Ecological and molecular studies on emerging schistosomiasis mansoni in Dhofar Governorate, Sultanate of Oman



The recent detection of some cases of autochtonous schistosomiasis mansoni in Dhofar, Oman, prompted a search for the transmission sites. The five field surveys we conducted from November 2000 to February 2002 provided ecological data on schistosomiasis in Dhofar. Twenty-eight water bodies situated within 8–160 km from Salalah, the largest city of Dhofar and at altitudes of up to 900 m, were surveyed for freshwater snails. Biomphalaria arabica was found in 15 of them. Three sites (Tibraq, Siginitti and Arazat) had Schistosoma infected snails, the first snails shedding cercariae of this parasite ever collected in Oman. The parasite from Dhofar was analysed by Random Amplified Polymorphic DNA comparisons using 11 primers and 167 polymorphic fragments and had 87–88% similarity with Schistosoma mansoni from Guadeloupe, but only 37–38% similarity with S. rodhaini from Burundi. Thus, it is a strain of S. mansoni. During the November 2000 survey, the prosobranch snail Melanoides tuberculata was associated with B. arabica in 10 of the 13 B. arabica sites. Cercariae from other species of Digenea emerged from five of the B. arabica sites, including the three named above. This paper presents the first finding of S. mansoni in the Dhofar Governorate and represents an initial study of the biology of S. mansoni transmission. This parasite and its cycle need further biological and molecular characterization, and the clarification of its epidemiological status in Dhofar Governorate is an urgent task.


Schistosomiasis in the Sultanate of Oman was first diagnosed in 1979 in two autochtonous patients at Sultan Qaboos Hospital in Salalah, the largest city of the Dhofar Governorate in the South-West of the Sultanate (Shaban 1995). Some imported cases were identified in Dhofar among immigrants from Sudan and Egypt (Arfaa 1982) and some additional endemic cases were diagnosed among labourers of the Arazat farm near Salalah (Githaiga 1983). The potential intermediate host for Schistosoma mansoni in Dhofar is the snail Biomphalaria arabica, a local variety of B. pfeifferi (DeJong, Albuquerque, USA, personal communication). The presence of B. arabica was first reported in 1896 and this snail has regularly been found in many sites in Dhofar (Arfaa 1982; Githaiga 1983; Idris et al. 1994). The development of this snail is favoured by the fact that the Dhofar Governorate receives the monsoon rains during June, July and August and is rich in temporary or permanent water bodies. However, snails infected with S. mansoni were never reported, and the presence ofS. mansoni in Oman was exclusively ascertained by occasional human infections.

The identification of schistosomiasis mansoni in Dhofar during the early 1980s was taken seriously and a control programme including mollusciciding, treatment and health education was instituted by an organizational committee (Shaban 1995). Several years after the start of the control programme, in 1990–91, few local individuals had schistosome antibodies, but no more eggs were detected (Idris et al. 1994). Since 1994, no additional human cases were detected, thus proving the efficacy of the control programme (Shaban 1995), and the disease was declared as eliminated (Scrimgeour et al. 1999).

Recently, between September and November 1999, few new cases of autochtonous schistosomiasis mansoni from Dhofar were diagnosed at Sultan Qaboos University Hospital in Muscat. One of the patients suffered from various complications as a result of neuroschistosomiasis (Scrimgeour et al. 2001; Koul et al. 2002). As a consequence, the following studies were conducted to identify the potential and active transmission sites of S. mansoni in Dhofar.

Materials and methods

Field studies

Five field surveys were conducted in November 2000, May, July and November 2001, and in February 2002. During the first survey, 28 water bodies were investigated. Information on their geographical coordinates and their physical–morphological characterization is recorded in Table 1. According to their physical–morphological characterization, the water bodies could be separated into two groups: springs with naturally running water courses and springs with large concrete-built reservoirs together with one or several attached concrete drinking reservoirs for animals and with the effluent water following the bed of the stream. One site (Arazat) is a mixture of both structures. During the following surveys, studies focused on selected water bodies. Each water site was visited for 1–2 h, snails were scooped using 30 × 30-cm2 nets. The snails were collected into individually labelled plastic cups and transported to the laboratory in Salalah.

Table 1.  Geographical coordinates and physical–morphological characterization of the visited aquatic habitats around Salalah, Dhofar Governorate, Sultanate of Oman
Name of siteSite no.Geographical coordinates of the sitePhysical–morphological site
Longitude*LatitudeAltitude above sea level (m)
  • *

     E, East and N, North (from a map with a 1/100.000 scale).

