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Table 1 Summary of available literature on Taenia spp. egg survival capacity

From: The survival and dispersal of Taenia eggs in the environment: what are the implications for transmission? A systematic review

Test conditions

Species

Egg viability test

Result

Year of publication

Reference

− 4 °C for 4.5, 12.3 and 76.1 days

T. saginata

In vivo: 300,000 eggs fed to one calf per condition

Heavy infection after 4.5 days, moderate after 12.3 days and only 2 cysticerci after 76.1 days

1960

[77]

Between − 9 °C and 38 °C

T. hydatigena and T. ovis

In vivo: feeding to 8 lambs on days 90 and 273 (2000 T. hydatigena eggs each (eggs stored at − 9 °C and 7 °C fed to lambs on days 90 and 273).

Cysticerci formed after 90 days (279 at 7 °C and 14 at −9 °C) and after 273 days at 7 °C (6 cysticerci), but not at − 9°C

1977

[74]

4 °C in saline for 28 and 91 days

T. taeniaeformis

In vivo: intragastric application to mice

36% cyst recovery after 28 days and 10% after 91 days

1990

[68]

5-min-long heat treatment at 50 °C or 60°C, with

22 °C as control

T. hydatigena

In vivo: 100–2000 eggs fed to lambs and cysticerci counted

The mean percentage of cysticerci recovered were 11.55, 1.22 and 0 % for 22 °C, 50 °C and 60°C, respectively

2013

[95]

4–5 °C in 1:10,000 merthiolate in normal saline

T. saginata

In vitro activation (Silverman’s hatching technique) and in vivo (calves)

Hatching (in vitro) and infectivity/survival (in vivo) for at least 168 days

1962

[73]

Between − 9 °C and 38 °C

T. hydatigena and T. ovis

In vitro hatching and activity: AGF and AIF

In vitro: Temperature-dependent decline in embryo activity

1977

[74]

At 4 °C and at − 20 °C, − 9 °C, − 4 °C, 0 °C, 10 °C, 18–22 °C, 25 °C and 37 °C in saline with antibiotics and mycostatin (for up to 42 days)

T. multiceps

In vitro hatching, activation

4°C: Activation levels increased up to 27 days (55%) but decreased afterwards (22% after 50 days). Eggs withstand freezing at − 20 °C for 42 days. Hatching ability lost after 7 days at 37 °C. Intermediate temperature shows no or negligible effects on activation

1984

[75]

5-min-long heat treatment at 40 °C, 45 °C, 50 °C, 55 °C or 60 °C; 22 °C as control

T. hydatigena

In vitro: hatching

In vitro: Activation of 6.14% of 3.07% recovered eggs after treatment at 40 °C. 99.47% reduction in activation or infectivity after treatment at 60 °C

2013

[95]

5 °C and 20 °C in water and in silt for 2, 4 and 6 months and − 18°C for 1 week

T. saginata

In vitro: hatching with NaClO and activation with AIF

Activation after 6 months at 5 °C. Decreased activation at 20 °C: 4 months in water and 2 months in silt. Activation after 1 week at − 18°C

2019

[78]

Desiccation (on glass slides until water is evaporated), mild temperature (38 °C)

T. pisiformis, T. ovis, T. hydatigena, Echinococcus granulosus

In vitro: treatment with AIF or AGF (integrity, hatching and activation)

Desiccation most restrictive for survival, T. pisiformis and E. granulosus more susceptible

1968

[72]

RH of 31, 47 and 89% (19.5 °C) for up to 365 dats

T. hydatigena

In vitro: vitality = ability to exclude 0.1% aqueous trypan blue

Vitality: 80–82% at 89% RH, 59.5–64.5% at 47% RH and 38–40% at 31% RH. Reduced vitality: 93.4% at 31% RH, 93.15% at 47% RH and 73.58% at 89% RH

2017

[96]

High T (37 - 39°C) or low T (3 - 5°C) AND high RH (89-94%) or low RH (32-33%)

T. pisiformis

In vivo: 2000 eggs fed to 7–10 rabbits in each group (control group received fresh sample of eggs at the beginning of the experiment)

High cyst count in control group (193 cysticerci). High RH: Average 3 cysticerci after 300 days (low temperature) and 0.5 after 7 days (high temperature). Low RH: 21 cysticerci after 56 days (low temperature) and no recovery (high temperature)

1975

[76]

Between 7 °C and 65 °C plus desiccation (water removed) (up to 300 days)

T. hydatigena, T. ovis and T, multiceps

In vitro hatching: AGF and AIF

No hatching after 4 days at 38 °C and higher (T. ovis and T. hydatigena). Hatching after 56 days at 21 °C and 294 days at 7°C

1977

[74]

High temperature (30–80 °C), different RH (10, 80, 90 and 95%) and different contact times

T. solium (and other helminth genera)

In vitro hatching with NaClO solution

For complete inactivation of T. solium eggs: combination of temperature > 70C and 80% RH for 120 min

2010

[97]

