Diphyllobothriasis

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Practice Essentials

Diphyllobothriasis is a fish-borne zoonotic infection with the cestode Diphyllobothrium latum (see the image below) or other similar species (eg, Diphyllobothrium nihonkaiense, Diphyllobothrium dendriticum, Adenocephalus pacificus, Diplogonoporus balanopterae). It is endemic in para-polar areas where humans consume raw or pickled fish. Diphyllobothriasis can manifest as symptoms of intestinal obstruction, vitamin B-12 deficiency, and/or, most commonly, passage of proglottids in the stool. The scope of infection has become more cosmopolitan with the increasing popularity of ethnic raw fish–containing food and the rapid global distribution of fresh foodstuff.



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Egg of Diphyllobothrium latum with arrow pointing to operculum.

Signs and symptoms

Most persons with diphyllobothriasis are asymptomatic. In symptomatic persons, the following are the most common symptoms:

Other, less common, symptoms include the following:

Most patients with diphyllobothriasis have no signs of illness. Very rare physical findings that may be noted include the following:

In patients who present with obstruction, the following physical findings may be noted:

See Presentation for more detail.

Diagnosis

Laboratory studies that may be helpful for diphyllobothriasis include the following:

Other studies that may be considered are as follows:

See Workup for more detail.

Management

Most patients with diphyllobothriasis, unless they have severe symptoms, can be safely treated as outpatients.

Treatment of the infection is pharmacologic, involving one of the following agents:

If the first course of treatment fails, a second identical course of therapy may be administered.

Other aspects of treatment include the following:

See Treatment and Medication for more detail.

Background

Diphyllobothriasis is defined as human intestinal infection with the cestode D latum, D nihonkaiense, or other broad tapeworm species. It is acquired by ingestion of inadequately cooked or frozen freshwater, anadromous, or marine fish containing larvae called plerocercoids, either in fish muscle or on serosal surfaces.[1] Most individuals with diphyllobothriasis have minimal or minor gastrointestinal symptoms, and the most common presentation is passage of worm segments (ie, proglottids).

Adult D latum is the largest human parasite and can grow to a length of greater than 20 meters and live for decades. It is capable of causing vitamin B-12 deficiency through dissociation of the vitamin from intrinsic factor and consumption of the vitamin.[2] This is rare today, but low vitamin B-12 levels have been reported in up to 40% of patients with D latum[1] infestation and 5% of patients with A pacificus infestation.[3] Clinical anemia and neurological disease is much rarer (< 2%).[1]

Evidence of human A pacificus infestation and D latum infestation dates to at least 6,000 years ago in Peru and Germany, respectively, and to 1,000 years ago in Japan (D nihonkaiense),[4] with the first clinical description in Switzerland in 1592. Diphyllobothriasis’s relationship to fish was first noted by Sporing in 1747. The disease appears to have been particularly widespread in Baltic and Alpine freshwater areas up through the early 20th century.[1]

In the early 1970s, an estimated 9 million people were infested with D latum worldwide, with 5 million in Europe, 4 million in Asia, and the remainder in the Americas.[1]

The disease has been notable for its association with temperate climate and rarity in the tropics. In the past 4 decades, with improvement in human sewerage treatment, prevalence has significantly decreased in developed areas. However, some zoonotic infection persists, especially with species other than D latum, owing to nonhuman definitive hosts, including bear, wolves, marine birds, and sea lions.

With the increased popularity of raw seafood as part of ethnic foods, wider and faster food distribution networks, and, possibly, fish aquaculture, diphyllobothriasis seems to be extending its traditional geography and resurging, particularly with species other than D latum.[5, 6]

Pathophysiology

Fish tapeworms have a complex life cycle, with humans, other fish-eating mammals, and birds as their definitive hosts (see image below).



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This illustration depicts the life cycle of different species of Diphyllobothrium parasitic cestodes, the causal agents of the disease diphyllobothria....

