Intestinal Nematode Infections in Romania: An Epidemiological Study and Brief Review of Literature

Abstract

Objectives:

The main aim of this report was to present the epidemiological, clinical, laboratory, and therapeutic aspects of a series of patients admitted to a reference hospital from Romania and found to be infected with intestinal nematodes. Additionally, we attempted to overview, for the first time in the international literature, the most relevant data regarding diseases caused by these helminthes in Romania.

Patients and Methods:

Results:

Forty-two patients were found to be infected with intestinal nematode worms, with the predominance of Enterobius vermicularis (42.8%). The mean age of patients in this series was 23.5 ± 16.4 years. Women were affected in 66.7% of cases and inhabitants of urban regions in 71.4% of cases. Of this series, 57.2% of patients were adults and most of them were people with limited formal education belonging to the low social class. Overall, abdominal pain was most frequently detected (59.5%) and the mean eosinophil count was 8.2% ± 10.9% (range 1%–56%). Piperazine was administered in most of the cases (33.3%).

Conclusions:

Infections with intestinal nematodes are less frequently diagnosed in hospitalized patients despite that they are quite common in the Romanian population. To further limit their occurrence, public health measures and informative campaigns for the whole population should be implemented.

Introduction

I ntestinal worms belonging to Phylum Nematoda can produce pathological manifestations in humans acting in either the small or large intestine. The most common species that may inhabit the small intestine are Ascaris lumbricoides (round worm), Strongyloides stercoralis (threadworm), Ancylostoma duodenale, and Necator americanus (both known as hookworms), whereas the large intestine may be inhabited by Trichuris trichura (whipworm) and Enterobius vermicularis (pinworm) (John and Petri 2006). The transmission of human infections occurs by ingestion of eggs in case of A. lumbricoides, T. trichiura, and E. vermicularis, or transcutaneously for the rest of helminthes (John and Petri 2006). Generally, intestinal nematodes cause clinical disease and severe symptoms only in case of intense infections (Gillespie 2001). Although these affections are usually well tolerated and rarely cause life-threatening complications (Gillespie 2001), they may have dramatic consequences especially on children's health and development.

The main aim of this report was to present the epidemiological, clinical, laboratory, and therapeutic aspects of a series of patients admitted to a reference infectious disease hospital from western Romania and found to be infected with intestinal nematodes. Additionally, we attempted to overview, for the first time in the international literature, the most relevant data regarding diseases produced by intestinal nematodes in Romania.

Patients and Methods

We have retrospectively investigated the medical records of patients admitted at Victor Babes Hospital of Infectious Diseases in Timisoara (Timis County) who presented infections with intestinal nematode helminthes. Data were collected beginning with 1971 (first year when the medical documents were available in the hospital's archive) until 2007.

The laboratory methods used in the diagnosis of parasitic infections included microscopic stool examination (iodine staining and Willis-Hung concentration method) in 28 cases (66.7%), macro/microscopic examination of the helminthes eliminated by stool or vomiting in 9 cases (21.4%), both methods mentioned above in 3 cases (7.1%), and the coal culture method in 2 cases (4.8%).

The brief overview of intestinal nematode helminthiases in Romania was based on reports published by Romanian authors in national and international journals and books.

Statistical evaluation was performed using the software package SPSS version 15.0 for Windows (SPSS Inc., Chicago, IL). Descriptive statistics (percentage, mean, and standard deviation) were calculated for each variable, as appropriate. Comparisons between patient subgroups were made by means of Mann–Whitney U statistics for quantitative data. A p-value of <0.05 was regarded as statistically significant.

Results

Forty-two patients were found to be infected with the following intestinal nematode worms: E. vermicularis (42.8%), A. lumbricoides (35.7%), T. trichiura (9.5%), S. stercoralis (4.8%), and 7.2% had coinfections with A. lumbricoides and T. trichiura, A. lumbricoides and E. vermicularis, and E. vermicularis and T. trichiura. Detailed demographical, clinical, and laboratory characteristics of this series are shown in Table 1.

Table 1.

