Seasonal Prevalence of Intestinal Parasites in the United States During 2000

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Seasonal Prevalence of Intestinal Parasites

in the United States During 2000

 

Omar M. Amin

 

Parasitology Center, Inc., Tempe, Arizona; Laboratorio Analisis

Clinicos, Nogales, Sonora, Mexico

 

Copyright 2002 by The American Society of Tropical Medicine and Hygiene

Am J. Trop. Med. Hyg., 66(6), 2002, pp. 799-803

 

Abstract.

 

One-third of 5,792 fecal specimens from 2,896 patients in 48 states

and the District of Columbia tested positive for intestinal parasites

during the year 2000. Multiple infections with 2 – 4 parasitic

species constituted 10% of 916 infected cases. Blastocystis hominis

infected 662 patients (23% or 72% of the 916 cases). Its prevalence

appears to be increasing in recent years. Eighteen other species of

intestinal parasites were identified. Cryptosporidium parvum and

Entamoeba histolytica/E. dispar ranked second and third in prevalence,

respectively. Prevalence of infection was lowest (22 – 27%) in

winter, gradually increased during the spring, reached peaks of 36 –

43% between July and October, and gradually decreased to 32% in

December. A new superior method of parasite detection using the

Proto-fixTM-CONSEDTM system for fixing, transport, and processing of

fecal specimens is described. In single infections, pathogenic

protozoa caused asymptomatic subclinical infections in 0 – 31% of the

cases and non-pathogenic protozoa unexpectedly caused symptoms in 73 –

100% of the cases. The relationship between Charcot-Leyden crystals

and infection with four species of intestinal parasites is examined

and the list of provoking parasitic causes is expanded.

 

INTRODUCTION

 

Parasitologic investigations of large patient populations are

rarely conducted in the United States, where the illusion of freedom

from parasitic infections still predominates. Such investigations are

considerably more common in third-world countries where endemic

parasitoses are more readily documented.1 In an attempt to address

this problem we reported the results of routine examination of fecal

specimen for parasites from 644 patients in the United States during

the summer of 1996.1 Prevalence, patient age and sex, and intestinal

and extra-intestinal symptoms, as well as variables related to foreign

travel, infected household contacts, and previous parasitic infections

were reported. An expanded version of the summer 1996 report is

herein presented, in which complete seasonal data of 12 species of

parasites from a considerably larger population is analyzed with

emphasis on prevalence, symptomology, and Charcot-Leyden crystals.

Few studies of large patient populations in the United States2,3 or

more geographically limited populations, e.g., California4 or Ontario,

Canada,5 have been reported.

 

MATERIALS AND METHODS

 

A total of 5,792 fecal specimens from 2,896 patients (two

specimens per patient) were collected and transported to Parasitology

Center, Inc., (Tempe, Az) in Proto-fixTM in plastic vials provided in

mailable kits by UROKEEP (Chandler, Az). Specimens were collected

throughout the United States between January and December 2000

following physician's orders. Tests were ordered either as part of

routine medical examinations or when patients experience changes in

bowel habits, energy level, or normalcy after a foreign trip, bad

meals, or other exposures. Specimens were processed and stained in

CONSEDTM according to manufacturer's (Alpha-Tec Systems, Inc.,

Vancouver, WA) directions. This procedure was used in 10, 358

specimens by 1998, and was described, fully evaluated, and compared

with other methods.6 The number of specimens found positive (number of

individuals and of species of parasites) was significantly higher than

in other methods compared, e.g., formalin-ethyl acetate or trichrome

stain.6 These observations were supported by findings of other

observers.7,8 The Proto-fixTM-CONSEDTM system involves filtering of

fixed specimens, mixing with CONSEDTM and ethyl acetate, vortexing,

centrifugation, decanting all but the fecal plug, and mixing with

CONSEDTM diluting reagent. The plug is then transferred to and

mounted on a slide for examination.6 All microscopic evaluations and

identification were made by the same observer(s) blinded to patient

information, e.g., symptoms, travel, etc. Positive results were

quantified (number of organisms per high-power field on a scale of 1

to 4) from duplicate samples from the same patient.