Adults are long ribbonlike creatures originally identified based on scolex and egg morphology; increasingly, cytochrome oxidase (cox1) molecular testing has clarified nosology and epidemiology.[6] Except for D latum, which appears specifically adaptive to humans as the preferential host and is by far the most common species involved in human infection, most other species rely on nonhuman definitive hosts, and humans are incidentally infected.[6]

A full-grown Diphyllobothrium worm can range from 1-15 m in length and is the longest human tapeworm. It consists of up to 3000-4000 proglottids. The scolex, as noted, has 2 sucking grooves, also called bothria, which attach to small-intestinal mucosa. Proglottids are typically wider than they are long and contain hermaphroditic sexual parts. Humans and other animals may be infested with multiple worms simultaneously.

In the gravid state, the worms have a distinctive rosettelike uterus in the center. Each adult worm sheds many thousands of operculated eggs every day. To complete their maturation, the eggs must reach water to be eaten by one of 40 species of crustacean copepods and cyclops, within which the procercoid matures.

Copepods that contain the procercoid are then eaten by fish that function as the second intermediate host. Here, the procercoid matures into the plerocercoid in fish muscle or, in the case of D dendriticum and A pacificus, a serosal body surface such as peritoneum or organ such as liver.[7, 3]

Fish surveys of infected lakes can be performed, monitoring risk via inspection of fish muscle or organs for encysted plerocercoids.[8] In 2013-2014, a study of fish caught in Lake Como, Italy, demonstrated infection rates of D latum in pike and perch of 84% and 25%, respectively. This was attributed to popularity of a local dish and breakdown of sewerage effectiveness.[9]

Infected fish are then consumed by progressively larger fish, with the plerocercoid being passed on until, finally, the fish is consumed by a human, the definitive host. Over the subsequent 2-4 weeks, the plerocercoid larva attaches to the host intestine and matures into an adult that can live for up to 20 years.

Table 1. Prevalence of Diphyllobothriasis Infections



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See Table

Plerocercoid larvae infect humans who have ingested infected and inadequately cooked or frozen fish. Because of the requirement for intermediate hosts, direct human-to-human transmission does not occur; therefore, no isolation measures are required.

Most humans with diphyllobothriasis (all forms) are asymptomatic, and the most common presentation is passage of worm parts, which can be alarming. Many patients retrospectively report diarrhea or may present with symptoms of obstruction[10] or even appendicitis[11] . Both vitamin B-12 deficiency and iron deficiency anemia have been attributed to infestation with D latum, but not other species.[1] Because of this, infection might be a concern for women who are pregnant.[12]

Etiology

Diphyllobothriasis is caused by ingestion of raw, undercooked, or unfrozen infected fish and subsequent intestinal infection. The main causative organisms are D latum and D nihonkaiense, but other Diphyllobothrium and similar species have also been reported as infecting agents, albeit much less frequently. Examples include the following:[5]

Epidemiology

Diphyllobothriasis has been traditionally considered an endemic disease of specific locations where consumption of uncooked fish is common, such as Finland, Scandinavia, alpine Europe, North American lakes (D latum), northern Japan (D nihonkaiense), and Peru (A pacificus). With improvements in sanitation and understanding of disease pathogenesis, the prevalence of infection in endemic areas appears to have fallen dramatically during the 20th century.[1] While Japan has mandated case reporting since 2012, little is known about the current prevalence and incidence of various fish tapeworm infections except for case reports and occasional surveys.[13]

Increasing travel, migration, and popularity of ethnic foods have contributed to a broadening of interest and, possibly, exposure to raw fish delicacies, particularly in Asia,[14] but also elsewhere owing to rapid food transport and fish aquaculture.[15]

Examples of foods responsible for infection include raw and salted or marinated fish filets in Scandinavia, Jewish gefilte fish, Italian carpaccio, French tartare maison (raw salmon) and poisson du lac façon nordique, Japanese sushi (raw fish on rice cakes or balls) and sashimi (sliced raw fish), and ceviche (lightly marinated fish) in Latin America. The quality and type of fish, as well as other animal products in dishes, varies by locale and cost, with the highest risk apparently associated with rural restaurants and street vendors. Types of fish and risk may vary by season. The peak risk for D nihonkaiense is associated with the spring catch of cherry and immature chum salmon in Northern Japan. The peak risk for D balanopterae in Northern Japan is associated with the harvest of anchovies from June to August.[13]

Concerns have been raised regarding salmon and other fish aquaculture, particularly in Chile, because of growing salmon smolt in lakes endemic for D latum and potential contamination and escape of infected fish grown in oceanic pens.[15] Such infection might account for infections with D latum in Brazil[16] and other tropical areas such as Taiwan[17] and South India[18] . Similarly, infection with A pacificus in Spain might be associated with heavy importation of chilled fish from Chile, Ecuador, and Peru.[3] Current methods of placing fish on ice for transport are inadequate to kill plerocercoids.

