The colposcopic atlas of schistosomiasis in the lower female genital tract based on studies in Malawi, Zimbabwe, Madagascar and South Africa

Hanne M Norseth, Patricia D Ndhlovu, Elisabeth Kleppa, Bodo S Randrianasolo, Peter M Jourdan, Borghild Roald, Sigve D Holmen, Svein G Gundersen, Jayanthilall Bagratee, Mathias Onsrud, Eyrun F Kjetland, Hanne M Norseth, Patricia D Ndhlovu, Elisabeth Kleppa, Bodo S Randrianasolo, Peter M Jourdan, Borghild Roald, Sigve D Holmen, Svein G Gundersen, Jayanthilall Bagratee, Mathias Onsrud, Eyrun F Kjetland

Abstract

Background: Schistosoma (S.) haematobium is a neglected tropical disease which may affect any part of the genital tract in women. Female genital schistosomiasis (FGS) may cause abnormal vaginal discharge, contact bleeding, genital tumours, ectopic pregnancies and increased susceptibility to HIV. Symptoms may mimic those typical of sexually transmitted infections (STIs) and women with genital schistosomiasis may be incorrectly diagnosed. An expert consensus meeting suggested that the following findings by visual inspection should serve as proxy indicators for the diagnosis of schistosomiasis of the lower genital tract in women from S. haematobium endemic areas: sandy patches appearing as (1) single or clustered grains or (2) sandy patches appearing as homogenous, yellow areas, or (3) rubbery papules. In this atlas we aim to provide an overview of the genital mucosal manifestations of schistosomiasis in women.

Methodology/principal findings: Photocolposcopic images were captured from women, between 1994 and 2012 in four different study sites endemic for S. haematobium in Malawi, Zimbabwe, South Africa and Madagascar. Images and specimens were sampled from sexually active women between 15 and 49 years of age. Colposcopic images of other diseases are included for differential diagnostic purposes.

