Cystic Echinococcosis in Children and Adults: A Seven-Year Comparative Study in Western Romania

Abstract

This study aims to compare the epidemiological, clinical, and laboratory aspects of cystic echinococcosis (CE) in children with those of adults from western Romania, and to determine the specifics of this disease in the younger population. The medical records of the patients diagnosed with CE and hospitalized during 2004–2010 in four western Romanian counties were retrospectively investigated. Overall, 82 children (mean age, 10.8 years) and 369 adults (mean age, 48 years) were diagnosed with CE during the study period. The yearly detection rate was 3.1/100,000 children and 3.4/100,000 adults. The incidence rate registered a peak in children aged 5–14 years (4.4/100,000) and adults aged 60–69 years (5/100,000). Female to male ratio was 1.6:1 in pediatric cases and 1.2:1 in adults. CE was almost twice more frequent in rural areas (4.4/100,000 children and 4.9/100,000 adults) as compared to urban regions (2.3/100,000 children and 2.6/100,000 adults). Hepatic cysts were found more frequently than pulmonary cysts, at a ratio of 3.6:1 in children and 12.8:1 in adults. Most of the cases had no complications (91.5% of children and 87% of adults). Children had higher eosinophil count (7%) and erythrocyte sedimentation rate (ESR) (29.7 mm/h) as compared with adults (eosinophil count, 5.3%, p<0.001; ESR, 22.4 mm/h, p=0.001). The active transmission of the parasite in western Romania is demonstrated by the high incidence of CE in children. Long-term prevention of this disease may be reached through joined legislative efforts focused on the registration of dogs, home slaughter of sheep and swine, veterinary control in abattoirs, destruction of infected materials, and restriction of dogs' access to vegetable gardens and children's parks.

Introduction

C ystic echinococcosis (CE), also known as hydatid disease or hydatidosis, is a foodborne parasitic disease highly prevalent in regions of Eurasia, Africa, Australia, and South America (King and Fairley, 2010; Brunetti and White, Jr., 2012). Following recent estimations, Echinococcus granulosus—the disease pathogen—is responsible for infections in up to 2–6% of endemic populations, and the yearly incidence is still on the rise in some European countries (King and Fairley, 2010). The asymptomatic presentation of the disease occurs frequently, and often the hydatid cysts are incidentally detected during screening abdominal echographies or necropsies. The symptomatology may vary largely and is never pathognomonic. The particular clinical picture depends upon the cystic location, size, and condition (Schantz et al., 2011). Most of the cysts are detected within the liver (55–75%) and lung (10–30%) (Cummings et al., 2009). Generally, the symptoms of slow-increasing pressure in the cyst-area accompanied by an increased percentage of eosinophils in a patient from an endemic region are suggestive for hydatid infection (Muller and Wakelin, 2002). Imaging techniques (particularly ultrasonography and chest x-ray) are the main diagnostic methods, and serologic tests (enzyme-linked immunosorbent assay [ELISA]), indirect hemagglutination [IHA], and Western Blot) are used to confirm the presumptive diagnoses established by the former (Brunetti and White, Jr., 2012). Besides surgery (the only therapeutic method until recently), chemotherapy with benzimidazoles and cyst puncture, percutaneous aspiration, injection of chemicals, and reaspiration (PAIR) technique are used nowadays on a large scale as an addition or even a replacement of the classical option (Schantz et al., 2011).

In Romania, CE is a significant parasitic disease in both children and adults. It has been shown that at least one person from 45.5% of the Romanian townships underwent surgery for this condition (Neghina et al., 2010a, 2011).

This study aims to bring new valuable data on human CE in western Romania by comparing the epidemiological, clinical, and laboratory aspects of hydatidosis in children with those of adults, and to determine the specifics of this disease in the younger population.