Pastures contaminated with egg suspensions (2000–4000 eggs/sq. yard): high rainfall vs dry (Kenya)

T. saginata

In vivo: 14 calves allowed to graze for 3 to 143 days (13–413 days after infection pasture)

Cysticerci found in 12 calves, for both pasture types. Highest number of recovered cysticerci was 233 in calf allowed to graze for 142 days, start of grazing 304 days after infection pasture (3400 eggs/ sq.yard)

1948

[28]

Outdoor on patch of 2 0m2 (Australia):

winter (0–20 °C) and summer (8–30 °C)

T. pisiformis

In vivo: rabbits grazing on patch (maximum 126 days)

Winter: Gradual decrease of infectivity over time, recovery after 126 days. Summer: No infection after 14 days

1975

[76]

Batches of 11,500 eggs deposited outdoors on natural soil surface (starting from May and September for up to 9.5 months)

T. saginata

In vivo: batches fed to calves

Deposited in May: Infective for 6.5 months, not for 9.5 months. Deposited in September: Infective for 5.5 months, not for 8.5 months

1990

[80]

Outdoor storage (May–June) in UK

T. multiceps

In vitro hatching, activation

Hatching ability lost after 28 days

1984

[75]

In freshwater stream in Denmark from December to February (fluctuating temperature: − 10 to 17 °C) and

outdoors for 1 week in February (− 6-5 °C)

T. saginata

In vitro: hatching with NaClO and activation with AIF

Activation after 4 months in stream AND repeated freezing, thawing outdoors 1 week

2019

[78]

Ensilation of eggs with minced potato (up to 28 days)

T. hydatigena

In vivo: 2000 eggs fed to lambs and cysticerci counted

359 cysticerci after 0 days, 5 cysticerci after 2 days, no cysticerci after 28 days. Reduction of 99.9% after 18.59 days of ensilation

2013

[98]

Gravid segments fixed in 70% EtOH or FA or frozen for 1 week

T. taeniaeformis

In vitro hatching (0.5% NaClO method)

No hatching of eggs from formalized segments. Hatching of eggs in all other conditions: eggs fragile after freezing; highest hatching rates after fixation in EtOH (12.6–69.2%)

1994

[99]

Exposure to UV radiation (eggs and eggs freed of the embryophore): 254 nm, dose rate of 0.6 mJ/cm2/s for 600 to 9600 s or 60 mJ/cm2/s for 6 to 192 s

T. taeniaeformis

In vivo: oral inoculation of 5000 eggs in rats

Number of cysticerci decreased dose dependently and no cysticerci were recovered after exposure to a total dose of 2880 mJ/cm2. After removal of embryophore, no cysticercus development after a total dose of 30 mJ/m2

1997

[100]

Exposure to UV radiation: UVA (near UV wavelength of 320–400 nm), UVB (mid UV, 290–320 nm) and UVC (far UV, 200–290 nm) for 30, 90, 270, 810, 2430 and 7290 s

T. taeniaeformis

In vivo: oral inoculation of 3,000 eggs in rats

UVC exposure significant effect on number of cysticerci from 90 s of exposure onwards (and smaller cysts), 100% reduction from 2430 s of exposure onwards. UVA reduction was 31.9 and 28.3% and UVB reduction was 51.8 and 54.8% at 2430 and 7290 s, respectively

2001

[101]

Sunlight (0 °C; 24 h) and UV light (20 °C; 24 h, 8 days)

T. pisiformis

In vitro: treatment with AIF or AGF (integrity, hatching and activation)

No difference in integrity, hatching and activation between control and treated eggs

1968

[72]

Exposure to UV radiation (250 nm), up to 48h

T. multiceps

In vitro hatching, activation

Hatching reduced to 3% after 24 h

1984

[75]

Lime dose of 15 and 20% CaO w/v dry basis with 80 or 90% humidity

T. solium (and other helminth genera)

In vitro: hatching with NaClO solution

For complete inactivation: 20% CaO dose (pH 12.5) and 80% humidity for 5 months

2010

[97]

High temperature (25–80 °C), different RH (10, 80, 90 and 95% RH), pH (neutral, 15 – 20% quicklime), contact times

T. solium (and other helminth genera)

In vitro: hatching with NaClO solution

For complete inactivation: combination of temperature > 70 °C and 80% humidity for 120 min OR pH 5.3, 45 °C, 90% RH for 6 days OR pH 12.7, 45 °C, 90% RH for 19 days

2012

[102]

  1. Studies are ordered by test conditions (temperature, RH, season, UV radiation, combination of conditions) and within this order by in vivo vs. in vitro studies, and then by publication year (oldest to most recent). In vitro studies focus on integrity (morphological), hatching and activation (movement of the larvae), and in vivo studies focus on infectivity and survival determined by recovery of cysticerci
  2. AGF, Artificial gastric fluid; AIF, artificial intestinal fluid; CaO, calcium oxide; EtOH, ethanol; FA, formaldehyde; NaClO, sodium hypochlorite; RH, relative humidity; UV ultraviolet