In addition to human migration and importation of disease, other factors might account for the increased incidence and range of disease, including, in the case of D dentriticum, migrating birds such as gulls around Lake Baikal and climate change affecting intermediate hosts.[7] In the absence of effective surveillance and reporting, these diseases will primarily be discovered incidentally. Fish surveys tend to show limited positivity, ranging from 50% of pike in Lake Como in 2013[9] and 51% of Tokyo chum salmon in 2001[4] to 20% of various species of Peruvian marine fish infested with A pacificus in 2014.[3]

Workers in the fish industry may be at some risk for diphyllobothriasis, particularly for serosal or organ-encysted worms such as D dendriticum and A pacificus, from gutting and either contamination or habits of consumption of roe and fish organs while working.[7, 3]

Diphyllobothriasis has no reported age predilection or sexual predilection. In addition, it has no known racial predilection, except as would be expected based on geographic and cultural factors.

Prognosis

Diphyllobothriasis carries an excellent prognosis. D latum is not invasive, and mortality due to diphyllobothriasis is rare. Patients are often frightened and emotionally upset at the passage of worm parts for a long period of time unless treated. Single-dose therapy is usually effective, although some treatment failures have been reported, and repeat treatment is occasionally needed.

Occasionally, infestation can lead to severe megaloblastic anemia or intestinal obstruction. Although it is well described, macrocystic anemia and neurological disease is extremely rare. Gastrointestinal (GI) obstruction is also rare but may occur, especially when numerous worms are present.

Patient Education

Because reinfection is possible, patients should be advised to modify their dietary habits so as to minimize the potential for reexposure.

Proper food preparation and hygiene should be encouraged, particularly during travel within endemic areas. Preventive public education has been generally inadequate, and the food and restaurant industry has generally been slow to adopt recommendations for freezing of fish. Simple icing of fish is insufficient to prevent infection.

The US Centers for Disease Control and Prevention (CDC) recommends cooking fish to an internal temperature of 63°C (145°F) or higher, freezing fish to -4°F (-20°C) for 7 days or -31°F (-35°C) or less until solid, and storing at either -31°F (-65°C) or below for 15 hours or -4°F (-20°C) for 24 hours.[19] These precautions kill the plerocercoid larvae. The fish must never be sampled before it is properly prepared.

History

Most persons with diphyllobothriasis are asymptomatic. The vast majority of patients who are diagnosed present with passage of proglottids.

Among persons with diphyllobothriasis who are symptomatic, the following are the most common symptoms:[20]

Other, less common, symptoms include the following:

One study evaluated a selection of symptoms in a group of patients who were affected but nonanemic. Increased symptoms of fatigue, extremity numbness, and anorexia occurred in the affected group. Abdominal pain was not a significant symptom. Gastrointestinal (GI) obstruction is rare, but when it does occur, it manifests as acute abdominal pain associated with vomiting, distention, or both.[10]

Megaloblastic anemia is also rare. Studies note that about 40% of patients have decreased serum vitamin B-12 levels, but fewer than 2% of patients are anemic.[21, 1] Patients with an underlying problem (eg, celiac disease or congenital malabsorption) are at higher risk of developing a symptomatic infection. Anemic patients can present with pallor, breathlessness, and neurologic symptoms such as weakness, numbness, and disturbances in coordination. The symptoms depend on the severity.

Physical Examination

D latum has an unusual affinity for vitamin B-12, and the presentation of diphyllobothriasis may resemble that of megaloblastic anemia. No typical examination findings are noted, except for those seen in severe cases of anemia. Because significant anemia affects less than 2% of persons infected with D latum, most patients with diphyllobothriasis have no signs of illness.

The following physical findings associated with diphyllobothriasis are rare and are most likely related to underlying nutritional anemia:

If the patient presents with obstruction, the following physical findings may be noted:

Complications

Rarely, patients with diphyllobothriasis may need surgical relief for obstruction or replacement of vitamin B-12 or iron.