 

RESULTS

 

Prevalence. Nine hundred sixteen (32%) of 2,896 tested patients

were infected with 18 species of intestinal parasites in the year 2000

(Table 1) in 48 states and the District of Columbia as follows:

Alabama (2 infected of 3 tested, 67%), Alaska (6 of 14, 43%), Arizona

(79 of 279, 28%), Arkansas (2 of 8, 25%), California (314 of 859,

36%), Colorado (17 of 88, 19%), Connecticut (4 of 24, 17%), Delaware

(0 of 3, 0%), Florida (18 of 64, 28%), Georgia (28 of 72, 39%), Hawaii

(5 of 9, 55%), Idaho (2 of 5, 40%), Illinois (30 of 92, 33%), Indiana

(20 of 74, 27%), Iowa (16 of 44, 36%), Kansas (1 of 2, 50%), Kentucky

(1 of 6, 17%), Louisiana (1 of 4, 25%), Maine (27 of 86, 31%),

Maryland (15 of 64, 23%), Massachusetts (18 of 61, 29%), Michigan (4

of 22, 18%), Minnesota (10 of 28, 36%), Mississippi (1 of 2, 50%),

Missouri (4 of 10, 40%), Montana (2 of 4, 50%), Nevada (7 of 28, 25%),

New Hampshire (2 of 9, 22%), New Jersey (20 of 81, 25%), New Mexico

(55 of 140, 39%), New York (75 of 230, 33%), North Carolina (3 of 16,

19%), Ohio (5 of 23, 22%), Oklahoma (1 of 2, 50%), Oregon (44 of 135,

33%), Pennsylvania (16 of 81, 20%), Rhode Island (2 of 9, 22%), South

Dakota (0 of 2, 0%), Tennessee (1 of 3, 33%), Texas (21 of 90, 25%),

Utah (2 of 7, 29%), Vermont (3 of 11, 27%), Virginia (5 of 20, 25%),

Washington (12 of 36, 33%), Washington DC (3 of 8, 37%), West

Virginia (2 of 4, 50%), Wisconsin (9 of 33, 27%), and Wyoming (1 of 5,

20%). Blastocystis hominis was the most frequently detected parasite

in single and multiple infections, with Cryptosporidium parvum and

Entamoeba histolytica/E. dispar ranking second and third,

respectively. All parasites and their prevalences are listed in Table 1.

 

Symptoms. The term symptom in this study is defined as any change

in normal body function induced by direct or indirect action of

parasites. Direct action includes invasiveness and tissue damage due

to parasite feeding or migration. Indirect action results from

parasite metabolic byproducts and toxic secretions. Symptoms are in

two categories: 1) gastrointestinal, including (in order of observed

frequency) flatulence, diarrhea, bloating, abdominal cramping,

constipation, malabsorption / maldigestion, bloody or odorous stool,

irritable bowel, mucus, and leaky gut, and 2) extra-intestinal

(systemic), including (in order of observed frequency) fatigue,

nervous/sensory disorders, pain, skin disorders, allergies, nausea,

muscle weakness/pain, immune deficiencies, headache, fever/ night

sweats, insomnia, and weight changes. Most infected patients with

parasitic symptoms experienced 1 – 4 gastrointestinal and/or

extra-intestinal symptoms; they are simply called symptoms.

 

Of the 826 patients with single infections, 584 (70%) experienced

overt symptoms and 242 (30%) had none (Table 2). Infections with

pathogenic protozoa included 0 – 31% asymptomatic infections.

Protozoans regards as non-pathogenic were associated with symptoms in

69 – 100% of the cases. Ascaris lumbricoides produced no symptoms in

one of 12 cases.