  •  R, spring with one or more cement-built water reservoir(s) followed by effluent water; W, natural running spring water.

Homran 154°18′ E17°6′ N200R
Tibraq 254°20′ E17°6′ N150R
Hasheir 354°37′ E17°4′ N300R
Siginitti 454°29′ E17°8′ N500W
Wadi Dharbat 554°28′ E17°7′ N500W
Sahanout 654°11′ E17°9′ N200R
Arazat 754°14′ E17°8′ N300W + R
Zaa 854°19′ E17°14′ N800–850R
Ankhar 954°19′ E17°14′ N800–850R
Birin1054°20′ E17°14′ N800–850R
Garziz1154°4′ E17°6′ N150R
Zaikat1254°10′ E17°12′ N550R
Afilayiah1354°7′ E17°14′ N650–700R
Aisham1454°7′ E17°14′ N650–700R
Jairah1554°7′ E17°14′ N650–700R
Aayyum1653°53′ E17°15′ N900W
Anaar1753°55′ E17°0′ N100W
Gaith1853°52′ E16°59′ N100W
Shemth1953°53′ E16°58′ N100W
Ghibrin2053°53′ E17°4′ N850R
Hota2153°30′ E16°46′ N  0W
Kharfut2253°20′ E16°44′ N  0W
Meghsil2353°13′ E16°45′ N600W
Sarfait2453°9′ E16°42′ N700R
Diim2553°10′ E16°41′ N150R
Farkanut2653°9′ E16°42′ N700R
Kohood2753°9′ E16°43′ N800W
Shakhmout2853°15′ E16°42′ N100R

Laboratory studies

The snails were tested for emission of digenean cercariae during the 24 h after their collection. The snails were tested first in groups of 50 individuals and, if cercariae were detected, snails were then individually re-screened. The infected snails were maintained separately and fed ad libitum with dried lettuce until transported to Perpignan, France.

In Perpignan, Swiss OF1 mice were experimentally exposed to the cercariae shed from the naturally infected snails following the protocol of Boissier and Moné (2001). All naturally infected snails from each positive site were pooled together for mouse infections. After 8 weeks, worms were obtained by perfusion of the mice according to Duwall and Dewitt (1967), washed in NaCl 8.5‰, fixed in 70% alcohol and preserved at −20 °C for molecular analysis.

DNA was extracted from one individual worm originating from each of the different sites in Dhofar and a set of 11 primers (from Kits A and B; Operon Technologies, Inc., Alameda, CA, USA: OP-A5, A6, A8, A11, A12, A13, A15, A16, B6, B14, B15) was used to generate Random Amplified Polymorphic DNA (RAPD) profiles following the protocol used by Sire et al. (2001).

The patterns of schistosomes from the different sites in Dhofar were compared with those of a S. mansoni strain from Guadeloupe and S. rodhaini from Burundi which are both maintained in our laboratory in Perpignan. The polymorphism detected between the parasites from Dhofar and the known species of schistosomes was quantified using a similarity index (S) based on the probability that an amplified marker from one individual will also be found in another and S = 2 × no. of shared markers between A and B/(no. of markers A + no. of markers B) (Nei & Li 1979).

Ethical approval

Ethical approval of animal studies was obtained from the French Ministère de l'Education Nationale, de la Recherche et de la Technologie and the French Ministère de l'Agriculture et de la Pèche (Agreement No. A 66040).


Malacological data

A comprehensive survey of the water bodies was carried out in November 2000. This survey showed that several species of freshwater snails live in the Dhofari valleys (Table 2). The pulmonate snail B. arabica was present in 13 of the 28 sites (46%) and its presence did not depend on the geographical position of the site: B. arabica was found at any altitude, in water bodies of both physical–morphological structures and at any distance from Salalah. With respect to earlier surveys (1982–94), this snail continued to be present in five sites (site nos. 2, 4, 5, 8 and 19) and was still absent from one site (site no. 1), it had disappeared from six (site nos. 3, 6, 7, 11, 17 and 18) and was newly detected in one site (site no. 16). During this survey, 15 additional sites were investigated for the first time (site nos. 9, 10, 12–15 and 20–28) and seven among them (site numbers 9, 10, 20, 21, 22, 24 and 27) harboured B. arabica. The prosobranch snail Melanoides tuberculata was present in 20 of the 28 sites visited (71%) and in 10 (site numbers 2, 4, 5, 9, 16, 19, 21, 22, 24 and 27) of the 13 sites (77%) occupied by B. arabica. The presence of M. tuberculata did not depend on the geographical coordinates of the site. These two species of freshwater snails were by far dominating over all other snails. Very few small Lymnaeids and small Planorbids (both undetermined) were found in one site only (site no. 4) and in two sites (site nos. 14 and 26), respectively. The pulmonate, Bulinus wrighti, continued to be present in the only pond (site no. 17) where it was first detected in 1994 (Idris et al. 1994).