Significance: This is the first atlas to present the clinical manifestations of schistosomiasis in the lower female genital tract. It will be freely available for online use, downloadable as a presentation and for print. It could be used for training purposes, further research, and in clinical practice.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1. Possible sites for disease by…
Figure 1. Possible sites for disease by S. haematobium in women.
Manifestations in the cervix and vagina are seen with a colposcope, but ova seem to be evenly distributed in all parts of the genital tract .
Figure 2. Schistosomiasis life cycle.
Figure 2. Schistosomiasis life cycle.
The most common species found to be pathogenic to humans; and Schistosoma (S.) haematobium, S. mansoni, S. japonicum. Eggs are excreted through faeces, urine and possibly through vaginal discharge from infected individuals, may hatch if they come in contact with water, releasing miracidia that infect fresh water snail hosts where they multiply, producing free-swimming cercariae that eventually may penetrate the skin of human hosts. The cercariae mature in the portal vein and migrate to venules draining the intestines, or the urinary and genital tracts, where they may deposit up to 300 eggs every day. Some of these eggs will be trapped in the tissues inducing a localised host response, while others will penetrate the vessel wall and the mucosa of the intestines, the bladder or the genitals, subsequently excreted in faeces, urine or vaginal discharge into fresh water in order to continue the parasite life cycle. This figure shows the venous plexus of the bladder only; however, the venous plexi surrounding the genital tract is also affected. (Source: CDC-DPDx, Atlanta, United States).
Figure 3. S. haematobium ovum as seen…
Figure 3. S. haematobium ovum as seen in urine microscopy.
Figure 4. Pap smear.
Figure 4. Pap smear.
S. haematobium ovum with terminal spine.
Figure 5. A typical transmission site.
Figure 5. A typical transmission site.
River water is used for personal, household, animal husbandry and recreational purposes. Even where there are taps the queues are often long. Water that is not for drinking purposes is acquired from fresh water bodies as the one shown in the photo.
Figure 6. Different speculums.
Figure 6. Different speculums.
In our experience speculum A was the only speculum that allowed rotation for full inspection if the vaginal walls. The others caused discomfort. Disposable speculums are expensive and often do not hold well rotated for the inspection of the anterior and posterior vaginal walls.
Figure 7. Homogeneous sandy patches.
Figure 7. Homogeneous sandy patches.
Sandy patches appearing as a homogenous, yellow area. There is also some white discharge at six o'clock. The colour analysis (black and white template) shows that the typical yellowish colour is found 1 to 2 o'clock and 6 o'clock (Holmen, submitted).
Figure 8. Grainy sandy patches and mucosal…
Figure 8. Grainy sandy patches and mucosal bleeding.
Grainy sandy patches on the entire anterior lip of the cervix, on the endo- and ectocervix, into the anterior and lateral fornices. Note the different shades of yellow; some areas are bright yellow, whereas other areas are beige to white. Mucosal bleeding is seen in especially in the anterior fornix.
Figure 9. Grainy sandy patches on the…
Figure 9. Grainy sandy patches on the vaginal wall.
Clusters of grainy sandy patches and mucosal bleeding of the lateral and posterior vaginal walls. The vaginal mucosa looks hyperaemic, but no vessel structures are seen at this magnification.
Figure 10. Sandy patches appearing as grains…
Figure 10. Sandy patches appearing as grains and homogenous, yellow areas of the vaginal wall.
Enlarged section of a part of the vaginal wall in Figure 9. At this magnitude we see the single grains' (arrows point to some examples) characteristic rice-grain shape and colour. The entire surface has a mottled appearance. We also see homogenous yellow areas with embedded grains.
Figure 11. Sandy patches appearing as grains,…
Figure 11. Sandy patches appearing as grains, homogenous, yellow areas, abnormal blood vessels and mucosal bleeding.
The entire cervical surface is mottled by clusters of grains and some homogeneous yellow areas with single grains embedded (arrows point to some examples). The whole transformation zone looks yellow, possibly due to the extensive amount of ova. We also see mucosal bleeding from around the cervical os.
Figure 12. Grains embedded in a homogeneous…
Figure 12. Grains embedded in a homogeneous yellow area.
Enlarged section of a part of the ectocervix in Figure 11. Single grains (arrows point to some of them) are embedded in the homogeneous yellow area. The different shades of yellow in this lesions range from a dull, almost brownish colour (x) to a sharp, gold-like colour seen in the single grains (y). Not every person in our group was able to see these nuances. The colour analysis (black and white template) may assist (Holmen, submitted). The magnified insert shows the contours of the adjacent typical abnormal blood vessels.
Figure 13. Grainy sandy patches and abnormal…
Figure 13. Grainy sandy patches and abnormal blood vessels.