 

Multiple infections. Ninety patients (10% of cases) were

concurrently infected with 2 – 4 species of parasites. Among these,

21 patients experienced no symptoms. These 21 cases involved 19

infections with B. hominis, 7 with C. parvum, 6 with Endolimax nana, 5

with E. histolytica/E. dispar, 4 with Giardia lamblia, 3 with

Entamoeba coli, 2 with Chilomastix mesnili, Cyclospora cayetanensis,

and Iodamoeba butschilii, and 1 with Retortomonas intestinalis. The

remaining 69 patients with concurrent infections were symptomatic.

These 69 cases involved 58 infections with B. hominis, 22 with C.

parvum, 19 with E. coli, 18 with E. histolytica/E. dispar, 16 with E.

nana, 5 with C. cayetansis and G. lamblia, 2 with Ascaris

lumbricoides, and 1 with C. mesnili, Dientamoeba fragilis, Entamoeba

hartmanni, I. Butschlii, R. intestinalis, and Taenia sp.

 

Seasonality. Monthly seasonal prevalence of single and multiple

infections gradually increased from a minimum in February to a maximum

between August and October, then decreased in December. Prevalence of

infection with Blastocystis hominis was lowest in May and highest in

September and November. Peak prevalences were observed in C. parvum

in the spring (March). Oscillations in seasonal frequencies were not

dramatic in other parasite species and most were represented in all

seasons (Table 1).

 

Charcot-Leyden crystals. These crystals were found in 34

specimens of which 21 (62%) were infected with B. hominis, C. parvum,

E. histolytica/E. dispar, and G. lamblia. No parasites were detected

in the remaining 13 (38%) species (Table 3).

 

DISCUSSION

 

This study population was demographically similar to the 644

patient population studied during the summer of 1996 under the same

circumstances by Parasitology Center Inc.1 In the present study,

overall infection prevalence rates were comparable throughout the

country and did not vary much between the southwest, the west coast,

the Midwest, and the east coast. Only the larger sample sizes are

considered. Patient age was between 0 and 80 years, approximately

twice as many females (1,945) than males (951) were tested, relatively

more cases (550 of 916, 60%) had a history of foreign travel than

non-cases (970 of 1980, 49%) within the last five (P< 0.001, by

Fisher's exact test relative risk [RR] = 1.36, confidence interval

[CI] = 1.22 – 1.52. Relatively more infected (110 of 916, 12%) than

uninfected (198 of 1980, 10%) patients lived with infected household

contacts (P = 0.117, not significant, by Fisher's exact test).

 

Our new methods of parasite detection, adopted since 1996,

reflected prevalence rates considered closer to true prevalences

compared with standard methods used.6 By 1998, 3,373 (32.6%) of 10,

358 specimens examined at Parasitology Center, Inc. were infected with

parasites.6 An almost identical prevalence of 32% is reported in this

study (Table 1). This prevalence is markedly higher than reported

prevalences in the United States of 20% (from 216,275 stool specimens)

and 19.7% (from 178,786 stool specimens) reported by state diagnostic

laboratories in 1987.2 The markedly higher prevalence in our study

(P<0.001 by Fisher's exact test, RR = 1.9, CI = 184 – 1.99) suggests

real increases in prevalence but does not exclude the possibility of

differences in test populations. The results of the latter report

also differ significantly from our finding in the composition of the

component parasites species found, e.g., B. hominis was diagnosed in

only 2.6% of the specimens examined compared with 23% (or 72% of all

infected cases) in our study. In a 1984 study of 2,360 patients in

the United States, prevalences of 20.6% for all parasitic species and

12.2% for cases of B. hominis infections were reported with B. hominis

constituting 59% of all infections.3 The latter figure is much closer

to our current finding of a B. hominis prevalence of 72% among all

parasitic infections (Table 1). In 1995, overall B. hominis

prevalences of 20 – 30% and greater than 15% were also reported from

an unspecified number of patients.9

 

The prevalence of B. hominis reported herein (23%) is one of the

highest ever reported in the United States and may be

epidemiologically significant. Increasing prevalences are noted in

more recent years. This prevalence is closest to that reported for

Argentina (25%)10 and Switzerland (16.7 – 19.0%)11 but considerably

lower than those in other studies from Argentina (43%)12 and Chile

(61.8%)13

 

The second most prevalent parasite found was C. parvum (Table 1).