Patients and Methods

We have retrospectively investigated the medical records of patients from four western Romanian counties (Timis, Arad, Caras-Severin, and Hunedoara) diagnosed with CE, who were hospitalized in surgical (and in some cases infectious disease/internal medicine) sections of the county and municipal hospitals in Arad, Deva, Petrosani, Resita and Timisoara between 2004 and 2010 (see Supplementary Fig. S1; Supplementary Data are available online at www.liebertpub.com/fpd).

The diagnosis of CE was based on imaging techniques (ultrasonography, radiology, computed tomography scan, magnetic resonance imaging) as the principal criterion, and additionally on serology (detection of anti-Echinococcus granulosus antibodies by ELISA). For hepatic cysts, abdominal ultrasonography was the golden diagnostic criterion according to the standard classification proposed by the World Health Organization–Informal Working Group on Echinococcosis (WHO-IWGE) (Eckert et al., 2002). The annual incidence of CE in western Romania was calculated by using all cases hospitalized each year divided by the total population as provided by the Romanian Census Bureau (INS, 2003). The specific annual incidences of age, sex, and rural versus urban inhabitance were also calculated (in cases per 100,000 inhabitants; or cases/100,000).

Statistical analysis

The statistical analysis was performed using the software package SPSS version 17.0 for Windows (SPSS Inc., Chicago, IL). Descriptive statistics were calculated for each variable as appropriate. Standard binomial tests for differences in proportions and Mann-Whitney U statistics for quantitative data were used to compare patient subgroups. Trends over time for the infection rates of children and adults were determined by linear regression analysis. A p-value of <0.05 was regarded as statistically significant.

Results

CE was diagnosed in 451 patients, of whom 82 were children (18.2%) and 369 were adults (81.8%). The mean age was 10.8 years (range, 4 months to 17 years) in children and 48 years (range, 18–88 years) in adults. Most of the affected children were in the age range of 10–14 years (40.2%), whereas most of the affected adults were 50–59 years old (22%). The lowest number of cases was noted in children aged 0–4 years (1.2%) and adults over 80 years old (2.2%).

The incidence rate registered a peak in children aged 5–14 years (4.4/100,000) and adults aged 60–69 years (5/100,000). Overall, the incidence of CE cases registered a general ascending trend in adults aged 18–69 years (R²=0.98, p=0.001) (Table 1).

Table 1.

Human Cystic Echinococcosis Cases in Western Romania in 2004–2010 by Age Group, Inhabitance Area, and Gender

	No. of cases and [mean annual incidence, in cases/100,000 inhabitants]
	Urban inhabitants			Rural inhabitants			Total cases
Age group (years)	Male	Female	Total	Male	Female	Total	Male	Female	Total
Children
0–4	1 [0.5]	0	1 [0.3]	0	0	0	1 [0.3]	0	1 [0.2]
5–9	4 [2]	5 [2.3]	9 [2.2]	7 [6.1]	13 [10.5]	20 [8.4]	11 [3.5]	18 [5.3]	29 [4.4]
10–14	7 [3]	14 [5.6]	21 [4.4]	3 [2.3]	9 [6.3]	12 [4.4]	10 [2.7]	23 [5.9]	33 [4.4]
15–17	3 [1.5]	5 [2.4]	8 [2]	7 [6.2]	4 [3.3]	11 [4.7]	10 [3.2]	9 [2.7]	19 [3]
Total	15 [1.8]	24 [2.7]	39 [2.3]	17 [3.6]	26 [5.2]	43 [4.4]	32 [2.5]	50 [3.6]	82 [3.1]
Adults
18–29	10 [1.3]	16 [2]	26 [1.7]	12 [2.8]	17 [3.7]	29 [3.2]	22 [1.9]	33 [2.6]	55 [2.2]
30–39	17 [2.5]	13 [1.8]	30 [2.2]	21 [5.5]	18 [4.4]	39 [4.9]	38 [3.6]	31 [2.7]	69 [3.2]
40–49	15 [2.7]	22 [3.7]	37 [3.2]	14 [4.4]	12 [3.5]	26 [3.9]	29 [3.3]	34 [3.6]	63 [3.5]
50–59	15 [2.7]	24 [4]	39 [3.4]	15 [4.7]	27 [7.8]	42 [6.3]	30 [3.4]	51 [5.4]	81 [4.4]
60–69	11 [2.8]	16 [3.7]	27 [3.3]	21 [9.2]	17 [7]	38 [8]	32 [5.1]	33 [4.9]	65 [5]
70–79	5 [1.7]	8 [2.6]	13 [2.2]	7 [4.2]	8 [4.5]	15 [4.4]	12 [2.6]	16 [3.3]	28 [3]
≥80	1 [1]	4 [3.8]	5 [2.5]	1 [1.8]	2 [3.4]	3 [2.6]	2 [1.3]	6 [3.7]	8 [2.5]
Total	74 [2.2]	103 [2.9]	177 [2.6]	91 [4.8]	101 [4.9]	192 [4.9]	165 [3.1]	204 [3.6]	369 [3.4]

