Trichinellosis,a Threatening and Re-Emerging Disease in a Romanian Western County

Abstract

Introduction:

Trichinellosis is frequently reported in east European countries like Romania, where the yearly incidence during 1990–1999 was 5.5 cases/100,000 inhabitants. Arad, a western Romanian county, is known as one of the most endemic regions of trichinellosis. A major and unforgettable epidemic of trichinellosis has developed at the beginning of 1973 in this county. The present study focuses on human trichinellosis patients from Arad County, emphasizing on epidemiological, clinical, laboratory, and therapeutic aspects.

Patients and Methods:

Retrospective analysis of the medical records of 335 patients found to have trichinellosis during 1996–2006 and hospitalized in Arad County. The mean age of the trichinellosis patients was 33.6 years, and majority (64.8%) were inhabitants of the rural areas.

Results:

Winter was the season with the highest number of cases (71.6%). Fever was the most frequent manifestation of the disease (85.4%), followed by myalgia (83%). Eosinophilia ranged predominantly between 20% and 20.99% (19.4%). Albendazole was the specific drug administered in 49.4% of the patients.

Conclusions:

Trichinellosis still remains a concern and a major issue of public health in Arad County. Implementation of strict hygienic measures, especially in the rural areas, must be a priority.

Introduction

N ematode helminthes from genus Trichinella are the etiological agent of a widespread disease called trichinellosis. It is a zoonosis, and the infective larvae are transmitted to human by foodborne infection (especially pork, but also other animal meat) (Dupouy-Camet and Murrell 2007, Pozio 2007). People contract the parasite by eating raw or insufficiently cooked infected meat (Bartuliene et al. 2005). The clinical diagnosis of trichinellosis is rather difficult due to the lack of pathognomonic signs and symptoms. Diagnosis of trichinellosis depends on correlating and identifying the multiple clinical manifestations and elevated nonspecific laboratory signs with the epidemiological data focused on a carefully taken case history and the parasite's life cycle (Capó and Despommier 1996, Dupouy-Camet and Murrell 2007).

Romania is the largest southeast European country (with approximately 23 million human inhabitants) sharing borders with Hungary and Serbia in the western part, Bulgaria in the south, the Republic of Moldavia in the east, and the Ukraine in the north. Romania is made up of 41 counties plus the capital city Bucharest. Arad is the fifth largest Romanian county with a population of 461,744 inhabitants (2003). It is situated in western Romania at the border with Hungary. Administratively, it includes nine towns and one city, Arad, which is the capital of the county. During January–March 1973, a major epidemic of trichinellosis, masked by a concomitant flu epidemic, spread in Arad County, comprising 757 clinical cases. The patients had consumed smoked raw sausages from illegally traded pork. Muscle biopsy samples were taken from patients to establish the final diagnosis. The hospitals were overcrowded, and a lot of physicians from the neighborhood county, Timis, supplied the medical assistance. Patients with benign forms of disease were ambulatory treated (Cironeanu and Ispas 2002).

The present study aimed to conduct a retrospective investigation on incidence of human trichinellosis in Arad County over a period of 11 years (1996–2006), outlining the epidemiological, clinical, laboratory, and therapeutic aspects in this Romanian endemic region.

Patients and Methods

The study group comprised 335 patients distributed throughout the 11-year period (Table 1), with ages ranging from 2 to 86 years (33.6 ± 17.7). Trichinellosis patients belonged to the following age groups: 0–9 years in 25 cases (7.5%), 10–19 years in 61 cases (18.2%), 20–29 years in 70 cases (20.9%), 30–39 years in 63 cases (18.8%), 40–49 years in 43 cases (12.8%), 50–59 years in 39 cases (11.6%), and over 60 years in 34 cases (10.2%). Seventy patients (20.9%) were children (0–17 years), and 265 patients (79.1%) were adults. Male patients were almost equally affected by the disease (50.5%, n = 169) like female patients (49.5%, n = 166). The mean age was comparable (p = 0.222) in both male (32.4 ± 18.2) and female (34.8 ± 17.2) patients.

Table 1.

