It is well-known that exposure to stressors alters the in utero development of a human fetus and has adverse health consequences for the offspring, including a short gestation period, reduced birth weight, increased risk of metabolic, cardiac and psychiatric disease, and overall reduced lifespan (Seckl 1998; Landrigan et al. 2004; Perera et al. 2004; Llop et al. 2010). Populations caught in war-zones or forced to live with severe nutritional restrictions (such as those imposed on the Iraqi population by U.N. sanctions from 1991 to 2003) suffer immediate and chronic stress that leads to long-lasting physical and mental damage. In addition to the harsh effects of sanctions, many Iraqi cities have experienced large-scale bombardment. An accurate tally of the types and volume of ammunition dropped on the Iraqi population is not available. However, reports have indicated that large numbers of bullets have been expended into the Iraqi environment (Buncombe 2011). Thus the environmental contamination of Iraqi cities with materials contained in bullets and bombs may be expected. Toxic metals such as mercury (Hg) and Pb are an integral part of war ammunition and are extensively used in the making of bullets and bombs (Departments of the Army, the Navy, the Air Force, Joint Technical Bulletin 1998; US Department of the Army Technical Manual 1990).

The case study of 56 Fallujah families and the metal analysis of hair samples from this population indicated public contamination with two well-known neurotoxic metals, Pb and Hg. Hair metal data from Fallujah showed Pb to be five times higher in the hair samples of children with birth defects (n = 44; mean ± SD 56,434 ± 217,705 μg/kg) than in the hair of normal children (n = 11; 11,277 ± 27,781 μg/kg). Mercury was six times higher (n = 44; 8,282 ± 25,844 μg/kg Vs n = 11; 1,414 ± 3,853 μg/kg) (Fig. 3). Fallujah mothers who participated in this study did not take any medication and described their diet as “good” during pregnancy. Only one couple was first cousins. Mothers did not drink or smoke during pregnancy. All families consumed water from local aqueducts or locally bottled waters. Siblings of the parents had no history of children with congenital defects. Figure 1 shows a chronological increase in the percentages of birth defects and miscarriages in these Fallujah families. Six photographs of Fallujah children and their conditions are provided in Fig. 2. Mercury and Pb, two toxic metals readily used in the manufacture of present-day bullets and other ammunition, were 6 and 5 times higher in hair samples from Fallujah children with birth defects compared to Fallujah children who appeared normal (Fig. 3). Uranium, Hg and Pb, (μg/kg, mean ± SD) in the hair samples of parents from Italy, Iran, and Fallujah (Iraq), are shown in Fig. 4. Though statistically not significant, the hair of parents of children with birth defects had more uranium, Pb and Hg than the hair of parents of normal children.

Fig. 2 Photos of some birth defects reported from Fallujah General Hospital between May and August 2010. a Gastroschisis, b Hydrocephalus, c Encephalocele, d Macrocephaly, e Spina Bifida; f Cleft lip and palate Full size image

Fig. 3 Mercury and lead, (μg/kg, mean ± SD) in hair samples from Fallujah children compared to children from Italy, Palestine, and Iran Full size image

Fig. 4 Uranium, mercury and lead, (μg/kg, mean ± SD) in hair samples from parents from Italy, Iran, and Fallujah Iraq Full size image

The most common abnormalities in Fallujah children were congenital heart defects (n = 24 out of 46), neural tube defects (n = 18 out of 46), and cleft lip/palate (n = 4 out of 46). Cardiac defects, neural tube defects, and facial clefting are known as folate-dependent birth defects since folate intake reduces their occurrence (MRC Vitamin Study Research Group 1991; Wilson et al. 2003; Obican et al. 2010). The Fallujah study has highlighted the role of metals in the manifestation of the current birth defect epidemic in that city. Recent data has linked metal exposure to oxidative stress and folate deficiency in humans (Wang et al. 2012). We also know that in utero metal exposure can culminate in birth deformities by increasing oxidative stress in the womb as the fetus grows (Apostoli and Catalani 2011).

In general, reports of health problems in the Iraqi population and in the surrounding countries have continued to surface (Rajab et al. 2000). News of increases in childhood cancers, of perinatal and infant morbidity and mortality, and of unusual increases in congenital birth defects, have continued to emerge from across Iraq. Data from a central Iraqi city, Al-Ramadi, have corroborated the Fallujah findings (Al-Ani et al. 2010).

Another Iraqi city where birth defects and cancers continue to climb is Al Basrah.

The earliest data on the occurrence of congenital birth defects in Al Basrah came from an article entitled “Incidence of Congenital Fetal Anomaly in Al Basrah Maternity Hospital” (Alsabbak et al. 1997). This research reported on the total number of live births (10,015) in Al Basrah Maternity Hospital between October 1994 and October 1995. The number of birth defects per 1,000 live births during this period was 1.37. Table 1 contains the yearly account of the number of birth defects per 1,000 live births in Al Basrah Maternity Hospital from 2003 to 2011. Central nervous system related defects occurred most frequently. Statistical analysis of this data has shown no significant difference between the number of children born with anencephaly and the number born with Spina Bifida (p = 0.28). There were significantly more cases of anencephaly than of hydrocephalus, limb deformity, omphalocele, or short extremities (p = 0.009, p = 0.005, p = 0.000, p = 0.000). In addition, the number of Spina Bifida cases was significantly higher than the number of hydrocephalus, limb deformity, omphalocele, or short extremity cases (p = 0.05, p = 0.005, p = 0.000, p = 0.001). Within 8 years, the occurrence of congenital birth defects in Al Basrah Maternity Hospital increased by an astonishing 17-fold.