The highest infection rates of CE occurred in 2004 in adults (4.4/100,000) and 2005 in children (5/100,000). The lowest infection rates occurred in 2010 (2.6/100,000 adults and 1.1/100,000 children (Fig. 1).

FIG. 1.

Distribution of child and adult cases over the studied period (2004–2010).

The yearly detection rate of new cases was 3.1/100,000 children and 3.4/100,000 adults. Overall, females were slightly more frequently affected (3.6/100,000 children and 3.6/100,000 adults) than males (2.5/100,000 children and 3.1/100,000 adults).

CE was almost twice more frequent in rural areas (4.4/100,000 children and 4.9/100,000 adults) as compared to urban regions (2.3/100,000 children and 2.6/100,000 adults) (Table 1).

The ratio of single to multiple organ infection was 9.4:1 in cases aged under 18 years and 16:1 in adult patients (see Supplementary Table S1).

Overall, liver involvement occurred more frequently in adult cases (83.5%) as compared to children (70.7%, p=0.012) (Table 2). Single infection of the lungs as well as multiple infection of the liver, lung, and kidney predominated in children as compared with adults (19.5% vs. 6.5%, p<0.001; and 2.4% vs. 0%, p=0.04, respectively). At a separate analysis, lung involvement predominated in children living in urban regions (20.5% vs. 5.1%, p=0.004), whereas liver, lung, and kidney involvement was found in children living in rural regions only (4.7% vs. 0, p=0.035). Pulmonary cysts were significantly more common in female children (28%) than in male children (6.3%, p=0.03).

Table 2.

Comparison of Clinical and Laboratory Findings Between Children and Adults with Cystic Echinococcosis

Variable		Children ^a	Adults ^a	p
Localization of the hydatid cyst	Liver (0)	58 (70.7)	308 (83.5)	0.012
	Lungs (1)	16 (19.5)	24 (6.5)	<0.001
	Spleen (2)	1 (1.2)	5 (1.4)	NS
	Kidney (3)	0	2 (0.5)	NS
	Peritoneum (7)	0	4 (1.1)	NS
	Femur (11)	0	2 (0.5)	NS
	Liver and lungs (4)	5 (6.1)	17 (4.6)	NS
	Liver and pelvis (5)	0	1 (0.3)	NS
	Liver and kidney (6)	0	2 (0.5)	NS
	Liver and spleen (9)	0	3 (0.8)	NS
	Liver and biliary tract (10)	0	1 (0.3)	NS
	Liver, lungs, and kidney (8)	2 (2.4)	0	0.04
Complications	None (0)	75 (91.5)	321 (87)	NS
	Rupture (1)	3 (3.7)	22 (6)	NS
	Liver abscess (2)	0	14 (3.8)	NS
	Mechanical icterus (3)	0	1 (0.3)	NS
	Diaphragmatic abscess (4)	0	1 (0.3)	NS
	Superinfection (without other specifications) (5)	4 (4.9)	10 (2.7)	NS
Eosinophil counts (%)^b	<5	32 (41)	224 (69.3)	<0.001
	≥5	46 (59)	99 (30.7)
Leukocyte counts (cells/mm³)^c	<10,000	61 (74.4)	271 (73.8)	NS
	≥10,000	21 (25.6)	96 (26.2)
Erytrocyte sedimentation rate (mm/h)^d	≤10	25 (31.3)	166 (49)	0.006
	>10	55 (68.7)	173 (51)
Length of hospital stay (days)	1–7	32 (39)	110 (29.8)	NS
	8–14	20 (24.4)	114 (30.9)	NS
	15–29	23 (28)	116 (31.4)	NS
	≥30	7 (8.5)	29 (7.9)	NS