Distribution of Trichinellosis Patients According to Year of Hospitalization

Year of hospitalization	No. of hospitalized cases	Total cases (%)
1996	19	5.7
1997	22	6.6
1998	31	9.2
1999	19	5.7
2000	23	6.9
2001	54	16.1
2002	8	2.4
2003	13	3.9
2004	102	30.4
2005	44	13.1
2006	0	0

Medical records of 335 patients found to have trichinellosis during 1996–2006 at Clinical Hospital in Arad, Department of Infectious Diseases, have been analyzed. We retrospectively collected the following data from their medical records: registration number of the medical record, age, sex, address, date and length of hospitalization, profession, clinical symptomatology, course of the disease, routine laboratory investigations, and specific therapy. Diagnosis was confirmed according to the algorithm for diagnosing an acute infection with Trichinella in humans (Dupouy-Camet et al. 2002, Dupouy-Camet and Murrell 2007). Four distinct groups (A–D) of diagnostic criteria have been employed; all patients presented any symptom from both group A (fever, eyelid/facial edema, and myalgia) and group B (diarrhea, neurological signs, cardiological signs, conjunctivitis, subungual hemorrhages, and cutaneous rash), at least one criterion from group C (eosinophilia [defined as eosinophil value over 5%], and increased serum creatine phosphokinase and lactate dehydrogenase levels), and one finding from group D (positive muscular biopsy, which was the main confirmation criterion, in 288 patients [86%] and positive serology [detection of anti-Trichinella-specific antibodies in serum by enzyme linked immunosorbent assay or Western blot techniques] in 47 patients (14%). Serology has been performed beginning with 2004 in private laboratories from abroad, and the costs were covered by the patients themselves. The main confirmation criteria followed the international guideline: any of group A or group B, one C, and one D. In addition, the result of trichinelloscopic examination of the meat consumed by the patients was positive in all cases.

The clinical stages of trichinellosis were reported according to the following criteria:

Severe form—very pronounced signs and symptoms of the disease (including myalgia lasting for 2 or 3 weeks, edema extended to extremities, prolonged fever persisting between 2 and 3 weeks, metabolic disturbances, and circulatory or neurological complications)

Moderately severe form—pronounced signs and symptoms of the disease (including myalgia lasting between 1 and 2 weeks, facial and eyelid edema, and fever persisting for between 1 and 2 weeks) with benign and transient complications (if present)

Benign form—mild signs and symptoms of the disease (including myalgia and fever lasting under 1 week) without complications

Statistical evaluation was performed using the software package SPSS version 15.0 for Windows. All patient characteristics are expressed as mean ± standard deviation. Patient groups were compared using the analysis of variance (ANOVA). A p-value less than 0.05 was regarded as statistically significant.

Results

Two hundred and seventeen patients (64.8%) were inhabitants of rural areas, and 118 (35.2%) lived in urban areas. There was a statistically significant difference (p = 0.024) between the mean age of urban (36.5 ± 17.2) and rural (31.9 ± 17.8) inhabitants. Winter was the season with the highest prevalence—240 cases (71.6%)—followed by spring with 88 cases (26.3%), summer with 4 cases (1.2%), and autumn with 3 cases (0.9%).

The length of hospital stay ranged between 2 and 86 days (11.2 ± 8.5) with the following distribution: 1–7 days in 115 cases (34.3%), 8–14 days in 154 cases (46%), and 15–30 days in 60 cases (17.9%), and it exceeded 30 days in 6 cases (1.8%). A maximum period of hospitalization was observed in patients belonging to the age group of 30–39 (12.5 ± 13.5 days) and over 60 (12.5 ± 6.3 days), respectively. There was no statistically significant difference between age groups as regard the hospitalization period (p = 0.408).

Most of the adult patients were semiskilled laborers and people with limited formal education (34.7%). The remaining groups by vocation were unemployed (23.8%), office workers (5.7%), retired (17.3%), and other (1.9%). For 44 patients (16.6%), the profession was not specified in the medical record.

The clinical pattern of the disease in the study group is shown in Table 2. For 49 patients (14.6%), the form of the disease was not specified in their medical records; 9 patients (2.7%) presented with a benign form; 188 patients (56.1%) presented with a moderately severe form of trichinellosis; 89 patients (26.6%) presented with a severe form, among whom one developed encephalitis and another one died of myocarditis.

Table 2.

The Clinical Pattern of Trichinellosis Patients (n = 335)

Symptom/sign	No. of patients	Symptom (%)
Fever	286	85.4
Myalgia	278	83
Eyelid, facial, or limb edema	217	64.8
Gastrointestinal manifestations (diarrhea, nausea, vomiting, constipation, and epigastric pain)	127	37.9
Headache	118	35.2
Asthenia	83	24.8
Cutaneous rash (accompanied or not by pruritus)	29	8.7
Ocular pain	15	4.5
Conjunctivitis, conjunctival hemorrhages	7	2.1

The eosinophil values for trichinellosis patients are shown in Table 3, and the leucocyte values are listed in Table 4. The normal range for eosinophils and leucocytes was considered 0–4.99% and 4000–10,000 cells/mm³, respectively. Among the muscle enzymes, elevated creatine phosphokinase values (over 200 U/L) were reported in 302 patients (90.2%), and lactate dehydrogenase values over 300 U/L were documented in 289 patients (86.3%).