Prevalences reported in surveys from North America (0.6 – 4.3%) and

Europe (1 – 2%) are significantly lower than those reported for Asia,

Australia, Africa, Central America, and South America (3 – 20%).14

Cryptosporidium parvum appears to be underdiagnosed in the western

hemisphere; its seroprevalence in Europe and North America is usually

between 25% and 35%.14 In a recent survey of 279 children from three

clinics along the Texas-Mexico border 96 children (70.2%) were found

infected with C. parvum.15 Children living in a large non-border

urban area were less frequently infected , drank more bottled water,

and came from households with higher income.15 Cryptosporidium

oocysts were observed in 27% of the drinking water samples taken from

66 surface water treatment plants in 14 states and one Canadian

province.16

 

The E. histolytica/E. dispar prevalence (Table 1) is markedly

higher than the prevalence of 0.9% reported in a large survey in 1987

in the United States, but lower than the estimated prevalence of 4% in

the United States.17 In developing countries with poor sanitation, the

prevalence may reach as high as 50%.17 prevalences quoted for E.

histolytica infections are clearly misleading since more than 90% of

these infections are due to E. dispar.17,18 In the Philippines, a

polymerase chain reaction survey of 1,872 patients detected 137 stools

(7.3%) containing E. dispar and 18 stools (1.0%) containing E.

histolytica.19 The importance of developing a simple and inexpensive

way of distinguishing the two species to obtain information on true

prevalence, pathogenecity, and treatment can not be overlooked.

 

The remaining parasites recovered in this study were of minor

importance and their overall prevalence was comparable or somewhat

lower than those reported in other surveys. The very low prevalence

of C. cayetensis agrees with other findings, suggesting under

diagnosis in indigenous populations in the United States.20

 

Symptoms in 826 singly infected patients did not always agree with

the purported pathogenecity of the parasites involved (Table 2).

Approximately one third of B. hominis infections were not associated

with symptoms. Asymptomatic infections with B. hominis varied between

30% and 60% in various populations in the United States.1,3,9,21,22

In Canada, B. hominis is usually asymptomatic.5 It is not known if

the degree of pathogenicity of B. hominis is related to the distinct

immunologic, serologic, and genetic identity of the demes constituting

that species.23,24 The epidemiologic significance of these findings

and the B. hominis species complex question remain to be resolved. We

regard B. hominis as a species complex usually showing pathogenicity

based on our findings (Table 2) and those reported by others; see the

review by Garcia.25 This parasite will cause asymptomatic subclinical

infections similar to most pathogens.

 

Asymptomatic periods in the intermittent and recurrent infectious

cycle of C. cayetensis are evident and may be attenuated with

long-term suppressive therapy. During the asymptomatic periods, C.

cayetensis is often absent (undetectable) in stool specimens.

Asymptomatic infections with C. parvum are directly related to the

immune status of the host26 and have been previously reported in

immuno-competent persons.14 The asymptomatic cases of E.

histolytica/E. dispar are attributed to E. dispar infections. These

observations also apply to the 21 asymptomatic patients of the 90

(23%) multiply infected cases.

 

Six species of presumably non-pathogenic protozoa singly infecting

72 patients were associated with symptoms (Table 2). It is our

experience that a host body, particularly if immune-compromised, will

not be indifferent to the presence of foreign organisms irrespective

of their purported non-pathogenic status. Until recently, B. hominis

was considered to be a harmless yeast. The literature is beginning to

show awareness of the pathogenic potential of such " harmless "

organisms such as Dientamoeba fragilis,25,26 E. coli,1,27,28 and E.

hartmanni.1,25,29 The non-pathogenic status of these organisms is

questioned in light of our findings.