Numbers in parentheses, percent of total cases (82 children and 369 adults unless otherwise specified).

Reported in 78 children and 323 adults.

Reported in 82 children and 367 adults.

Reported in 80 children and 339 adults.

NS, nonsignificant.

Most of the cases had no complications (91.5% of children and 87% of adults) (Table 2). Of complicated cases, 62.7% were adults with liver involvement.

Generally, children had higher eosinophil count (7%, range of 1–28) and erythrocyte sedimentation rate (ESR) (29.7 mm/h, range of 2–135) as compared with adults (eosinophil count of 5.3%, range of 1–70, p<0.001; ESR of 22.4 mm/h, range of 0–140, p=0.001) (see Supplementary Table S2). Most of the children (59%) and almost one third of the adults (30.7%) had eosinophil counts of ≥5%. ESR values higher than 10 mm/h predominated in children (68.7%) as well as adults (51%) with CE (Table 2).

Pediatric and adult cases with multiple liver and lung involvement had the highest eosinophil count (11%, range of 7–15; and 11%, range of 1–70, respectively), whereas those with lung involvement had the highest ESR (35.3 mm/h, range of 2–95; and 42.8 mm/h, range of 5–120, respectively). The average leukocyte count was <10,000 cells/mm³ regardless of age, gender, and the affected organ (see Supplementary Table S2).

The hospitalization period was similar in children (13.4 days, range of 2–49) and adult cases (14.1 days, range of 1–65). Male adults required significantly longer hospital stay (15.2 days, range of 2–65) as compared with female adults (13.1 days, range of 1–58, p=0.047) (see Supplementary Table S2). This may be explained by the predominance of liver involvement among adult cases (83.5%) of whom males had more complications (17.6%) than females (7.9%, p=0.01).

A 57-year-old man with liver involvement died because of other comorbidities.

Discussion

Over a period of 7 years (2004–2010), the annual average incidence of CE was similar in children and adults in western Romania, although the former accounted for 18.2% of all CE cases only.

The incidence rates reported in this survey fit within the range for the entire Europe (1–8/100,000) (Mandal and Mandal, 2012). In Bulgaria, a country that borders Romania to the south, the annual incidence of CE among adults (3.12/100 000) is similar to that reported in this study, but this figure is lower in Bulgarian children (1.48/100 000) (Todorov and Boeva, 2000) as compared to the Romanian ones. CE was highly endemic (15–27/100 000) in some regions of southern Bulgaria during the period of 1991–2000 (Kurdova, 2001), but as a result of the national control program for CE implemented between 2004 and 2008 the average incidence rate in the country declined to 5.6/100,000 in 2008 (Kurdova, 2010). Nowadays, CE is most intensely endemic in parts of Spain, southern Italy and Sardinia (Conchedda et al., 2010; Dakkak, 2010; Mastrandrea et al., 2012).

The mean age of pediatric cases in this study is similar to that reported by a study performed in Serbia (10.1 years old) (Djuricic et al., 2010), a country that borders Romania to the southwest. The mean age of adult patients fit within the figures reported by other studies (42.2–47.3 years old) (Tsaroucha et al., 2005; Dopchiz et al., 2007; Inan et al., 2007).