Laboratory Studies

Laboratory studies that may be used in the diagnosis of diphyllobothriasis include the following:

Diagnosis of D latum infection is based on identification of the operculated eggs in the stool (see the images below). Usually, this is not difficult, because of the large quantity of eggs (≥1 million) produced each day.



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Proglottids of Diphyllobothrium latum.



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Egg of Diphyllobothrium latum with arrow pointing to operculum.

The anemia produced by diphyllobothriasis is typically associated with increased free hydrochloric acid in gastric juice, in contrast to the relative achlorhydria invariably observed in true pernicious anemia.

A multiplex polymerase chain reaction (PCR) has been described.[24]

Other Studies

In general, no imaging studies are required to evaluate diphyllobothriasis, unless they are clinically indicated by other aspects of the patient’s presentation. For example, patients who present with obstruction require appropriate testing, starting with both flat and upright abdominal radiography.

On occasion, cases of diphyllobothriasis have been successfully identified by means of upper endoscopy or capsule endoscopy.[25, 26, 2]

Approach Considerations

Most patients with diphyllobothriasis, unless they have severe symptoms, can be safely treated as outpatients. Inpatient care is not generally required but may have to be considered in advanced, resistant, or complicated cases.

Diphyllobothriasis is treated by pharmacologic means; surgical treatment is not required unless otherwise indicated (eg, in a patient presenting with intestinal obstruction). Even in the face of decreased vitamin B-12 levels, less than 2% of patients with diphyllobothriasis develop anemia. Vitamin supplementation may be required in severe cases. As a rule, no activity limitations or restrictions are necessary.

Pharmacologic Therapy

Treatment of diphyllobothriasis is pharmacologic. Because the parasite’s biochemical pathways are different from those of the human host, drug toxicity is directed toward the parasite, the egg, or the larvae. Mechanisms of action vary within a drug class. Antiparasitic actions may include the following:

Praziquantel is considered the drug of choice for D latum infection, with niclosamide as an alternative.[27]

The neurologic and hematologic manifestations of vitamin B-12 deficiency respond well to supplementation. In the case of vitamin B-12 deficiency secondary to diphyllobothriasis, the signs and symptoms may resolve with antiparasitic therapy alone.

Consultations

Resistant or advanced cases of diphyllobothriasis may require consultation with a gastroenterologist and an infectious disease specialist. Consultation with a hematologist may be considered, depending on the severity of anemia. In the case of suspected obstruction, consultation with a surgeon is indicated.

Long-Term Monitoring

The patient’s stool should be reexamined on day 7 after therapy to test for cure. The presence of any Diphyllobothrium segments or ova in the stool on posttherapy day 7 constitutes a treatment failure. If the first course of treatment fails, a second identical course of therapy may be administered.

Medication Summary

The goals of pharmacotherapy are to eradicate the infection, to reduce morbidity, and to prevent complications.

Niclosamide (Niclocide)

Clinical Context:  DOC; inhibits mitochondrial oxidative phosphorylation and glucose uptake in the parasite.

Praziquantel (Biltricide)

Clinical Context:  Praziquantel is used in the treatment of several different infestations and is the drug of choice for diphyllobothriasis. It increases cell membrane permeability in susceptible worms, resulting in loss of intracellular calcium, massive contractions, and paralysis of musculature. Tablets should be swallowed with liquid during meals; keeping the tablets in the mouth may result in a bitter taste that can induce nausea or vomiting.

Class Summary

Antimicrobial agents are used to eradicate the infecting organism (most often, D latum). Praziquantel is the drug of choice; niclosamide is an alternative.

Author

David R Haburchak, MD, FACP, Professor Emeritus of Medicine, Department of Medicine, Division of Infectious Diseases, Medical College of Georgia at Augusta University

Disclosure: Nothing to disclose.

Chief Editor

Pranatharthi Haran Chandrasekar, MBBS, MD, Professor, Chief of Infectious Disease, Department of Internal Medicine, Wayne State University School of Medicine

Disclosure: Nothing to disclose.

Additional Contributors

Coburn H Allen, MD, Assistant Professor of Pediatrics, Dell Children's Hospital

Disclosure: Nothing to disclose.

