and timely opportunity to reduce viral, fungal, and bacterial transmission in many rural areas of sub-Saharan Africa and other developing countries.
The most effective way to reduce the prevalence and spread of helminthiases is through well-coordinated prevention and control programs. Interventions that focus on early diagnosis and treatment can reduce the prevalence and the infection rates of these infections considerably and consequently improve the community's health status.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Tandan T, Pollard AJ, Money DM, Scheifele DW. Pelvic inflammatory disease associated with Enterobius vermicularis
. Arch Dis Child 2002; 86:439-440.
Dold C, Holland CV. Ascaris
and ascariasis. Microbes Infect 2011; 13:632-637.
Koura GK, Ouedraogo S, Le Port A, Watier L, Cottrell G, Guerra J, et al.
Anemia during pregnancy: impact on birth outcome and infant hemoglobin level during the first 18 months of life. Trop Med Int Health 2012;17:283-291.
Freedman LP, Isaacs SL. Human rights and reproductive choice. Stud Fam Plann 1993; 24:18-30.
Faundes A, Hardy E, Pinotti JA. Commentary on women′s reproductive health: means or end? Int J Gynaecol Obstet 1989; 3:115-118.
Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Invest 2008; 118:1311-1321.
Amir A, Majid P. Are pregnant women with chronic helminth infections more susceptible to congenital infections? Front Immunol 2014; 5:53.
Salgame P, Yap GS, Gause WC. Effect of helminth-induced immunity on infections with microbial pathogens. Nat Immunol 2013; 14:1118-1126.
Abiola FA, Babatunji EO, Bolajoko IO, Abidemi PA. Impact of human schistosomiasis in sub-saharan Africa. Braz J Infect Dis. 2015; 19:196-205.
Feldmeier H, Daccal RC, Martins MJ, Soares V, Martins R. Genital manifestations of schistosomiasis mansoni
in women: important but neglected. Mem Inst Oswaldo Cruz 1998; 93:217-233.
Qunhua L, Jiawen Z, Bozhao L, Zhilan P, Huijie Z, Shaoying W, et al.
Investigation of association between female genital tract diseases and Schistosomiasis japonica
infection. Acta Trop 2000; 77:179-183.
Kurtis JD, Higash A, Wu WH, Gundagain F, McDonald AE, Sharma S, et al
. Maternal Schistosomiasis japonica
is associated with maternal, placental and fetal inflammation. Infect Immun 2010; 3:1254-1261.
Iburg T, Balemba OB, Danizer V, Leifsson PS, Johansen MV. Congenital infections with Schistosomiasis japonica
in pigs. J Parasitol 2002; 88:1021-1024.
Willingham AL, Johansen MV, Bogh HO, Ito A, Andreassen J, Lindberg R, et al.
Congenital transmission of Schistosoma japonicum
in pigs. Am J Trop Med Hyg 1999; 60:311-312.
Feldmeier H, Krantz I, Poggensee G. Female genital schistosomiasis as a risk factor for the transmission of HIV. Int JSTD AIDS 1994; 5:368-372.
Poggensee G, Kiwelu I, Weger V, Daniela G, Thomas D, Ingela K, et al.
Female genital schistosomiasis of the lower genital tract: prevalence and disease-associated morbidity in Northern Tanzania. J Infect Dis 2000;181:1210-1213.
Bouvarda V, Baana R, Straifa K. A review of human carcinogens - part B: biological agents. Lancet Oncol 2009; 10: 321-322.
Kjetland EF, Leutscher PD, Ndhlovu PD. A review of female genital schistosomiasis. Trends Parasitol 2012;28:58-65.
Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD. Schistosomiasis and pregnancy. Trends Parasitol 2007; 23:159-164.
Ajanga A, Lwambo N, Blair L, Nyandindi U, Fenwick A, Brooker S. Schistosoma mansoni
in pregnancy and associations with anemia in northwest Tanzania. Trans R Soc Trop Med Hyg 2006; 100:59-63.
Siegrist D, Siegrist-Obimpeh P. Schistosoma haematobium
infection in pregnancy. Acta Trop 1992; 50:317-321.
Helling-Giese G, Kjetland EF, Gundersen SG, Poggensee G, Richter J, Krantz I, et al.
Schistosomiasis in women: manifestations in the upper reproductive tract. Acta Trop 1996; 62:225-238.
Nawal MN. Schistosomiasis: health effects on women. Rev Obstet Gynecol 2010; 3:28-32.
Bahrami S, Alatassi H, Slone SP, O′Connor DM. Tubal gestation and schistosomiasis: a case report. J Reprod Med 2006; 51:595-599.