Characteristics of Patients Included in the Study

Variable					Coinfections
Disease	Ascariasis, n = 15 (c/a)	Trichuriasis, n = 4 (c/a)	Enterobiasis, n = 18 (c/a)	Strongyloidiasis, n = 2	AE, n = 1	AT, n = 1	ET, n = 1	Total (%), n = 42
Age
Children (0–17 years)	5	2	9	—	—	1	1	18 (42.8)
Adults (≥18 years)	10	2	9	2	1	—	—	24 (57.2)
Mean ± SD (years)	24.9 ± 17.7	25 ± 18.9	20.6 ± 14.5	49.5 ± 0.7		14.3 ± 8.7		23.5 ± 16.4
Sex
Female	7 (3/4)	3 (2/1)	13 (6/7)	2	1	1	1	28 (66.7)
Male	8 (2/6)	1 (0/1)	5 (3/2)	—	—	—	—	14 (33.3)
Area of inhabitance
Rural	5 (1/4)	2 (1/1)	3 (3/0)	—	1	1	—	12 (28.6)
Urban	10 (4/6)	2 (1/1)	15 (6/9)	2	—	—	1	30 (71.4)
Symptoms^a
Abdominal pain	6 (2/4)	4 (2/2)	10 (6/4)	2	1	1	1	25 (59.5)
Anal pruritus	1 (1/0)	—	2 (1/1)	—	—	—	—	3 (7.1)
Asthenia	3 (0/3)	2 (1/1)	6 (3/3)	1	—	—	1	13 (30.1)
Constipation	—	—	1 (1/0)	—	—	—	—	1 (2.4)
Cough	3 (1/2)	—	—	—	—	—	—	3 (7.1)
Diarrhea	7 (2/5)	1 (0/1)	3 (1/2)	—	—	—	—	11 (26.2)
Dizziness	1 (0/1)	—	1 (0/1)	1	—	—	—	3 (7.1)
Fever	4 (2/2)	—	8 (3/5)	—	—	—	—	12 (28.6)
Headache	1 (0/1)	—	2 (1/1)	—	—	1	—	4 (9.5)
Hepatomegaly	2 (1/1)	—	—	—	—	—	—	2 (4.8)
Icterus	1 (0/1)	—	—	—	—	—	—	2 (4.8)
Loss of appetite	5 (2/3)	3 (1/2)	5 (3/2)	2	—	1	—	16 (38.1)
Nausea	4 (2/2)	2 (1/1)	8 (4/4)	2	—	—	—	16 (38.1)
Tenesmus	—	—	1 (0/1)	—	—	—	—	1 (2.4)
Urticaria	2 (1/1)	1 (1/0)	3 (3/0)		—	—	—	6 (14.3)
Vomiting	2 (0/2)	—	7 (3/4)	2	—	—	—	11 (26.2)
Weight loss	1 (0/1)	—	1 (0/1)	—	—	1	—	3 (7.1)
Eosinophil counts^b
<5%	9 (4/5)	—	5 (2/3)	1	—	—	—	15 (50)
≥5%	2 (1/1)	2 (1/1)	7 (4/3)	1	1	1	1	15 (50)
Mean ± SD (%)	3.7 ± 3	9.5 ± 6.4	7.3 ± 6.4	13.5 ± 16.3	23.7 ± 28			8.2 ± 10.9
Erytrocyte sedimentation rate^c
<10 mm/h	—	—	—	—	—	—	—	—
≥10 mm/h	5 (1/4)	—	8 (4/4)	1	—	—	—	14 (100)
Mean ± SD (mm/h)	46.4 ± 33.6	—	25 ± 20.2	NA		—		31.6 ± 26.7

Listed symptoms are not mutually exclusive.

Reported in 30 cases of the study group (14 children and 16 adults).

Reported in 14 cases of the study group (5 children and 9 adults).

%, percent of total cases (n = 42) unless otherwise specified; a, adults; AE, Ascaris lumbricoides and Enterobius vermicularis coinfection; AT, A. lumbricoides and Trichuris trichiura coinfection; c, children; ET, E. vermicularis and T. trichiura coinfection; n, total number of cases with the disease; NA, not applicable; SD, standard deviation.

The mean age of the patients was 23.5 ± 16.4 years (range 4 months–51 years). Overall, women and inhabitants of urban regions were predominantly affected (66.7% and 71.4%, respectively). Ascariasis predominated in patients from rural areas (41.7%); moreover, two out of three cases with nematode coinfections were inhabitants of rural regions and both had ascariasis.

Most of the cases were adults (57.2%) and their professional status was as follows: laborers (41.7%), unemployed (20.8%), retired (8.3%), intellectuals/office workers (4.2%), other categories (12.5%), and unspecified (12.5%).

Abdominal pain prevailed in patients with trichuriasis (100%) and enterobiasis (55.6%). Most of the patients with ascariasis had diarrhea (46.7%) and abdominal pain (40%). Both patients with strongyloidiasis had abdominal pain, loss of appetite, weight loss, and nausea.

Coinfections with protozoans were identified in three cases: T. trichiura and Giardia lamblia, E. vermicularis and G. lamblia, and S. stercoralis and Blastocystis hominis.

The mean hospital stay was 10.5 ± 5.5 days (range 3–25 days).

Where available, routine laboratory parameters such as eosinophil count and erythrocyte sedimentation rate (ESR) were analyzed. The mean eosinophil count was 8.2% ± 10.9% (range 1–56); the mean ESR was 31.6 ± 26.7 mm/h (range 10–92). Patients with coinfections had the highest eosinophil count (23.7% ± 28%, range 6–56), whereas those with ascariasis had the lowest eosinophil count (3.73% ± 3%, range 2–11, p = 0.03) and the highest ESR value (46.4 ± 33.6 mm/h, range 10–92).