 

Seasonal studies of human parasite infections are rarely conducted

in the United States. An increase in the prevalence of C. parvum

(comparable to ours) in the spring observed in patients from New

Orleans30 and elsewhere14 was attributed to the warm wet spring

weather. However, our overall seasonal data and that of B. hominis

show the highest prevalence between August and October. The latter

dates do not essentially negate possible spring/early summer

prevalence peaks. Exposure, experiencing symptoms, seeking medical

help, and testing may explain this time lag.

 

Charcot-Leyden crystals are breakdown products of eosinphils found

usually in feces and occasionally in sputum and body tissues.31 The

crystals have been traditionally associated with E. histolytica

infections,32 but have been more recently found in patients infected

with Ancylostoma spp., A. lumbricoides, Isospora belli, and Trichuris

trichura.25 In the present study, it was also found in patients

singly infected with B. hominis, C. parvum, and G. lamblia. The 13

patients with crystals but with no detectable infections were probably

infected with a cyclic parasite such as E. histolytica.

 

REFERENCES

 

1. Amin OM, 1997. Prevalence and host relationships of intestinal

protozoan infections during the summer of 1996. Explore 8: 26 – 35

2. Kappus KD. Lundgren RG Jr, Juranek DD, Roberts JM, Spencer HC,

1994. Intestinal parasitism in the United States: update on a

continuing problem. Am J Trop Med Hyg 50: 705-713

3. Garcia LS, Bruckner DA, Clancy MN, 1984 Clinical relevance of

Blastocystis hominis (letter). Lancet ii: 1233-1234

4. Conteas CN, Berlin OGW, Lariviere MJ, Pandhumas SS, Speck CE,

Forschen R. Nakaya T. 1998. Examination of the prevalence and

seasonal variation of intestinal microsporidiosis in the stools of

persons with chronic diarrhea and human immunodeficiency virus

infection. Am J Trop Med Hyg 58: 559 – 561

5. Senay H. MacPherson D, 1990. Blastocystis hominis: epidemiology

and natural history. J Infect Dis 162: 987 – 990

6. Amin OM, 2000. Evaluation of a new system for the fixation,

concentration, and staining of intestinal parasites in fecal

specimens, with critical observations on the trichrome stain. J.

Microbiol. Meth 39: 127 – 132

7. Allen K, Frankel JW, 1997. Comparison of CONSEDTM and

formalin-Ethyl Acetate Methods for Concentrating Intestinal Parasites

and Eggs. American Society for Microbiology. Annual Meeting, Helen,

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8. Jensen B, Kepley W. Gauner J, Anderson K, Anderson D, Clairmont

J, Austin GE, 2000. Comparison of polyvinyl alcohol fixative with

three less-hazardous fixatives for the detection of intestinal

parasites. J. Clin Microbiol 38: 1592 – 1598

9. Lee MJ, 1995. Parasites, yeasts and bacteria in health and

disease. J Adv Med 8: 121 – 130

10. Ponce de Leon P, Svetaz MJ, Zdero M, 1991. Importance of

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1990. Etiology of acute enteritis in immunocompetent and HIV-infected

patients Schweiz Med Wochenschr 120: 1253 – 1256

12. Borda CE, Rea MJF, Rosa JR Maidana C, 1996. Intestinal

parasitism in San Cayetano, Corrientes, Argentina. Bol Oficina Sanit

Panam 120: 110 – 116

13. Torres P, Miranda JC, Flores L, Riquelme J, Franjola R, Perez J,

Auda S, Hermosilla C, Riqhelme S, 1992. Blastocystis and other

intestinal protozoan infections in human riverside communities from

Valdivia River Basin, Chile. Rev Inst Med Trop Sao Paulo 34: 557 – 564

14. Current WL, Garcia LS, 1991. Crytosporidiosis. Clin Lab Med 11:

873 – 895

15. Leach CT, Koo FC, Kuhls TL, Hilsenbeck SG, Jenson HB 2000.

Prevalence of Cryptosporidium parvum infection in children along the

Texas-Mexico border and associated risk factors. Am J Trop Med Hyg

62: 656 – 661.

