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Intestinal helminthes and protozoan infections among children of Chechen refugees in Poland.


Poland is a transit, or infrequently, a destination country for a number of refugees from different parts of the world, mainly from East Europe or Asia. This is influenced by Poland's geographical position in Europe--it is the first European (EU) country on the way of refugees fleeing from former autonomous and federate republics of the Soviet Union, where military operations still continue (the territory of Caucasus) as well as refugees emigrating from South-East Asia due to a difficult economic situation (Vietnam, Laos, Cambodia). Poland is the first country in the eastern parts of Europe were consolidated EU immigration regulations are in force. In case of being granted the refugee status in Poland it is easier for an emigrant to function in other EU member states. Persons who solicit the status of a displaced person in Poland are placed in temporary refugee centers located in 4 provinces: Lubelskie, Mazowieckie, Podlaskie, Slaskie. Their stay in such a center is voluntary; the only condition to obtain a temporary residence permit is to present appropriate documents at the Office for Foreigners.

Each resident of temporary reception centers is obliged to comply with the law which is in force in the territory of Poland and other EU member states as well as the regulations of residence enforced by virtue of a decree issued by the Ministry of Interior and Administration in 2003. (1) A diversity of nationalities, cultures, traditions and historical conditioning of refugees' home countries results in the fact that the Office for Foreigners is not merely responsible for ensuring suitable living conditions, but also arises issues concerning refugee security or respect for religion.

Refugees residing in temporary centers are provided with health care by medical staff employed in outpatient clinics set up on the premises of the centers. The range of medical services provided in the aforementioned centers is determined by the Health Minister's Decree of 2004 concerning medical examinations and sanitary procedures of the body and clothing of refugees applying for a refugee status. (2) Medical examination includes general assessment of a refugee's health condition, with particular attention being paid to possible occurrence of contagious diseases. In justified cases a refugee is subjected to diagnostic tests in the direction of HIV, syphilis, diphtheria, cholera, typhoid fever, paratyphoid A, B or C, salmonellosis, shigellosis, poliomyelitis, tuberculosis. As regards laboratory tests stated in the abovementioned decree it needs to be pointed out that diagnostic tests for parasitic diseases, which so commonly occur among refugees (people inhabiting areas where public utilities are in poor condition and where access to health service is considerably limited) are excluded from the list. The aim of this article is to discuss the prevalence and structure of parasitic diseases in the population of Chechen refugees' children residing in 14 temporary centers in the territory of Poland in 2005.

Experimental procedures

Study subjects

In January 2005 a decision was taken to carry out diagnostic tests for parasitic diseases of the digestive tract in the population of Chechen children staying in temporary centers in Poland. It was arranged to conduct parasitological diagnostics among nearly 1.500 children located in 14 centers in the territory of 4 provinces.

Data collection

Material collected from 426 patients of Chechen Nationality aged 1-18 residing in 14 temporary centers was subjected to analysis. The collection and fixation of the selected material was conducted by medical staff of the given centers from May 30th to June 30th 2005. The fecal specimens were collected from each of the Examined child for three consequent times (on Mondays, Wednesdays, and Fridays). The specimens were then fixed in formalin 10% in the ratio of 1:1. As soon as all the material was collected, the samples were sent to the Department of Maritime and Tropical Medicine of the Military Institute of Medicine in Gdynia where they were subjected to analysis.

Analytic methods

Diagnostics of parasitic diseases of the digestive tract in the population of Chechen children residing in temporary centers in the territory of Poland was conducted on the basis of the following laboratory testing methods:

* direct preparation in Lugol's solution

* preparation of sedimentation procedures by means of Parasep Fecal Control

--in a flow cytometer--FE2 workstation

--in Lugol's solution

* preparation of decantation procedures in distilled water

* preparation of Faust's flotation procedures.

Direct preparation in Lugol's solution

Approximately 2 gr of feces was taken with a glass rod and applied onto a slide, a drop of Lugol's solution was added and the material was smeared over the surface of around 4[cm.sup.2]. Next, a cover slide was placed on top of the preparation and the material was examined microscopically under correct magnification. The material prepared by means of such a method allowed to conduct an initial analysis of non-concentrated material, staining the preparation with Lugol's solution improved the quality of the picture of detected parasites. Direct preparations were not made in isotonic solution as the material sent for analysis was fixed in formalin 10%, which caused destruction of all parasites and the inability to evaluate their survival forms.

