Tropical diseases such as malaria, schistosomiasis, intestinal helminths, and filariasis have a dramatic impact on reproductive health. Many cases of unexplained pregnancy loss are due to undiagnosed tropical diseases. Malnutrition or anemia caused by intestinal worms may be worsened by pregnancy and make the pregnancy difficult [2].

In the developing world, young women, pregnant women, and their infants and children frequently experience a cycle, where undernutrition (macronutrient and micronutrient) and repeated infection, including parasitic infections, lead to adverse consequences that can continue from one generation to the next. Among parasitic infections, malaria and intestinal helminths coexist widely with micronutrient deficiencies and contribute importantly to anemia and this cycle of retarded growth and development. In somewhat more limited or focal geographic settings, other parasitic diseases (eg, schistosomiasis, filariasis) contribute similarly to this cycle. It is undoubtedly much better to enter a pregnancy free of infection and nutritionally replete than the various alternatives [3].

Intestinal parasitic infections, especially due to the helminths, increase anemia in pregnant women [2, 3, 4, 5,6]. Additionally, hookworm infections induce deficiencies of iron, total energy, protein, and possible folate and zinc [4,7]. The results of this are low pregnancy weight gain and intrauterine growth retardation (IUGR), followed by low birth weight (LBW), with its associated greater risks of infection and higher perinatal mortality rates; this has been reported in the majority of studies, although a causal link remains to be completely proven [7, 8, 9].

Evaluation of those women included, as a part of their routine prenatal control, an initial interrogation, physical examination, and laboratory studies: count of blood cells (CBC) (including thick and thin films, stained with Giemsa), serological screening studies for HIV-1 and -2 (ELISA), HBV (HbsAg and IgM anti-HBc), VDRL, and FTA-ABS, and toxoplasmosis (antibody titers by DAT). For this study, we considered as normal levels of Hb in women those between 12–16g/dL, and between 37–48% for the hematocrit. An eosinophils proportion up to 4% was considered normal.

All women were asked for a fresh stool sample each for coproparasitological study. The stool samples were masked, coded, and processed for parasitological examination. All stool samples were processed within 2 hours of collection. Isolation of enteric bacterial and viral pathogens was not studied in these samples. Different stool examinations were used for efficacy in detecting parasites. These were direct wet-mount, formaldehyde-ether sedimentation method and modified acid-fast staining techniques [10,11]. The WHO Guide for Diagnosis of Intestinal Parasitosis (1994) was used as an identification reference [12]. All data were collected with a unique structured questionnaire, and then this information was integrated after being sent by electronic mail to a central database.

At clinical evaluations, no apparent significant obstetrical alterations were observed. All women were asymptomatic. All serological studies were negative in all women (HIV, HBV, VDRL, Toxoplasmosis).

Hematological evaluation showed that 65.1% of women presented anemia. The mean hemoglobin levels were g/dL, mean hematocrit was %. Eosinophils relative mean proportion was %. Eosinophilia was seen in 22.3% women. No other alterations were seen in these women.

Intestinal parasitosis was seen in 767 women (73.9%). From this total, 360 (46.9 %) presented infections due to two simultaneous intestinal parasite species, 84 (10.9 %) with three intestinal parasite species, and only 2 women presented infections due to more than three intestinal parasite species (0.3 %).

In this studied group of women, ten different species of intestinal parasites were found, 2 nonpathogenic protozoans, 3 pathogenic protozoans, and 5 helminths species (Table 1). Ascaris lumbricoides was the most common parasite and helminth identified in this study (57.0 %) followed by Trichuris trichiura (36.0 %). From those women with dual infection (360), 104 (28.9 %) corresponded to A lumbricoides with Trichuris.

Univariated and multivariated analyses made to assess risk factors for intestinal parasitosis and related anemia only found significance for the presence of intestinal parasitosis as a risk to have anemia during pregnancy, relative risk (RR) was 2.56 (95%CI 2.13–3.08) (Table 2). When this was adjusted for helminth infection, RR = 1.56 (95%CI 1.43–1.69), and for protozoan infection, RR = 1.49 (95%CI 1.38–1.61). Additionally relative risk was adjusted for helminth species; for A. lumbricoides, RR = 2.01 (95%CI 1.83–2.20); trichiura, RR = 1.18 (95%CI 1.08–1.30); Necator americanus, RR = 1.23 (95%CI 1.07–1.41). Finally, relative risk was also adjusted for dual helminth infections and those due to A lumbricoides and T trichiura, RR = 1.99 (95%CI 1.83–2.15) and RR = 1.60 (95%CI 1.51–1.70), respectively (Table 2). No association was made with any other variable evaluated.