Derek Ryan Linklater, MD, Assistant Professor of Military and Emergency Medicine, F Edward Hebert School Of Medicine; Assistant Clinical Professor of Emergency Medicine, Texas A&M Health Science Center College of Medicine; Clinical Instructor of Pediatrics, Baylor College of Medicine

Disclosure: Nothing to disclose.

Acknowledgements

Thomas M Kerkering, MD Chief of Infectious Diseases, Virginia Tech Carilion School of Medicine

Thomas M Kerkering, MD is a member of the following medical societies: Alpha Omega Alpha, American College of Physicians, American Public Health Association, American Society for Microbiology, American Society of Tropical Medicine and Hygiene, Infectious Diseases Society of America, Medical Society of Virginia, and Wilderness Medical Society

Disclosure: Nothing to disclose.

Alia Rai, MD Adolescent Medicine Fellow, Department of Pediatrics, West Virginia University

Alia Rai, MD is a member of the following medical societies: American Academy of Pediatrics, American Medical Association, and Society for Adolescent Medicine

Disclosure: Nothing to disclose.

Russell W Steele, MD Head, Division of Pediatric Infectious Diseases, Ochsner Children's Health Center; Clinical Professor, Department of Pediatrics, Tulane University School of Medicine

Russell W Steele, MD is a member of the following medical societies: American Academy of Pediatrics, American Association of Immunologists, American Pediatric Society, American Society for Microbiology, Infectious Diseases Society of America, Louisiana State Medical Society, Pediatric Infectious Diseases Society, Society for Pediatric Research, and Southern Medical Association

Disclosure: Nothing to disclose.

Francisco Talavera, PharmD, PhD Adjunct Assistant Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Medscape Salary Employment

Mark R Wallace, MD, FACP, FIDSA Clinical Professor of Medicine, Florida State University College of Medicine; Head of Infectious Disease Fellowship Program, Orlando Regional Medical Center

Mark R Wallace, MD, FACP, FIDSA is a member of the following medical societies: American College of Physicians, American Medical Association, American Society of Tropical Medicine and Hygiene, and Infectious Diseases Society of America

Disclosure: Nothing to disclose.

Martin Weisse, MD Program Director, Associate Professor, Department of Pediatrics, West Virginia University

Martin Weisse, MD is a member of the following medical societies: Ambulatory Pediatric Association, American Academy of Pediatrics, and Pediatric Infectious Diseases Society

Disclosure: Nothing to disclose.

Mary L Windle, PharmD Adjunct Associate Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Nothing to disclose.

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Egg of Diphyllobothrium latum with arrow pointing to operculum.

This illustration depicts the life cycle of different species of Diphyllobothrium parasitic cestodes, the causal agents of the disease diphyllobothriasis. Courtesy of the Public Health Image Library (PHIL), Centers for Disease Control and Prevention (CDC) (https://phil.cdc.gov/Details.aspx?pid=3388).

Proglottids of Diphyllobothrium latum.

Egg of Diphyllobothrium latum with arrow pointing to operculum.

Life cycle of diphyllobothrium.

Egg of Diphyllobothrium latum with arrow pointing to operculum.

Proglottids of Diphyllobothrium latum.

This illustration depicts the life cycle of different species of Diphyllobothrium parasitic cestodes, the causal agents of the disease diphyllobothriasis. Courtesy of the Public Health Image Library (PHIL), Centers for Disease Control and Prevention (CDC) (https://phil.cdc.gov/Details.aspx?pid=3388).

Species Geography Fish Definitive Host Human Prevalence
D latum Finland, Baltic States, Danube Delta, Karelia, Manitoba, Great LakesPerch, pike, burbotHumans, dogs, wolvesMillions
D nihonkaiense North Pacific Coast, Japan, Korea, East RussiaSalmon (cherry, chum, pink, sockeye)Brown and black bears, wolves, dogs, foxes, minkThousands (March-June peak)
D dendriticum Lake Baikal region, Subarctic North America, Russia, Rocky Mountains, PatagoniaWhitefish, salmonidsGulls, bears, otterThousands (600/year mostly)
A pacificus Peru, Chile, Ecuador, Sakhalin IslandMarine fish (bonito, mackerel, lorna drum, croaker)Sea lions, sealsThousands
D balanopterae Japan, Spain, Norway, KoreaAnchovy, sardines, skipjack tunaWhalesHundreds (June-July peak)