The distribution of our pediatric patients by age is similar to the distribution of infected children in Serbia (Djuricic et al., 2010), Bulgaria (Todorov and Boeva, 2000), and the south-east of Buenos Aires province, Argentina (Dopchiz et al., 2009). CE is rarely identified in patients under 4 years old (Matsaniotis et al., 1983; Zahawi et al., 1999; Todorov and Boeva, 2000; Tiaoying et al., 2005; Dopchiz et al., 2009; Gonlugur et al., 2009; Miman et al., 2010), and only one infected child in our study was in the 0–4 year age group. Previous studies have shown both decrease and increase of CE cases with patients' age (Karpathios et al., 1985; Shambesh et al., 1999; Zahawi et al., 1999; Todorov and Boeva, 2000; Tiaoying et al., 2005; Oudni-M'Rad et al., 2007; Dopchiz et al., 2009; Djuricic et al., 2010; Ernest et al., 2010; ECDC, 2010; Al-Shibani et al., 2012), but this study did not show a trend in either direction. Female to male ratio was 1.6:1 in pediatric cases and 1.2:1 in adults with CE. Female predominance was also reported in other studies performed in children (Inan et al., 2007; Al-Shibani et al., 2012) and adults (Karpathios et al., 1985; Todorov and Boeva, 2000; Al-Qaoud et al., 2003; Tsaroucha et al., 2005; Inan et al., 2007; Pierangeli et al., 2007; Rostami Nejad et al., 2007; Ahmadi and Hamidi, 2008). The proportion of females to males with CE in any given group is determined by local customs involving the housing, contact with contaminated vegetables, and handling of dog's feces in contaminated soil (Al-Shibani et al., 2012). In Romania, women are more active in herding and cooking, and most of them use hygienically poor practices, especially in rural areas (Neghina et al., 2010b).

CE is generally considered a rural disease because of the characteristics of the parasite life cycle, which involves domestic herbivorous animals (e.g., cattle, sheep) and dogs (McManus et al., 2003). The significantly higher incidence rates in rural inhabitants reported in this study may be due to their poor compliance with the hygienic rules and close contact with animals (Neghina et al., 2010b). The average prevalence of infection in dogs from the entire Romania (1956–1992) was estimated at 21.6%. During 2001–2004, Veterinary and Food Safety Authorities reported that 19% of cattle, 12.7% of sheep, 3.8% of swine, and 12.1% of horses that were slaughtered in Romania were infected (Neghina et al., 2010a).

Single organ involvement was more prevalent in this study as compared to the reports of Conchedda et al. (2010) (single to multiple organ involvement ratios of 8.1:1 in persons under 20 years old and 7.7:1 in adults), Talaiezadeh and Maraghi (2006) (5.7:1 in children), and Oudni-M'Rad et al. (2007) (4.3:1 in children). The highest single to multiple organ involvement ratios were reported by Al-Shibani et al. (2012) (38.1:1 in cases under 20 years old and 111.2:1 in adult patients).

Hepatic cysts were found more frequently than pulmonary cysts, at a ratio of 3.6:1 in children and 12.8:1 in adults. These figures are much higher than those reported by other studies either in children (Matsaniotis et al., 1983; Kalani et al., 1984; Chaouachi et al., 1989; Todorov and Boeva, 2000; Talaiezadeh and Paziar, 2006; Oudni-M'Rad et al., 2007; Dopchiz et al., 2009; Djuricic et al., 2010) or adults (Todorov and Boeva, 2000). Pathophysiological influences on the anatomic location of cysts are still unknown (Zahawi et al., 1999); however, it is likely that the liver is more commonly infected because oncospheres penetrating the intestinal wall are preferentially disseminated to the liver via the portal vein (Djuricic et al., 2010).

The ratio of lung/liver involvement was higher in children (0.28) than in adults (0.08) in accordance with the data published in the literature (Todorov and Boeva, 2000; Santivanez and Garcia, 2010).