Preparation of sedimentation procedures by means of Parasep[R] Fecal Control

Special equipment, which makes it easier to conduct sedimentation procedures and at the same time protects the person working with fecal specimens against getting dirty and subsequently against accidental infection, was constructed to carry out the process of condensation of parasites. In the process of analyzing the material, 6 ml of formalin 10% and a drop of detergent was poured into a ready-made test tube of Parasep[R] Fecal Control as well as the fecal specimen (0.5 [cm.sup.3]). All the material was emulsified once, 2 ml of ethyl acetate was added. Concentration occurred following filtration of the material which was centrifuged at the rotation of 1000 times per hour for 1 minute. After decanting the supernatant liquid, a drop of the specimen was applied onto a glass slide, was stained with Lugol's solution and examined microscopically. In addition to this, observation in a flow cytometer (FE2 workstation) was conducted. This piece of equipment was constructed in such a way so that specimens could be automatically taken from the test tubes and sent into the optical slide assembly under the microscope. The specimen was halved in the assembly and it got into two transparent observation tubes. One piece of the specimen was mixed with NaCl solution and the other with Lugol's solution. The equipment was automatically rinsed in water between consecutive trials. Additionally, after a fixed number of trials, it was thoroughly rinsed with detergent in order to clean the optical slide assembly and the tubes leading to it.

Preparation of decantation procedures in distilled water

Approximately 2 gr of fecal specimen was thoroughly mixed with a small amount of water in a test tube. Next, water was added to the top of the tube. After 30 minutes the supernatant liquid was decanted and another portion of water was added. This procedure was repeated three times until clear supernatant was obtained--generally 3-4 times. After that, slides were prepared for microscopic examination--the sediment was placed on a slide and stained with Lugol's solution.

Preparation of Faust's flotation procedures

Approximately 2 gr of fecal specimen was mixed with saturated NaCl solution in a test tube and water was added to the top of the tube. A cover slide was placed gently on the top of the tube and in contact with the suspension. After 30 minutes the cover slide was gently removed with tweezers and placed the wet side down on a slide. The preparation was ready for microscopic examination.

Parasitological diagnostics is commonly based on laboratory testing methods, such as microscopic, immunological, biochemical or molecular techniques. Microscopic methods provide the basis for detecting the life cycle of a parasite, which in most cases suffices to diagnose the disease. Whenever it is impossible (biological material cannot be obtained) or difficult (similar species, indistinct diagnostic traits) other procedures are employed. Techniques that detect specific antibodies, antigens in bodily liquids or in feces (coproantigens) or nucleic acid of a parasite (PCR) may be used. Isoenzymatic analysis allows to differentiate similar species of parasites on condition that their culture (protozoa) or much material (helminthes) can be obtained.


From May to July 2005 fecal specimens collected from 426 persons were subjected to analysis. The examination revealed 160 cases of infestations by parasites of the digestive tract in 144 patients of all the examined Chechen children (percentage of the infected 33.8%). In most cases they were cases of simple invasion (128, 30%). Cases of complex invasion were diagnosed in 16 of all specimens (3.8%); those were combinations of infestation by Giardia intestinalis with helminthiases. Infestation with Giardia intestinalis prevailed (97 cases, 22.8% of the examined population). Also, cosmopolitan helminthiases were diagnosed: Strongyloides stercoralis (29 cases, 6.8%), Ascaris lumbricoides (24 cases, 5.6%), Enterobius vermicularis (6 cases, 1.4%). Moreover, 2 cases of Entamoeba histolytica (0.5%) and Hymenolepis nana (0.5%) each were detected (Table 1).

Parasitic diseases of the digestive tract detected in the population of Chechen refugees' children residing in the territory of Poland remain the most commonly occurring health problems in the world. Infestations by Enatamoeba histolytica were diagnosed in merely 2 patients. However, it needs to be taken into account that amebiasis remains a disease of endemic character in the territory of Chechnya. Enterobius vermicularis is the most frequently occurring nematode infesting the human digestive tract and both its ova and mature forms are rarely detected during examination of fecal specimens. When it comes to detecting the nematode, the principal testing method remains conducting a rectal swab. This, however, had not been intended while performing the abovementioned examinations.


Nowadays, high incidence of parasitic diseases is widespread. It has been estimated that over half of the world's population is infected with various types of helminthes or protozoa. Prevalence of parasitoses is notably higher in areas of poor sanitary and epidemiological standards. In addition to this, ongoing military operations might facilitate increased incidence of infectious and invasive diseases. Also, they diminish significantly the possibilities to conduct screening examinations or to report diagnosed diseases and asymptomatic carrier states.