Table 3.

Distribution of Trichinellosis Patients According to Eosinophil Values

Eosinophil value (%)	No. of cases	Total cases (%)
0–4.99	53	15.8
5–9.99	23	6.9
10–19.99	57	17
20–29.99	65	19.4
30–39.99	35	10.5
40–49.99	42	12.5
Over 50	18	5.4
Unspecified	42	12.5

Table 4.

Distribution of Trichinellosis Patients According to Leucocyte Values

Leucocyte value (cells/mm³)	No. of cases	Total cases (%)
Less than 10,000	195	58.2
10,000–20,000	93	27.8
Over 20,000	4	1.2
Unspecified	43	12.8

Regarding the specific treatment of the disease (antihelminthics and corticotherapy), 184 patients (54.9%) were treated only with an antihelminthic drug, 87 patients (26%) received an association of an antihelminthic drug and corticotherapy, and 15 patients (4.5%) received only corticotherapy. None of the above-mentioned categories of drugs were administered in 49 cases (14.6%). Among the antihelminthic drugs, 94 patients (34.7%) were treated with Thiabendazole, 43 patients (15.9%) with Mebendazole, and 134 patients (49.4%) with Albendazole.

Consumption of pork was responsible for the disease in all cases.

The trichinellosis-affected localities are shown in Figure 1. Most of the cases diagnosed during the above-mentioned period of time occurred in Arad city (26.2%, n = 88), Zimandu Nou (9.2%, n = 31), Simand (7.7%, n = 26), Fantanele (6.8%, n = 23), Sagu (6.6%, n = 22), Sepreus (6.6%, n = 22), Chisindia (4.5%, n = 15), Bata (3.6%, n = 12), and Secusigiu (3.3%, n = 11). The most relevant outbreaks (involving at least 10 patients with confirmed trichinellosis) occurred as follows: 22 patients in Sagu village (2004), 19 patients in Arad city (1996), 18 patients in Sepreus village (2001), 17 patients in Zimandul Nou village (1998), 15 patients in Chisindia village (2005), 12 patients in Bata village (2001), and 11 patients in Simand village (2004).

FIG. 1.

Map of Arad County's localities. The shadowed areas correspond to the localities where trichinellosis cases were registered during 1996–2006.

Discussion

Human trichinellosis is estimated to affect an average of 10,000 people per year worldwide (Dupouy-Camet and Murrell 2007), being most frequently reported in east European countries like Serbia, Croatia, Montenegro, Bosnia-Herzegovina, Romania, Bulgaria, Slovakia, and Poland (Pozio 2007).

Trichinella spiralis and Trichinella britovi are the main infective species in Romania (International Trichinella Reference Center—The database of Trichinella strains, http://www.iss.it/site/Trichinella/scripts/dedb.asp). During 1963–1968, human trichinellosis in Romania averaged 79.7 cases per year, and from 1969 to 1986, between 250 and 400 cases were reported each year (Cuperlovic et al. 2005). In some cases, diagnosis was retrospectively established at necropsy or accidentally during a circumstantial public health investigation (Cironeanu and Ispas 2002). Between 1990 and 1999, the yearly incidence of the disease in Romania was 5.5 cases/10⁵ inhabitants (Olteanu 2001, Blaga et al. 2007, Pozio 2007). The large Romanian industrial farms did not contribute to the eradication of the disease among swine; on the contrary, they were the source for Trichinella spreading to the small holdings (Cuperlovic et al. 2005).

Political and economic changes, and revolutions and wars have contributed to an increase of trichinellosis among the human population (Cuperlovic et al. 2005, Pozio and Zarlenga 2005, Pozio 2007). Since 1989, the year that brought a change in social, economic, and political systems (a transition from communism to capitalism), there have been reports of human trichinellosis, as follows: 1031 cases in 1990, 1965 cases in 1995, 1175 cases in 2000, and 780 cases in 2004 (Centre of Sanitary Calculation, Statistics and Documentation CCSS, Bucharest). Most of the human outbreaks occurred in the western parts of the Romania, an area where some of the favorite traditional dishes are prepared from raw or under-cooked pork (Neghina et al. 2009).