We have found combined liver and lung involvement in 6.1% of children and 4.6% of adults, similar to other studies performed in children (6–16%) (Talaiezadeh and Paziar, 2006; Oudni-M'Rad et al., 2007; Djuricic et al., 2010) and adults (4%) (Tsaroucha et al., 2005; Talaiezadeh and Paziar, 2006).

The frequency of hepatic and lung cysts is particularly important as it has been estimated that, at 2 years after medical treatment initiation, 40% of these cysts are still active or become active again (Stojkovic et al., 2009), which leads to psychical and physical impairments as well as major socioeconomic distress.

The literature suggests that the prevalence of hydatid cysts in uncommon anatomic locations (i.e., other than the liver and lungs) is lower in children (4.5–9.4%) (Durakbasa et al., 2006; Oudni-M'Rad et al., 2007; Djuricic et al., 2010) than in adults (17.8%) (Tsaroucha et al., 2005). In our study, the prevalence of CE in uncommon anatomic locations was 3.6% in children and 5.4% in adults, with spleen being the most frequent site of infection (1.2% of children and 2.2% of adults), followed by kidney (1% of adults). These findings fit within the prevalence range reported in the literature for spleen (0.9–8%) and kidney (1–6.1%) involvement (Prousalidis et al., 1998; Zahawi et al., 1999; Col et al., 2003; Hamamci et al., 2004; Tsaroucha et al., 2005; Oudni-M'Rad et al., 2007; Rostami Nejad et al., 2007; Dopchiz et al., 2009; Moreno et al., 2009; Djuricic et al., 2010; Sarkari et al., 2010; Ernest et al., 2010).

Few studies report on eosinophil counts and ESR values in cases with hydatidosis (Safioleas et al., 1999; Col et al., 2003; Ahmadi and Hamidi, 2008; Gonlugur et al., 2009). In their review, Moro and Schantz (2009) estimated that eosinophilia occurs in <25% of CE cases. When the results of this study were analyzed and compared to those of Cubas-Castillo et al. (2011), which included patients with hepatic CE older than 17 years, similar figures were noticed with respect to eosinophil counts of >10% (10.3% vs. 9% of cases) and ESR <50 mm/h (38.6% vs. 40% of cases). The only difference was that ESR values of 50–100 mm/h were less frequent in patients over 17 years old with liver CE from this study (10.5%) as compared to the study of Cubas-Castillo et al. (2011) (23%, p=0.017). On the other hand, 30% of CE cases older than 17 years, with lung involvement reported in this study, had ESR values between 50 and 100 mm/h.

The average hospitalization period was longer in this study as compared to other reports in children (11 days) (Dopchiz et al., 2009) and adults (12 days) (Cubas-Castillo et al., 2011). In Romania, the costs for the management of CE were estimated at about 1500–2000 USD for an uncomplicated case and approximately twice more (3000 USD) for a complicated case (Neghina et al., 2011). Therefore, besides physical and psychical impairments that may impact negatively on patients' life, CE consumes considerable healthcare resources, and these may be fully preventable through an efficient social awareness campaign.

Generally, the exact incidence of CE is unknown because most epidemiologic reports are based on hospital-based surveys, which underestimate the actual rates of infection, especially in low socio-economic groups with limited resources (Brunetti and White, Jr., 2012). Thus, the figures presented in this report may be underestimated. Hydatid disease is preventable, and education is one of the most effective tools to achieve this. Special attention should be given to the young population, because the overall high incidence of CE in children demonstrates the active transmission of the parasite in western Romania. Legislative efforts should be made for the registration of dogs, home slaughter of sheep and swine, veterinary control in abattoirs, destruction of infected materials, and restriction of dogs' access to vegetable gardens, public gardens, and children's parks. Therefore, the control of this parasite in the studied region requires long-term cooperation between public health, agriculture, and local authorities in order to o achieve significant decrease in prevalence or eradication.

Footnotes

Disclosure Statement

No competing financial interests exist.

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