Caucasus, and particularly Chechnya, is characterized by catastrophic epidemiological situation. Two Russian-Chechen wars which had taken place in the territory of Chechnya within the past decade have led to a humanitarian catastrophe and exodus of the local people. A volume of 220,000 Chechen refugees, citizens of the republic whose population was estimated at approximately 1 million people, have left their homes and migrated to camps established in the territories of Dagestan and Ingushetia. (3) Moreover, there are further thousands of Chechen people trying to obtain a refugee status in European countries.

Apart from drastic reduction in the quality of life in Chechnya, numerous epidemics of infectious diseases, such as cholera, typhoid fever or diphtheria have broken out. (4,5) The number of infectious and non-infectious diseases in Chechnya is 5-10 times higher than in other parts of Russia, which has been the result of ongoing military operations and also destroyed infrastructure of the health services. The most frequently occurring health problems in the population of adult Chechens are tuberculosis, psychiatric diseases or disorders, abuse of medication, drugs and alcohol as well as HIV infections. (6) It has been estimated that as much as 84% of all Chechen children require medical care, in particular due to infectious diseases of the digestive tract, tuberculosis, diseases of the nervous system, anemia, psychiatric diseases or disorders. (7) Infant mortality rate is estimated at 21.7/28.9 per 1000 live births (world average 13.3). A 50% of the Chechen population need to survive for less than 1 USD per day. The unemployment rate is estimated at 80%. (8)

Parasitic diseases detected in refugees staying in temporary centers in Poland are subjected to compulsory treatment. Following the completion of laboratory tests conducted in the Institute of Maritime and Tropical Medicine in Gdynia patterns of treatment of particular infections were formulated and sent to suitable organs of the Ministry of Interior and Administration. Difficulties which emerged in the course of treatment were predominantly connected with the high rotation of refugees in temporary centers as well as the unwillingness of parents to agree to have their children treated which undoubtedly resulted from their ignorance of existing health hazards. Owing to high rotation of refugees, the possibility of their unrestricted departures from temporary centers and the ease of transmitting parasitic diseases there is an increased risk of an outbreak of an epidemic of parasitic diseases among the local people.

From 2002 to 2003 a research into infestations by intestinal parasites was conducted in the population of 31,504 children aged 7 in both urban (N=19,623) and rural (N=11 881) areas in the territories of 15 out of 16 Polish provinces (the Pomeranian province was excluded). The aim of the abovementioned research was to assess the epidemiological situation concerning the prevalence of intestinal parasitoses in Poland. The examined age group (7-year-old) was selected deliberately as it had been previously observed that the extensiveness of intestinal parasitoses is the highest at this particular age. The examination included microscopic analysis of both fecal specimens and rectal swab by means of 5 different methods: direct smear in isotonic NaCl solution and in Lugol's solution, Faust's flotation procedures, decantation procedures and Graham's cellophane adhesive. Parasites of the digestive tract were detected in 4.584 children (14.55% of the examined), including 10.4% of children from urban areas and 19% of children from rural areas. The highest percentage of the infected children was found in the northern and eastern parts of Poland, in the Warmian-Masurian province (29.6%) and the Lublin province (20.8%). The most frequently detected parasites were Enterobius vermicularis (12.15% of all the examined), Ascaris lumbricoides (0.83%) and Trichuris trichiura (0.12%). (9) A significant drop in the number of infections among children aged 7 years was observed in relation to the results of similar research conducted in Poland from 1997 to 1998 (21.55% infected children, N=30 110) (10) and from 1992 to 1993 (22.6% infected children, N=60 288). (11)

In the United States (US), there are clear procedures concerning health condition of refugees. Each refugee applying for granting asylum in the US is obliged to undergo tests for HIV and syphilis and chest radiograph to assess for evidence of tuberculosis. Infectious diseases screening for all refugees is recommended, it includes as follows: tuberculin skin test, hepatitis B screening, complete blood cell count, urinalysis and stool examination for ova and parasites. Parasitic diseases of the digestive tract are commonly detected among refugees; this fact poses a significant epidemiological hazard considering that most individuals are asymptomatic. The most frequently detected parasites in the population of refugees are: Ascaris lumbricoides, Enatamoeba histolytica, Gardia lamblia, Ancylostoma duodenale, Necator americanus, Trichuris trichiura, Hymenolepis nana. (12) Research conducted among refugees and immigrants in the US has demonstrated that the prevalence of gastrointestinal parasites ranged from 20 to 80%. (13-15)

Although the incidence of parasitic infections is lower in moderate climate areas in relation to the tropics, the sanitary conditions under which refugees have lived before resettlement may place them at increased risk for gastrointestinal parasites. For example, 22% of 252 refugees and asylum seekers from Eastern Europe (among other, Bosnia, Russia, Macedonia) residing in Sweden were found to have parasites. (16)