Table 2.  Baseline survey on the occurrence of freshwater snails in the water bodies around Salalah, Dhofar Governorate, Sultanate of Oman (November 2000)
Name of siteSite no.Presence/absence of snails*
B. a.M. t.B. w.B. a. (in previous surveys)
  • *

     B. a., Biomphalaria arabica; M. t., Melanoides tuberculata; B. w., Bulinus wrighti.

  • † The presence or absence of B. arabica according to earlier reports: A, Arfaa (1982); BG, Brown and Gallagher (1985); G, Githaiga (1983); I, Idris et al. (1994); NA, observations not available from previous reports.

  •  S, only shells, but no living snails detected; ‘+’, presence; ‘–’, absence.

  • §

     Very few small Lymnaeids found.

  •  Very few small Planorbids found.

Homran 1+A(–) BG(–) G(–) I(–)
Tibraq 2++I(+)
Hasheir 3S+I(+)
Siginitti§ 4++I(+)
Wadi Dharbat 5++A(+) G(+) I(+)
Sahanout 6S+A(+) G(+) I(+)
Arazat 7+A(+) G(+) I(+)
Zaa 8+I(+)
Ankhar 9++NA
Garziz11+A(+) G(–) I(+)
Gaith18G(+) I(+)

The results of the later surveys in 2001 and 2002 (Table 3) confirm those obtained in 2000 concerning the presence or absence of B. arabica in each site, except for Arazat (site no. 7) and Hasheir (site no. 3) which were recolonized by B. arabica in May 2001 and for Sahanout (site no. 6) where neither snails nor shells could be detected in February 2002.

Table 3.  Follow-up surveys of water bodies in search for Biomphalaria arabica around Salalah, Dhofar Governorate, Sultanate of Oman (May 2001 to February 2002)
Name of siteSite no.Presence or absence of Biomphalaria arabica*
May 2001July 2001November 2001February 2002
  • *

     ‘+’, presence; ‘–’, absence; NV, not visited; S, only shells, but no living snails detected.

Homran 1NVNVNV
Tibraq 2++++
Hasheir 3++++
Siginitti 4+NV++
Wadi Dharbat 5++++
Sahanout 6SNVNV
Arazat 7++++

Parasitological data

Digenean parasites were searched for in all B. arabica collected during the five surveys. A total of 10 798 B. arabica were tested and the results are shown in Table 4. Among the sites where B. arabica was detected, five sites (site nos. 2–5 and 7) had digenean infections and all of these sites were located east or north-east and 16–60 km from Salalah. Among these sites, three (Tibraq-site no. 2, Siginitti-site no. 4 and Arazat-site no. 7) had schistosome-infected snails. In the remaining water bodies, no snails with digenean infections were detected during any of the surveys.

Table 4.  Prevalences of schistosomes and other digeneans in Biomphalaria arabica from Dhofar Governorate, Sultanate of Oman, during five field surveys
Name of
November 2000May 2001July 2001November 2001February 2002
NSchisto- someOther
NSchisto- someOther
NSchisto- someOther digeneansNSchisto- someOther
NSchisto- someOther
  1. N, number of B. arabica tested; numbers in bold indicate total numbers; numbers in parentheses indicate number of infected snails; ‘–’, not infected.

Tibraq2897.86% (7)23.60% (21)6645% (33)1.95% (13)1990.50% (1)2% (4)3505530.40% (2)0.50% (3)
Hasheir30  9722.50% (24)3472.30% (8)408360
Siginitti44530.22% (1) 4.42% (20)2290  1434741% (5)
Wadi Dharbat51504100.24% (1)1380.70% (1)592190.50% (1)
Arazat70  13372.70% (1)19512840.40% (5)
Zaa82250  0  0  0  
Ankhar910080  0  0  0  
Birin1012060  0  0  0  
Aayyum16400  520  0  
Shemth1970  380  0  
Ghibrin201100  0  0  0  
Hota2110  0  0  0  
Kharfut22190  0  0  0  
Sarfait242320  0  0  0  
Kohood271140  0  0  0  
3654  2288  811  1155  2890  

The prevalence of the schistosome infections inB. arabica ranged from 0.4% to 7.9% for the same site in different surveys and from 0.2% to 7.9% during the same survey but for different sites. No influence of the season on the schistosome infection rates could be detected. The prevalence of digenean infections other than schistosomes ranged from 0.5% to 23.6% for the same site in different surveys and from 4.4% to 23.6% during the same survey but for different sites. Again, no influence of the season on the digenean infection rates was detectable. The systematic identification of these larval digeneans remains to be performed. None of the 46 B. wrighti collected in 2000 was infected with schistosomes or other digeneans.