The prevalence of congenital hydrocephalus in California (US) has been reported as 0.6 per 1,000 (Jeng et al. 2011). Worldwide hydrocephalus affects about one in every 1,000 live births. The reported numbers of hydrocephalus from Al Basrah Maternity Hospital were 3.5 times higher than the world average and six times higher than in the United States. Defects of the abdominal wall, like omphalocele and gastroschisis, were also frequently reported in Al Basrah. Omphalocele generally occurs in 0.25/1,000 live births and is associated with a high rate of mortality and severe malformation, such as cardiac anomalies and neural tube defects. The average number of omphalocele observed in Al Basrah Maternity Hospital between 2003 and 2011 was 3.3/1,000 live births.

Neural tube defects (NTDs) occur very early in human development. The prevalence of NTDs in the mainland United States is 1/1,000 live births (CDC; Williams et al. 2002). Some of the highest numbers of NTDs have been reported from coal mining regions in China (10/1,000) (Li et al. 2006). The occurrence of NTDs in Al Basrah (12/1,000) is the highest ever reported and it is increasing. Our data has shown that in Al Basrah, the total number of birth defects more than doubled between 2003 and 2009.

A comparison between the metal levels in the hair (n = 6) and toenail (n = 7) of parents of children with birth defects from Al Basrah, and the associated p values, has been presented in Table 2. For most metals (Al, Mn, Co, Cu, Zn, Mo, Pb, Th, and U), hair contained significantly higher amounts of the metal than did toenail, suggesting that hair is a better biomarker of exposure. Examining the Pb hair levels of parents from Al Basrah and Fallujah revealed that the hair of parents of children with birth defects in Al Basrah had 6,500 ± 8,589 (μg/kg); in Fallujah this value was 3,950 ± 3,133 μg/kg; both values being considerably higher than Pb found in the hair samples of parents of normal children from Fallujah (2,012 ± 2,052 μg/kg). The 1.6-fold higher Pb in the Al Basrah parents’ hair compared to Fallujah parents’ hair may be explained by the fact that Al Basrah is an oil-industry dominated area whereas Fallujah is not. Overall, parents of children with birth defects from Al Basrah and Fallujah had twofold, and one-fold, higher Pb in their hair than did parents of normal children respectively. Al Basrah parents who had children with birth defects also had 1.4 times higher enamel Pb (n = 5, 2,497 ± 1,400) than did parents of normal children (n = 5, 1,826 ± 1,619). Additional samples of teeth from the parents of children with and without birth defects from Al Basrah are necessary to help draw reliable statistical conclusions for this population.

Table 2 Comparison of metal levels in hair verses toenail from parents of children with birth defects from Al Basrah, Iraq Full size table

Table 3 contains a literature review of the metal levels in whole deciduous teeth of children from different geographical locations. Enamel is a hard and dense material which is formed during fetal life and it receives small amounts of systemic blood flow thereafter. For this reason it is considered to primarily reflect prenatal exposure to metals. Whole-tooth metal analysis would include enamel, dentin, cementum, and dental pulp. The impact of living in a large city with dangerous levels of air pollution is evident in the high levels of Pb in teeth from Mexico City and Karachi. Similarly, the level of Pb in teeth from Canadian mining areas is indicative of an exposed or impacted population. Mean whole tooth Pb reported from other locations was 1.5 μg/g. Hence, the tooth Pb level of an unimpacted population is more accurately estimated by this 1.5 μg/g value. The enamel portion of the deciduous tooth from a child with birth defects from Al Basrah (4.19 μg/g) had nearly three times higher Pb than the calculated value for a whole tooth from an unimpacted population. Additional samples of deciduous teeth from Al Basrah children with birth defects are necessary to help draw reliable statistical conclusions for this population. Samples of deciduous teeth are currently being collected from impacted (Al Basrah, Iraq) and unimpacted (Isfahan, Iran) areas to enable us to draw meaningful conclusions in this regard. Interestingly, mining, smelting, and living near industry or hazardous waste sites have all been associated with an increased risk of birth defects (Ahern et al. 2011; Zheng et al. 2012; Suarez et al. 2007).

Table 3 A literature review of selected metal levels in the whole deciduous teeth of children from various geographical locations verses the sample from Al Basrah, Iraq Full size table

Present knowledge on the effects of prenatal exposure to metals, combined with our results, suggests that the bombardment of Al Basrah and Fallujah may have exacerbated public exposure to metals, possibly culminating in the current epidemic of birth defects. Large-scale epidemiological studies are necessary to identify at-risk populations in Iraq. The recognition that birth defects reported from Iraq are mainly folate-dependent offers possible treatment options to protect at-risk populations.