In this study, where more than a thousand young asymptomatic pregnant women were evaluated, we observed a high prevalence of intestinal parasitosis (more than 70%), higher than those previously reported for pregnant women in Congo (9%) [6], Nigeria (12.5%) [5], Mexico (38.2%) [16], Brazil (Sao Paulo State, 45.1%; Rio de Janeiro State, 69.2%) [17, 18], and Indonesia (69.7%) [4]. Although current evaluated women were transversally analyzed and more than 65% had anemia, those with anemia corresponded mainly to infected women (more than 80% of those with anemia). Almost the half of infected women presented mixed infections, due to two different parasite species which represented a significant risk to have anemia, almost twice than those women who did not. But the most important risk factor to be found with anemia in pregnancy at this series was to be simply presented an intestinal parasitic infection at pregnancy (RR = 2.56), independently if this was due helminths or protozoans. Species adjusted analysis showed that for this study the most important parasite representing a risk to be found with anemia at pregnancy was A lumbricoides (RR = 2.01); the risk of anemia has been frequently reported for N americanus, Ancylostoma duodenale, T trichiura, Strongyloides stercoralis and Enterobius vermicularis [7,19,20], but rarely for A lumbricoides [21], which may cause intestinal obstruction, liver abscess, local irritation, and damage with malabsorption as main cellular related events associated with the infection [21,22]; A lumbricoides plays an important role in precipitating protein-energy malnutrition in undernourished children [23], this infectious disease is a form of malnutrition [21]. Those women infected presented not just a higher frequency of anemia but also significant lower levels of hemoglobin and hematocrit and, obviously, higher levels of eosinophilia. This last, at least in this series, evidenced to be a diagnostic marker for intestinal parasitosis, and with it, this type of infection in pregnant women at endemic zones could be suspected, even if a stool screening is negative (which should be repeated at least 3 consecutive times). Intestinal parasites (especially helminths) can be tissue dwelling or intestinal but all induce a dramatic expansion of the Th2 lymphocyte subset [24,25]. It remains unclear whether these Th2-derived responses, including IgE, eosinophilia, and mastocytosis are important in the protective immune response to the parasite, or are responsible for immune-mediated pathology, or both [24], but at least is a paraclinical marker of infection.

Given these results, the importance and potential impacts of intestinal parasitosis at pregnancy, such as the anemia, are quietly obvious. Independently to etiology, parasitoses are associated with conditions for development of anemia at pregnancy [7]. This indicates the need for periodical stool examinations during pregnancy as part of routine laboratory test in the prenatal control of women. Considering this, systematic screening and treatment of anemia and associated factors such as intestinal helminthiasis and protozoasis is needed for the pregnant women population, as has been established in other countries [6], to significantly improve the health of mothers and children, because it is undoubtedly much better to enter a pregnancy free of infection and nutritionally replete than the various alternatives. Existing intervention strategies for micronutrient support and for the control of common parasitic infections before or during pregnancy, particularly intestinal parasitosis, should be followed. However, further research to identify barriers and priority approaches to achieving this goal remain very important in resource-poor settings, where targeted public health efforts are required [3].

As has been stated in other studies, it is necessary to modify some preventive measures of information and education and to give specific treatment before the pregnancy in order to increase some of the pregnant women's health indicators. The newborn of mothers with intestinal parasitosis have a greater probability of being born with less weight than what is expected [16], although we did not evaluate this issue on the current study.

These results enhanced the need for wide implementation of intermittent iron and folic acid supplementation as a valid strategy when used as a preventive intervention in prenatal care settings [14]. But that antihelminthic therapy could be given to infected women before conception as public health strategy to improve iron status may be also considered. Additionally once diagnosed, if the woman is on the second or third gestation trimester, it could be treated. In the current study, all women in this condition were treated with mebendazol 500mg after first trimester, as has been recommend by some authors who consider a possible national strategy for prevention and control is to give a single dose of this drug during the second or third gestation trimesters [26].