Identification of the Omani schistosomes

The Omani schistosomes were identified by RAPD analysis using adult worms obtained from the mice exposed to cercariae from snails collected at Tibraq and Siginitti. Male and female adult worms were obtained from Tibraq, but only female adult worms from Siginitti. To avoid differences because of sex, only female worms were used for the comparisons. The 11 primers employed in this study revealed a genetic polymorphism between the individual females of the different strains and species with a total of 167 polymorphic fragments that were used for comparison. Figure 1 is an example of the patterns obtained with four primers (A12, A13, A15, A16). Obviously, S. rodhaini gives a different pattern compared with the three other samples for each of the four primers. According to the similarity indices shown in Table 5, the schistosomes from Tibraq and Siginitti were 95% similar, both shared 87–88% similarity with S. mansoni from Guadeloupe, but only 37–38% with S. rodhaini from Burundi. The species from Guadeloupe and from Burundi shared only 34% of the DNA fragments. Thus, the schistosomes from Dhofar are S. mansoni.

Figure 1.

Amplification of genomic DNA from Schistosoma rodhaini (lanes 1), Schistosoma from Tibraq (lanes 2), Schistosoma from Siginitti (lanes 3) and S. mansoni (lanes 4) by using one arbitrary primer, A12, A13, A15 and A16, respectively. Amplified products were electrophoresed through a 1% agarose gel stained with ethidium bromide.

Table 5.  Similarity indices between the Omani schistosomes and Schistosoma mansoni and S. rodhaini
 Tibraq schistosome
Siginitti schistosome
S. mansoni
S. rodhaini (Burundi)0.380.370.34
Tibraq schistosome  (Oman)0.950.88
Siginitti schistosome  (Oman)0.87


This is the first report on active transmission sites of S. mansoni in Dhofar Governorate, Sultanate of Oman. The sites investigated are of different morphological structures, including a natural water course (Siginitti), a reservoir constructed in concrete (Tibraq), and a mixture of both (Arazat). The range of percentages of snails infected (prevalences) as obtained here for Dhofar (0.5–7.9%) is comparable with ranges recorded in two geographical areas of low endemicity, e.g. in Guadeloupe (0.2–5.0% of B. glabrata with S. mansoni; Sire et al. 1999) or in South Africa (0.6–10.4% of B. pfeifferi with S. mansoni; Donnelly & Appleton 1985). However, the total prevalence of infected snails in the three active transmission sites in Dhofar Governorate (Siginitti, Tibraq and Arazat) (45 of 4683, 0.96%) was significantly different from that found in Guadeloupe (43 of 6972, 0.62%; χ2 = 3.98, P = 0.046) and from that found in South Africa (62 of 3062, 2.02%; χ2 = 14.61, P = 0.0001). Further work is required to study the biological and molecular differences between the populations of S. mansoni in Dhofar. Studies on the B. arabica–S. mansoni compatibility, between the different S. mansoni populations from Dhofar as well as from African countries should help in the understanding of the biogeographical coevolution of schistosomes with their snail hosts in this region, as was the case of S. bovis (Monéet al. 2000).

Any type of freshwater body in Dhofar appears to provide a suitable habitat for B. arabica, independent on its distance from Salalah or the altitude above sea level. Consistent with this view, among the sites visited for the first time either during our earlier survey more than 10 years ago (Idris et al. 1994) or in the present report, B. arabica were mostly detected, and these sites added to those recorded already by Arfaa (1982) and Githaiga (1983). Thus, the potential transmission sites forS. mansoni in Dhofar, particularly around Salalah, are numerous and have been so at least over the past 20 years. Taking into consideration the nearly ubiquitous presence of B. arabica in this area, it might be worth investigating why schistosomiasis mansoni was nevertheless absent for many years or prevalent to a much lower degree than could have been expected.