Drugs administered against the nematode helminthes included piperazine (33.3%), mebendazole (19%), pyrvinium (4.8%), metronidazole (4.8%), thiabendazole (4.8%), and gentian violet (Oxiuran) (4.8%). The above-listed drugs are not mutually exclusive because in some cases initial treatment was changed during hospitalization. After therapy, all patients had favorable outcomes.

Discussion

Infections with A. lumbricoides have been long known in Romania. The first case of infection with this worm was described in 1872 (Olteanu et al. 1999). The reported prevalence of ascariasis varies largely in the Romanian population (4%–82%), being generally higher in children (Table 2) (Dancescu 1968, Panaitescu et al. 1995, Olteanu et al. 1999, Varga et al. 2001, Neghina et al. 2006, 2010). Similarly to a previous survey performed in a neighboring county—Caras Severin (Neghina et al. 2010), the present study performed in Timis County shows that A. lumbricoides is one of the most frequent etiologic agent of intestinal nematode infections in hospitalized patients.

Table 2.

Overview of Relevant Romanian Reports on Intestinal Nematodes

Source	Intestinal nematode	Year(s)	Region	Study group	Prevalence
Dancescu (1968)	A. lumbricoides	1966	—	755	23.40%(range 12.9%–31.4%)
Olteanu et al. (1999)	A. lumbricoides	1968	Entire country	—	Mean 51.9% (range 20.9%–79%) for the entire population, and mean 63.3% (range 31.3%–83.5%) among infections with intestinal helminthes
Olteanu et al. (1999)	A. lumbricoides	1968	—	286	51.70%
Olteanu et al. (1999)	A. lumbricoides	1991	Entire country	—	4%–62% in the entire population and over 82% in the sub-Carpathian population
Panaitescu et al. (1995)	A. lumbricoides	—	—	231 children with disabilities found with 294 parasitic infections	39.90%
Varga et al. (2001)	A. lumbricoides	2001	Transylvania	55 children	69.10%
Neghina et al. (2006)	A. lumbricoides	2001–2006	Western Romania	187 positive stool examinations performed in a reference university lab	1.10%
Neghina et al. (2010)	A. lumbricoides	1996–2007	Caras-Severin County	19 hospitalized patients found with intestinal nematodal infections	52.60%10.5% coinfected with T. trichiura
Ionescu (1976)	E. vermicularis	1970–1973	Region of Oradea town	Infantile population	Decrease from 21.9% to 3.9% (active detection)Decrease from 22.6% to 16.1% (passive detection)
Panaitescu et al. (1995)	E. vermicularis	—	—	231 children with disabilities found with 294 parasitic infections	3%
Neghina et al. (2006)	E. vermicularis	2001–2006	Western Romania	187 positive stool examinations performed in a reference university lab	5.80%
Dancescu (1968)	T. trichiura	1966	—	755	32.10%(range 10.2%–47.8%)
Olteanu et al. (1999)	T. trichiura	1968	—	286	49.70%
Panaitescu et al. (1995)	T. trichiura	—	—	231 children with disabilities found with 294 parasitic infections	16.40%
Neghina et al. (2010)	T. trichiura	1996–2007	Caras-Severin County	19 hospitalized patients found with intestinal nematodal infections	36.20%10.5% coinfected with A. lumbricoides
Dancescu (1968)	Strongyloides stercoralis	1942–1965	—	—	0.01%–9.3%
Dancescu (1968)	S. stercoralis	1966	—	755	10.70%(range 2.2%–16.5%)
Olteanu et al. (1999)	S. stercoralis	—	Region of Beius town	—	1.1%–3.2%
Olteanu et al. (1999)	S. stercoralis	1971	Rural regions	5097	1%–16%
Olteanu et al. (1999)	S. stercoralis	1972	—	Laborers from 13 coal culture mines	1.5%–4.4%
Olteanu et al. (1999)	S. stercoralis	1972	Northern Transylvania	—	5%–13.3%
Olteanu et al. (1999)	S. stercoralis	1985–1990	Transylvania	95 children from orphanage	13.4%–21.3%
Olteanu et al. (1999)	S. stercoralis	1985–1990	Transylvania	30 children from orphanage	30%, among whom 65% coinfected with Giardia lamblia or Hymenolepis sp.
Panaitescu et al. (1995)	S. stercoralis	—	—	231 children with disabilities found with 294 parasitic infections	6.90%

General information about enterobiasis and trichuriasis in Romania are limited (Table 2).