The real Babel Tower in Europe has been Germany, where immigrants account for as much as 9% of the country's population (over 7 million people); in Berlin they account for 13% of the city's inhabitants. Diagnostic research into infectious diseases conducted among 153 immigrants (mainly from the Sub-Saharan Africa, 85.6%) staying in Germany for less than a year from 1999 to 2004 has demonstrated that only 26% of the examined individuals were asymptomatic. The 48% of the examined required an immediate treatment, while 38% were diagnosed with communicable diseases, mainly nematodes (trichuriasis, ancylostomiasis, ascariasis, strongyloidiasis) and intestinal protozoa (giardiasis, amebiasis). (17)

Mass migration of people coming from the Third World, where infectious diseases of endemic character prevail, result in the fact that laboratory diagnostics of individuals at risk from such infections has become quite a challenge. (18) Even though citizens of industrialized countries are infrequently diagnosed with infestations of the digestive tract, it seems to be an absolute necessity to conduct screening tests among local and alien populations. There is disagreement as to the number of stool specimens to test in asymptomatic patients. (19) Some protocols test three stool samples, others test just one. (20), 21 Symptomatic individuals should be assessed with three specimens. (12)


1. Parasitic diseases occurring among refugees in temporary centers in Poland are not subjected to compulsory treatment.

2. This is mainly due to high rotation of refugees in the abovementioned centers as well as parents' unwillingness to agree to have their children treated, which undoubtedly results from their ignorance of existing health hazards.

3. Owing to the large volume of refugees and the possibility of unrestricted departures from temporary centers there exists an increased risk of the occurrence of parasitic diseases of epidemic character among the local people.


The authors of this article would like to thank Dr Adam Tolkacz MD, PhD (Central Hospital of Ministry of the Interior and Administration), coordinator of Team of Medical Services for people applied for refugee status in Poland, for the permission to conduct the research and for providing the data.


(1.) The Interior and Administration Minister's Decree of 12th August 2003 on the regulations of residence in temporary centers for aliens applying for granting a refugee status [in Polish].

(2.) The Interior and Administration Minister's Decree of 30th August 2004 on medical examination and sanitary procedures of the body and clothing for aliens applying for granting a refugee status [in Polish].

(3.) Parfitt T. EC grant helps counter Chechen refugee-camp closures. Lancet 2004;363:136.

(4.) Onishchenko GG, Grizhebovski GM, Efremenko VI, Evchenko IM, Bogdanom IK, Mezentsev VM, et al. Epidemic situation in the Chechen Republic. Zhournal Mikrobiologii, Epidemiologii & Immunobiologii 2001;6 (Suppl): 5-9.

(5.) Grizhebovski GM, Onishchenko GG, Taran VI, Ivanov SI, Evchenko IM, Galimshin SS, et al. Outbreak of typhoid fever in the Chechen Republic in 2000: epidemiological characterization. Zhournal Mikrobiologii, Epidemiologii & Immunobiologii 2001;6 (Suppl):45-47.

(6.) Aliyev T. Illness rate in Chechnya five-to-ten times higher than in Russia. Prague Watchdog (website,, Released at 5 March 2005.

(7.) Aliyev T. Over 80 percent of Chechen children suffer from illnesses. Prague Watchdog (website,, Released at 14 November 2003.

(8.) UNICEF at work in the North Caucasus. Accessed: 26 August 2005. Available at:

(9.) Bitkowska E, Wnukowska N, Wojtyniak B, Dzbenski TH. The analysis of prevalence of intestinal parasites in the population of children aged 7 within the 2002/2003 school year. Epidemiological Review 2004;58:295-302 [in Polish].

(10.) Plonka W, Dzbenski TH. The analysis of prevalence of intestinal parasites in the population of aged 7 in Poland within the 1997/1998 school year in the territory of selected provinces. Epidemiological Review 1999;53:331-338 [in Polish].

(11.) Plonka W, Dzbenski TH. The analysis of prevalence of intestinal parasites in the population of children aged 7 within the 1992/1993 school year. Epidemiological Review 1995;45:285-294 [in Polish].

(12.) Burnett ED. Infectious Disease Screening for Refugees Resettled in the United States. Travel Medicine 2004:39:833-841.

(13.) Geltman PL, Ochran J, Hedgecock C. Intestinal parasites among African refugees resettled in Massachusetts and the impact of an overseas pre-departure treatment program. American Journal of Tropical Medicine and Hygiene 2003;69:657-662.