Undoubtedly, control and surveillance measures have a great impact on transmission. With respect to mollusciciding, some sites (Garziz and Sahanout) that were sprayed with Bayluscide a few years ago (Shaban, unpublished) proved to be free of B. arabica in our surveys, whereas another site (Arazat farm) was again populated by many snails. These observations illustrate that mollusciciding may be an important element of the schistosomiasis control programme in Dhofar, however, it may fail to achieve long-term snail control. In fact it may be relevant to investigate how snails succeed in recolonizing water bodies in Dhofar, although these are separated from each other by arid mountain chains, and water streams do not communicate. Supplementary snail control measures such as biological control using competitor snails or competitor parasites could be considered.

The host–parasite system B. arabica–S. mansoni in Dhofar is often associated with the prosobranch snail M. tuberculata. This association may influence the transmission dynamics of S. mansoni, as M. tuberculata is known to have an influence on both growth and reproduction of the snail intermediate hosts of schistosomes (Moné 1991) and, consequently on the development of the parasite in the snail. Thus, under experimental conditions, the presence of M. tuberculata significantly stimulates the cercarial production of S. mansoni by B. glabrata (Monéet al. 1986; Moné 1991). Another prosobranch, Melanopsis praemorsa, showed experimentally the same cercariae-stimulating effect on S. bovis in B. wrighti (Mouahid et al. 1992) and, under semifield conditions, stimulated both growth and reproduction of B. truncatus, an important intermediate host for S. haematobium (El Ouali et al. 1999). On the other hand, as M. tuberculata is known to be a competitor of Biomphalaria in the West Indies (Pointier 1993), and as it was found in the majority of the water bodies studied here, it is worth investigating whether this snail may also lead to a decline of B. arabica populations in Dhofar.

The host–parasite system B. arabica–S. mansoni in Dhofar is often associated with other digeneans which also use B. arabica as intermediate host. As digenean sporocysts may negatively interfere with the development of schistosome sporocysts (Lim & Heyneman 1972; Mouahid & Moné 1990), and as we discovered several species of digeneans other than S. mansoni, it seems worth to determine whether they may play a role in, or could be exploited for, the control of schistosomiasis transmission in Dhofar.

The sites found to be infected with schistosomes are all situated around Salalah city which is an extending urban zone with a rapid human population growth. Indeed, the population of Oman is growing at a rapid rate. The average annual growth rate of the total population for Oman between 1995 and 2000 was 3.29%, as a result of considerable decline in mortality and continued high fertility, and its estimated trajectories for the coming decade are similarly high (United Nations Population Division 2002). The particular elements of local human behaviour, which may have led in Dhofar to autochtonous transmission of schistosomiasis need to be identified. However, it should be recalled that man is not necessarily the only definitive host for the parasite and rodents may significantly contribute to the cycle of S. mansoni as shown in Guadeloupe (Théron et al. 1992). Our current research is concerned with the human populations at risk and the potential role of other hosts such as rodents in the transmission of the disease.


We are grateful to Mr Salim Al Yafae for guidance to the water bodies and for competent help during the field work. This research was financially supported by the Sultan Qaboos University (IG/MED/MICR/00/01), The Ministry of Health in Oman, the French CNRS, Sciences de la Vie (01 N92/0745/1 and 02 N60/1340), the French Ministry of Foreign Affairs, and the German Academic Exchange Service (DAAD).

Ali A. Al labri, Department of Microbiology and Immunology, College of Medicine and Health Sciences, Sultan Qaboos University, PO Box 35, Muscat, Oman. E-mail:
Jérôme Boissier, UMR5555 CNRS-UP Parasitologie Fonetionnelle et Evolutive, Université, 52 Avenue de Villeneuve, 66860 Perpignancedex, France. E-mail:
Mohamed A. Idris, Department of Microbiology and Immunology, College of Medicine and Health Sciences, Sultan Qaboos University, PO Box 35, Muscat, Oman. E-mail:
Héléne Moné, UMR5555 CNRS-UP Parasitologie Fonetionnelle et Evolutive, Université, 52 Avenue de Villeneuve, 66860 Perpignancedex, France. Tel.: +33 4 68 66 21 84; Fax: +33 4 68 66 22 81; E-mail: (corresponding author).
Gabriel Mouahid, UMR5555 CNRS-UP Parasitologie Fonetionnelle et Evolutive, Université, 52 Avenue de Villeneuve, 66860 Perpignancedex, France. E-mail:
Andreas Ruppel, Institute of Tropical Hygiene, University of Heidelberg, Im Neuenheimer Feld 324, 69120 Heidelberg, Germany. E-mail:
Mahmoud A. Shaban, Public Health Affairs, Ministry of Health, PO Box 98, Dhofar, Oman. E-mail: