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Keywords:

  • Adults;
  • children;
  • epidemiology;
  • parasitology;
  • pork;
  • Romania;
  • trichinellosis

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

Clin Microbiol Infect 2012; 18: 86–90

Abstract

Trichinellosis continues to represent a major concern in Romania, a country that, over the years, has had favourable conditions for the transmission and maintenance of this disease. During the years 2007–2009, Romania has reported to the WHO’s Regional Office for Europe the highest incidence of trichinellosis in humans. This study was aimed at analysing the epidemiological, clinical, laboratory and therapeutic aspects of trichinellosis in a well-known Romanian endemic area, and at determining the particular aspects of this disease in children and the adult population. We retrospectively investigated the medical records of patients from two western Romanian counties, diagnosed with trichinellosis and hospitalized between 2007 and 2009. During this period, a total of 91 persons presented with this disease, and the corresponding yearly average incidence was 2.7 cases per 100 000 inhabitants. Patients were aged 3–80 years (mean age 33.3 ± 17.9 years), and most of them were adults (78%). Males accounted for 51.6% of cases. Unemployed adults belonging to the gypsy minority predominated within the study group (46.5%). Myalgia, fever and oedema were the most common symptoms. The mean eosinophil count was 25.1% ± 17.1% (range 1–75.8%), and was significantly higher in adults than in children. All patients were treated with albendazole, and 52.7% had associated corticotherapy. Trichinellosis is still probably the most important parasitic disease in Romania. Recent reports have revealed inadequate application of prophylactic and control measures against this disease. Consequently, public health strategies should be reconsidered, and more efficient and rigorous education of the population is required.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

Trichinellosis is a cosmopolitan foodborne parasitic zoonosis, and is still endemic in many regions of Asia, Latin America and eastern Europe [1]. In Romania, a country that, over the years, had had favourable conditions for the transmission and maintenance of this disease, trichinellosis continues to be a major concern [2–4].

During the years 2007–2009, Romania reported the highest incidence of human trichinellosis to the WHO Regional Office for Europe (http://data.euro.who.int/CISID/, [5]).

Clinically, trichinellosis is divided into two phases: an intestinal (enteric) phase and an extraintestinal (systemic) phase. The symptoms of the enteric phase include anorexia, nausea, vomiting, diarrhoea or constipation, and upper abdominal pain. During the systemic phase, the affected person may have fever and sweating, facial oedema, myalgia, muscle swelling and weakness, headache, ocular manifestations (conjunctivitis, orbital/eyelid oedema, conjunctival haemorrhages, and eye pain), and splinter haemorrhages in the fingernail beds [6,7]. Leukocytosis with eosinophilic predominance is a general characteristic of trichinellosis. Eosinophilia is considered to be the earliest and the most common laboratory finding. It can be detected in almost all cases, and reaches a peak value 3–4 weeks after infection [7,8]. Diagnosis largely depends on correlating the symptomatology and the laboratory test results with a carefully taken anamnesis [8]. Confirmation may be achieved by muscle biopsy or by serological detection of anti-Trichinella antibodies [9]. The treatment consists of specific antihelminthic drugs (benzimidazoles) and corticosteroids in selected cases [7].

Arad and Timis counties are situated in western Romania in an area where traditional pork products are consumed on a large scale and trichinellosis has deep roots. It is worth noting the major trichinellosis epidemic that involved 757 people from Arad in 1973 [4,10].

This study was aimed at analysing the epidemiological, clinical, laboratory and therapeutic aspects of human trichinellosis in a well-known Romanian endemic area, and at determining the particular aspects of this disease in children (0–19 years) and the adult population (over 20 years).

Material and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

We retrospectively investigated the medical records of patients from two western Romanian counties (Timis and Arad) diagnosed with trichinellosis, who were hospitalized in two infectious disease hospitals (Timisoara and Arad) from 2007 to 2009. From their medical records, the following data were extracted for each patient: registration number, age, sex, address, date and duration of hospitalization, profession, clinical symptomatology, course of disease, routine laboratory investigation results, and specific therapy received.

The diagnosis was established according to the algorithm for diagnosing acute Trichinella infections in humans [11], and confirmed by positive serology or positive muscle biopsy results. Serum detection of anti-Trichinella antibodies was performed by indirect ELISA at Istituto Superiore di Sanita, Department of Infectious, Parasitic and Immunomediated Diseases (method MI-03, for 12 patients of the study group—CRLP codes 053-070/09 and 06/02/09) and in private laboratories in Timisoara. The clinical course of the disease (where available) was established in conformity with the WHO guidelines [11].

Statistical analysis was performed with the software package SPSS version 17.0 for Windows (SPSS, Chicago, IL, USA). Descriptive statistics (percentage, mean ± standard deviation) were calculated for each variable as appropriate. Mann–Whitney U-statistics for quantitative data were used to compare different patient subgroups. A p-value of <0.05 was regarded as statistically significant.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

During 2007–2009, trichinellosis was diagnosed in a total of 91 persons from Arad (n = 49) and Timis (n = 42) counties. The yearly average incidence (cases per 100 000 inhabitants) was 2.7. The subgroup analyses performed showed the following incidence rates: 2.9 in males vs. 2.5 in females, 2.4 in children vs. 2.7 in adults, and 2.7 in inhabitants of both urban and rural regions. All cases occurred in winter, and most of them (69.2%) were identified in 2009. Patients were aged 3–80 years (mean age 33.3 ± 17.9 years), and the majority of them were in the 35–44-year (17.6%), 30–34-year (14.3%) and 5–14-year (14.3%) age groups. Most of them were adults (78%), and 51.6% were male. Of the total cases, 56% were inhabitants of urban areas.

Unemployed adults belonging to the gypsy minority predominated within the study group (46.5%). The remaining groups, by vocation, were semiskilled labourers and people with limited formal education (21.1%), retired people (12.7%), office workers (11.3%) and others (2.8%). For four patients (5.6%), the profession was not specified in the medical record.

The clinical pattern of the disease in the study group is shown in Table 1. Myalgia, fever and oedema were the most common symptoms (81.3%, 68.1% and 60.4%, respectively).

Table 1.   The clinical pattern of the patients diagnosed with trichinellosis in Arad and Timis Counties during 2007–2009
Symptom/signTrichinellosis casesa
TotalChildrenAdults
  1. aNumbers in parentheses, percentage of total cases (n = 91), of whom 20 were children and 71 were adults.

Myalgia74 (81.3)10 (50)64 (90.1)
Fever62 (68.1)14 (70)48 (67.6)
Eyelid, facial or limb oedema55 (60.4)8 (40)47 (66.2)
Asthenia42 (46.2)7 (35)35 (49.3)
Gastrointestinal manifestations (diarrhoea, nausea, vomiting, constipation, and epigastric pain)40 (44)9 (45)31 (43.7)
Headache36 (39.6)9 (45)27 (38)
Cutaneous rash9 (9.9)3 (15)6 (8.5)
Ocular pain6 (6.6)06 (8.5)
Conjunctivitis, conjunctival haemorrhages5 (5.5)1 (5)4 (5.6)

The clinical course of the disease was mainly moderately severe (38.5%) or severe (28.6%) (Table 2). One patient developed encephalitis, and another had myocarditis. No fatalities were registered.

Table 2.   The clinical course, laboratory findings and hospitalization period in patients diagnosed with trichinellosis in Arad and Timis Counties during 2007–2009
VariableTrichinellosis casesa
TotalChildrenAdults
  1. aNumbers in parentheses, percentage of total cases (n = 91), of whom 20 were children and 71 were adults, unless otherwise specified.

  2. bReported in 14 children and 54 adults.

  3. cReported in 70 adults.

  4. dReported in 12 children and 51 adults.

Course of diseaseb
 Benign5 (5.5)2 (14.3)3 (5.6)
 Moderately severe35 (38.5)9 (64.3)26 (48.1)
 Severe26 (28.6)3 (21.4)23 (42.6)
 Complicated by myocarditis1 (1.1)01 (1.9)
 Neurological complications1 (1.1)01 (1.9)
Eosinophil counts (%)c
 <55 (5.5)1 (5)4 (5.7)
 ≥585 (94.5)19 (95)66 (94.3)
Leukocyte counts (cells/mm3)c
 <10 00036 (39.6)11 (55)25 (35.7)
 ≥10 00054 (60.4)9 (45)45 (64.3)
Erythrocyte sedimentation rate (mm/h)d
 <1016 (17.6)5 (41.7)11 (21.6)
 ≥1047 (82.4)7 (58.3)40 (78.4)
Length of hospital stay (days)
 1–735 (38.5)12 (60)23 (32.4)
 8–1446 (50.5)6 (30)40 (56.3)
 15–2910 (11)2 (10)8 (11.3)

Children with severe trichinellosis were significantly younger (4.3 ± 1.5 years, range 3–6 years, p 0.01) than those with moderately severe trichinellosis (12.1 ± 2.9 years, range 9–17 years). Similarly, the adult patients with a benign course of the disease were significantly older (68.3 ± 6.1 years, range 63–75 years) than those with moderately severe (37 ± 10.8 years, range 20–62 years, p 0.005) and severe (43.3 ± 16.3 years, range 23–80 years, p 0.03) trichinellosis.

The mean eosinophil count was 25.1% ±17.1% (range 1–75.8%), and was significantly higher in adults (27.6% ±17.8%, range 1–75.8%, p 0.01) than in children (16.6% ±10.8%, range 4–42%). The leukocyte count ranged between 4200 and 28 600 cells/mm3, with a mean value of 12 113.7 ± 5295.8 cells/mm3. Overall, patients with severe trichinellosis had significantly higher leukocyte counts (13 536.9 ±5521.3 cells/mm3, range 6190–28 000, p 0.04) than those with a moderately severe course of the disease (11 132.6 ±5315.9 cells/mm3, range 4200–28 600).

The mean erythrocyte sedimentation rate (ESR) value was 20.3 ± 12.6 mm/h (range 4–65 mm/h), and was significantly higher in adults (22 ± 13 mm/h, range 4–65 mm/h, p 0.01) than in children (13.2 ± 7.9 mm/h, range 5–34 mm/h). Adult patients with a benign course of the disease had significantly higher ESR values (38.3 ± 15.3 mm/h, range 25–55 mm/h) than those with moderately severe (19.2 ± 11.1 mm/h, range 4–44 mm/h, p 0.04) and severe (20.8 ± 8 mm/h, range 6–37 mm/h, p 0.03) trichinellosis. All patients were treated with albendazole, and 52.7% received associated corticotherapy.

The mean hospitalization period was 8.9 ± 3.9 days (range 3–19 days). Of the adult cases, 56.3% required between 8 and 14 days of hospital stay, whereas 60% of children were admitted to hospital for <7 days. Moreover, patients aged 20–24 years required the longest hospital stay (10.5 ± 3.7 days, range 8–19 days), and those aged 15–19 years were hospitalized for the shortest period of time (6.7 ± 0.6 days, range 6–7 days, p 0.01).

Adults who received combination therapy with albendazole and a corticosteroid required a significantly longer hospitalization period (10.5 ± 3.7 days, range 3–18 days, p 0.001) than those who were treated with the antiparasitic drug alone (7.6 ± 3.7 days, range 3–19 days).

Cases were registered during six winter outbreaks (one outbreak per year and county). The sources of infection were pork (five outbreaks) and mixed sausages prepared from wild boar meat and pork (one outbreak [2]). In one of the outbreaks, larvae were collected from the infected pork, and molecular identification at the species level revealed Trichinella spiralis [12].

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

Trichinellosis in humans may be considered to be important public health issue in this western Romanian area, considering that the average yearly incidence is higher than that in the entire country (two cases per 100 000 inhabitants during 2007–2009) [5,13,14]. A detailed analysis shows that the incidence rate in urban areas is almost two times higher than the value reported for the entire country during the same period of time (1.5 cases per 100 000 inhabitants), whereas the value reported in rural areas is identical to the national figure (2.7 cases per 100 000 inhabitants) [5,13,14].

All cases occurred in winter, when, according to national customs, each family in the rural regions slaughter a pig raised in their own household (not always in adequate hygienic conditions). Pork products are prepared (sometimes from meat unverified by trichinelloscopic investigation) and largely consumed on special occasions such as Christmas and New Year’s Eve [2]. Moreover, these traditional products are often given as gifts to relatives or friends residing in urban regions. Frequently, people from urban areas buy their own pigs, which are raised and slaughtered by their relatives or friends in the countryside. Generally, there is a preference for home-made products over commercially processed meat products, the latter being considered non-appetizing.

Adults predominated in this study (78%), as in a previous extensive study performed in five Romanian hospitals during 1996–2005 (74%) [15]. As well as adults being involved in the slaughtering process and in preparing the traditional pork products, their predominance may also be explained by the demographic characteristics of the population in this area.

Dependence on home-made traditional products is likely to prevail in persons on low incomes, and most of the patients in this study were unemployed, as in other studies performed in the neighbouring counties: Caras-Severin (31%) [16] and Hunedoara (40.1%) [17]. The general rate of 2.9% unemployed people in this region could explain the high percentage of trichinellosis patients from this social category. Furthermore, the unemployment rate increased almost two-fold in 2009 as compared with 2007 and 2008 (http://www.mmuncii.ro/en/statistici-55-view.html), and this may also partly explain the high rate of trichinellosis in 2009.

Overall, myalgia was the most common clinical finding, as in other studies [18,19]. Unlike in our previous report, in which fever predominated in both children and adults [15], in this study it was the most frequent clinical symptom in children only.

As in other Romanian clinical surveillance studies [10,16,17,20], the moderately severe course of disease was detected most frequently, and the hospitalization period ranged between 8 and 14 days for most of the patients. The mean eosinophil count and ESR were significantly higher in adults than in children, as in the prior extensive comparative surveillance [15].

All of our patients were treated with albendazole, which is a well-tolerated drug and one of the two antihelminthics of choice used for the treatment of Trichinella infections [21,22]. Corticosteroids were also used in about half of our patients. Recently, it has been shown that physicians treat trichinellosis more frequently with combined therapy based on albendazole (Zentel) and corticosteroids [1].

Trichinellosis remains one of the three major parasitic diseases in Romania (besides cystic echinococcosis and toxoplasmosis) [4], and is probably the most important one. Recent national reports [5,13,14] have revealed inadequate application of prophylactic and control measures against this disease. Consequently, at the beginning of 2011, a new trichinellosis focus developed in this area (Neghina R, Neghina AM, Marincu I, unpublished data).

Public health strategies should be reconsidered, and more efficient and rigorous education of the population (especially through the mass media) is required in order to fully prevent and eradicate trichinellosis in this endemic area.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

Authors are grateful to Dr. Edoardo Pozio from Istituto Superiore di Sanita, Department of Infectious, Parasitic and Immunomediated Diseases in Rome, Italy for organizing the transport and analyzing the serum samples from patients hospitalized for trichinellosis in 2009 in Timisoara, Romania.

Author Contribution

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

R. Neghina collected most of the data and wrote the main part of the manuscript. A. M. Neghina performed the statistical analysis, wrote a part of the manuscript, and was reponsible for the final draft and editing of the manuscript. I. Marincu managed some of the patients from this study and participated in the collection and analysis of data. All authors have read and approved the final version of the manuscript.

Transparency Declaration

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References

No funding was available for this study. The authors have no commercial relationship or any potential conflict of interest of any nature related to this manuscript.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Author Contribution
  9. Transparency Declaration
  10. References
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