16. LeChevallier MW, Norton WD Lee RG, 1991. Giardia and

Cryptosporidium spp. in filtered drinking water supplies. Appl Env

Microbiol 57: 2617 – 2621

17. Kelsall BL, Ravdin JI, 1994. Amebiasis: Human infection with

Entamoeba histolytica. Tsieh S, ed. Progress in Clinical

parasitology. Ann Arbor, Mi: CRC Press 4: 27 – 54

18. Clark CG, 1998. Entamoeba dispar, an organism reborn. Trans R

Soc Trop Med Hyg 92: 361 – 364

19. Rivera WL, Tachibana H, 1998. Field study on the distribution

of Entamoeba histolytica and Entamoeba dispar in the northern

Philippines as detected by the polymerase chain reaction. Am J Trop

Med Hyg 59: 916 – 921

20. Soave R, 1996. Cyclospora: An overview. Clin Infect Dis 23:

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21. Udkow MP, Markell EK, 1993. Blastocystis hominis: Prevalence

in asymptomatic versus symptomatic hosts. J Infect Dis 168: 242 – 244

22. Grossman I, Weiss LM, Simon D, Tanowitz HB Wittner M, 1992.

Blastocystis hominis in hospital employees. Am J Gastroentrol 87:

729 – 732

23. Boreham PFL, Upcroft JA, Dunn LA, 1992. Protein and DNA

evidence for two demes of Blastocystis hominis from humans. Int J

Parasitol 22: 49 – 53

24. Mueller HE, 1994. Four serologically different groups within

the species Blastocystis hominis. Zentralbl Bakteriol 280: 403 – 408

25. Garcia LS, 2001. Diagnostic Medical Parasitology. Washington,

DC; American Society for Microbiology

26. Cuffari C, Oligny L, Seidman EG, 1998. Dientamoeba fragillis

masquerading as allergic colitis. J Pediatr Gastroenterol Nutr 26:

16 – 20

27. Corcoran GD, O'Connell B, Gilleece A, Mulvihill TE, 1991.

Entamoeba coli as a possible cause of diarrhea (letter). Lancet 338:

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28. Wahlgren M, 1991. Entamoeba coli as a cause of diarrhea

(letter). Lancet 334: 675

29. Marquardt WC, Demaree RS Jr, 1985. Parasitology. New York:

MacMillan

30. Inungu JN, Morse AA, Gordon C, 2000. Risk factors seasonality,

and trends of cryptosporidiosis among patients intected with human

immunodeficiency virus Am J Trop Med Hyg 62: 384-387.

31. Ash LR, Orihel TC, 1997. Atlas of Human Parasitology. Chicago:

American Society of Clinical Pathologists.

32. Belding DL, 1942. Textbook of Clinical Parasitology. New York:

D. Appleton-Century Co.

 

Acknowledgments: Appreciation is extended to Karim O. Amin for

technical help and support

 

Author's address: Omar M. Amin, Parasitology Center Inc., 903 South

Rural Road, #101-318, Tempe, Az 85281 and Laboratorio Analisis

Clinicos, Av. Obregon 28-9, Nogales, Sonora, Mexico.

 

Reprint requests: Omar M. Amin, PO Box 28372, Tempe, Az 85285.

The Parasitology Center, Inc., PCI, offers laboratory testing for the

detection of human parasitic infections and toxicities from

neurocutaneous syndrome; practitioners and patients can contact the

lab: phone (480) 767-2522; fax (480) 767-5855

 

email OmarAmin

 

Web address: www.parasitetesting.com