Atta O, Tawiah OA, Tieru DE. Genital schistosomiasis leading to ectopic pregnancy and subfertility: a case for parasitic evaluation of gynaecologic patients in schistosomiasis endemic areas. Case Rep Obstet Gynecol 2013 (2013), 634264.
Randrianasolo BS, Jourdan PM, Ravoniarimbinina P, Ramarokoto CE, Rakotomanana F, Ravaoalimalala VE, et al.
Gynecological manifestations, histopathological findings, and Schistosoma
specific polymerase chain reaction results among women with Schistosoma haematobium
infection: a cross-sectional study in Madagascar. J Infect Dis 2015; 212:275-284.
Kjetland EF, Kurewa EN, Mduluza T. The first community-based report on the effect of genital Schistosoma haematobium
infection on female fertility. Fertil Ster, 2010; 94:1551-1553.
Laxman VV, Adamson B, Mahmood T. Recurrent ectopic pregnancy due to Schistosoma haematobium
. J Obstet Gynaecol 2008; 28:461-462.
Tweyongyere R, Mawa P, Emojong N, Mpairwe H, Jones FM, Duong T, et al.
Effect of praziquantel treatment of Schistosoma mansoni
during pregnancy on intensity of infection and antibody responses to schistosome antigens: results of a randomized, placebo-controlled trial. BMC Inf Dis 2009; 9:32.
Helling-Giese G,Sjaastad A, Poggensee G, Eyrun FK, Joachim R, Lester C, et al.
Female genital schistosomiasis (FGS): relationship between gynecological and histopathological findings. Acta Trop 1996; 62:257-267.
Barsoum RS, Garmal E, Tamer E. Human schistosomiasis: clinical perspectives: reveiw. J Adv Res, 2013; 4:433-444.
Poggensee G, Feldmeier H. Female genital schistosomiasis: facts and hypotheses. Acta Trop, 2001;79:193-210.
Barlow BA, Meleney HE. A voluntary infection with S. haematobium
. Am J Trop Med Hyg 1949; 29:79-87.
McKenna G, Schousboe M, Paltridge G. Subjective change in ejaculate as symptoms of infection with Schistosoma haematobium
in travelers. BMJ 1997; 315:1000-1001.
Feldmeier H, Leutscher P, Poggensee G, Gundel H. Male genital schistosomiasis and haemospermia. Trop Med Int Health 1999; 4:791-793.
Lewis DA, al-Adnani MS, Murphy SM. Altered seminal ejaculate consistency due to schistosomiasis. Br J Urol 1996; 78:956-957.
Corachan M, Valls ME, Gascon J, Almeda J, Vilana R. Hematospermia: a new etiology of clinical interest. Am J Trop Med Hyg 1994; 50:580-584.
Vilana R, Corachan M, Gascon J, Valls ME, Bru C. Schistosomiasis of the male genital tract: transrectal sonography findings. J Urol 1997; 158:1491-1493.
Githae GM. Testicular schistosomiasis simulating a malignant tumor or tuberculosis. S Afr Med J 1992;81:338.
Steinberger RM, Lindsay KG, Alassandri R, Wise GJ. Infarction of testicle and Schistosoma mansoni
. Urology 1975; 5:567-569.
Kazzaz BA, Salmo NA. Epididymitis due to Schistosoma haematobium
infection. Trop Geog Med 1974; 26:333-336.
Badejo OA, Soyinka F, Laja AO. Ectopic lesion of schistosomiasis of the penis simulating an early carcinoma. Acta Trop 1978; 35:263-267.
Girgis SM,Wassef NF. Bilharziasis and azoospermia. Arch Androl 1988; 5:369-372.
Harouny A, Pedersen H. Pelvo-peritoneal schistosomiasis as a cause of primary infertility. Int J Gynaecol Obstet 1988; 27:467-469.
Ville Y, Leruez M, Picaud A, Walter P, Fernandez H. Tubal schistosomiasis as a cause of ectopic pregnancy in endemic areas? A report of three cases. Eur J Obstet Gynecol Reprod Biol 1991; 42:77-79.
Elliot D. Intestinal worms. Volume 2. In. edited by Feldman M, Friedman L, Brandt L. Sleisenger and Fortdtran′s gastrointestinal and liver disease
, 8th ed. Philadelphia: Elsevier Saunders; 2006. 2442-2443.
Russell LJ The pinworm, Enterobius vermicularis
. Prim Care 1991; 18:13-24.
Tsung SH, Loh WP. Invasion of the fallopian tube by Enterobius vermicularis
. Ann Clin Lab Sci 1979; 9:393-395.