(14.) Parish RA. Intestinal parasites in Southeast Asian refuge children. The Western Journal of Medicine 1985;143:47-49.

(15.) Salas SD, Heifetz R, Barrett-Connor E. Intestinal parasites in Central American immigrants in the United States. Archives of Internal Medicine 1990;150:1514-1516.

(16.) Benzeguir AK, Capraru T, Aust-Kettis A, Bjorkman A. High frequency of gastrointestinal parasites in refugees and asylum seekers upon arrival in Sweden. Scandinavian Journal of Infectious Diseases 1999;31:79-82.

(17.) Lenz K, Bauer-Dubau K, Jelinek T. Delivery of Medical Care for Migrants in Germany: Delay of Diagnosis and Treatment. Journal of Travel Medicine 2006;13:133-137.

(18.) Garg PK, Perry S, Dorn M, Hardcastle L, Parsonnet J. Risk of intestinal helminth and protozoan infection in a refugee population. American Journal of Tropical Medicine a nd Hygiene 2005;73:386-391.

(19.) Hiatt RA, Markell EK, NG E. How many stool examinations are necessary to detect pathogenic intestinal protozoa? American Journal of Tropical Medicine and Hygiene 1995;53:36-39.

(20.) Commonwealth of Massachusetts. Department of Public Health. Refugee health assessment: a guide for health care clinicians. Accessed: 18 August 2004. Available at: index.htm.

(21.) Walker PF, Jaranson J. Refugee and immigrant health care. The Medical Clinics of North America 1999;83:1103-1120.

Zbigniew Dabrowiecki [1], Krzysztof Korzeniewski [2], Bartosz Morawiec [1], Malgorzata Dabrowiecka [2], Romuald Olszanski [1]

Department of Maritime Medicine [1] & Department of Epidemiology and Tropical Medicine [2], Military Institute of Health Service, Gdynia, Poland

Corresponding author:

Col. Assoc. Prof. Krzysztof Korzeniewski MD, PhD Military Institute of Health Service Department of Epidemiology and Tropical Medicine Grudzinskiego St. 4 81-103 Gdynia 3, Poland E-mail:
Table 1. Prevalence of intestinal parasites in the child population of
Chechen refugees in Poland (N = 426).

 Number of Protozoa
Location of patients
 temporary under Giardia
 centers investiga- intesti- Entamoeba
 tion nalis histolytica

 Debak 24 9 0

 Ciolka 22 1 1

 Radom 37 2 0

 Czerwony 29 6 0

 Bielany 39 14 0

 Lomiza 43 12 1

 Bialystok 41 9 0

 Bialystok 48 12 0

 Wolomin 4 1 0

 Lukow 50 11 0

 Jadwisin 17 6 0

 Moszna 27 6 0

 Siekierki 10 0 0

 Legionowo 35 8 0

 TOTAL 426 97 2

Location of
 temporary Strongy- Ascaris Enterobius Hyme-
 centers loides lumbri- vermicu- nolepis
 stercoralis coides laris nana

 Debak 3 0 1 0

 Ciolka 1 0 0 1

 Radom 4 4 1 1

 Czerwony 3 2 0 0

 Bielany 1 5 0 0

 Lomiza 0 2 0 0

 Bialystok 2 1 2 0

 Bialystok 4 1 1 0

 Wolomin 1 0 0 0

 Lukow 1 3 1 0

 Jadwisin 0 0 0 0

 Moszna 2 1 0 0

 Siekierki 2 3 0 0

 Legionowo 5 2 0 0

 TOTAL 29 24 6 2

Location of
 Temporary Number Number of Simple Multiple
 centers of infes- infected infesta- infesta-
 tations patients tions tions

 Debak 13 11 9 2

 Ciolka 4 4 4 0

 Radom 12 10 8 2

 Czerwony 11 11 11 0

 Bielany 20 18 16 2

 Lomiza 15 14 13 1

 Bialystok 14 13 12 1

 Bialystok 18 16 14 2

 Wolomin 2 2 2 0

 Lukow 16 15 14 1

 Jadwisin 6 6 6 0

 Moszna 9 9 9 0

 Siekierki 5 5 5 0

 Legionowo 15 10 5 5

 TOTAL 160 144 128 16

Source: Own Studies
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Title Annotation:Original Article
Author:Dabrowiecki, Zbigniew; Korzeniewski, Krzysztof; Morawiec, Bartosz; Dabrowiecka, Malgorzata; Olszansk
Publication:Experimental Medicine
Article Type:Report
Geographic Code:4EXPO
Date:Jan 1, 2009
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