Although enterobiasis is one of the most common helminthic infections worldwide (Gillespie 2001), previous Romanian studies reported low prevalence values for this infection (3%–5.8%) (Ionescu 1976, Panaitescu et al. 1995, Neghina et al. 2006). The present study shows that enterobiasis alone is much more frequent among patients found to have intestinal nematode infections, and coinfections with other nematodes (A. lumbricoides or T. trichiura) occur rarely in hospitalized cases. Ionescu (1977) studied the relationship between E. vermicularis and appendectomy from 1968 to 1973, and noted a decrease in the number of children aged 0–15 years who underwent surgery for appendicitis following the successful campaigns undertaken against infections with this helminth.

In Romania, trichuriasis is known to be spread especially in rural regions and areas of rough terrain (Dancescu 1981). The prevalence of this infection ranges between 10.2% and 49.7% (Dancescu 1968, Panaitescu et al. 1995, Olteanu et al. 1999, Neghina et al. 2010). About 16% of the investigated children were found to have trichuriasis (Table 2) (Panaitescu et al. 1995). In the present study, the prevalence of trichuriasis was almost fourfold lower than the value reported in a similar study we performed recently in Caras-Severin County (Neghina et al. 2010). Further, coinfection with A. lumbricoides was four times more frequent in our previous report (Neghina et al. 2010) as compared to the present study. Abdominal pain was the most common complaint in the present study and also in patients found to have trichuriasis by colonoscopy in Korea (Ok et al. 2009).

Several studies showed that strongyloidiasis occurred rarely in Romania (0.01%–16%) (Table 2) (Dancescu 1968, Panaitescu et al. 1995, Olteanu et al. 1999). Higher prevalence values were reported in institutionalized children (13.4%–30%) (Olteanu et al. 1999). In our study, infection with S. stercoralis had the lowest prevalence of all intestinal helminths.

The impact of intestinal nematodes on children's health and educational achievements has been demonstrated worldwide. These helminthes may be a major source of chronic ill-health, disturbance of the growth process, decreased intellectual performance, and school absenteeism. The cognitive impairment may be due to nutritional deficiencies caused by the worms as well as to subclinical symptoms of heavy intestinal infection that lead to reduced attention during school classes (Gillespie 2001). Moreover, severe complications such as intestinal obstruction (possibly followed by perforation and peritonitis), biliary obstruction, pancreatitis (Seltzer et al. 2006), or even asphyxia (Maletin et al. 2009) may also occur in children with ascariasis. Anemia and rectal prolapse are other possible complications of trichuriasis (Cooper 2006). Even if adults predominated slightly in our series, two out of three patients with coinfections were children: one had trichuriasis and ascariasis, and the other one had trichuriasis and enterobiasis. Most of the patients hospitalized with intestinal nematode infections in Caras-Severin County were children (Neghina et al. 2010), and both patients with nematode coinfections (ascariasis and trichuriasis) were under 18 years of age (Neghina R, unpublished data).

Women and residents of urban areas predominated in the present study, similarly to the study performed in the neighboring county—Caras Severin (Neghina et al. 2010).

Most of the affected adults had limited formal education and belonged to the low social class: laborers, unemployed, and retired. The association of the patients suffering of intestinal nematode infections with the above-mentioned social categories was also noticed previously (Gillespie 2001, Neghina et al. 2010).

The onset of clinical symptomatology was the main reason for the patients from our series to address the hospital. However, in some cases, they were admitted for other diseases and were found to have the intestinal nematode-related condition by chance.

Although cases with intestinal nematode infections detected in this hospital were rather few over a long period, and this constitutes a limitation of our study, these infections are indeed more frequently diagnosed by general physicians and treated as outpatients. Unfortunately, no official report of such cases is available.

Noteworthy are the unusual situations revealed by Dancescu (1981), who consequently emphasized that physicians must be cautious in establishing the diagnosis of these helminthiases especially when dealing with adult patients. According to his experience, patients' straightforwardness in providing detailed information may be questionable in some cases. He noticed cases, related to the field of psychiatry, when people reported movements of ascarid worms in their intestines. More dramatic was the situation when helminthes of animal origin (eliminated by dogs and cats, or found in the intestines of chickens) were brought to physicians by patients who claimed that those were eliminated by themselves.

In conclusion, infections with intestinal nematodes are less frequently diagnosed in hospitalized patients despite that these affections are quite common in the Romanian population. To further limit their occurrence, public health measures and informative campaigns should be focused on compliance with the basic hygienic rules, hand washing and washing of the vegetables and fruits before consumption, proper disposal of feces, and wearing of protective shoes especially by persons who come in contact with potentially contaminated soil. Periodic stool examinations especially in children are necessary for early diagnosis of parasitic diseases and should be officially required at the beginning of each school year; this measure is meant to avoid severe delayed complications with negative consequences for patients and the healthcare system.

Footnotes

Disclosure Statement

No competing financial interests exist.

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