Schnell VL,Yandell R, Van Zandt S, Dinh TV. Enterobius vermicularis
salpingitis: a distant episode from precipitating appendicitis. Obstet Gynecol 1992;80:553-555.
Kogan J, Alter M, Price H. Bilateral Enterobius vermicularis
salpingo-oophoritis. Postgrad Med 1983;73:309-310.
Erhan Y, Zekioglu O, Ozdemir N, Sen S. Unilateral salpingitis due to Enterobius vermicularis
. Int J Gynecol Pathol 2000; 19:188-189.
Khan JS, Steele RJ, Stewart D. Enterobius vermicularis
infestation of the female genital tract causing generalized peritonitis. Case report. Br J Obstet Gynaecol 1981; 88:681-683.
Chung DI, Kong HH, Yu HS, Kim J, Cho CR. Live female Enterobius vermicularis
in the posterior fornix of the vagina of a Korean woman. Korean J Parasitol 1997; 35:67-69.
Al-Rufaie HK, Rix GH, Perez Clemente MP, Al-Shawaf T. Pinworms and postmenopausal bleeding. J Clin Pathol 1998; 51:401-402.
Pearson RD, Irons RP Sr, Irons RPJr. Chronic pelvic peritonitis due to the pinworm Enterobius vermicularis
. JAMA 1981;245:1340-1341.
McMahon JN, Connolly CE, Long SV, Meehan FP. Enterobius
granulomas of the uterus, ovary and pelvic peritoneum. Two case reports. Br J Obstet Gynecol 1984; 91:289-290.
Sun T, Schwartz NS, Sewell C, Lieberman P, Gross S. Enterobius
egg granuloma of the vulva and peritoneum: review of the literature. Am J Trop Med Hyg 1991; 45:249-253.
Sinniah B, Leopairut J, Neafie RC, Connor DH, Voge M. Enterobiasis: a histopathological study of 259 patients. Ann Trop Med Parasitol 1991; 85:625-635.
Knuth KR, Fraiz J, Fisch JA, Draper TW. Pinworm infestation of the genital tract. Am Fam Physician 1988; 38:127-130.
Mendoza E, Jorda M, Rafel E, Simón A, Andrada E. Invasion of human embryo by Enterobius vermicularis
. Arch Pathol Lab Med 1987; 111:761-762.
Dalrymple JC, Hunter JC, Ferrier A, Payne W. Disseminated intraperitoneal oxyuris granulomas. Aust N Z J Obstet Gynaecol 1986; 26:90-91.
McDonald GS, Hourihane DO Ectopic Enterobius vermicularis
. Gut 1972; 13:621-626.
Chandrasoma PT, Mendis KN. Enterobius vermicularis
in ectopic sites. Am J Trop Med Hyg 1977; 26:644-649.
Vinuela A, Fernandez-Rojo F, Martinez-Merino A. Oxyuris granulomas of pelvic peritoneum and appendicular wall. Histopathology 1979; 3:69-77.
Simon RD. Pinworm infestation and urinary tract infection in young girls. Am J Dis Child 1974; 128:21-22.
Pletcher JR, Slap GB. Pelvic inflammatory disease. Pediatr Rev 1998; 19:363-367.
Dundas KC, Calder AA, Alyusuf R. Enterobius vermicularis
threadworm infestation of paraovarian tissue in a woman who has had a hysterectomy. BJOG 1999; 106:605-607.
Silvio P, Francesco R. Enterobiasis in ectopic locations mimicking tumor-like lesions. Int J Microbiol 2009; Article ID 642481:5 pageshttp://dx.doi.org/10.1155/2009/642481
Smolyakov R, Talalay B, Yanai-Inbar I, Pak I, Alkan M. Enterobius vermicularis
infection of female genital tract: a report of three cases and review of literature. Eur J Obstet Gyne Repr Biol 2003; 107:220-222.
Thomson JC. Pelvic pain caused by intraperitoneal Enterobius vermicularis
(threadworm) ova with an associated systemic autoimmune reaction. J Obstet Gynaecol Res 2004; 30:90-95.
Manokaran G. Management of genital manifestations of lymphatic filariasis. Indian J Urol 2005; 21:39-43.
Bernhard P, Makunde RW, Magnussen P, Lemnge, MM. Genital manifestations and reproductive health in female residents of a Wuchereria bancrofti
endemic area in Tanzania. Trans R Soc Trop Med Hyg 2000; 94:409-412.