This 11-year surveillance reports an incidence rate for Arad County of 6.6 cases per 10⁵ persons per year, during 1996–2006. Most of the patients belonged to the age group of 20–29 years (20.9%), similar to another Romanian extensive study (23.22%) performed in Timis County, Romania, during 1990–2005 (Neghina et al. 2009). A recent study on 95 cases of trichinellosis in Germany during exactly the same period, 1996–2006, has also found the highest age-specific incidence for patients 20 to 29 years old (Jansen et al. 2008). The present study, similar to the other two studies mentioned above, shows a slight higher predominance of trichinellosis in males: 50.5% versus 53% in the German surveillance (Jansen et al. 2008), and 53.17% in Timis County surveillance (Neghina et al. 2009), respectively. This could be explained by the fact that men are more involved in the slaughtering process and in preparing the traditional homemade pork products. Most of the patients (64.8%) were inhabitants of the rural areas where a lot of pigs are raised and slaughtered in improper hygienic conditions and where there is a preference for homemade products over commercially processed meat products, the latter being considered nonappetizing by rural farmers.

This study registered a peak of trichinellosis cases (30.4%, n = 102) in 2004 due to some regional outbreaks. As a result, another 31 human patients were found to have in the neighborhood county, Timis, in the same year (Neghina et al. 2009). Winter was the season with most of the cases (71.6%) both in this study and in other studies from Timis County (81%) (Neghina et al. 2007) and from Jiu Valley region, Romania (84.9%) (unpublished data). This finding is unsurprising considering that backyard pigs are slaughtered at home without veterinary inspection especially during the winter holidays when, traditionally, a lot of pork homemade products (sausages, ham, bacon, blood pudding, and mosaic salami) are consumed.

The majority of the trichinellosis patients are laborers or unemployed, generally persons with low incomes who live in very poor hygienic conditions.

The most frequent signs of the disease were fever (85.4%), similar to the major epidemic from 1973 (89%), and myalgia (83%), which was found in the same percentage in the German study (83%) (Jansen et al. 2008) and in a similar percentage in another Romanian study performed by the authors in Hunedoara County (1996–2005) (85.5%) (unpublished data). The moderately severe form of the disease was predominant (56.1%), and the length of the hospital stay ranged from 8 to 14 days for most of the cases (46%). One 70-year-old patient developed myocarditis and died of cardiac failure (2001), an incident also observed in the Timis County surveillance. Myocardial damage due to trichinellosis has been observed worldwide (Compton et al. 1993, Siwak et al. 1994, Franco-Paredes et al. 2007). Hospitalization of the affected patients required considerable healthcare resources.

Albendazole, one of the principal antihelmintics used for trichinellosis, was the specific drug administered for the most of the patients. The hospitalization period was shorter for patients who were treated either with Albendazole alone (8.2 ± 4.1 days) when compared to those treated with Mebendazole alone (11.7 ± 5.5 days) and Thiabendazole alone (14.8 ± 12.5 days), respectively. In patients who required corticosteroid-associated therapy, Albendazole proved as the most efficient antihelmintic drug—the mean hospitalization period was 8.8 ± 3.3 days. Those who received Thiabendazole in combination with corticotherapy required a longer period of hospital stay (14.8 ± 4.7 days). Thiabendazole, a drug no longer being considered of choice due to its multiple side effects (intolerable dizziness, urticarial and maculopapular rash, tinnitus, and gastrointestinal disturbances) (Dupouy-Camet et al. 2002, Dupouy-Camet and Murrell 2007), was administered in some patients due to economical and practical reasons: during some time it was the only specific drug available, received as a donation from abroad.

This retrospective study demonstrates that trichinellosis still remains a concern and a major public health issue in Arad County, Romania. Implementation of routine meat inspection for Trichinella larvae is the primary effort in the prevention and control of trichinellosis. Proper food preparation steps must be followed to prevent infection (Neghina et al. 2009). Contributions toward successful prevention and early diagnosis of the disease are expected to be brought about by the family medicine physicians from the primary medical assistance system, who can easily facilitate the access of their patients to some trichinellosis informational brochures during regular visits. The later the patient addresses to the physician, the more difficult the treatment is and the greater the risk is in turning into the chronic form of the disease with severe sequelae and sometimes fatal outcome (Cironeanu and Ispas 2002). Another major issue is represented by the limited hospital funds that cannot cover the costs of serologic tests required for the confirmation of the disease; therefore, these are replaced by muscular biopsy in most of the cases. The only laboratory tests available for the physicians are the routine ones, among which eosinophil value plays an important role.

According to the historical references that bear similarities to the clinical aspects of trichinellosis, this severe infection first striking in antiquity (Pozio and Murrell 2006) must be carefully followed up as a sanitary priority especially in high endemic countries like Romania.

Footnotes

Disclosure Statement

Funding, none; competing interests, none declared; ethical approval, not required.

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