Enlarged section of a part of the ectocervix. Clusters of grains and single grains are spread over the ectocervical surface. The single grains (arrows point to some examples) are approximately 0.05 by 0.2 mm in size with a rice-grain shape and yellow colour. The grains are surrounded by a network of convoluted blood vessels. The insert shows the contours of the adjacent abnormal blood vessels.
Figure 14. Sandy patch appearing as a…
Figure 14. Sandy patch appearing as a homogenous, yellow area.
The homogeneous yellow area can be seen as a yellow discolouring of the mucosa. A lesion like this can be very difficult to spot if one does not have the correct light source.
Figure 15. Sandy patches appearing as single…
Figure 15. Sandy patches appearing as single grains and homogenous, yellow areas surrounded by abnormal blood vessels.
Ectocervical mucosa with single grains (arrows point to some examples) scattered all over and surrounded by a network of abnormal blood vessels. When looking at this closely and from different angles, perhaps by tilting the computer monitor or adjusting the brightness level, one can see small areas with a yellow colour, representing homogeneous yellow areas. The insert shows the contours of the adjacent abnormal blood vessels.
Figure 16. Rubbery papules and abnormal blood…
Figure 16. Rubbery papules and abnormal blood vessels.
Rubbery papules and mucosal bleeding on the cervical surface and anterior fornix. Papules look like pustules but are firm like rubber, the diameters range between 0.3 to 1.2 millimetres. Near the papules are minute-spiral blood vessels (arrows point to some examples).
Figure 17. Rubbery papules.
Figure 17. Rubbery papules.
Enlarged section of the lesion in Figure 16. The black and white template shows that the colour of the rubbery papules is recognised by the colour analysis (Holmen, submitted). Near the papules are minute-spiral blood vessels (in red). Tilt the monitor to see more detail.
Figure 18. Histological correlate of a rubbery…
Figure 18. Histological correlate of a rubbery papule to Figures 17 and 18 .
In rubbery papules viable-looking (with intact structures) schistosome ova (x) are surrounded by intense eosinophilia.
Figure 19. Histological correlate to the sandy…
Figure 19. Histological correlate to the sandy patch in Figure 9 .
Numerous calcified (xc) and viable-looking ova (x) are seen in the stroma beneath the epithelium. Lymphocytes, eosinophils and immature fibroblasts surround the schistosome eggs.
Figure 20. Cervical intraepithelial neoplasia stage I–II…
Figure 20. Cervical intraepithelial neoplasia stage I–II after application of acetic acid.
Aceto-white lesion in the transformation zone abutting the squamo-columnar junction (dashed line). The white area is dense and has feathery margins (arrows), possibly with some mosaic pattern (ovals). This finding probably represents cervical intra-epithelial neoplasia (CIN) stage one to two. CIN refers to the premalignant neoplastic changes taking place in the squamous epithelium in the transformation zone of the cervix before the possible development of cervical squamous carcinoma. These changes can be divided into three groups based on the proportion of epithelium thickness involved in the dysplastic process. Early stages of CIN may be confused with homogenous yellow areas of the sandy patches, and late stages may involve some of the same vessel patterns that can be seen in schistosome lesions . However, the schistosome lesions are not aceto positive, and they are not confined to the transformation zone.
Figure 21. Malignant looking lesion.
Figure 21. Malignant looking lesion.
Severe cervicitis caused by schistosomiasis. Hysterectomy and cone biopsies have been performed in lesions like this due to lack of pathology services and ignorance .
Figure 22. Nabothian cyst.
Figure 22. Nabothian cyst.
Normal cervical surface with a small yellow Nabothian cyst (arrow) 11 o'clock in the anterior lip of the transformation zone. These may be confused with rubbery papules but the Nabothian cysts are often bigger, do not protrude so acutely, and they are only found in the transformation zone. Rubbery papules, however, may be situated anywhere on the vaginal and cervical surface. Also note, next to the Nabothian cyst (left arrow) a small irregular-shaped leukoplakia area (right arrow) that could be a herpes simplex viral infection.
Figure 23. Nabothian cyst.
Figure 23. Nabothian cyst.
Typical blood vessels across a Nabothian cyst. The underlying cyst is pale yellow adjacent to the squamo-columnar junction (dashed line) and the vascular network shows regular branching.
Figure 24. Grainy sandy patches and trichomoniasis…
Figure 24. Grainy sandy patches and trichomoniasis together.
Clusters of grains on the posterior lip of the ectocervix are both superficial and deep, millimetres to centimetres from the squamo-columnar junction (dashed line). This case is however also positive for Trichomonas vaginalis and an erythematous surface is seen with microscopic, punctate haemorrhages typical for trichomoniasis (the so-called ‘strawberry patches’). We also see fresh blood from the mucosal surface. Both diseases may cause such inflammation.
Figure 25. Grainy sandy patches, trichomoniasis, petechiae…
Figure 25. Grainy sandy patches, trichomoniasis, petechiae and mucosal bleeding.
We see single grains (arrows point to some examples) scattered over the ectocervical surface. Petechiae are present on the posterior lip. We also see fresh blood from the mucosa (b). The surface is uneven.

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