Nmorsi OP, Oladokun IA, Egwunyenga OA, Oseha E. Eye lesions and orchocerciasis in a rural farm settlement in Delta state, Nigeria. Southeast Asian J Trop Med Public Health 2002; 33:28-32.
Mengistu G, Balcha F, Britton S. Clinical presentation of onchocerciasis among indigenous and migrant farmers in Ethiopia. East Afr Med J 1999; 76:635-638.
Dreyer G,Norões J, Figueredo-Silva J, Piessens WF. Pathogenesis of lymphatic disease in bancroftian filariasis: a clinical perspective. Parasitol Today 2000; 16:544-548.
World Health Organization. Lymphatics filariasis fact sheet No. 102, 2014.
Ahorlu CK, Dunyo SK, Asamoah G, Simonsen PE. Consequences of hydrocele and benefits of hydrocelectomy: a qualitative study in lymphatic filariasis endemic communities on the coast of Ghana. Acta Trop 2001; 80:215-221.
Keiser J, Utzinger J. The drugs we have and the drugs we need against major helminth infections. Adv Parasitol 2010; 73:197-230.
Fenwick A. The global burden of neglected tropical diseases. Public Health 2012; 126: 233-236.
Lozano R. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for Global Burden of Disease Study 2010. Lancet 2012; 380:2095-2128.
Sklyarova V. Gynecological disorders and eruptions on the skin of face in ascariasis. Internet J Fam Pract 2008; 1:1-5.
Bouaouda LH, Rhrab B, Sendid M, Oukhouia B, Agoumi A, Osstowar K. Genital ascariasis. Apropos of a case. J Gynecol Obstet Biol Reprod 1987; 16:743-746.
Sanjeevi CB, Vivekanandan S, Narayanan PR. Fetal response to maternal ascariasis as evidenced by anti Ascaris lumbricoides
IgM antibodies in the cord blood. Acta Paediatr Scand 1991; 80:1134-1138.
Irene G, Edward M, Susana B, Martha EC. Evidence for in utero sensitization to Ascaris lumbricoides
in newborns of mothers with ascariasis. J Infect Dis 2009; 199:1846-1850.
Cooper PJ, Barreto M, Rodrigues LC. Human allergy and intestinal helminth infections: a review of the literature and discussion of a conceptual model to investigate the possible causal association. Br Med Bull 2006; 79:203-218.
Da Costa-Macedo LM, Rey L. Ascaris lumbricoides
in neonate: evidence of congenital transmission of intestinal nematodes. Rev Inst Med Trop Sao Paulo 1990; 32:351-354.
MacLoed CL. Intestinal nematodes. In: Macleod CL Parasitic infections in pregnancy and new born
. New York, 1988; Oxford University Press. 192-215.
Sousa-Figueiredo JC, Gamboa D, Pedro JM, Fançony C, Langa AJ, Magalhães RJ, et al.
Epidemiology of malaria, schistosomiasis, geohelminths, anemia and malnutrition in the context of a demographic surveillance system in northern Angola. PLoS One 2012; 7: e33189.
Brooker S, Hotez PJ, Bundy DA. Hookworm-related anemia among pregnant women: a systematic review. PLoSNegl Trop Dis 2008; 2:e291.
Fairley JK, Bisanzio D, King CH, Kitron U, Mungai P, Muchiri E, et al.
Birth weight in offspring of mothers with high prevalence of helminth and malaria infection in coastal Kenya. Am J Trop Med Hyg 2013; 88:48-53.
McLean E, Egli I, Cogswell M (ed) (2012) Worldwide prevalence of anemia 1993-2005: WHO global database on anaemia
. Geneva: World Health Organization.
Dotters-Katz S, Kuller J, Heine RP. Parasitic infections in pregnancy. Obstet Gynecol Surv 2011; 66:515-525.
Nwizi EN, Iliyasu Z, Ibrahim SA, Galadanci HS. Socio-demographic and maternal factors in anemia in pregnancy at booking in Kano. North Nigeria Afr J Reprod Health 2011;15:33-41.
Huchon C, Dumont A, Traoré M, Abrahamowicz M, Fauconnier A, Fraser W, Fournier P. A prediction score for maternal mortality in Senegal and Mali. Obstet Gynecol 2013;121:1049-1056.
Elizabeth MM, Steven RM, Peter M, Indu M, Christopher L. The association of parasitic infections in pregnancy and maternal and fetal anemia: a cohort study in coastal Kenya. PLoSNegl Trop Dis 2014; 8:e2724.
Shiba KR, Ganesh R. Ascaris, ascariasis and its present scenario in Nepal. J Institute Med 1999; 21:1-250.